What Are the Evolutionary Origins of Stomatal Responses to Abscisic Acid in Land Plants?FA

Journal of Integrative JIPB Plant Biology

What are the evolutionary origins of stomatal responses to abscisic acid in land plants?FA

Frances C. Sussmilch, Timothy J. Brodribb and Scott A. M. McAdam *

School of Biological Sciences, University of Tasmania, Hobart, Tasmania, Australia doi: 10.1111/jipb.12523

structures first appeared, prior to the divergence of bryophyte and vascular plant lineages. In contrast, a gradualistic model for stomatal control proposes that the most basal vascular plant stomata responded passively to changes in leaf water status. This model suggests that active ABA-driven mechanisms for stomatal responses to water Scott A. M. McAdam status instead evolved after the divergence of seed plants, Invited Expert Review *Correspondence: culminating in the complex, ABA-mediated responses [email protected] observed in modern angiosperms. Here we review the findings that form the basis for these two models, including recent work that provides critical molecular insights into Abstract The evolution of active stomatal closure in resolving this intriguing debate, and find strong evidence to response to leaf water deficit, mediated by the hormone support a gradualistic model for stomatal evolution. abscisic acid (ABA), has been the subject of recent debate. Edited by: Jianhua Zhang, The Chinese University of Hong Kong, Two different models for the timing of the evolution of this China response recur in the literature. A single-step model for Received Dec. 17, 2016; Accepted Jan. 15, 2017; Online on Jan. 17, stomatal control suggests that stomata evolved active, ABA- 2017 mediated control of stomatal aperture, when these FA: Free Access, paid by JIPB

THE STOMATAL RESPONSE TO ABA observed in the stomatal response to water deficit Stomata are turgor-operated pores on the leaves of (Franks and Farquhar 1999; Klein 2014), with this process vascular plants that engage in two opposing functions: being controlled by a combination of passive changes in opening to allow entry of carbon dioxide for photosyn- guard cell turgor due to changes in hydration of thesis, and closing to minimize water loss into the epidermal and guard cells (Mott and Franks 2001), and atmosphere by transpiration. Changes in guard cell active regulation of ion transport across guard cell turgor have been well studied in angiosperms and are membranes (Schroeder and Keller 1992). In this review controlled by both active (metabolic) and passive we refer to “passive” closure of stomata in response to (hydraulic) processes (Figure 1). Active stomatal opening leaf water deficit as the scenario where guard cells are in the light, triggered by the proton pumping adenosine tightly connected to the plant hydraulic system. Under þ triphosphatase (H -ATPase), is a ubiquitous stomatal these circumstances, guard cell turgor declines in parallel High-Impact Article response that likely evolved in the earliest stomata, prior with declining water potential in the leaf, causing to divergence of vascular land plants (Doi et al. 2015). stomatal closure (Figure 1). “Active” closure of stomata This response is a means of increasing the porosity of the in response to increased leaf water deficit primarily fi leaf epidermis, which is otherwise impermeable to CO2, involves ion traf cking through the guard cell membrane an essential requirement for atmospheric photosynthe- in response to increases in the plant hormone abscisic sis. In contrast, significant diversity across land plants is acid (ABA; Figure 1).

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Figure 1. Model for the two pathways to stomatal closure in response to leaf water deficit in the light: passive and active An increase in vapor pressure deficit (VPD) or a period of drought causes a decrease in leaf water potential (cl) and triggers stomatal closure via one of two pathways. For passive hydraulic stomatal closure, stomata are controlled directly by leaf hydration and a decrease in water potential results in a decrease in guard cell turgor pressure (Pg). For active metabolic stomatal closure, the decrease in water potential triggers an increase in abscisic acid (ABA) levels via increased ABA biosynthesis. The ABA signaling pathway activates ion channels in the guard cells, and the resulting efflux of ions decreases the guard cell osmotic pressure (pg) and turgor. Photos show a stoma of the angiosperm Senecio minimus when open (left) and closed (right); scale bars ¼ 5 mm.

ABA is synthesized in response to water stress, and theliterature(Figure 2). The first, which we refer to triggers a loss of guard cell turgor and stomatal here as the single-step model for stomatal control, closure by activating anion channels in the guard cell suggests that stomata evolved active, ABA-mediated membrane (Mittelheuser and Van Steveninck 1969; control of stomatal aperture in response to changes Kriedemann et al. 1972; MacRobbie 1981). Levels of in leaf water status very early during the evolution of ABA are controlled through the balanced regulation of stomatophytes, prior to the divergence of bryophyte key genes in the ABA biosynthesis and catabolism and vascular plant lineages at least 410 million years pathways (Qin and Zeevaart 1999; Kushiro et al. 2004; ago (Figure 2A)(Chater et al. 2011; Ruszala et al. Saito et al. 2004). ABA can be found synthesized in all 2011). In contrast, the gradualistic model for stomatal plants, from algae through to angiosperms, where it control proposes that the first vascular land plant acts as a signaling molecule to control a variety of stomata responded passively to changes in leaf different plant processes, including growth, sex water status (Figure 2B)(Brodribb and McAdam determination, seed/spore dormancy and stress toler- 2011). This model argues that active ABA-driven ance (Hartung 2010; Takezawa et al. 2011; Kobayashi mechanisms for stomatal responses to water status et al. 2016; McAdam et al. 2016a; Moody et al. 2016). evolved after the divergence of seed plants (Figure Accordingly, ABA-signaling genes and associated 2B), which were likely the first homiohydric plants to transcriptional networks are conserved between live in seasonally dry environments (Stewart and angiosperms and extant representatives of the Rothwell 1993). earliest land plant clades, even those which lack Here we review the findings that form the basis for stomata (Richardt et al. 2010; Hauser et al. 2011; Lind these two models, including recent work that provides et al. 2015). Stomatal closure by ABA provides an axis critical molecular insights into resolving this intriguing for ecological variation and adaptation within seed debate. We begin with the current understanding of plants (Tardieu and Simonneau 1998), as well as a the stomatal response to ABA in angiosperms, where means of ensuring minimal stomatal apertures during we have a detailed understanding of the molecular drought and thus persistent survival of plants in mechanisms underlying these responses, based largely seasonally dry environments (Brodribb et al. 2014). on studies in Arabidopsis thaliana. We then work While a simple and ancient evolutionary origin is backward through the plant lineages to the bryo- generally recognized for active stomatal opening in phytes, at the base of the land plant phylogeny, the light in vascular plants, the evolution of active comparing stomatal physiology and the extent to stomatal closure in response to leaf water deficit via which the genes governing stomatal responses to ABA ABA has been the subject of recent debate. are functionally and phylogenetically conserved, to Two different models for the timing of the examine how stomatal responses to ABA have evolution of the stomatal response to ABA recur in evolved through time. www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 242 Sussmilch et al.

lacking in angiosperms when leaf water status changes, due to mechanical interactions between guard cells and epidermal cells (Buckley et al. 2003; Buckley 2005; Franks and Farquhar 2007). Second, there is strong hysteresis during reversible transitions in VPD, whereby the rate of stomatal opening on returning to low VPD is slower than the rate of closure at high VPD, which cannot be accounted for by plant hydraulics (Schulze et al. 1974; McAdam and Brodribb 2015). Finally, there is significant evidence of dysfunctional responses to Figure 2. Models for the evolution of abscisic acid humidity in ABA biosynthetic and signaling mutants (ABA)-mediated control of stomatal aperture (Xie et al. 2006; Bauer et al. 2013; Merilo et al. 2015). fi (A) The single-step model suggests that the rst A number of studies have confirmed that the stomata evolved with the ability to respond to all responses of angiosperm stomata to an increase in environmental conditions, including mechanisms for complex ABA-mediated regulation of stomatal aper- VPD occur through a rapid increase in ABA levels ture. (B) The gradualistic model proposes that stomatal (Bauerle et al. 2004; Waadt et al. 2014; McAdam and function has evolved through time from ancestral Brodribb 2016). This change in ABA level also accounts passively controlled valves in the earliest vascular for the strong hysteresis observed in the recovery of plants, which acquired ABA-mediated stomatal re- stomatal opening, particularly in herbaceous angio- sponses in the earliest seed plants by co-opting an sperm species, as ABA levels decline slowly on returning ancient ABA-signaling pathway to control guard cell turgor. Major evolutionary transitions required for to low VPD, preventing stomatal reopening (McAdam these two models are indicated on the current, most and Brodribb 2015). In addition to the VPD response, parsimonious phylogeny for land plants that recognizes most angiosperms respond to long-term drought stress current uncertainty in the relationships between with sustained high levels of ABA, which maintain bryophytes (B) and vascular plants (VP), particularly stomatal closure (Harrison and Walton 1975). A link has regarding the placement of the moss and liverwort also been established between ABA and stomatal clade in relation to the hornwort and VP clades (Wickett et al. 2014). closure in response to high atmospheric CO2 levels. While CO2 does not appear to influence ABA levels, ABA

enhances stomatal sensitivity to atmospheric CO2 ANGIOSPERMS concentration and vice versa, and the stomatal response to CO2 is compromised in ABA biosynthesis Environmental triggers of ABA-mediated stomatal and perception mutants (Raschke 1975; McAdam et al. responses 2011; Chater et al. 2015). Lastly, pathogens can gain entry ﬂ Of all environmental conditions in uencing leaf water to a plant via open stomata, and links have been made status in the natural environment, the humidity of the between the mechanisms triggering stomatal closure in air is among the fastest and most dynamically changing. response to pathogens, with those involved in ABA It is in response to these changes in humidity, or, more signaling (Melotto et al. 2006; Adie et al. 2007; Guzel precisely, the vapor pressure difference between the Deger et al. 2015). leaf and the atmosphere (VPD), that active ABA- mediated stomatal responses in angiosperms are ABA biosynthesis most obvious. While there are numerous examples of ABA was long thought to be synthesized predominantly diversity in angiosperm stomatal behavior, discussed at in the roots and transported to leaves via the xylem the end of this section, for the majority of angiosperm (Zhang et al. 1987). However, this theory has been species examined to date, there is substantial evidence challenged by considerable evidence that leaves act as a implicating active metabolic processes, particularly major source for ABA biosynthesis, and even transport driven by ABA, in the regulation of stomatal responses ABA to the roots (Setter et al. 1980; Holbrook et al. to changes in VPD. First, a direct relationship between 2002; Christmann et al. 2007; Manzi et al. 2015; McAdam stomatal aperture and leaf or epidermal cell turgor is et al. 2016b). Hydrolysis of an inactive glucose ester

April 2017 | Volume 59 | Issue 4 | 240–260 www.jipb.net Evolution of stomatal responses to ABA in land plants 243 conjugate of ABA (ABA-GE) stored in the vacuole, by b- suggesting guard cell-autonomous ABA biosynthesis glucosidases, has also been proposed as a mechanism may play a role in the closure of an individual stoma in for rapid increases in ABA concentration (Lee et al. response to local atmospheric conditions (Bauer et al. 2006; Xu et al. 2012). However, a number of studies have 2013). However, NCED3, and genes that control subse- shown that foliar ABA-GE levels are either too low quent steps of the biosynthetic pathway, ABA DEFICIENT initially, or do not show an adequate decrease, to 2 (ABA2) and ABSCISIC ALDEHYDE OXIDASE 3 (AAO3), account for the increase in foliar ABA level that occurs in appear to be expressed predominantly in leaf vascular response to water stress in a variety of angiosperm tissues, suggesting that transport of vascular-derived species (Zeevaart 1980; Lehmann and Schutte€ 1984; ABA to guard cells may also play an important role in Cornish and Zeevaart 1985; McAdam et al. 2016c). driving stomatal closure (Koiwai et al. 2004; Endo et al. The most plausible model for the involvement of 2008). The “ionic trap model” explains the flux of ABA ABA in stomatal responses to VPD is rapid de novo by passive diffusion of ABA through the membrane lipid biosynthesis of ABA in the leaf. This model is supported bilayer (Boursiac et al. 2013). A number of proteins that by data indicating that a single gene within the ABA actively transport ABA across the cell membrane have biosynthesis pathway, NCED3, encoding the rate-limiting also been identified in A. thaliana, including the ATP- 9-cis-epoxycarotenoid dioxygenase enzyme, is upregu- BINDING CASSETTE (ABC) transporters ABCG25 and lated in the leaf within minutes of an increase in VPD ABCG40, which export ABA out of vascular tissues, and (Iuchi et al. 2001; Waadt et al. 2014; McAdam et al. into cells (particularly guard cells), respectively (Kang 2016c). The molecular signalling pathway linking expo- et al. 2010; Kuromori et al. 2010). In addition, the sure to high VPD or drought stress to transcriptional ABA-IMPORTING TRANSPORTER 1 (AIT1) appears to upregulation of NCED3 has not yet been elucidated, but have a specific role mediating ABA uptake into guard cell turgor is likely the physiological trigger for ABA cells of inflorescence stems (Kanno et al. 2012), while biosynthesis under high VPD (Pierce and Raschke 1980; AtDTX50 has been identified as an ABA efflux carrier, Davies et al. 1981; McAdam and Brodribb 2016; Zhang which exports excess ABA from cells in vascular tissues et al. 2016b). Arabidopsis Histidine Kinase1 (AHK1) has and guard cells (Zhang et al. 2014). been investigated as a likely candidate for the turgor- sensing receptor upstream of NCED3 in this pathway, ABA signaling but recent evidence indicates that AHK1 does not fulfila Once synthesized, ABA is detected by nucleocytoplas- critical role in triggering ABA-mediated stomatal closure mic receptors within the PYRABACTIN RESISTANCE 1 (Wohlbach et al. 2008; Kumar et al. 2013; FC Sussmilch, (PYR)/PYR1-LIKE (PYL)/REGULATORY COMPONENT OF TJ Brodribb and SAM McAdam, unpubl. data). Based on ABA RECEPTOR (RCAR) family (Ma et al. 2009; Park knowledge of osmosensing in the simple eukaryote et al. 2009; Santiago et al. 2009). Binding of ABA to yeast, a number of other possible candidates have been these proteins causes a conformational change, allow- suggested, including histidine kinases related to AHK1, ing these receptors to bind to the catalytic site of clade receptor-like kinases and integrin-like proteins A protein phosphatase type 2C (PP2C) proteins and (Christmann et al. 2013; Osakabe et al. 2014). However, alleviate their inhibitive enzymatic activity (Melcher these candidates still remain to be investigated, and it is et al. 2009; Miyazono et al. 2009; Nishimura et al. 2009; possible that this receptor may be an as yet unidentified Yin et al. 2009). In the absence of ABA, PP2C plant-specific protein. For now the turgor sensor central phosphatases, including ABA INSENSITIVE1 (ABI1), to ABA-mediated control of daytime transpiration in ABI2 and HOMOLOG OF ABI1/2 (HAB1), physically bind angiosperms remains elusive. to and inactivate the SNF1-RELATED KINASE 2 (SnRK2) The NCED enzyme catalyzes the first committed step family protein OPEN STOMATA1 (OST1), a positive for ABA biosynthesis, and is conserved as the rate- regulator and critical limiting component for the ABA- limiting enzyme across angiosperms, including mono- mediated stomatal response (Umezawa et al. 2009; cot, asterid and rosid species (Tan et al. 1997; Burbidge Vlad et al. 2009; Soon et al. 2012; Acharya et al. 2013). et al. 1999; Qin and Zeevaart 1999; Chernys and Zeevaart When PP2C inhibition is alleviated, OST1 quickly 2000; Thompson et al. 2000). All genes involved in ABA becomes active; indeed just 2 minutes of ABA treatment biosynthesis are expressed within guard cells, is sufficient to cause strong OST1 activity in A. thaliana www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 244 Sussmilch et al. cells (Yoshida et al. 2002). OST1 then activates multiple pyr1pyl1pyl2pyl4pyl5pyl8, lacks a stomatal response to downstream targets, including S- and R-type anion ozone-induced ROS (Merilo et al. 2013), suggesting that channels in the guard cell membrane, resulting in a flow ABA perception may be critical for a ROS-induced of ions and loss of osmotic potential from the guard stomatal response. A contrasting model of ROS cells, which deflate, closing the stomatal pore (Geiger involvement in stomatal closure has recently been et al. 2009; Lee et al. 2009; Ng et al. 2011; Imes et al. proposed, suggesting that ROS may in fact act by 2013). There is also evidence of the involvement of the directly catalyzing the sequential oxidation of ABA magnesium-chelatase H subunit/putative ABA receptor precursors to ABA (McAdam et al. 2017). This model is (CHLH/ABAR) as an upstream regulator of OST1 and based on the results from a series of studies. Firstly, important component of the ABA signaling pathway in lipoxygenase enzyme, which generates strong ROS chloroplasts, although there is controversy over from polyunsaturated fatty acids, including linoleic acid whether this receptor actually binds to ABA (Shen (Hamberg 1971), can oxidize violaxanthin to xanthoxin et al. 2006; Muller€ and Hansson 2009; Tsuzuki et al. 2011; in the presence of linoleic acid (Firn and Friend 1972). In Liang et al. 2015). The S-type anion channels SLAC1 and addition, the oxidation of subsequent precursors in the homolog SLAH3 are activated by an additional OST1- ABA-biosynthesis pathway, xanthoxin and abscisic independent pathway of calcium-dependent protein aldehyde, can rapidly occur in air (Taylor and Burden kinases (CPKs) (Geiger et al. 2010; Demir et al. 2013). This 1972; Willows and Milborrow 1992). Most recently, foliar OST1-independent pathway is also ABA-sensitive, as ABA levels were found to rapidly increase upon PP2Cs inhibit sensitivity to calcium ions in the absence of exposure to ozone, a treatment that causes ROS ABA, by direct inhibition of these anion channels production, in angiosperm species that show stomatal þ (Brandt et al. 2012; Brandt et al. 2015). As Ca2 has a closure in response to ozone, but not in those that lack similar influence on stomatal sensitivity to CO2 as ABA this response (McAdam et al. 2017). Coupled with an does, it seems likely that these anion channels ABA-mediated increase in ROS production, this mecha- represent the point of convergence between these nism would result in a positive feedback loop that may pathways (Young et al. 2006; Vahisalu et al. 2008). OST1, enhance stomatal closure during water stress (Mittler SLAC1 and SLAH3 further inhibit stomatal re-opening and Blumwald 2015). under conditions of water stress by inhibiting the activity of an inward-rectifying potassium channel, KAT1 ABA catabolism (Sato et al. 2009; Acharya et al. 2013; Zhang et al. 2016a). ABA is catabolized into inactive forms via either There are also many reports indicating the involve- oxidation or conjugation. During prolonged periods of ment of ABA-induced reactive oxygen species (ROS) as drought stress, catabolism of ABA occurs continuously, important secondary messengers in ABA-mediated but is balanced by de novo biosynthesis to maintain high stomatal closure. OST1 activates plasma membrane- ABA levels until the stress is alleviated (Harrison and bound nicotinamide adenine dinucleotide phosphate Walton 1975; Ren et al. 2007). (NADPH) or respiratory burst oxidase (RBOH) enzymes The first (and key) step of the oxidative pathway for 0 that catalyze superoxide production, as well as H2O2 via ABA catabolism is catalyzed by ABA 8 -hydroxylases, apoplastic superoxide dismutases (Mustilli et al. 2002; encoded by the CYP707A family of cytochrome P450 Sirichandra et al. 2009). The ROS are thought to induce monoxygenase genes (Krochko et al. 1998; Kushiro stomatal closure via calcium channels, by promoting an et al. 2004; Saito et al. 2004; Yang and Zeevaart 2006). increase in cytosolic calcium levels, which activates The four CYP707A genes present in A. thaliana are all anion efflux channels (Hedrich et al. 1990; Pei et al. upregulated by ABA, dehydration and rehydration 2000; Chen et al. 2010; Wang et al. 2013). In accordance (Kushiro et al. 2004; Saito et al. 2004; Chan 2012). with this, ABA-regulated stomatal closure is impaired CYP707A1 and CYP707A3, in particular, have been in mutants with impaired ROS production (Kwak et al. shown to have specific roles in regulating transpiration. 2003). However, ROS accumulation does not affect Under high humidity, CYP707A1 is essential for the stomatal aperture in the absence of ABA (Jannat et al. catabolism of local pools of ABA inside guard cells, 2011a, 2011b). Furthermore, the most severe loss of while CYP707A3 is important for reducing levels of function ABA receptor sextuplet mutant, mobile ABA in vascular tissues (Okamoto et al. 2009;

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Arve et al. 2015). The resulting catabolite, 80-hydroxy- More broadly, the stomata of grasses are capable ABA, is unstable and spontaneously isomerizes to of opening and closing faster than eudicots in phaseic acid (PA) (Saito et al. 2004). PA can be response to light and increased VPD, respectively recognized by a subset of the PYR/PYL/RCAR family of (Grantz and Zeiger 1986; Grantz and Assmann 1991). ABA receptors and can trigger similar plant responses to Although, the mechanistic basis for this difference is ABA, including stomatal closure (Sharkey and Raschke not currently well understood, it is possible that the 1980; Weng et al. 2016). While bioactivity of PA, in terms unique subsidiary cells of grass stomata, which serve of stomatal behavior, is generally much weaker than as a powerful source and sink for ions shuttled into ABA, it can vary greatly between angiosperm species and out of guard cells (Pallaghy 1971; Raschke and (Sharkey and Raschke 1980). PA is further metabolized Fellows 1971; Mumm et al. 2011), contribute to this to inactive dihydrophaseic acid (DPA) (Walton et al. difference in speed. In addition, in contrast to the 1973; Sharkey and Raschke 1980), by a PA reductase eudicot A. thaliana SLAC1 anion channel, which is within the family of NAD(P)H-dependent reductases, permeable to both chloride and nitrate ions (Geiger represented by a single gene, ABA HYPERSENSITIVE 2 et al. 2009), OsSLAC1 in rice is strongly selective to (ABH2), in A. thaliana (Weng et al. 2016). CYP707A nitrate, which is considered an optimal anion for proteins also catalyze the 90-hydroxylation of ABA to the stomatal movement (Sun et al. 2016). inactive neophaseic acid (neoPA), as a minor byproduct ABA has also been implicated in inducing crassula- (Zhou et al. 2004; Kepka et al. 2011; Okamoto et al. 2011). cean acid metabolism (CAM), whereby stomata remain ABA is conjugated to ABA-GE for vacuolar storage by closed during the day and open only at night, in an ABA-inducible glucosyl transferase (GTase) (Zeevaart facultative CAM plants, which can naturally be induced

1980, 1983; Xu et al. 2002; Palaniyandi et al. 2015). to shift from the typical C3 carbon metabolism to CAM Although ABA conjugation does not appear to be a under water stress (Ting 1981). In addition, ABA is principal pathway of inactivation (Priest et al. 2006), thought to be involved in inducing a shift from CAM to there is feedback between the ABA conjugation and CAM-idling in CAM plants, whereby stomata remain oxidation pathway, with increased expression of GTase closed day and night, during conditions of extreme genes prompting transcriptional upregulation of the water stress (Bastide et al. 1993). The molecular CYP707A genes in A. thaliana (Dong et al. 2014). mechanisms for these specialized responses remain to be determined. ABA as a mechanism for diversity in plant responses to water deficit GYMNOSPERMS The metabolic regulation of stomata by ABA, governed by complex molecular components controlling both Intermediate ABA-mediated stomatal responses ABA homeostasis and perception, provides ample At the base of the seed plants, the gymnosperms offer genetic resources on which selection and adaptation valuable insight into the evolution of ABA-mediated can operate. The possibility that active regulation of stomatal responses. Detailed studies of the molecular stomatal responses to leaf water deficit by ABA might mechanisms controlling stomatal aperture have been contribute to diversity in seed plant responses to the largely limited to angiosperm models. However, there is environment is a promising hypothesis that has considerable physiological evidence of differences in received little attention thus far. In support of this stomatal behavior between plant lineages, and the hypothesis, considerable variation between angio- molecular basis for these differences are only now sperm species in terms of ABA sensitivity, synthesis starting to reveal fascinating examples of molecular and metabolism in response to water stress and evolution. Physiological studies have demonstrated changes in VPD has been described (Tardieu and that the control of stomatal responses to leaf water Simonneau 1998; McAdam and Brodribb 2015). In status in the light in gymnosperms is functionally addition, ecological differences between species in intermediate between angiosperms and basal seedless terms of responses to seasonal changes in water vascular plants (McAdam and Brodribb 2014). Similar to availability may derive from differences in ABA synthesis angiosperm species, gymnosperm stomata close in (McAdam and Brodribb 2015). response to ABA, and foliar ABA levels rise in response www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 246 Sussmilch et al. to exposure to drought (Jackson et al. 1995; Perks et al. turgor-sensing protein acting transcriptionally up- 2002; Brodribb and McAdam 2011; McAdam et al. 2011; stream of the NCED gene encoding the rate-limiting Zuccarini et al. 2011; McAdam and Brodribb 2014, 2015). enzyme for ABA biosynthesis. NCED homologs are However, there are considerable differences between upregulated by dehydration even in the most basal land aspects of ABA-mediated stomatal closure in gymno- plant clades (Richardt et al. 2010), but the speed of sperms compared to angiosperms, indicating that some upregulation of NCED genes in response to VPD changes mechanisms involved in this process evolved after remains to be determined in gymnosperms. divergence of these two extant seed plant lineages, There is evidence that some of the enzymes which we will outline in this section. These findings are catalyzing the later, committed steps of ABA biosyn- difficult to integrate into the single step model thesis in angiosperms have acquired greater functional describing joint acquisition of stomata and complex specificity than homologs in earlier land plant lineages, ABA-mediated control mechanisms in early stomato- which could affect their efficiency and the rate of phytes, but instead support a gradualistic model of completion of de novo ABA biosynthesis. First, angio- stomatal evolution. sperm species have a dedicated ABA-specific short- chain dehydrogenase/reductase (SDR) enzyme to cata- Major differences in ABA biosynthetic enzymes may lyze the penultimate step in the ABA biosynthesis account for slow ABA biosynthesis in conifers pathway, encoded by genes from the ABA2 clade, which While foliar ABA levels rise slightly in some gymnosperm is not represented in current versions of the genomes of species in response to high VPD, they do not reach sequenced representatives of gymnosperm, lycophyte the considerable levels required to trigger stomatal or moss clades (Figure 3) (Cheng et al. 2002; Moummou closure (McAdam and Brodribb 2015). In contrast to the et al. 2012; McAdam et al. 2015). Although incomplete predominantly active, ABA-mediated stomatal response genome coverage can make it more difficult to conclude to VPD seen in angiosperms, stomatal responses to VPD gene absence than presence from sequence data, this in gymnosperms are highly predictable, being passively observation suggests that a specialized ABA2 enzyme controlled by leaf water status (McAdam and Brodribb for catalysis of this step of ABA biosynthesis likely 2015; Martins et al. 2016). Similar passive responses to evolved after divergence of the gymnosperm and VPD are also seen in fern and lycophyte species, angiosperm lineages. The conversion of xanthoxin to indicating that this behavior is ancestral, and that the abscisic aldehyde can be catalyzed to a limited degree active ABA-mediated stomatal response to VPD seen in by SDRs other than ABA2 in angiosperms, as evidenced angiosperms evolved after the divergence of the by the residual level of ABA produced in aba2 null gymnosperm lineage (McAdam and Brodribb 2015; mutants (Batge et al. 1999; Gonzalez-Guzman et al. Martins et al. 2016). The ability to rapidly upregulate 2002; McAdam et al. 2015). However, these non-specific ABA levels within a timeframe suitable to respond to enzymes are slower at catalyzing this step, as evidenced rapid fluctuations in VPD, which angiosperm species by the reduced speed at which ABA levels increase in possess, is critical for an ABA-mediated stomatal drought-stressed Pisum aba2 mutant plants (Wang et al. response to VPD. However, there is a dramatic 1984; McAdam et al. 2015). difference in the time taken for ABA levels to rise to The two enzymes that catalyze the final step within sufficient levels for stomatal closure on desiccation the ABA biosynthesis pathway, belonging to the between gymnosperm (6 h) and angiosperm (<30 min) aldehyde oxidase (AO) group of molybdo-flavo proteins species (Zeevaart 1980; McAdam and Brodribb 2014). and the molybdenum cofactor (MoCo)-sulfurase en- This difference indicates that either (i) the signal to zymes required for their activity, predate the divergence trigger ABA biosynthesis occurs more rapidly in of the major eukaryote lineages, thus are present even in angiosperms compared to gymnosperms, or (ii) once the earliest land plants (Bittner et al. 2001; Terao et al. triggered, de novo ABA biosynthesis occurs more 2001; Sagi et al. 2002). The characterized angiosperm AO quickly in angiosperms than gymnosperms. The genes that have specific roles in ABA-biosynthesis are all mechanism(s) linking changes in turgor to increased more similar to other AO genes within the same species, ABA biosynthesis is not well understood, even in than to any other AO genes from other species (Harrison angiosperm species, but this pathway would involve a et al. 2011), which likely reflects convergent evolution due

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Figure 3. Phylogenetic tree of the SDR110C protein family from the sequenced gymnosperm model Picea abies (Pa) All SDR110C proteins from Arabidopsis thaliana (At), Selaginella moellendorfﬁi (Sm) and Physcomitrella patens (Pp), and members of the angiosperm ABA2 group from Amborella trichopoda (AmTr), rice (Os), sorghum (Sobic), maize (Zm), 1 poplar (Potri), pea (Ps) and soybean (Glyma) were included. The neighbor-joining tree was produced using Geneious 7.1.9 from a MAFFT alignment of full-length protein sequences rooted to the closely related family of A. thaliana SDR68C proteins. Bootstrap values from 10,000 trees are shown next to each branch. Sequences were obtained from ConGenIE (Pa; congenie.org; Nystedt et al. 2013), Phytozome (At TAIR10, AmTr v1.0, Os v7_JGI, Sobic v3.1, Zm Ensembl- 18, Potri v3.0, Glyma Wm82.a2.v1; phytozome.jgi.doe.gov; Goodstein et al. 2012) and GenBank (Ps). tBLASTn searches were also conducted against transcript databases for Cryptomeria japonica, Cycas rumphii, Ginkgo biloba, Gnetum gnemon, Picea glauca, Picea menziesii, Picea sitchensis, Pinus banksiana, Pinus contorta, Pinus lambertiana, Pinus pinaster, Pinus sylvestris, Pinus taeda, Podocarpus macrophyllus, Sciadopitys verticillata, Sequoia sempervierns and Taxus baccata at ConGenIE using AtABA2 protein sequence as a query to determine if an ABA2 gene was present in current sequence resources for other gymnosperm models, but reciprocal blasts of identiﬁed hits back against A. thaliana revealed that all hits were more closely related to other genes within the SDR110C family than to ABA2. www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 248 Sussmilch et al.

to the necessity of functional interaction between these Sensitivity to CO2 genes (Akaba et al. 1999; Omarov et al. 2003; Zdunek- Unlike angiosperm models, ABA does not appear to

Zastocka et al. 2004). It remains to be determined enhance sensitivity to CO2 in conifers (McAdam et al. whether gymnosperm AO enzymes are capable of 2011). Indeed, among land plants, a number of studies catalyzing the oxidation of abscisic aldehyde to ABA have concluded that angiosperm species have a uniquely with the same efficiency as specific enzymes character- high sensitivity to CO2, particularly in the dark, with this ized in angiosperm models. sensitivity weak or absent in conifers and basal vascular In contrast to the AO gene family, wherein most land plant lineages (Beadle et al. 1979; Medlyn et al. 2001; species examined have 3–4 AO gene members (Zdunek- Doi and Shimazaki 2008; Brodribb et al. 2009; Field et al. Zastocka 2008; Seiler et al. 2011), each plant species 2015). One explanation is that calcium-dependent examined so far contains only a single gene that activation of SLAC/SLAH anion channels may be angio- encodes a MoCo-sulfurase (Xiong et al. 2001; Sagi et al. sperm-specific(Brodribb and McAdam 2013b). However, 2002). This MoCo-sulfurase is required for the function this has been debated, with evidence that stomatal of all AO and the closely related xanthine dehydroge- aperture decreases in response to CO2 in moss and nase (XDH) enzymes (Xiong et al. 2001). As MoCo- lycophyte models (Chater et al. 2011; Ruszala et al. 2011), sulfurases are not specific to the ABA-pathway, it seems and that ferns and angiosperms have similar stomatal less likely that this enzyme would account for differ- responses to high CO2 in the light (Franks and Britton- ences in the rate of ABA biosynthesis between Harper 2016), although fern responses may be highly gymnosperms and angiosperms. variable and fern stomata may even open rather than

close under high CO2 (Creese et al. 2014). Stomatal responses to ABA first evolved to ensure stomatal closure during drought FERNS, LYCOPHYTES AND BRYOPHYTES Between gymnosperm species, there are differences in foliar ABA dynamics during long-term sustained water Are stomata monophyletic? stress. In species from basal clades of conifers, stomatal A central premise of the single-step model for closure during prolonged water stress is maintained by stomatal evolution, is the hypothesis that the stomata the accumulation of high levels of foliar ABA, similar to of all land plants are monophyletic structures, sharing angiosperm species, suggesting that this strategy a single evolutionary origin. Bryophytes are the most evolved prior to divergence of the seed plant lineages basal extant clade of land plants in which stomata are (Brodribb and McAdam 2013a; Brodribb et al. 2014). found. Among the bryophytes, stomata are found in Some conifer species belonging to more recently derived mosses and hornworts, but are limited to the clades of Cupressaceae and Taxaceae show initial sporophyte generation and are not present in the accumulation of foliar ABA, peaking 7–20 d after the dominant, photosynthetic gametophyte generation, initiation of a drought period, but then falling back to while liverworts completely lack stomata (Paton and low, pre-drought levels as water stress progresses Pearce 1957; Raven 2002). In support of a single (Brodribb et al. 2014). These species are anisohydric developmental origin for stomata, most of the genes (Tardieu and Simonneau 1998), being able to prolong involved in stomatal development in angiosperms are stomatal opening and photosynthesis during drought, represented in the model moss Physcomitrella patens have stomata that reopen rapidly on rehydration, and (MacAlister and Bergmann 2011), and mutants of moss rely on cavitation-resistant xylem to survive leaf desicca- homologs of these key genes lack stomata (Chater tion (Brodribb and McAdam 2013a; Brodribb et al. 2014). et al. 2016). Although there is considerable uncertainty It remains to be determined whether these two regarding relationships between the bryophyte line- strategies are managed by differences in the mainte- ages and vascular plants, particularly regarding the nance of signals triggering ABA biosynthesis, upregula- relative positioning of the hornwort clade, strong and tion of catabolism genes, or a combination of both, or robust support has been found for a monophyletic whether ABA levels during prolonged drought also clade of mosses and liverworts (Figure 2)(Wickett decline in angiosperms with cavitation-resistant xylem. et al. 2014). These ﬁndings reject the previous, widely

April 2017 | Volume 59 | Issue 4 | 240–260 www.jipb.net Evolution of stomatal responses to ABA in land plants 249 held view that liverworts, mosses and hornworts are, There are considerable differences in the develop- in that order, successive sister groups to vascular ment, structure and function of bryophyte stomata, plants, which has dominated previous discussions of when compared to the stomata of vascular plants. Moss stomatal evolution. stomata are located at the base of spore capsules and Based on our current understanding of land plant their predominant function, as well as the function of phylogeny (Wickett et al. 2014), a model for the hornwort stomata, appears to be to open to allow the monophyly of all land plant stomata assumes the spore capsule to dry as it matures (Duckett et al. 2009; presence of stomata in the last common ancestor of Pressel et al. 2014; Field et al. 2015). Consistent with a all bryophyte and vascular plant lineages, and subse- role for moss stomata in spore capsule desiccation, a quent losses of stomata in liverworts after divergence recent study characterized the phenotypes of knock- from mosses (Figure 2). This hypothesis also assumes out mutants for moss stomatal development genes, multiple losses within the mosses, as “true” stomata are and observed that these astomatal moss mutants only found in the derived peristomate mosses (including showed delayed dehiscence of the sporophytes (Chater the Polytrichales and Tetraphidales) and the gymnost- et al. 2016). Unlike the sub-stomatal cavities of vascular omous Oedipodiales, while members of basal moss plants, which play an important role in photosynthetic lineages, including Andreaeopsida and the Takakiopsida, gas exchange and are gas-filled from the onset of lack stomata (Cox et al. 2004; Cox et al. 2010). A further development, the intercellular spaces subtending moss complication is the pseudostomata found in Sphagnum and hornwort stomata are initially filled with liquid, species, which some studies have concluded are not which is replaced by gas only after the pore opens homologous with the stomata of other moss clades (Cox (Pressel et al. 2014; Field et al. 2015; Merced and et al. 2004; Duckett et al. 2009), while others could not Renzaglia 2016). In addition, close inspection of the rule out the possibility that these pseudostomata structure of mature moss and hornwort stomata has represent primitive stomata that share the same origin revealed mechanical constraints, including the thicken- (Merced 2015). A hypothesis for the monophyly of ing of guard cell walls and waxes lining the stomatal stomata relies on the loss of stomata in at least two moss chambers, which would hamper the ability of these lineages, Andreaeopsida and Takakiopsida, and either an stomata to repeatedly open and close (Merced and additional loss in Sphagnum, or for these pseudostomata Renzaglia 2013; Merced and Renzaglia 2014; Pressel to have arisen from the same ancestral structure as the et al. 2014). This suggests that, once mature, these stomata found in the peristomate mosses, in addition to stomata open once and never close, in line with a role in the loss in the liverworts. In contrast, a second spore capsule desiccation (Lucas and Renzaglia 2002; hypothesis suggests that stomata evolved separately Duckett et al. 2009; Pressel et al. 2014). Taking this into in the peristomate/gymnostomous mosses and horn- consideration, a hypothesis for the monophyly of worts (Cox et al. 2004; Duckett et al. 2009). If the stomata would suggest that modern stomata evolved hornworts are resolved as a sister group to vascular from ancestral structures that opened rather than plants, this hypothesis is most parsimonious with only closed under desiccation (Beerling and Franks 2009). two gains, in the peristomate mosses and in an ancestor Studies describing stomatal responses to environ- of hornworts/vascular plants (Haig 2013). A third mental conditions have focused on young stomata, and hypothesis, that stomata evolved three times, separately it appears that there may be a brief window of a few in moss, hornwort and early vascular plant lineages, days when these stomata are physically capable of accounts for major differences in stomatal morphology opening and closing, leading to suggestions that and function between hornworts, mosses and vascular stomata may play a role in photosynthetic gas exchange plants (Renzaglia et al. 2000; Pressel et al. 2014). Given and respond to the environment in the same way as the clear evolutionary advantages of stomatal pores for angiosperm stomata during this brief developmental plant success, it is conceivable that these structures may window (Garner and Paolillo Jr 1973; Hartung et al. 1987; be the result of convergent evolution due to strong Chater et al. 2011; Ruszala et al. 2011; Merced and developmental bias, a phenomenon that has received Renzaglia 2014; Villarreal and Renzaglia 2015). However, more attention in animals (Kavanagh et al. 2013; Ellis et al. the importance of endogenous photosynthesis within 2015) than plants. sporophytes has been questioned, as stomata only www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 250 Sussmilch et al. open once the sporophyte has grown to its final plants (McAdam and Brodribb 2012; Brodribb et al. dimensions, and a significant proportion (>90%) of 2016). Importantly, it has yet to be shown that sugars involved in sporophyte development are derived endogenous ABA levels can control stomatal aperture from the parent gametophyte (Thomas et al. 1978; in mosses, hornworts, lycophytes or ferns. Ligrone et al. 1993). Indeed, in considerable contrast Additional evidence from P. patens supporting the with astomatal A. thaliana mutants, which exhibit a single-step model for stomatal control, is that this moss small, pale plant phenotype (Ohashi-Ito and Bergmann species contains a functional OST1/SLAC1 homolog pair, 2006; MacAlister et al. 2007; Pillitteri et al. 2007), the molecular mechanism required for ABA-mediated comparable P. patens astomatal mutants showed no changes to guard cell turgor (Lind et al. 2015). While difference in sporophyte size when compared with wild- these genes are expressed during sporophyte develop- type plants (Chater et al. 2016). Bearing this, and that ment (O’Donoghue et al. 2013), they do not appear to the intercellular spaces subtending bryophyte stomata exhibit a guard cell-specific expression pattern (Chater are initially filled with water, in mind (Lucas and et al. 2011; Vesty et al. 2016), which is considered Renzaglia 2002; Pressel et al. 2014), a role in photosyn- essential for active ABA-mediated stomatal control thetic gas exchange seems unlikely. (Levchenko et al. 2005; Lind et al. 2015). Furthermore, recent results from the lycophyte Selaginella moellen- Was aperture controlled by ABA in the earliest dorffii and the fern Ceratopteris richardii have revealed stomata? that lycophytes and ferns lack functional pairs of OST1/ The single-step model for the evolution of stomata SLAC1 homologs (McAdam et al. 2016a). Given that with complex ABA-mediated control of aperture in the these species represent two lineages that are evolu- most basal stomatal-bearing land plant, is supported tionarily intermediate between the bryophytes and the by reports that stomatal aperture and/or conductance seed plants, the observation of OST1/SLAC functional decrease in response to extremely high concentra- interaction in a moss species is intriguing (Lind et al. tions of exogenous ABA in the lycophyte Selaginella 2015). It will be interesting to determine if a guard cell- uncinata (Ruszala et al. 2011), and the moss species P. specific expression pattern for the functional moss patens and Funaria hygrometrica,butnotintheP. OST1/SLAC1 homolog pair can be identified in other patens ost1-1 deletion mutant (Chater et al. 2011). moss and hornwort species, to understand the Interestingly, although ABA was applied at levels evolutionary origins of this trait. approximately 1 000 higher than endogenous levels measured in droughted plants, these studies found Alternative ancestral roles for ABA only a relatively small reduction in stomatal aperture A recent characterization of normal stomatal behavior in and conductance. This is in sharp contrast to the mutants in a C. richardii OST1 homolog contrasts with the profound stomatal closure that occurs in response to characteristic constitutively open stomatal phenotype of much lower levels of ABA in seed plants (Weyers and corresponding angiosperm mutants (Merlot et al. 2002; Hillman 1979; Henson and Turner 1991; Trejo et al. Mustilli et al. 2002; Yoshida et al. 2002; McAdam et al. 1993; Brodribb and McAdam 2011). Application of more 2016a). Instead, these fern mutants lack ABA-mediated natural levels of ABA, although still 7 in excess of control of gametophyte sex determination and spore endogenous levels in droughted plants, has been dormancy (McAdam et al. 2016a). This finding indicates showntohavenoinfluence on stomatal conductance that the ABA-SnRK2 signaling pathway played an early in either lycophytes or species from the more derived role in sex determination and spore dormancy in ferns fern lineage (Brodribb and McAdam 2011). Hornwort and was later co-opted for the regulation of stomatal stomata have also been found to lack a response to aperture in seed plants, highlighting the alternative roles ABA (Lucas and Renzaglia 2002), unless extremely that ABA plays in land plant development. While the high concentrations are used (Hartung et al. 1987). presence of a functional stomatal response to ABA in Accordingly, stomatal opening is not hampered in basal land plant lineages has been debated, there is clear basal vascular land plants, including lycophytes and evidence that ABA levels increase in response to severe ferns by any level of endogenous ABA synthesized by water stress in all land plants tested, and even in algae the plant during drought stress, in contrast to seed (Marsalek et al. 1992; McAdam and Brodribb 2012).

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Furthermore, all land plants have the molecular capacity models for the evolution of the stomatal response to to perceive ABA (Hauser et al. 2011; Wang et al. 2015). In ABA in land plants, and the physiological and molecular contrast to the conclusions of a recent report (Chen et al. evidence on which these models are based. Considering 2016), homologous PYR/PYL/RCAR receptors, for the evidence from each land plant lineage, particularly perception of ABA, have been identified in all land plants, physiological data from fern and gymnosperm models even in a representative of the stomata-lacking liverwort and recent molecular findings from basal vascular lineage, Marchantia polymorpha (Hauser et al. 2011; Wang plants, we find strong support for a gradualistic model et al. 2015). Rather than indicating a role for ABA in the for the evolution of ABA-mediated stomatal responses. prevention of desiccation via stomatal closure, this This gradualistic model for stomatal control explains the instead likely reflects an important ancestral role for ABA evolution of stomata from simple, passively controlled in desiccation tolerance. This critical function for ABA is valves in early land plants, to the tightly regulated pores widely documented in both liverworts and mosses, and with complex, ABA-mediated control mechanisms seen is believed to occur through the upregulation of proteins in modern angiosperms (Figure 4). This model is not that function in osmoregulation, including aquaporins, contingent on the monophyly of stomata, and can be sugar transporters and metabolic enzymes (Hellwege applied to other hypotheses suggesting two or even et al. 1994; Cuming et al. 2007; Khandelwal et al. 2010). three independent origins for stomata, regardless of This response involves PP2Cs, which appear to have the uncertainty surrounding stomatal homology within evolved in the first land plants (Tougane et al. 2010; Wang the bryophytes. et al. 2015), leaving it tempting to speculate that It is clear that key genes central to ABA-mediated alleviation of PP2C inhibition via the binding of ABA to stomatal closure evolved early during land plant PYR/PYL/RCAR-type receptors may be an ancient and evolution, prior to the divergence of the bryophyte well-conserved mechanism. However, this has yet to be and vascular plant lineages (Chater et al. 2011; confirmed, and evidence from P. patens indicates that O’Donoghue et al. 2013; Lind et al. 2015). However, PP2Cs may have acted downstream of SnRK2s in a moss evidence from fern mutants suggest that these genes ancestor, rather than upstream, suggesting that early fulfilled highly divergent ancestral roles (McAdam et al. steps of the ABA-signaling may have changed through- 2016a), as ABA has many important functional roles in out land plant evolution more than first thought plant development, desiccation signaling and propagule (Komatsu et al. 2013). In contrast to an increase in ABA dormancy (McCourt et al. 2005; Hartung 2010; level when plants are severely drought-stressed, no Vanstraelen and Benkova 2012; Vesty et al. 2016). increase in ABA level has ever been shown to occur in Instead, these findings suggest that these genes were basal land plants during changes in VPD. This contrasts co-opted to facilitate stomatal closure during periods of sharply with observations in angiosperms and is a central drought stress later, in the common ancestor of modern requirement for ABA-mediated stomatal closure seed plants. (Bauerle et al. 2004; McAdam and Brodribb 2015; While this review summarizes the considerable McAdam and Brodribb 2016). progress that has been made in this field to date, many questions remain to be answered by future studies. The development of sequence resources for CONCLUSION representatives of the bryophyte, lycophyte and gymnosperm lineages, as well as limited resources The important role that ABA plays in mediating stomatal for ferns, are particularly exciting for the field of plant closure, allowing improved plant survival in dry evolutionary biology and physiology, and will assist terrestrial environments, has been highlighted through toward this goal (e.g., Banks et al. 2011; Nystedt et al. decades of research focusing on angiosperm models. 2013; Aya et al. 2015). While it may be tempting to rely While relatively fewer studies have examined stomatal on these in silico resources for speculation on the level behavior in other plant lineages, and the extent to of conservation of key processes in land plants, it which the role of ABA has evolved over time, this has will be important to delve deeper into investigating become a topic of growing interest in more recent the extent to which the function of these genes, and years. Here we have examined the two prominent the proteins encoded, has changed over time. In www.jipb.net April 2017 | Volume 59 | Issue 4 | 240–260 252 Sussmilch et al.

Figure 4. An updated gradualistic model for the evolution of abscisic acid (ABA)-mediated control of stomatal aperture The relative timing of appearance of key traits is indicated on the current, most parsimonious phylogeny for land plants that recognizes current uncertainty in the relationships between bryophytes (B) and vascular plants (VP) (Wickett et al. 2014). The hypothesis of a monophyletic origin of stomata is adopted for simplicity. particular, studies integrating results from physiologi- Alignment Search Tool (BLAST) searches and per- cal experiments with molecular data will yield a formed the phylogenetic analysis. greater understanding of how these processes are controlled. The phenotypes of mutants of homologs of each of the ABA-biosynthesis and signaling genes REFERENCES from multiple different bryophyte, lycophyte, fern and even basal seed plant species, would be of particular Acharya BR, Jeon BW, Zhang W, Assmann SM (2013) Open Stomata 1 (OST1) is limiting in abscisic acid responses of interest. In addition, the diversity in ABA-mediated Arabidopsis guard cells. New Phytol 200: 1049–1063 stomatal responses within the angiosperm lineage Adie Bat, Perez-P erez J, Perez-P erez MM, Godoy M, remains to be fully explored, especially in view of the Sanchez-Serrano J-J, Schmelz EA, Solano R (2007) ABA ever-increasing need to develop new varieties of crops is an essential signal for plant resistance to pathogens with improved drought tolerance. With the continu- affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19: 1665–1681 ous development of powerful new gene editing Akaba S, Seo M, Dohmae N, Takio K, Sekimoto H, Kamiya Y, techniques, including the revolutionary CRISPR (clus- Furuya N, Romano T, Koshiba T (1999) Production of tered regularly interspersed short palindromic re- homo- and hetero-dimeric isozymes from two aldehyde peats) technology, opening up new possibilities for oxidase genes of Arabidopsis thaliana. J Biochem 126: – functional analyses, we may not have too long to wait 395 401 for answers. Arve LE, Kruse OMO, Tanino KK, Olsen JE, Futsæther C, Torre S (2015) Growth in continuous high air humidity increases the expression of CYP707A-genes and inhibits stomatal closure. Environ Exp Bot 115: 11–19 ACKNOWLEDGEMENTS Aya K, Kobayashi M, Tanaka J, Ohyanagi H, Suzuki T, Yano K, Takano T, Yano K, Matsuoka M (2015) De novo tran- Work in the authors’ laboratories was funded by the scriptome assembly of a fern, Lygodium japonicum, and a Australian Research Council grants DE140100946 (SM) web resource database, Ljtrans DB. Plant Cell Physiol 56: e5 and DP140100666 (TB). Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LGG, Dacre M, AUTHOR CONTRIBUTIONS DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, F.S. and S.M. conceived and wrote the manuscript Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, with the assistance of T.B. F.S. carried out Basic Local Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y,

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