Evolution of the Stomatal Regulation of Plant Water Content

Plant Physiology Preview. Published on April 12, 2017, as DOI:10.1104/pp.17.00078

1 Research Update

2 Evolution of the stomatal regulation of plant water content.

3 Timothy J. Brodribb & Scott A.M. McAdam

4 *both authors contributed equally to this work

5 Abstract

6 Terrestrial productivity today is regulated by stomatal movements, but this has only been the case 7 since “stomatophytes” became dominant on the land 390 million years ago. In this review we 8 examine evidence for the function of early stomata, found on or near the reproductive structures of 9 bryophyte-like fossils, and consider how this function may have changed through time as vascular 10 plants evolved and diversified. We explore the controversial insights that have come from observing 11 natural variation, rather than genetic manipulation, as a primary tool for understanding the function 12 of the stomatal valve system.

14 Why is stomatal evolution important?

15 The variation in stomatal behaviour among extant plant groups has stimulated great interest 16 recently across diverse fields of science. Behavioural differences in the responses of stomata to 17 water stress within plant communities have been recognized as an important axis of variation in 18 ecological strategy (Martínez-Vilalta and Garcia-Forner, 2016; Meinzer et al., 2016), while systematic 19 variation in stomatal size, density and response characteristics (Santelia and Lawson, 2016) among 20 plant clades have important implications for interpreting plant-atmosphere interactions (Franks et 21 al., 2012) (Franks this issue; Buckley this issue). Understanding how stomatal behaviour feeds into 22 processes of plant selection is a fundamental goal in plant science, and much progress over the past 23 three decades has been made towards this goal by applying the tools of genetic manipulation to the 24 model angiosperm, Arabidopsis (Schroeder et al., 2001; Hetherington and Woodward, 2003; Kim et 25 al., 2010; Hedrich, 2012) (De Angeli & Eisenach, this issue)(Jezek and Blatt, this issue). A very 26 different, but potentially complementary approach, especially as we approach a post-genomics era, 27 is the use of natural evolutionary variation as a lens through which the function of stomata can be 28 viewed from a perspective of plant selection over evolutionary time. This novel evolutionary 29 approach to understanding stomatal function presents huge potential for enhancing our 30 understanding of not only the influence of stomatal behaviour on the colonisation of land by plants, 31 but also the key processes that govern stomatal responses in modern species.

32 Stomatal evolution has become a focus of some debate in recent years (Brodribb et al., 2009; 33 Brodribb and McAdam, 2011; Chater et al., 2011; Ruszala et al., 2011; Franks and Britton-Harper, 34 2016), largely initiated by evidence that although the stomata of ancient lineages of vascular plants

35 opened similarly to angiosperms in response to light and CO2, they close differently. In particular, the 36 observation that stomatal conductance and transpiration of ferns and lycophytes does not decline 37 significantly in response to ABA (Brodribb and McAdam, 2011), led to the theory that stomatal 38 closure during water stress originated in early vascular plants as a passive response of guard cells to 39 dehydration, and that the “active” closure mechanism, mediated by ABA, evolved much later in seed

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40 plants. Debate about this theory has seen apparently contradictory evidence presented from 41 researchers using diverse approaches. Genetic techniques are seen as the ideal means of resolving 42 such debates, but so far this evidence has also provided confusing results about the presence and 43 localization of necessary components required for ABA signalling in stomata (see below). In the face 44 of equivocal physiological evidence, it is critical to consider stomatal evolution from first principles, 45 in terms of how differences in stomatal regulation impacts plant performance. Here we focus on the 46 evolution of stomatal regulation of plant water content, from the perspective of selection and 47 adaptation, considering the functional role of stomata, and how this relates to variation in form, 48 positioning and macroscopic function observable across the phylogeny of land plants. This 49 macroscopic perspective is essential when considering core plant processes, such as stomatal action, 50 because adaptive changes in function are expected to have profound and measureable effects on 51 plant performance (McElwain, this issue).

52 The evolution of ABA responsiveness in land plants represents a fascinating example of how 53 different perspectives can lead to profoundly different conclusions. For example we know that ferns 54 are capable of very fast stomatal closure to >10% maximum aperture during dehydration, a 55 necessary response to prevent damage to the plant (see below). The size, speed and shape of this 56 closure response in ferns appears to be well explained by passive stomatal closure through guard 57 cell dehydration, without any need for active processes of ion trafficking (Brodribb and McAdam, 58 2011). When combined with the fact that, unlike angiosperms, fern and lycophyte stomata do not 59 respond to endogenous levels of ABA (McAdam and Brodribb, 2012), the conclusion is that ABA- 60 mediated closure is not important in basal vascular plants seems robust. However reports regularly 61 emerge of small stomatal responses in fern guard cells artificially exposed to ABA levels typically 62 hundreds of thousands to millions of times higher than endogenous levels (Ruszala et al., 2011; Cai 63 et al., 2017) Merilo et al. this issue)). The reasonable conclusion from these data is that fern guard 64 cells react to exceedingly high levels of ABA, but the challenge remains to understand such 65 observations in an evolutionary context.

66 Here we review recent discoveries made using an evolutionary approach to reconstructing stomatal 67 function, and consider how this adds to the classical genetic manipulation approach in a model 68 angiosperm that has dominated stomatal biology for the past three decades.

69 Developmental homology but functional divergence?

70 The opening and closing of stomata is a conspicuous feature of vascular land plant physiology 71 (Darwin, 1898) and the presence of stomata on moss and hornwort sporophytes (Ziegler, 1987) as 72 well as the epidermes of species from the oldest vascular land plant fossil assemblage, the 410 73 million year old Rhynie Chert (Edwards and Axe, 1992), suggest that these features are a critical ‘tool’ 74 for terrestrial plant survival. Despite numerous losses of stomata in the bryophytes, including in the 75 liverworts and a number of basal moss clades (Paton and Pearce, 1957; Haig, 2013), the structure 76 and developmental genes that guide epidermal cell fate and ultimately the differentiation of guard 77 cells appear to be ancient and highly conserved (Vatén and Bergmann, 2012; Renzaglia et al., this 78 issue). This archaic developmental origin of stomata, raises the intriguing question of what selective 79 pressure drove the evolution of these first adjustable pores in the earliest land plants? If the 80 function of the earliest stomata was the same as in vascular plants, facilitating the dynamic 81 optimisation of water use against carbon gain (Cowan, 1977), then common elements of the

82 stomatal control process likely evolved with these first stomata. This angiosperm-centric hypothesis 83 has been long held as the best explanation for stomatal evolution (Haberlandt, 1886; Paton and 84 Pearce, 1957; Ziegler, 1987; Chater et al., 2011), but has been recently challenged by key differences 85 in the general behaviour and apparent role of early stomata as well as recent molecular and 86 physiological evidence indicating a highly divergent functional role for stomata in these most basal 87 stomata-bearing land plants (Haig, 2013; Pressel et al., 2014; Field et al., 2015; Chater et al., 2016; 88 Renzaglia et al., this issue).

89 While the regulation of gas exchange by stomata to facilitate photosynthesis is a canon of plant 90 physiology, based upon the well described behaviour of millions of stomata concentrated on the 91 primary photosynthetic organs of derived vascular plants (Ziegler, 1987), the placement and number 92 of stomata in non-vascular plants and the earliest, leaf-less vascular plants is vastly different (Figure 93 1). In the most basal land plant species there are no stomata on the primary photosynthetic organ, 94 the gametophyte, with guard cells located solely on the reproductive sporophyte and, in mosses, on 95 the apophysis at the base of the capsule (Haberlandt, 1886). This is similar to a number of the 96 earliest vascular land plant fossils, particularly the cooksonioids, which are likely the common 97 ancestor of extant vascular plants (Gonez and Gerrienne, 2010), and from which the first evidence of 98 the oldest stomata is recorded (Edwards and Axe, 1992). These species had stomata (rarely more 99 than 3) similarly clustered around the base of the reproductive sporangia (Edwards et al., 1998). 100 There is compelling evidence that the main sporophyte axes of these plants were not capable of 101 autonomous photosynthesis given their anatomy, and instead relied on primary photosynthesis 102 occurring in a basal gametophyte (Boyce, 2008), much like extant bryophytes which have very low 103 photosynthetic activity in the sporophyte (Paolillo and Bazzaz, 1968; Thomas et al., 1978).

104 Suggestions, based upon the frequency and positioning of the earliest fossil stomata, that ancestral 105 stomata did not perform a photosynthetic role, are supported by observations of living examples of 106 hornwort and moss stomata. In these plants the stomatal pore forms and opens only once then 107 never closes (Pressel et al., 2014; Field et al., 2015; Renzaglia et al., this issue). This single opening 108 event corresponds to a subsequent evaporation of the fluid-filled intercellular spaces in the 109 sporangial tissue, facilitating the desiccation of the sporophyte prior to spore release. Additionally it 110 has been proposed that enhanced transpiration caused by stomatal opening may also drive a strong 111 transpirational flux of nutrients and photosynthates from the basal gametophyte into the developing 112 sporophyte (Haig, 2013). Recently these observations have received considerable molecular support 113 by a study in the moss species Physcomitrella patens in which a major delay in the dehiscence of 114 capsules was observed in astomatal, guard cell developmental knockout mutants (Chater et al., 115 2016). Indeed, this lack of capsule dehiscence was the only reported functional difference between 116 astomatal mutants and wildtype plants.

117 Ancient stomatal opening driven by photosynthesis in the guard cells

118 While a divergent role for stomata seems likely between basal land plants and more derived vascular 119 plants, the observation that all stomata are apparently capable of opening suggests that a conserved 120 opening mechanism may operate across stomatal-bearing land plants. The one possible exception 121 seems to be the basal moss genus Sphagnum where stomatal opening is likely a derived mechanism, 122 being triggered by the loss of guard cell turgor (Duckett et al., 2009). This conspicuous inversion of 123 the normal positive relationship between aperture and guard cell turgor pressure in the stomata of

124 Sphagnum however is not apparent in more derived mosses or hornworts, suggesting that, like 125 vascular plants, stomatal opening in basal species other than Sphagnum requires an increase in 126 guard cell turgor (Wiggans, 1921; Heath, 1938). In vascular plants particularly angiosperms, active 127 metabolic processes essential for increasing guard cell turgor and opening the pore are well 128 described, particularly in the light (Schroeder et al., 2001; Shimazaki et al., 2007)(Kinoshita, this 129 issue). This opening process is driven by the hyperpolarisation of the guard cell membrane potential 130 through the activation of the plasma membrane proton pump (H+-ATPase). Photosynthesis inside 131 the guard cells (Zeiger and Field, 1982) provides a source of ATP (Tominaga et al., 2001; Lawson, 132 2009; Suetsugu et al., 2014), however in angiosperms this guard cell response alone is not sufficient 133 to fully open stomata (Willmer and Pallas, 1974; Mumm et al., 2011; Chen et al., 2012). 134 Photosynthesis in the mesophyll also provides a strong additional signal for opening (Roelfsema et 135 al., 2002; Sibbernsen and Mott, 2010; Lawson et al., 2014) Santiella and Lawson, this issue) 136 potentially via an unknown aqueous signal (Fujita et al., 2013), possibly combined with starch 137 metabolism (Horrer et al., 2016). Like vascular plants, bryophyte stomata contain chloroplasts 138 (Butterfass, 1979; Lucas and Renzaglia, 2002). Indeed, the presence of chloroplasts in guard cells 139 appears to be an ancestral trait, with distinctive colouring of the guard cells in comparison to 140 epidermal pavement cells noted in rhyniophytoids (Edwards et al., 1998), suggesting that these 141 earliest fossilised stomata similarly contained chloroplasts. While in angiosperms photosynthesis in 142 the mesophyll appears to provide a major signal for driving stomatal opening in the light (Roelfsema 143 et al., 2002; Lawson et al., 2014), in basal vascular plants, stomatal opening in the light can be driven 144 by guard-cell autonomous photosynthesis alone, with rapid stomatal opening occurring in the 145 isolated epidermis of leptosporangiate ferns (McAdam and Brodribb, 2012), which lack stomatal 146 responses to blue light and hence open only by photosynthetic processes (Doi et al., 2006; Doi and 147 Shimazaki, 2008; Doi et al., 2015). This data indicates that a mesophyll signal for stomatal opening in 148 the light likely evolved after the divergence of seed plants (McAdam and Brodribb, 2012). The 149 ancestral ability of non-seed plant stomata to respond to light in the absence of the mesophyll may 150 be due to the comparatively high number of chloroplasts in the guard cells of these species 151 (Butterfass, 1979).

152 An association between guard cell photosynthesis and stomatal opening in the earliest stomatal- 153 bearing land plants provides the ideal mechanism for actively triggering stomatal opening to 154 desiccate the sporophyte. 390 million years ago however, the rise of extant clades of basal vascular 155 land plants including the lycophytes, and followed by the ferns, marked a major anatomical 156 transition in land plants, namely the evolution of an independent, dominant sporophyte generation 157 with dedicated photosynthetic organs covered in stomata. This evolutionary transition associating 158 stomata with photosynthesis required a major change in the way land plants used stomata, from 159 facilitating the desiccation of the sporophyte to maximising of photosynthetic gas exchange in the 160 light, and the regulation of plant water status. Maximising leaf gas exchange for photosynthesis in 161 the light likely required no evolutionary transformation in guard cell control, as this process could 162 easily be achieved by allowing stomata to rapidly increase in turgor on exposure to light, presumably 163 in the same way basal vascular land plants open stomata. The apparent involvement of the H+- 164 ATPase in stomatal opening of the bryophyte Physomitrella appears to confirm a common 165 mechanism with higher plants (Chater et al., 2011), although more work in bryophytes is required to 166 confirm this potentially ancient mechanism. Extant lycophyte and fern stomata have the capacity to 167 open rapidly in the light (Mansfield and Willmer, 1969; Doi and Shimazaki, 2008; McAdam and

168 Brodribb, 2012), with lycophyte stomata possessing both photosynthetically driven stomatal 169 opening in red light as well as blue triggered opening, while leptosporangiate ferns (which comprise 170 more than 96% of fern specific diversity (Palmer et al., 2004)) have lost blue light stomatal signalling 171 (Doi et al., 2015). The reason behind this loss of blue light stomatal signalling in derived ferns is, as 172 yet, unknown, but maybe due to a chimeric red-blue photoreceptor in leptosporangiate ferns, an 173 adaptation associated with photosynthesis in low light environments (Kawai et al., 2003).

174 Stomata on the primary photosynthetic organ and the maintenance of homeohydry

175 Although a role for stomatal opening seems apparent across all land plants, the role and process of 176 stomatal closure seems much less uniform, particularly if basal plants are considered. In vascular 177 plants however, a primary stomatal function is the action to close the pore during water stress to 178 reduce transpiration and maintain plant hydration and avoid damage to the plant vascular system 179 (Fig. 2). The possible selective pressures driving the evolution of stomatal closure in the light is 180 typically cited as; (1) being a mechanism for increasing water use efficiency (during stomatal closure 181 at low humidity) or (2) as a means of protecting tissues from desiccation. It is hard to understand 182 how selection for efficient water use can operate at the level of the individual plant due to the fact 183 that water conservation inevitably provides more water for competitors (Cowan, 2002). The 184 alternative, protective role, provides a much more convincing selective advantage to plants, and 185 seems likely to underpin the evolution of stomatal responses in the light (Wolf et al., 2016). However, 186 as mentioned above, several lines of evidence suggest that this action may not be an ancestral 187 character in stomatal evolution, including the widespread capacity for desiccation-tolerance 188 (Peñuelas and Munné-Bosch, 2010) in bryophytes and the fact that ancestral stomata probably aided 189 rather than inhibited desiccation (of sporangia) in basal land plants (Caine et al., 2016). Desiccation- 190 tolerance obviates the need to control evaporation from leaves, but was likely to be incompatible 191 with the evolution of massive plants that began to dominate forests during the radiation of land 192 plants (Kenrick and Crane, 1997). The reason for this is that the internal water transport system in all 193 plants becomes cavitated during acute water stress causing leaves to be cut off from water in the 194 soil (Tyree and Sperry, 1989). This type of damage can be easily repaired in small plants where 195 capillary action can redissolve air embolisms in the vascular system after rain (Rolland et al., 2015), 196 but larger woody plants are unable to repair cavitated xylem tissues by capillarity or root pressure 197 (Charrier et al., 2016), and therefore xylem becomes irreversibly damaged during water stress 198 (Brodribb and Cochard, 2009; Cochard and Delzon, 2013). Stomatal closure to protect the xylem 199 from cavitation must have thus been an evolutionary prerequisite for the increase in plant size that 200 occurred during the radiation of vascular plants. Indeed it has been demonstrated that the stomata 201 of early vascular plants such as ferns close before the decline in hydraulic function associated with 202 desiccation (Brodribb and Holbrook, 2003). New techniques that visualize the process of xylem 203 cavitation, clearly demonstrate that a similar role of stomatal closure in protecting the xylem from 204 cavitation during water stress (Fig. 2) is also common to gymnosperms and angiosperms (Brodribb et 205 al., 2016; Hochberg et al., 2017). There are good examples of interaction between opening and 206 closing signals to stomata during the early onset of plant desiccation, for example the opening of

207 stomata at high VPD by exposure to low CO2 (Bunce, 2006). However the closure mechanism during 208 drying appears to override all other signals as plants approach turgor loss (Aasamaa and Sõber, 2011; 209 Bartlett et al., 2016), and subsequent xylem cavitation (Hochberg et al., 2017).

210 The simplest and most effective means of closing a turgor-operated valve, such as the stomatal pore, 211 when leaf water status declines is to establish a strong hydraulic connection between guard cells and 212 surrounding leaf tissue, such that the hydration of the guard cells is physically linked to the 213 hydration of the leaf. Such a linkage means that guard cells lose turgor as leaf water potential 214 declines, passively closing the pore and dramatically reducing evaporation (Brodribb and McAdam, 215 2011). This extremely simple means of stomatal closure in response to declining leaf water status 216 requires no metabolic input or complex signalling intermediates, and is well described in lycophytes 217 and ferns (Lange et al., 1971; Lösch, 1977, 1979; Brodribb and McAdam, 2011; Martins et al., 2016). 218 Stomatal responses to changes in vapour pressure deficit (or the humidity of the air) are thus highly 219 predictable in these early vascular plants based on a passive model that links leaf turgor with guard 220 cell turgor (Brodribb and McAdam, 2011; Martins et al., 2016). However, there is an important 221 prerequisite for this passive mechanism to function correctly in these basal species; a minimal 222 influence of epidermal cell mechanics on stomatal aperture, meaning that only guard cell turgor 223 influences the aperture of the pore (Franks and Farquhar, 2007). This prerequisite is very much 224 absent in angiosperms.

225 In angiosperms the passive response of stomata to rapid changes in leaf hydration is completely 226 inverted, causing stomata to passively move in the wrong direction, opening when evaporation 227 increases and closing as leaves hydrate. This peculiar characteristic arises because of a complicated 228 mechanical relationship between guard cells and epidermal cells that results in “wrong-way” passive 229 responses to leaf water content (Darwin, 1898; Iwanoff, 1928). An absence of this mechanical 230 advantage in ferns and lycophytes appears consistent with passive control in these early clades, 231 while cuticle analysis of the rhyniophytoids suggests that this lack of epidermal mechanical 232 advantage is ancestral in stomatophytes. The stomata in these ancient plants apparently opened 233 towards the periclinal wall of the guard cell (Edwards and Axe, 1992), much the same way as extant 234 lycophytes and ferns (Franks and Farquhar, 2007; Apostolakos et al., 2010) for which there is no 235 movement of the dorsal guard cell walls into the surrounding epidermal cells, a major contrast with 236 modern angiosperms (Fig. 3).

237 Metabolically controlled stomatal closure in response to leaf water deficit

238 A passive linkage between leaf water status and guard cell turgor observed in extant basal vascular 239 plants appears to be sufficient to prevent xylem cavitation during diurnal changes in evaporative 240 demand (Martins et al., 2015). However, without more sophisticated mechanisms to reduce guard 241 cell turgor and produce complete stomatal closure it has been hypothesized that passive closure 242 does not provide a sufficiently tight stomatal seal capable of preventing ferns and lycophytes from 243 rapidly reaching critical leaf water potentials when soil water is depleted during drought (McAdam 244 and Brodribb, 2013). As a result, ferns and lycophytes in dry environments rely on either a high 245 plant capacitance or low stomatal density (McAdam and Brodribb, 2013), desiccation tolerance 246 (Hietz, 2010) and in some cases, rather cavitation resistant xylem (Baer et al., 2016) to survive 247 drought. An active stomatal closing signal has the potential to restrict transpiration to rates 248 approaching cuticular transpiration (Tardieu and Simonneau, 1998; Brodribb and Holbrook, 2003, 249 2004) providing the ability for species to preserve plant water even if leaves have low capacitance 250 and large numbers of stomata. In seed plants the presence of an active regulator of stomatal 251 responses to leaf water status is evident from diverse observations from the field (Schulze et al., 252 1974), under controlled conditions (Tardieu and Davies, 1993) and in electrophysiological

253 experiments on isolated guard cells (Grabov and Blatt, 1998; Pei et al., 2000; Raschke et al., 2003; 254 Negi et al., 2008)(Jezek and Blatt, This issue) indicating the presence of a non-hydraulic signal driving 255 stomatal closure. This signal is the phytohormone abscisic acid (ABA), which is synthesised as leaves 256 loose turgor and which actively closes seed plant stomata (Mittelheuser and Van Steveninck, 1969; 257 Pierce and Raschke, 1980; Davies et al., 1981).

258 Co-option of an ancient and highly conserved ABA signalling pathway into the guard cells of seed 259 plants

260 The molecular signalling pathway eliciting an ABA response is well described from RCAR/PYR/PYL 261 receptors, which in the absence of ABA bind to PP2Cs (Ma et al., 2009; Park et al., 2009), when ABA 262 is present RCAR/PYR/PYL binding to PP2Cs is eliminated allowing PP2Cs to activate SnRK2 263 phosphorylators (Yoshida et al., 2006). In seed plants, once activated by PP2Cs in the presence of 264 ABA these SnRK2s phosphorylate guard cell specific membrane-bound anion channels (the best 265 described of these are the S-type anion channels, SLACs) initiating the efflux of ions and 266 consequently decreasing cell turgor and closing the stomatal pore (Geiger et al., 2009). There is an 267 array of membrane bound channels and transporters that facilitate the efflux of most osmolytes 268 once SnRK2s signal the presence of ABA and activate anion channels (Hills et al., 2012). The 269 dominant role for SnRK2s in this ABA signalling cascade is strongly supported by experimental data. 270 The phenotype of single gene mutants in the key SnRK2 for stomatal responses to ABA, OST1, are 271 profound, displaying no sensitivity to ABA (Mustilli et al., 2002) or VPD (Merilo et al., 2013; Merilo et 272 al., 2015). While other SnRK2-independent signalling pathways for ABA perception and SLAC 273 activation have been suggested (Geiger et al., 2010; Brandt et al., 2012; Pornsiriwong et al., 2017), 274 these are redundant and many either converge or require cross-talk with functional OST1 to activate 275 anion channels (Brandt et al., 2015). Whether these alternative SnRK2-independent ABA signalling 276 pathways play an adaptively relevant role in stomatal function is yet to be determined. The core 277 SnRK2-centric ABA signalling pathway is highly conserved across land plants with all lineages, 278 including those species without stomata, such as liverworts, displaying functional physiological 279 responses to ABA (Ghosh et al., 2016), RCAR/PYR/PYL ABA receptors present in genomes (Hauser et 280 al., 2011) and functional PP2Cs (Tougane et al., 2010). This highly conserved ABA signalling pathway 281 is known to regulate desiccation tolerance mechanisms (Tougane et al., 2010), spore dormancy and 282 sex determination in non-seed plants (McAdam et al., 2016), amongst other processes.

283 Three essential evolutionary steps (Fig. 4) were required for the co-option of the ancient ABA signal 284 into a functionally relevant metabolic regulator of gas exchange in the earliest seed plants; (1) an 285 operational SnRK2-SLAC pairing, (2) guard cell specific expression of this pairing, and (3) the ability to 286 synthesise ABA over a time-frame relevant to stomatal responses. One or more of these 287 requirements for ABA driven stomatal responses does not occur in non-seed plants. In lycophytes 288 and ferns native SnRK2s are unable to activate native SLACs (McAdam et al., 2016), while a 289 functional SnRK2-SLAC pairing, albeit weak, observed in P. patens (Lind et al., 2015) is not specific to 290 the guard cells (Chater et al., 2011; Vesty et al., 2016), and likely plays a role in nitrate homeostasis. 291 In well studied angiosperms there is a potent pairing of native SnRK2s and SLACs that are specifically 292 expressed in guard cells (Li and Assmann, 1996; Geiger et al., 2009; Fujii et al., 2011). Whether this 293 also occurs in the first group of land plants to possess functional stomatal responses to endogenous 294 ABA, the gymnosperms, remains to be tested. The third requirement relates to the speed of ABA 295 synthesis over a timeframe that matches apparent ABA-driven stomatal responses. In terms of

296 changing soil water deficit, this condition is met in all vascular land plants (Kraus and Ziegler, 1993; 297 Hoffman et al., 1999; Kong et al., 2009; McAdam and Brodribb, 2013), but only in angiosperm does 298 ABA synthesis appear to occur over a timeframe that corresponds to the dynamics of stomatal 299 response to VPD (McAdam and Brodribb, 2015).

300 Diversity in the regulation of water use amongst seed plants is driven by differences in ABA 301 metabolism

302 The first group of land plants to unequivocally respond to endogenous ABA, the gymnosperms, are 303 able to synthesise ABA in leaves after at least six hours of sustained water stress (McAdam and 304 Brodribb, 2014) and utilise these high levels to close stomata during drought (Brodribb et al., 2014). 305 Evidence suggests that the earliest gymnosperms used ABA to prevent cavitation of the xylem when 306 growing in seasonally dry environments (Brodribb et al., 2014), which is unlike fern and lycophyte 307 species which appear incapable of dominating dry forest communities. While survival in dry 308 environments likely provided the selective pressure to co-opt ABA signalling into the guard cells, the 309 evolution of this trait appears to have become an important axis of variation in water use strategies 310 and responses to leaf water status. Diversity in water use strategies stemming from differences in 311 ABA metabolism is apparent in the gymnosperms. Species that have vulnerable xylem to cavitation 312 synthesise high levels of ABA in order to close stomata and persist in seasonally dry environments 313 (Brodribb and McAdam, 2013). By contrast, other conifer species produce cavitation-resistant xylem 314 (Pittermann et al., 2010; Larter et al., 2015) that allows plants to survive when leaf water potentials 315 drop below -4.5 MPa during drought. Once leaves reach this low leaf water potential stomata will 316 close passively due to declining guard and epidermal cell turgor even in the absence of ABA 317 (Brodribb et al., 2014; Deans et al., This issue). In these cavitation-resistant species, drought stress 318 beyond this critical point leads to a decline in ABA levels to pre-stress values despite the plant 319 experiencing extreme but recoverable water stress. This alternative strategy is also associated with 320 anisohydric stomatal responses to drought, and is thought to prolong gas exchange and 321 photosynthesis during drought (Brodribb and McAdam, 2013).

322 While ABA metabolism provides an important explanation for variation in stomatal behaviour within 323 the gymnosperms, it also appears to explain differences between gymnosperms and angiosperms in 324 their stomatal responses to water deficit. In gymnosperms, ABA synthetic rates are too slow to 325 effectively regulate stomatal responses to changes in VPD. This is either due to a lack of specific 326 enzymes late in the ABA biosynthetic pathway (Hanada et al., 2011; McAdam et al., 2015), or a 327 general delay in the upregulation of critical rate-limiting enzymes for ABA biosynthesis (McAdam and 328 Brodribb, 2015), both of which require further testing. The result of this slow ABA synthesis in 329 gymnosperms is that conifer stomata have predictable and passive, non ABA-mediated responses to 330 short term changes in VPD (McAdam and Brodribb, 2014), just like the two most basal lineages of 331 vascular plants. In angiosperms however, ABA biosynthesis is extremely rapid (Christmann et al., 332 2005; Waadt et al., 2014; McAdam et al., 2016) and can be upregulated by a drop in leaf turgor over 333 the time frame of minutes (Pierce and Raschke, 1981; McAdam and Brodribb, 2016). Thus 334 angiosperms respond to VPD using ABA, as is evidenced by the change in ABA levels in angiosperm 335 leaves in response to step changes in VPD (Bauerle et al., 2004; McAdam and Brodribb, 2015), while 336 mutants in ABA biosynthetic and signalling genes have compromised stomatal responses to VPD (Xie 337 et al., 2006; Merilo et al., 2013; McAdam et al., 2016). The result of this regulation of stomatal 338 responses to VPD by ABA is that, unlike all other vascular land plant clades, the stomatal response to

339 VPD in angiosperms is often hysteretic and unable to be predicted by passive hydraulic processes 340 (O'Grady et al., 1999; McAdam and Brodribb, 2015). Contributing to this hysteresis in stomatal 341 response to VPD is an internal balance between the rates of ABA biosynthesis and catabolism, both 342 of which are regulated in different tissues. While ABA biosynthesis in response to a drop in leaf 343 turgor is hypothesised to occur very near to the vascular tissue (Kuromori et al., 2014), ABA 344 catabolism in an Arabidopsis leaf is primarily controlled by two CYP707 genes, one expressed in 345 vascular tissue, the other predominantly in guard cells (Okamoto et al., 2009). These two genes 346 have different rates of expression in leaves that are exposed to high humidity, suggesting temporal 347 variation in ABA catabolism across the leaf (Okamoto et al., 2009). Whether alternative expression 348 profiles for these two key leaf ABA catabolism genes, or indeed ABA transport genes (Kuromori et al., 349 2011; Kanno et al., 2012) occurs across angiosperm species to explain reported differences in the 350 sensitivity of species to VPD remains to be tested.

351 On-going questions in the field of stomatal evolution

352 Given the ever-growing multitude of genomic data from representative species spanning the land 353 plant phylogeny, in silico analyses are becoming an increasingly popular means of discussing 354 physiological evolution (Pabón-Mora et al., 2014; Yue et al., 2014; Chen et al., 2016). Stomatal 355 evolution however provides some excellent examples of why gene phylogenies should always be 356 used in combination with experimental studies of stomatal behaviour in situ. Evidence of highly 357 conserved stomatal developmental genetics among land plants (Vatén and Bergmann, 2012; Caine 358 et al., 2016) appears to support the long held notion of conserved stomatal function (Haberlandt, 359 1886; Paton and Pearce, 1957; Ziegler, 1987; Chater et al., 2011). However, a recent combination of 360 molecular and whole plant experiments by Chater et al. (2016) suggests a divergent functional role 361 for stomata in bryophytes. All that is required to transform the function of guard cells from passive 362 to functionally ABA-sensitive is the relocation or concentration of an ancestral and highly conserved 363 ABA signalling pathway into the guard cells (McAdam et al., 2016). However, this evolutionary 364 transition could never be realised by in silico analysis of genomes alone, which instead find all 365 stomata-bearing plants have the genetic capacity to perceive and respond to ABA, therefore 366 providing the foundation for the assumption that all stomata respond to ABA. Whether recent in 367 silico suggestions of major differences in the ABA biosynthetic pathway across land plant lineages 368 (McAdam et al., 2015) explains differences in ABA synthetic rates (McAdam and Brodribb, 2014) 369 remains to be tested.

370 There are a number of environmental signals regulating stomatal aperture that have not been 371 discussed in this review for which either we have little regulatory understanding of, like inverted 372 stomatal rhythms in CAM plants (Ting, 1987), or little functional understanding of, like stomatal 373 responses to phytohormones other than ABA (Dodd, 2003). Future work to resolve these questions 374 and place these responses in the context of evolution is essential. There remains much debate in

375 the literature on the evolution of the stomatal response to CO2 (Brodribb et al., 2009; Franks and 376 Britton-Harper, 2016). A common feature of all studies in this area is a conserved tendency to

377 respond to CO2, particularly low CO2, which likely reflects a common photosynthetic signalling in all 378 stomata (Brodribb et al., 2009; Franks and Britton-Harper, 2016). However, major differences across

379 lineages in the way stomata instantaneously respond to CO2 in the dark (Doi and Shimazaki, 2008;

380 Brodribb and McAdam, 2013) as well as the influence of ABA on the sensitivity of stomata to CO2 381 (McAdam et al., 2011) reflect, as yet undescribed and potentially important, mechanistic differences

382 in the way stomata respond to more natural endogenous and environmental signals. Further work 383 in this field is required to reveal these key mechanistic differences.

384 Figure Legends

385 Figure 1. Vast differences exist across land plant lineages in terms of stomatal density and size. 386 Images of stomata-bearing epidermis from two unexceptional and highly representative species of 387 respective lineages are presented to illustrate this phylogenetic difference. (Left panel) The 388 epidermis of the sporophyte of a temperate, globally distributed, stomata-bearing hornwort species 389 (Phaeoceros carolinianus), is the only organ of this non-vascular plant to bear stomata. Non-vascular 390 plant species are characterised by a similar and extremely limited number of stomata (Paton and 391 Pearce, 1957; Field et al., 2015). (Right panel) The epidermis of the angiosperm, canopy tree species 392 (Elaeocarpus kirtonii) is the primary stomata-bearing organ of this and most other angiosperm 393 species. Stomatal density in this leaf is approximately 230 stomata mm-2 which is quite modest for 394 the leaves of an angiosperm tree (Franks and Beerling, 2009; Brodribb et al., 2013). Images were 395 taken at the same magnification, scale bar = 100 µm.

396 Figure 2. Stomata in early vascular plants probably first closed to prevent cavitation of the vascular 397 system, a function that appears to remain conserved until the present. Data here show the 398 trajectory of stomatal closure (blue line) with respect to leaf water potential as three tomato plants 399 were subjected to gradual soil drying (green, red and black crosses). Close to the water potential of 400 complete stomatal closure, the process of xylem cavitation begins (three traces for leaves from three 401 individuals are shown; black, red and green circles). Cavitation curves show the accumulation of 402 cavitation events in the leaf veins of three tomato plants as they desiccate (data from Skelton et al. 403 (2017)).

404 Figure 3. A schematic representation illustrating the difference in the main mode of guard and 405 epidermal cell deformation during stomatal opening in non-angiosperms compared to angiosperms. 406 The arrows indicate the direction of cell movement.

407 Figure 4. Top. Three key evolutionary transitions are required for ABA to regulate diurnal gas 408 exchange in land plants. 1. The ability of native SnRK2 kinases (as in AtOST1 from Arabidopsis 409 thaliana) to interact with, and activate, native anion channels (like the S-type anion channel AtSLAC1 410 from A. thaliana). Representative plots of a positive activation of A. thaliana proteins are taken from 411 McAdam et al. (2016). 2. If native SnRK2s can activate native SLACs then the genes encoding these 412 proteins must be uniquely expressed in guard cells, and this is the case in angiosperms (Li and 413 Assmann, 1996), including A. thaliana, where AtOST1 is expressed in the guard cells as illustrated by 414 the profound GUS staining of the promoter of AtOST1 in these cells (Fujii et al., 2007). 3. In order to 415 regulate diurnal leaf gas exchange, foliar ABA levels must change over a timeframe that is relevant to 416 the stomatal response to changes in VPD. Data for the gymnosperm Metasequoia glyptostroboides, 417 taken from McAdam and Brodribb (2014), show strong increases in ABA level in branches that are 418 dehydrated and maintained at specific leaf water potentials for a minimum of 6 hours. This contrasts 419 with data from the angiosperm species Pisum sativum, taken from McAdam et al. (2016) which like 420 most angiosperms displays a strong increases in ABA level after only 20 minutes following a doubling 421 in vapour pressure deficit from 0.7 to 1.5 kPa. Bottom. Mapping these key transitions to a phylogeny 422 of land plants, which assumes that mosses are sister to liverworts (Wickett et al., 2014) and 423 divergent from hornworts, shows that only in angiosperms do all three of these essential

424 physiological and molecular requirements for diurnal gas exchange control by ABA occur. As 425 gymnosperms have functional stomatal responses to ABA (McAdam and Brodribb, 2014) and ferns 426 do not have guard cell specific expression of native SnRK2 or SLAC genes (McAdam et al., 2016) it is 427 likely that seed plants were the first land plants to evolve a guard cell specific expression of these 428 genes. Only in angiosperms is ABA synthesis the same speed as the stomatal response to an 429 increase in VPD (McAdam and Brodribb, 2015).

430

Downloaded from www.plantphysiol.org on May11 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Parsed Citations Aasamaa K, Sõber A (2011) Responses of stomatal conductance to simultaneous changes in two environmental factors. Tree Physiology 31: 855-864 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Apostolakos P, Livanos TL, Nikolakopoulou TL, Galatis B (2010) Callose implication in stomatal opening and closure in the fern Asplenium nidus. New Phytologist 186: 623-635 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Baer A, Wheeler JK, Pittermann J (2016) Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought. New Phytologist 210: 122-132 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bartlett MK, Klein T, Jansen S, Choat B, Sack L (2016) The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci U S A 113: 13098-13103 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bauerle WL, Whitlow TH, Setter TL, Vermeylen FM (2004) Abscisic acid synthesis in Acer rubrum L. leaves—a vapor-pressure- deficit-mediated response. Journal of the American Society for Horticultural Science 129: 182-187 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Boyce CK (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34: 179-194 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemain M, Stephan AB, Hu H, Schroeder JI (2012) Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action. Proc. Natl. Acad. Sci. U.S.A. 109: 10593-10598 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang PG, Poretsky E, Belknap TF, Waadt R, Alemán F, Schroeder JI (2015) Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4: e03599 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Cochard H (2009) Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers. Plant Physiology 149: 575-584 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132: 2166-2173 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162: 663-670 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199: 559-570 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331: 582-585 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Brodribb TJ, McAdam SAM (2013) Abscisic acid mediates a divergence in the drought response of two conifers. Plant Physiology 162: 1370-1377 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM (2013) Unique responsiveness of angiosperm stomata to elevated CO2 explained by calcium signalling. PLoS ONE 8: e82057 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytologist 183: 839-847 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences of the United States of America 111: 14489-14493 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Skelton RP, McAdam SA, Bienaimé D, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209: 1403-1409 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bunce JA (2006) How do leaf hydraulics limit stomatal conductance at high water vapour pressure deficits? Plant Cell and Environment 29: 1644-1650 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Butterfass T (1979) Patterns of chloroplast reproduction: a developmental approach to protoplasmic plant anatomy. Springer- Verlag, Vienna, Austria Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cai S, Chen G, Wang Y, Huang Y, Marchant B, Wang Y, Yang Q, Dai F, Hills A, Franks PJ, Nevo E, Soltis D, Soltis P, Sessa E, Wolf PG, Xue D, Zhang G, Pogson BJ, Blatt MR, Chen Z-H (2017) Evolutionary conservation of ABA signaling for stomatal closure in ferns. Plant Physiol: doi: 10.1104/pp.1116.01848 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Caine RS, Chater CC, Kamisugi Y, Cuming AC, Beerling DJ, Gray JE, Fleming AJ (2016) An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens. Development 143: 3306-3314 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Charrier G, Torres-Ruiz JM, Badel E, Burlett R, Choat B, Cochard H, Delmas CE, Domec J-C, Jansen S, King A (2016) Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiology: pp. 01079.02016 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 21: 1025-1029 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Current biology 21: 1025-1029 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater CC, Caine RS, Tomek M, Wallace S, Kamisugi Y, Cuming AC, Lang D, MacAlister CA, Casson S, Bergmann DC, Decker EL, Frank W, Gray JE, Fleming A, Reski R, Beerling DJ (2016) Origin and function of stomata in the moss Physcomitrella patens. Nature Plants 2: 16179 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Chen Z-H, Chen G, Dai F, Wang Y, Hills A, Ruan Y-L, Zhang G, Franks PJ, Nevo E, Blatt MR (2016) Molecular evolution of grass stomata. Trends in Plant Science doi: 10.1016/j.tplants.2016.09.005 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chen Z-H, Hills A, Baetz U, Amtmann A, Lew V, Blatt MR (2012) Systems dynamic modelling of the stomatal guard cell predicts emergent behaviours in transport, signalling and volume control. Plant Physiol.: doi: 10.1104/pp.1112.197350 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiology 137: 209-219 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cochard H, Delzon S (2013) Hydraulic failure and repair are not routine in trees. Annals of Forest Science 70: 659-661 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cowan I (2002) Fit, fitter, fittest; where does optimisation fit in? Silva Fennica 36: 745-754 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cowan IR (1977) Stomatal behaviour and environment. Advances in Botanical Research 4: 117-228 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Darwin F (1898) Observartions on stomata. Proc R Soc Lond 63: 413-417 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Darwin F (1898) Observations on stomata. Proceedings of the Royal Society of London. Series B: Biological Sciences 63: 413-417 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Davies WJ, Wilson JA, Sharp RE, Osonubi O (1981) Control of stomatal behaviour in water-stressed plants. In PG Jarvis, TA Mansfield, eds, Stomatal Physiology. Cambridge University Press, Cambridge, pp 163-185 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Deans RM, Brodribb TJ, McAdam SAM (This issue) An integrated hydraulic-hormonal model of conifer stomata predicts water stress dynamics. Plant Physiol Dodd IC (2003) Hormonal interactions and stomatal responses. Journal of Plant Growth Regulation 22: 32-46 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Kitagawa Y, Shimazaki K-i (2015) Stomatal blue light response is present in early vascular plants. Plant Physiol 169: 1205- 1213 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Shimazaki KI (2008) The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiology 147: 922-930 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Wada M, Shimazaki KI (2006) The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant and Cell Physiology 47: 748-755 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Duckett JG, Pressel S, P'Ng KMY, Renzaglia KS (2009) Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum. New Phytologist 183: 1053-1063 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Edwards D, Axe L (1992) Stomata and mechanics of stomatal functioning in some early land plants. Cour. Forschungsinst. Senckenberg 147: 59-73 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Edwards D, Kerp H, Hass H (1998) Stomata in early land plants: an anatomical and ecophysiological approach. J. Exp. Bot. 49: 255- 278 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Field KJ, Duckett JG, Cameron DD, Pressel S (2015) Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Ann Bot 115: 915-922 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106: 10343-10347 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Britton-Harper ZJ (2016) No evidence of general CO2 insensitivity in ferns: one stomatal control mechanism for all land plants? New Phytologist: doi:10.1111/nph.14020 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143: 78-87 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philosophical Transactions of the Royal Society B-Biological Sciences 367: 537-546 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujii H, Verslues PE, Zhu J-K (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19: 485-494 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujii H, Verslues PE, Zhu J-K (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl. Acad. Sci. U.S.A. 108: 1717-1722 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujita T, Noguchi K, Terashima I (2013) Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol. 199: 395-406 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KAS, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc. Natl. Acad. Sci. U.S.A. 107: 8023-8028 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci U S A 106: 21425-21430 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ghosh TK, Kaneko M, Akter K, Murai S, Komatsu K, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2016) Abscisic acid-induced gene expression in the liverwort Marchantia polymorpha is mediated by evolutionarily conserved promoter elements. Physiologia Plantarum 156: 407-420 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Gonez P, Gerrienne P (2010) A new definition and a lectotypification of the genus Cooksonia Lang 1937. International Journal of Plant Sciences 171: 199-215 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Grabov A, Blatt MR (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proceedings of the National Academy of Sciences 95: 4778-4783 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Haberlandt G (1886) Beiträge zur Anatomie und Physiologie der Laubmoose. Jahrbücher für wissenschafliche Botanik 17: 457-477 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Haig D (2013) Filial mistletoes: the functional morphology of moss sporophytes. Annals of Botany 111: 337-345 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hanada K, Hase T, Toyoda T, Shinozaki K, Okamoto M (2011) Origin and evolution of genes related to ABA metabolism and its signaling pathways. Journal of Plant Research 124: 455-465 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Current Biology 21: R346- R355 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Heath OVS (1938) An experimental investigation of the mechanism of stomatal movement, with some preliminary observations upon the response of the guard cells to "shock". New Phytologist 37: 385-395 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hedrich R (2012) Ion channels in plants. Physiological Reviews 92: 1777-1811 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hietz P (2010) Fern adaptations to xeric environments. In K Mehltreter, LR Walker, JM Sharpe, eds, Fern Ecology. Cambridge University Press, pp 140-176 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hochberg U, Bonel AG, David-Schwartz R, Degu A, Fait A, Cochard H, Peterlunger E, Herrera JC (2017) Grapevine acclimation to water deficit: the adjustment of stomatal and hydraulic conductance differs from petiole embolism vulnerability. Planta doi: 10.1007/s00425-017-2662-3 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hoffman A, Shock C, Feibert E (1999) Taxane and ABA production in yew under different soil water regimes. Hortscience 34: 882- 885 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Horrer D, Flütsch S, Pazmino D, Matthews Jack SA, Thalmann M, Nigro A, Leonhardt N, Lawson T, Santelia D (2016) Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Current Biology 26: 362-370 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Iwanoff L (1928) Zur Methodik der Transpirationsbestimmung am Standort. Berichte der Deutschen Botanischen Gesellschaft 46: 306-310 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America 109: 9653-9658 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota A, Wada M (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421: 287-290 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33-39 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61: 561-591 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kong L, Abrams SR, Owen SJ, Van Niejenhuis A, Von Aderkas P (2009) Dynamic changes in concentrations of auxin, cytokinin, ABA and selected metabolites in multiple genotypes of Douglas-fir (Pseudotsuga menziesii) during a growing season. Tree Physiol. 29: 183-190 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kraus M, Ziegler H (1993) Quantitative analysis of abscisic acid in needles of Abies alba Mill. by electron capture gas chromatography. Trees 7: 175-181 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant Journal 67: 885-894 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kuromori T, Sugimoto E, Shinozaki K (2014) Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiology 164: 1587-1592 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lange OL, Lösch R, Schultze E-D, Kappen L (1971) Responses of stomata to changes in humidity. Planta 100: 76-86 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Larter M, Brodribb TJ, Pfautsch S, Burlett R, Cochard H, Delzon S (2015) Extreme aridity pushes trees to their physical limits. Plant Physiology 168: 804-807 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytologist 181: 13-34 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lawson T, Simkin AJ, Kelly G, Granot D (2014) Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytologist 203: 1064-1081 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Li J, Assmann SM (1996) An abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8: 2359-2368 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lind C, Dreyer I, López-Sanjurjo Enrique J, von Meyer K, Ishizaki K, Kohchi T, Lang D, Zhao Y, Kreuzer I, Al-Rasheid Khaled AS, Ronne H, Reski R, Zhu J-K, Geiger D, Hedrich R (2015) Stomatal guard cells co-opted an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Curr Biol 25: 928-935 Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lösch R (1977) Responses of stomata to environmental factors-experiments with isolated epidermal strips of Polypodium vulgare - I. Temperature and Humidity. Oecologia 29: 85-97 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lösch R (1979) Responses of stomata to environmental factors-experiments with isolated epidermal strips of Polypodium vulgare - II. Leaf bulk water potential, air humidity, and temperature. Oecologia 39: 229-238 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lucas JR, Renzaglia KS (2002) Structure and function of hornwort stomata. Microsc. Microanal. 8: 1090CD Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mansfield TA, Willmer CM (1969) Stomatal responses to light and carbon dioxide in the Hart's-tongue fern, Phyllitis scolopendrium Newm. New Phytologist 68 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Martínez-Vilalta J, Garcia-Forner N (2016) Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ doi: 10.111/pce.12846 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Martins SCV, McAdam SAM, Deans RM, DaMatta FM, Brodribb TJ (2016) Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves. Plant, Cell and Environment 39: 694- 705 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2012) Stomatal innovation and the rise of seed plants. Ecol Lett 15: 1-8 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2013) Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytologist 198: 429-441 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2014) Separating active and passive influences on stomatal control of transpiration. Plant Physiology 164: 1578-1586 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapour pressure deficit. Plant Physiology 167: 833-843 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2016) Linking turgor with ABA biosynthesis: implications for stomatal responses to vapour pressure deficit across land plants. Plant Physiology 171: 2008-2016 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ, Banks JA, Hedrich R, Atallah NM, Cai C, Geringer MA, Lind C, Nichols DS, Stachowski K, Geiger D, Sussmilch FC (2016) Abscisic acid controlled sex before transpiration in vascular plants. Proceedings of the National Academy of Sciences 113: 12862-12867 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only TitleDownloaded Only Author from and www.plantphysiol.org Title on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. McAdam SAM, Brodribb TJ, Ross JJ, Jordan GJ (2011) Augmentation of abscisic acid (ABA) levels by drought does not induce short-term stomatal sensitivity to CO2 in two divergent conifer species. J. Exp. Bot. 62: 195-203 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Sussmilch FC, Brodribb TJ (2016) Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant, Cell and Environment 39: 485-491 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Sussmilch FC, Brodribb TJ, Ross JJ (2015) Molecular characterization of a mutation affecting abscisic acid biosynthesis and consequently stomatal responses to humidity in an agriculturally important species. AoB Plants 7: plv091 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Meinzer FC, Woodruff DR, Marias DE, Smith DD, McCulloh KA, Howard AR, Magedman AL (2016) Mapping 'hydroscapes' along the iso-to anisohydric continuum of stomatal regulation of plant water status. Ecology Letters 19: 1343-1352 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Merilo E, Jalakas P, Kollist H, Brosché M (2015) The role of ABA recycling and transporter proteins in rapid stomatal responses to reduced air humidity, elevated CO2, and exogenous ABA. Molecular Plant 8: 657-659 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonzalez-Guzman M, Rodriguez PL, Schroeder JI, Broschè M, Kollist H (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiol 162: 1652-1668 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mittelheuser CJ, Van Steveninck RFM (1969) Stomatal closure and inhibition of transpiration induced by (RS)-abscisic acid. Nature 221: 281-282 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mumm P, Wolf T, Fromm J, Roelfsema MRG, Marten I (2011) Cell type-specific regulation of ion channels within the maize stomatal complex. Plant Cell Physiol 52: 1365-1375 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14: 3089-3099 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452: 483-486 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title O'Grady AP, Eamus D, Hutley LB (1999) Transpiration increases during the dry season: patterns of tree water use in eucalypt open-forests of northern Australia. Tree Physiology 19: 591-597 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149: 825-834 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pabón-Mora N, Wong GK-S, Ambrose BA (2014) Evolution of fruit development genes in flowering plants. Frontiers in Plant Science 5: 300 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Palmer JD, Soltis DE, ChaseDownloaded MW (2004) from The www.plantphysiol.org plant tree of life: anon overviewMay 18, 2017 and - Publishedsome points by www.plantphysiol.org of view. American Journal of Botany 91: Copyright © 2017 American Society of Plant Biologists. All rights reserved. 1437-1445 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Paolillo DJ, Bazzaz FA (1968) Photosynthesis in sporophytes of Polytrichum and Funaria. The Bryologist 71: 335-343 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-fF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Paton JA, Pearce JV (1957) The occurrence, structure and functions of the stomata in British bryophytes. T. Brit. Bryol. Soc. 3: 228- 259 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731-734 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Peñuelas J, Munné-Bosch S (2010) Potentially immortal? New Phytologist 187: 564-567 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pierce M, Raschke K (1980) Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148: 174-182 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pierce M, Raschke K (1981) Synthesis and metabolism of abscisic acid in detached leaves of Phaseolus vulgaris L. after loss and recovery of turgor. Planta 153: 156-165 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiology 153: 1919-1931 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pressel S, Goral T, Duckett JG (2014) Stomatal differentiation and abnormal stomata in hornworts. Journal of Bryology 36: 87-103 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Raschke K, Shabahang M, Wolf R (2003) The slow and the quick anion conductance in whole guard cells: their voltage-dependent alternation, and the modulation of their activities by abscisic acid and CO2. Planta 217: 639-650 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Renzaglia KS, Villarreal JC, Piatkowski BT, Lucas JR, Merced A (this issue) Hornwort stomata: architecture conserved in plants without leaves over hundreds of millions of years. Plant Physiol Roelfsema MRG, Hanstein S, Felle HH, Hedrich R (2002) CO2 provides an intermediate link in the red light response of guard cells. Plant J. 32: 65-75 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Rolland V, Bergstrom DM, Lenné T, Bryant G, Chen H, Wolfe J, Holbrook NM, Stanton DE, Ball MC (2015) Easy come, easy go: capillary forces enable rapid refilling of embolized primary xylem vessels. Plant Physiol 168: 1636-1647 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21: 1030-1035 Pubmed: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Santelia D, Lawson T (2016) Rethinking Guard Cell Metabolism. Plant Physiology 172: 1371-1392 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52: 627-658 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Schulze E-D, Lange OL, Evenari M, Kappen L, Buschbom U (1974) The role of air humidity and leaf temperature in controlling stomatal resistance of Prunus armeniaca L. under desert conditions. Oecologia 17: 159-170 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Shimazaki KI, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annual Review of Plant Biology 58: 219-247 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Sibbernsen E, Mott KA (2010) Stomatal responses to flooding of the intercellular air spaces suggest a vapor-phase signal between the mesophyll and the guard cells. Plant Physiol. 153: 1435-1442 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol doi: 10.1111/nph.14450 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Suetsugu N, Takami T, Ebisu Y, Watanabe H, Iiboshi C, Doi M, Shimazaki K-i (2014) Guard cell chloroplasts are essential for blue light-dependent stomatal opening in Arabidopsis. PLOS ONE 9: e108374 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16: 341-349 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49: 419-432 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Thomas RJ, Stanton DS, Longendorfer DH, Farr ME (1978) Physiological evaluation of the nutritional autonomy of a hornwort sporophyte. Botanical Gazette 139: 306-311 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ting IP (1987) Stomata in plants with Crassulacean Acid Metabolism. In E Zeiger, GD Farquhar, IR Cowan, eds, Stomatal Function. Stanford University Press, California, pp 353-366 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tominaga M, Kinoshita T, Shimazaki K-i (2001) Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol. 42: 795-802 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tougane K, Komatsu K, Bhyan SB, Sakata Y, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1-like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiol. 152: 1529-1543 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology. 40: 19-38 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Vatén A, Bergmann D (2012) Mechanisms of stomatal development: an evolutionary view. EvoDevo 3: 1-9 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Vesty EF, Saidi Y, Moody LA, Holloway D, Whitbread A, Needs S, Choudhary A, Burns B, McLeod D, Bradshaw SJ, Bae H, King BC, Bassel GW, Simonsen HT, Coates JC (2016) The decision to germinate is regulated by divergent molecular networks in spores and seeds. New Phytol 211: 952-966 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. eLife 3: e01739 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, Der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, dePamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian Z, Yan Z, Wu X, Sun X, Wong GK-S, Leebens-Mack J (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci U S A 111: E4859-E4868 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wiggans RG (1921) Variations in the osmotic concentration of the guard cells during the opening and closing of stomata. Am. J. Bot. 8: 30-40 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Willmer CM, Pallas JE (1974) Stomatal movements and ion fluxes within epidermis of Commelina communis L. Nature 252: 126-127 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wolf A, Anderegg WRL, Pacala SW (2016) Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proc Natl Acad Sci U S A 113: E7222-E7230 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E, Theobald J, Knight MR, Davies WJ, Leyser HMO, Hetherington AM (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Current Biology 16: 882-887 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. Journal of Biological Chemistry 281: 5310-5318 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Yue J, Hu X, Huang J (2014) Origin of plant auxin biosynthesis. Trends in Plant Science 19: 764-770 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Zeiger E, Field C (1982) Photocontrol of the functional coupling between photosynthesis and stomatal conductance in the intact leaf: blue light and PAR-dependent photosystems in guard cells. Plant Physiol. 70: 370-375 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ziegler H (1987) The evolution of stomata. In E Zeiger, GD Farquhar, I Cowan, eds, Stomatal Function. Stanford University Press, Stanford, California, pp 29-57 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Aasamaa K, Sõber A (2011) Responses of stomatal conductance to simultaneous changes in two environmental factors. Tree Physiology 31: 855-864 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Apostolakos P, Livanos TL, Nikolakopoulou TL, Galatis B (2010) Callose implication in stomatal opening and closure in the fern Asplenium nidus. New Phytologist 186: 623-635 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Baer A, Wheeler JK, Pittermann J (2016) Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought. New Phytologist 210: 122-132 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bartlett MK, Klein T, Jansen S, Choat B, Sack L (2016) The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci U S A 113: 13098-13103 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bauerle WL, Whitlow TH, Setter TL, Vermeylen FM (2004) Abscisic acid synthesis in Acer rubrum L. leaves—a vapor-pressure- deficit-mediated response. Journal of the American Society for Horticultural Science 129: 182-187 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Boyce CK (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34: 179-194 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasjärvi J, Ghassemain M, Stephan AB, Hu H, Schroeder JI (2012) Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action. Proc. Natl. Acad. Sci. U.S.A. 109: 10593-10598 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang PG, Poretsky E, Belknap TF, Waadt R, Alemán F, Schroeder JI (2015) Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4: e03599 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Cochard H (2009) Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers. Plant Physiology 149: 575-584 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132: 2166-2173 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162: 663-670 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199: 559-570 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM (2011) Passive Origins of Stomatal Control in Vascular Plants. Science 331: 582-585 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM (2013) Abscisic Acid Mediates a Divergence in the Drought Response of Two Conifers. Plant Physiology 162: 1370-1377 Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM (2013) Unique responsiveness of angiosperm stomata to elevated CO2 explained by calcium signalling. PLoS ONE 8: e82057 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM, Jordan GJ, Feild TS (2009) Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytologist 183: 839-847 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences of the United States of America 111: 14489-14493 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Brodribb TJ, Skelton RP, McAdam SA, Bienaimé D, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209: 1403-1409 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Bunce JA (2006) How do leaf hydraulics limit stomatal conductance at high water vapour pressure deficits? Plant Cell and Environment 29: 1644-1650 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Butterfass T (1979) Patterns of chloroplast reproduction: a developmental approach to protoplasmic plant anatomy. Springer- Verlag, Vienna, Austria Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cai S, Chen G, Wang Y, Huang Y, Marchant B, Wang Y, Yang Q, Dai F, Hills A, Franks PJ (2017) Evolutionary Conservation of ABA Signaling for Stomatal Closure in Ferns. Plant Physiology: pp. 01848.02016 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Caine RS, Chater CC, Kamisugi Y, Cuming AC, Beerling DJ, Gray JE, Fleming AJ (2016) An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens. Development 143: 3306-3314 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Charrier G, Torres-Ruiz JM, Badel E, Burlett R, Choat B, Cochard H, Delmas CE, Domec J-C, Jansen S, King A (2016) Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiology: pp. 01079.02016 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Curr Biol 21: 1025-1029 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution. Current biology 21: 1025-1029 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chater CC, Caine RS, Tomek M, Wallace S, Kamisugi Y, Cuming AC, Lang D, MacAlister CA, Casson S, Bergmann DC, Decker EL, Frank W, Gray JE, Fleming A, Reski R, Beerling DJ (2016) Origin and function of stomata in the moss Physcomitrella patens. Nature Plants 2: 16179 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Chen Z-H, Chen G, Dai F, Wang Y, Hills A, Ruan Y-L, Zhang G, Franks PJ, Nevo E, Blatt MR (2016) Molecular evolution of grass stomata. Trends in Plant Science doi: 10.1016/j.tplants.2016.09.005 Pubmed: Author and Title CrossRef: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Google Scholar: Author Only Title Only Author and Title Chen Z-H, Hills A, Baetz U, Amtmann A, Lew V, Blatt MR (2012) Systems dynamic modelling of the stomatal guard cell predicts emergent behaviours in transport, signalling and volume control. Plant Physiol.: doi: 10.1104/pp.1112.197350 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Christmann A, Hoffmann T, Teplova I, Grill E, Müller A (2005) Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiology 137: 209-219 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cochard H, Delzon S (2013) Hydraulic failure and repair are not routine in trees. Annals of Forest Science 70: 659-661 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cowan I (2002) Fit, fitter, fittest; where does optimisation fit in? Silva Fennica 36: 745-754 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Cowan IR (1977) Stomatal behaviour and environment. Advances in Botanical Research 4: 117-228 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Darwin F (1898) Observartions on stomata. Proc R Soc Lond 63: 413-417 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Darwin F (1898) Observations on stomata. Proceedings of the Royal Society of London. Series B: Biological Sciences 63: 413-417 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Davies WJ, Wilson JA, Sharp RE, Osonubi O (1981) Control of stomatal behaviour in water-stressed plants. In PG Jarvis, TA Mansfield, eds, Stomatal Physiology. Cambridge University Press, Cambridge, pp 163-185 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Deans RM, Brodribb TJ, McAdam SAM (This issue) An integrated hydraulic-hormonal model of conifer stomata predicts water stress dynamics. Plant Physiol Dodd IC (2003) Hormonal interactions and stomatal responses. Journal of Plant Growth Regulation 22: 32-46 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Kitagawa Y, Shimazaki K-i (2015) Stomatal blue light response is present in early vascular plants. Plant Physiol 169: 1205- 1213 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Shimazaki KI (2008) The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiology 147: 922-930 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Doi M, Wada M, Shimazaki KI (2006) The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant and Cell Physiology 47: 748-755 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Duckett JG, Pressel S, P'ng KMY, Renzaglia KS (2009) Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum. New Phytologist 183: 1053-1063 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Edwards D, Axe L (1992) Stomata and mechanics of stomatal functioning in some early land plants. Cour. Forschungsinst. Senckenberg 147: 59-73 Pubmed: Author and Title CrossRef: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Google Scholar: Author Only Title Only Author and Title Edwards D, Kerp H, Hass H (1998) Stomata in early land plants: an anatomical and ecophysiological approach. J. Exp. Bot. 49: 255- 278 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Field KJ, Duckett JG, Cameron DD, Pressel S (2015) Stomatal density and aperture in non-vascular land plants are non-responsive to above-ambient atmospheric CO2 concentrations. Ann Bot 115: 915-922 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. Proceedings of the National Academy of Sciences of the United States of America 106: 10343-10347 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Britton-Harper ZJ (2016) No evidence of general CO2 insensitivity in ferns: one stomatal control mechanism for all land plants? New Phytologist: doi:10.1111/nph.14020 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Farquhar GD (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143: 78-87 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philosophical Transactions of the Royal Society B-Biological Sciences 367: 537-546 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujii H, Verslues PE, Zhu J-K (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19: 485-494 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujii H, Verslues PE, Zhu J-K (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc. Natl. Acad. Sci. U.S.A. 108: 1717-1722 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Fujita T, Noguchi K, Terashima I (2013) Apoplastic mesophyll signals induce rapid stomatal responses to CO2 in Commelina communis. New Phytol. 199: 395-406 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KAS, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc. Natl. Acad. Sci. U.S.A. 107: 8023-8028 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Geiger D, Scherzer S, Mumm P, Stange A, Marten I, Bauer H, Ache P, Matschi S, Liese A, Al-Rasheid KAS, Romeis T, Hedrich R (2009) Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci U S A 106: 21425-21430 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ghosh TK, Kaneko M, Akter K, Murai S, Komatsu K, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2016) Abscisic acid-induced gene expression in the liverwort Marchantia polymorpha is mediated by evolutionarily conserved promoter elements. Physiologia Plantarum 156: 407-420 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Gonez P, Gerrienne P (2010) A new definition and a lectotypification of the genus Cooksonia Lang 1937. International Journal of Plant Sciences 171: 199-215 Pubmed: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Grabov A, Blatt MR (1998) Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proceedings of the National Academy of Sciences 95: 4778-4783 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Haberlandt G (1886) Beiträge zur Anatomie und Physiologie der Laubmoose. Jahrbücher für wissenschafliche Botanik 17: 457-477 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Haig D (2013) Filial mistletoes: the functional morphology of moss sporophytes. Annals of Botany 111: 337-345 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hanada K, Hase T, Toyoda T, Shinozaki K, Okamoto M (2011) Origin and evolution of genes related to ABA metabolism and its signaling pathways. Journal of Plant Research 124: 455-465 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hauser F, Waadt R, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Current Biology 21: R346- R355 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Heath OVS (1938) An experimental investigation of the mechanism of stomatal movement, with some preliminary observations upon the response of the guard cells to "shock". New Phytologist 37: 385-395 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hedrich R (2012) Ion channels in plants. Physiological Reviews 92: 1777-1811 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424: 901-908 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hietz P (2010) Fern adaptations to xeric environments. In K Mehltreter, LR Walker, JM Sharpe, eds, Fern Ecology. Cambridge University Press, pp 140-176 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hills A, Chen Z-H, Amtmann A, Blatt MR, Lew VL (2012) OnGuard, a computational platform for quantitative kinetic modeling of guard cell physiology. Plant Physiology 159: 1026-1042 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hochberg U, Bonel AG, David-Schwartz R, Degu A, Fait A, Cochard H, Peterlunger E, Herrera JC (2017) Grapevine acclimation to water deficit: the adjustment of stomatal and hydraulic conductance differs from petiole embolism vulnerability. Planta doi: 10.1007/s00425-017-2662-3 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Hoffman A, Shock C, Feibert E (1999) Taxane and ABA production in yew under different soil water regimes. Hortscience 34: 882- 885 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Horrer D, Flütsch S, Pazmino D, Matthews Jack SA, Thalmann M, Nigro A, Leonhardt N, Lawson T, Santelia D (2016) Blue light induces a distinct starch degradation pathway in guard cells for stomatal opening. Current Biology 26: 362-370 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Iwanoff L (1928) Zur Methodik der Transpirationsbestimmung am Standort. Berichte der Deutschen Botanischen Gesellschaft 46: 306-310 Pubmed: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kanno Y, Hanada A, Chiba Y, Ichikawa T, Nakazawa M, Matsui M, Koshiba T, Kamiya Y, Seo M (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America 109: 9653-9658 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota A, Wada M (2003) Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421: 287-290 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389: 33-39 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu. Rev. Plant Biol. 61: 561-591 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kong L, Abrams SR, Owen SJ, Van Niejenhuis A, Von Aderkas P (2009) Dynamic changes in concentrations of auxin, cytokinin, ABA and selected metabolites in multiple genotypes of Douglas-fir (Pseudotsuga menziesii) during a growing season. Tree Physiol. 29: 183-190 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kraus M, Ziegler H (1993) Quantitative analysis of abscisic acid in needles of Abies alba Mill. by electron capture gas chromatography. Trees 7: 175-181 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kuromori T, Sugimoto E, Shinozaki K (2011) Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant Journal 67: 885-894 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Kuromori T, Sugimoto E, Shinozaki K (2014) Intertissue signal transfer of abscisic acid from vascular cells to guard cells. Plant Physiology 164: 1587-1592 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lange OL, Lösch R, Schultze E-D, Kappen L (1971) Responses of stomata to changes in humidity. Planta 100: 76-86 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Larter M, Brodribb TJ, Pfautsch S, Burlett R, Cochard H, Delzon S (2015) Extreme aridity pushes trees to their physical limits. Plant Physiology 168: 804-807 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lawson T (2009) Guard cell photosynthesis and stomatal function. New Phytologist 181: 13-34 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lawson T, Simkin AJ, Kelly G, Granot D (2014) Mesophyll photosynthesis and guard cell metabolism impacts on stomatal behaviour. New Phytologist 203: 1064-1081 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Li J, Assmann SM (1996) An abscisic acid-activated and calcium-independent protein kinase from guard cells of fava bean. Plant Cell 8: 2359-2368 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Lind C, Dreyer I, López-SanjurjoDownloaded Enrique from J, www.plantphysiol.org von Meyer K, Ishizaki on May K, Kohchi18, 2017 T, - PublishedLang D, Zhaoby www.plantphysiol.org Y, Kreuzer I, Al-Rasheid Khaled AS, Copyright © 2017 American Society of Plant Biologists. All rights reserved. Ronne H, Reski R, Zhu J-K, Geiger D, Hedrich R (2015) Stomatal guard cells co-opted an ancient ABA-dependent desiccation survival system to regulate stomatal closure. Curr Biol 25: 928-935 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lösch R (1977) Responses of stomata to environmental factors-experiments with isolated epidermal strips of Polypodium vulgare - I. Temperature and Humidity. Oecologia 29: 85-97 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lösch R (1979) Responses of stomata to environmental factors-experiments with isolated epidermal strips of Polypodium vulgare - II. Leaf bulk water potential, air humidity, and temperature. Oecologia 39: 229-238 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Lucas JR, Renzaglia KS (2002) Structure and function of hornwort stomata. Microsc. Microanal. 8: 1090CD Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mansfield TA, Willmer CM (1969) Stomatal responses to light and carbon dioxide in the Hart's-tongue fern, Phyllitis scolopendrium Newm. New Phytologist 68 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Martínez-Vilalta J, Garcia-Forner N (2016) Water potential regulation, stomatal behaviour and hydraulic transport under drought: deconstructing the iso/anisohydric concept. Plant Cell Environ doi: 10.111/pce.12846 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Martins SCV, McAdam SAM, Deans RM, DaMatta FM, Brodribb TJ (2016) Stomatal dynamics are limited by leaf hydraulics in ferns and conifers: results from simultaneous measurements of liquid and vapour fluxes in leaves. Plant, Cell and Environment 39: 694- 705 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2012) Fern and Lycophyte Guard Cells Do Not Respond to Endogenous Abscisic Acid. Plant Cell 24: 1510-1521 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2012) Stomatal innovation and the rise of seed plants. Ecol Lett 15: 1-8 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2013) Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytologist 198: 429-441 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2014) Separating active and passive influences on stomatal control of transpiration. Plant Physiology 164: 1578-1586 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapour pressure deficit. Plant Physiology 167: 833-843 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ (2016) Linking turgor with ABA biosynthesis: implications for stomatal responses to vapour pressure deficit across land plants. Plant Physiology 171: 2008-2016 Pubmed: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ, Banks JA, Hedrich R, Atallah NM, Cai C, Geringer MA, Lind C, Nichols DS, Stachowski K, Geiger D, Sussmilch FC (2016) Abscisic acid controlled sex before transpiration in vascular plants. Proceedings of the National Academy of Sciences 113: 12862-12867 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Brodribb TJ, Ross JJ, Jordan GJ (2011) Augmentation of abscisic acid (ABA) levels by drought does not induce short-term stomatal sensitivity to CO2 in two divergent conifer species. J. Exp. Bot. 62: 195-203 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Sussmilch FC, Brodribb TJ (2016) Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms. Plant, Cell and Environment 39: 485-491 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title McAdam SAM, Sussmilch FC, Brodribb TJ, Ross JJ (2015) Molecular characterization of a mutation affecting abscisic acid biosynthesis and consequently stomatal responses to humidity in an agriculturally important species. AoB Plants 7: plv091 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Meinzer FC, Woodruff DR, Marias DE, Smith DD, McCulloh KA, Howard AR, Magedman AL (2016) Mapping 'hydroscapes' along the iso-to anisohydric continuum of stomatal regulation of plant water status. Ecology Letters 19: 1343-1352 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Merilo E, Jalakas P, Kollist H, Brosché M (2015) The role of ABA recycling and transporter proteins in rapid stomatal responses to reduced air humidity, elevated CO2, and exogenous ABA. Molecular Plant 8: 657-659 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Merilo E, Laanemets K, Hu H, Xue S, Jakobson L, Tulva I, Gonzalez-Guzman M, Rodriguez PL, Schroeder JI, Broschè M, Kollist H (2013) PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation. Plant Physiol 162: 1652-1668 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mittelheuser CJ, Van Steveninck RFM (1969) Stomatal closure and inhibition of transpiration induced by (RS)-abscisic acid. Nature 221: 281-282 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mumm P, Wolf T, Fromm J, Roelfsema MRG, Marten I (2011) Cell type-specific regulation of ion channels within the maize stomatal complex. Plant Cell Physiol 52: 1365-1375 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14: 3089-3099 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K (2008) CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452: 483-486 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title O'Grady AP, Eamus D, Hutley LB (1999) Transpiration increases during the dry season: patterns of tree water use in eucalypt open-forests of northern Australia. Tree Physiology 19: 591-597 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8'-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149: 825-834 Pubmed: Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pabón-Mora N, Wong GK-S, Ambrose BA (2014) Evolution of fruit development genes in flowering plants. Frontiers in Plant Science 5: 300 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Palmer JD, Soltis DE, Chase MW (2004) The plant tree of life: an overview and some points of view. American Journal of Botany 91: 1437-1445 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Paolillo DJ, Bazzaz FA (1968) Photosynthesis in sporophytes of Polytrichum and Funaria. The Bryologist 71: 335-343 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-fF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Paton JA, Pearce JV (1957) The occurrence, structure and functions of the stomata in British bryophytes. T. Brit. Bryol. Soc. 3: 228- 259 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pei Z-M, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731-734 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Peñuelas J, Munné-Bosch S (2010) Potentially immortal? New Phytologist 187: 564-567 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pierce M, Raschke K (1980) Correlation between loss of turgor and accumulation of abscisic acid in detached leaves. Planta 148: 174-182 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pierce M, Raschke K (1981) Synthesis and metabolism of abscisic acid in detached leaves of Phaseolus vulgaris L. after loss and recovery of turgor. Planta 153: 156-165 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) The Relationships between Xylem Safety and Hydraulic Efficiency in the Cupressaceae: The Evolution of Pit Membrane Form and Function. Plant Physiology 153: 1919-1931 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pornsiriwong W, Estavillo GM, Chan KX, Tee EE, Ganguly D, Crisp PA, Phua SY, Zhao C, Qiu J, Park J (2017) A chloroplast retrograde signal, 3'-phosphoadenosine 5'-phosphate, acts as a secondary messenger in abscisic acid signaling in stomatal closure and germination. eLife 6: e23361 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Pressel S, Goral T, Duckett JG (2014) Stomatal differentiation and abnormal stomata in hornworts. Journal of Bryology 36: 87-103 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Raschke K, Shabahang M, Wolf R (2003) The slow and the quick anion conductance in whole guard cells: their voltage-dependent alternation, and the modulation of their activities by abscisic acid and CO2. Planta 217: 639-650 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title

Renzaglia KS, Villarreal JC,Downloaded Piatkowski from BT, www.plantphysiol.org Lucas JR, Merced onA (this May 18,issue) 2017 Hornwort - Published stomata: by www.plantphysiol.org architecture conserved in plants Copyright © 2017 American Society of Plant Biologists. All rights reserved. without leaves over hundreds of millions of years. Plant Physiol Roelfsema MRG, Hanstein S, Felle HH, Hedrich R (2002) CO2 provides an intermediate link in the red light response of guard cells. Plant J. 32: 65-75 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Rolland V, Bergstrom DM, Lenné T, Bryant G, Chen H, Wolfe J, Holbrook NM, Stanton DE, Ball MC (2015) Easy come, easy go: capillary forces enable rapid refilling of embolized primary xylem vessels. Plant Physiol 168: 1636-1647 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, A.M. H (2011) Land plants acquired active stomatal control early in their evolutionary history. Current Biology 21: 1-6 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM (2011) Land plants acquired active stomatal control early in their evolutionary history. Curr Biol 21: 1030-1035 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Santelia D, Lawson T (2016) Rethinking Guard Cell Metabolism. Plant Physiology 172: 1371-1392 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Annu Rev Plant Physiol Plant Mol Biol 52: 627-658 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Schulze E-D, Lange OL, Evenari M, Kappen L, Buschbom U (1974) The role of air humidity and leaf temperature in controlling stomatal resistance of Prunus armeniaca L. under desert conditions. Oecologia 17: 159-170 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Shimazaki KI, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Annual Review of Plant Biology 58: 219-247 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Sibbernsen E, Mott KA (2010) Stomatal responses to flooding of the intercellular air spaces suggest a vapor-phase signal between the mesophyll and the guard cells. Plant Physiol. 153: 1435-1442 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol doi: 10.1111/nph.14450 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Suetsugu N, Takami T, Ebisu Y, Watanabe H, Iiboshi C, Doi M, Shimazaki K-i (2014) Guard cell chloroplasts are essential for blue light-dependent stomatal opening in Arabidopsis. PLOS ONE 9: e108374 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tardieu F, Davies WJ (1993) Integration of hydraulic and chemical signalling in the control of stomatal conductance and water status of droughted plants. Plant Cell Environ 16: 341-349 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49: 419-432 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Thomas RJ, Stanton DS, Longendorfer DH, Farr ME (1978) Physiological evaluation of the nutritional autonomy of a hornwort sporophyte. Botanical GazetteDownloaded 139: 306-311 from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. sporophyte. Botanical Gazette 139: 306-311 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ting IP (1987) Stomata in plants with Crassulacean Acid Metabolism. In E Zeiger, GD Farquhar, IR Cowan, eds, Stomatal Function. Stanford University Press, California, pp 353-366 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tominaga M, Kinoshita T, Shimazaki K-i (2001) Guard-cell chloroplasts provide ATP required for H+ pumping in the plasma membrane and stomatal opening. Plant Cell Physiol. 42: 795-802 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tougane K, Komatsu K, Bhyan SB, Sakata Y, Ishizaki K, Yamato KT, Kohchi T, Takezawa D (2010) Evolutionarily conserved regulatory mechanisms of abscisic acid signaling in land plants: characterization of ABSCISIC ACID INSENSITIVE1-like type 2C protein phosphatase in the liverwort Marchantia polymorpha. Plant Physiol. 152: 1529-1543 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology. 40: 19-38 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Vatén A, Bergmann D (2012) Mechanisms of stomatal development: an evolutionary view. EvoDevo 3: 1-9 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Vesty EF, Saidi Y, Moody LA, Holloway D, Whitbread A, Needs S, Choudhary A, Burns B, McLeod D, Bradshaw SJ, Bae H, King BC, Bassel GW, Simonsen HT, Coates JC (2016) The decision to germinate is regulated by divergent molecular networks in spores and seeds. New Phytol 211: 952-966 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Waadt R, Hitomi K, Nishimura N, Hitomi C, Adams SR, Getzoff ED, Schroeder JI (2014) FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis. eLife 3: e01739 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA, Ruhfel BR, Wafula E, Der JP, Graham SW, Mathews S, Melkonian M, Soltis DE, Soltis PS, Miles NW, Rothfels CJ, Pokorny L, Shaw AJ, DeGironimo L, Stevenson DW, Surek B, Villarreal JC, Roure B, Philippe H, dePamphilis CW, Chen T, Deyholos MK, Baucom RS, Kutchan TM, Augustin MM, Wang J, Zhang Y, Tian Z, Yan Z, Wu X, Sun X, Wong GK-S, Leebens-Mack J (2014) Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc Natl Acad Sci U S A 111: E4859-E4868 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wiggans RG (1921) Variations in the osmotic concentration of the guard cells during the opening and closing of stomata. Am. J. Bot. 8: 30-40 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Willmer CM, Pallas JE (1974) Stomatal movements and ion fluxes within epidermis of Commelina communis L. Nature 252: 126-127 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Wolf A, Anderegg WRL, Pacala SW (2016) Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proc Natl Acad Sci U S A 113: E7222-E7230 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Xie X, Wang Y, Williamson L, Holroyd GH, Tagliavia C, Murchie E, Theobald J, Knight MR, Davies WJ, Leyser HMO, Hetherington AM (2006) The identification of genes involved in the stomatal response to reduced atmospheric relative humidity. Current Biology 16: 882-887 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Downloaded from www.plantphysiol.org on May 18, 2017 - Published by www.plantphysiol.org Copyright © 2017 American Society of Plant Biologists. All rights reserved. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. Journal of Biological Chemistry 281: 5310-5318 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Yue J, Hu X, Huang J (2014) Origin of plant auxin biosynthesis. Trends in Plant Science 19: 764-770 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Zeiger E, Field C (1982) Photocontrol of the functional coupling between photosynthesis and stomatal conductance in the intact leaf: blue light and PAR-dependent photosystems in guard cells. Plant Physiol. 70: 370-375 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title Ziegler H (1987) The evolution of stomata. In E Zeiger, GD Farquhar, I Cowan, eds, Stomatal Function. Stanford University Press, Stanford, California, pp 29-57 Pubmed: Author and Title CrossRef: Author and Title Google Scholar: Author Only Title Only Author and Title