Geobiology (2010), 8, 112–139 DOI: 10.1111/j.1472-4669.2010.00232.x

The evolution of water transport in plants: an integrated approach J. PITTERMANN Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA

ABSTRACT

This review examines the evolution of the plant vascular system from its beginnings in the green algae to modern arborescent plants, highlighting the recent advances in developmental, organismal, geochemical and climatolog- ical research that have contributed to our understanding of the evolution of xylem. Hydraulic trade-offs in vascu- lar structure–function are discussed in the context of canopy support and drought and freeze–thaw stress resistance. This qualitative and quantitative neontological approach to palaeobotany may be useful for interpret- ing the water-transport efficiencies and hydraulic limits in fossil plants. Large variations in atmospheric carbon dioxide levels are recorded in leaf stomatal densities, and may have had profound impacts on the water conser- vation strategies of ancient plants. A hypothesis that links vascular function with stomatal density is presented and examined in the context of the evolution of wood and ⁄ or vessels. A discussion of the broader impacts of plant transport on hydrology and climate concludes this review.

Received 14 September 2009; accepted 26 December 2009

Corresponding author: J. Pittermann. Tel.: +1 831 459 1782; fax: +1 831 459 5353; e-mail: pittermann@ biology.ucsc.edu

Chaloner & McElwain, 1997; McElwain et al., 1999; Retal- INTRODUCTION lack, 2001; Beerling, 2002; Roth-Nebelsick, 2005; Kurschner Plants can control climate as well as respond to it. Recent et al., 2008). Apparently, a greater number of smaller stomata models supported by independent isotopic evidence suggest are needed to counter CO2 deficits at low ambient CO2, that it was the evolution of large, Devonian land plants that rather than fewer, but larger stomata (Franks & Beerling, may have contributed to the dramatic reductions in atmo- 2009a). However, stomata must also regulate water loss from spheric CO2 in the Late Devonian (Beerling & Berner, 2002; the leaf because, for each CO2 molecule fixed by the plant, Berner, 2005, 2006) while progressively deeper and more 200–400 molecules of water may escape through the stomatal complex root systems accelerated pedogenesis and carbon pore. At any point in time, the stomata must optimize plant sequestration (Retallack, 1997; Algeo & Scheckler, 1998; water use efficiency, which is the carbon gain for a given Raven & Edwards, 2001; Berner, 2005). Although the contri- amount of water lost. This trade-off and its implications on bution of plants to atmospheric and biogeochemical processes plant water balance, hydraulics and structure–function may continues to be well explored (Pataki et al., 2003; Bonan, have been apparent early in the evolution of vascular land 2008; Malhi et al., 2008), the role of plant water transport in plants. responding to or acting on both of these components has What are the climatic consequences of transpiration for been somewhat overlooked. atmosphere–biosphere interactions and does the answer lie There is a direct link, however, between plant water once again in the stomatal impressions of ancient leaves? How transport and climate. Indeed, important inferences about the has the evolution of water transport impacted the overall levels of palaeoatmospheric CO2 have been based on measure- design of both ancient and modern flora? The goal of this ments of stomatal distributions in fossil plants. Stomata are review is to address these issues in an interdisciplinary and microscopic pores on surfaces of green leaves and stems that accessible manner that draws not only on the fossil record, but allow CO2 to diffuse into photosynthetic tissue, while letting also on the recent advances in molecular, physiological and water escape. Analysis of fossil plant material across the Phan- evolutionary plant biology. Parts I and II introduce the basics erozoic suggests that low stomatal densities reflect elevated of the cohesion–tension (C–T) theory of water transport and palaeoatmospheric CO2 levels, whereas the opposite is true examine the evolutionary and developmental transitions that for high stomatal densities (McElwain & Chaloner, 1996; selected for this ubiquitous and broadly accepted mechanism

112 2010 Blackwell Publishing Ltd The evolution of water transport in plants 113 from the earliest vascular land plants to trees. Part III high- 1991; Bateman et al., 1998; Boyce et al., 2003; Wilson et al., lights recent advances in our understanding of the structure 2008). For this reason, macroevolutionary and neontological and function of plant vascular tissue (xylem), and its potential approaches can be fruitfully applied to research addressing utility for the reconstruction of water transport in extinct taxa evolution of plant water transport, or the relationships of fossil from climates that were radically different from today. The plants to their climates. review concludes with a discussion of the significance of plant water transport on ecosystem and global hydrology. The mechanism of water transport in plants Water transport in plants is not difficult to understand, but nei- PART I: THE EVOLUTION OF WATER ther is it inherently intuitive. In his book ‘Vegetable Staticks’ TRANSPORT IN TERRESTRIAL PLANTS (1727), the English physiologist Stephen Hales first remarked Much of the information in Part I draws from the fossil that water is released from a plant by ‘perspiration’. He thus record, which is both rich with information yet fundamentally captured an important element of the C–T theory, which incomplete. Indeed, the fossil record has limited resolution requires that water is lost from the plant by evaporation in with respect to the physiological, biochemical and life-history order for bulk flow to occur. The C–T theory was fully devel- traits that are integral to understanding the transition of oped by Dixon and Joly (1894), and remains to this day the photosynthesis from an aquatic to a terrestrial setting. Com- most parsimonious and experimentally supported explanation puter models, systematics and developmental approaches can of plant hydration. The fundamental tenet of the C–T mecha- fill some of these gaps, but the veracity of these hypotheses is nism is that the water column can sustain a very high degree of ultimately tested against fossils. tension without ‘breaking’. This phenomenon is entirely con- Thus, fossil specimens are scrutinized with much caution. sistent with the properties of water, yet so unusual that a few The majority of fossils are preserved in riverine depositional workers find the C–T mechanism disturbing. Despite recent environments, meaning that they may have travelled great controversy, the C–T mechanism has withstood vigorous distances from potentially very different habitats before experimental scrutiny and remains the most widely accepted settling permanently (Stewart & Rothwell, 1993; Taylor explanation of water movement in land plants (Pockman et al., et al., 2009). Furthermore, fragmentation can disassociate 1995; Cochard et al., 2001; Angeles et al., 2004). fragile structures such as leaves from the rest of the plant body, Water may be transpired at a high rate from the stomatal thereby obscuring relationships between various tissue sam- pores, so effective hydraulic transport must efficiently replace ples and potentially inflating species numbers. For instance, it this lost water. Failure to supply water to the shoot as quickly was not until the discovery of an intact specimen bearing both as it is lost results in the familiar phenomenon of wilting fol- wood and foliage that Archaeopteris was treated as a single lowed by damage to cell membranes and ending with death species rather than two separate genera (Beck, 1960; Meyer- (McDowell et al., 2008). Roots are a crucial component for Berthaud et al., 1999). Lastly, diagenesis, that is the chemical water entry into the plant yet for the most part, it is the aerial and physical alteration of fossil and sediment during the tissues that drive water movement, much like cut flowers in a conversion to rock, can also cause substantial changes to the vase. structure and character of a specimen (Taylor et al., 2009). The process of water transport begins when water is lost Sampling biases may affect approximations of species from the mesophyll cell walls located in the interior of the leaf. diversity in the fossil record leading to errors in estimates of Plant cell walls are a tight but porous weave of cellulose and the rates of evolution, particularly if workers focus on particu- pectin that act much like a wick. This evaporation creates lar localities or intervals. In general, if diversity is constant, capillary suction on the menisci within the cell wall pores, sampling intensity will not affect results (Raymond & Metz, causing tension to be transmitted down the water column in 1995; Tarver et al., 2007). However, evidence suggests that the xylem (Pickard, 1981). The xylem tension exists because earlier estimates of diversity of Mid-Silurian through Late the water column is engaged in a ‘tug-of-war’ between Devonian land plants may be higher than expected due to sam- adhesion to soil particles and evaporation from the leaf sur- pling bias, usually attributed to workers’ preferential interest face. This tension can also be described as a ‘negative pressure’ in one era or locality over another (Raymond & Metz, 1995). that is quantitatively referred to as the water potential (W) and Fortunately, plant vasculature is often the most abundant typically measured in Pascals (Pa) such that increasingly nega- and best preserved plant tissue. Indeed, some xylem samples tive water potentials indicate greater tension imposed on the from the earliest land plants appear as though they were water column. Because water moves down a water potential frozen in time, with little distortion to the cell structure. gradient and the water potential of the roots is more negative Remarkably, even the chemical composition of early vascular than that of the surrounding soil, water enters the roots. tissue can be discerned to the point where we can reasonably Water movement in plants is referred to as the C–T mecha- speculate about the biomechanical properties of the stem, as nism because hydrogen bonding holds the water molecules well physiological ecology of the plant (Kenrick & Crane, together and their movement is the result of the pulling action

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(i.e. tension) created by evaporation from the cell wall pores nized transition of green algae to land has been the one leading (Sperry, 2000; Tyree & Zimmermann, 2002; Taiz & Zeiger, to land plants, recent evidence indicates that the green algae 2006). have colonized terrestrial surfaces on at least a dozen separate Because transpiration is chiefly driven by sunlight, water occasions (Lewis & Lewis, 2005). Molecular clock hypotheses movement through plants is a passive and therefore cheap suggest that the first green algae may have appeared in the process that selected for low resistance, efficient transport Mid-to-Late Mesoproterozoic (1.4–1.0 billion years ago; conduits (Sperry, 2003). These are dead, empty, require little Yoon et al., 2004) but the date of their venture onto land is to no metabolic input and can provide a network that allows unclear due to poor preservation (Taylor et al., 2009). The water to reach tree canopies over 100 m in height (Koch oldest observed silicaceous or calcium carbonate remains of et al., 2004; Burgess et al., 2006; Domec et al., 2008). green algae are from the Upper Silurian (Feist et al., 2005). Underlying this transport capacity is a fundamentally simple Molecular phylogenies show high support for the two mechanism whose origins required little more than a hydro- Chlorophytic and Charophytic lineages of the green algae philic cell wall to move water by capillarity. Green algae (Lewis & McCourt, 2004; Fig. 1), and there is a general possess such a cell wall for the purpose of osmoregulation, so consensus for the placement of the Charophytic lineage as the framework for the evolutionary transition from wicking ancestral to land plants because of the high number of shared water over the surface of a cell to bulk flow within the special- derived molecular, biochemical, reproductive, developmental ized conduits of vascular plants was realized well before the and morphological traits between these groups (Graham, colonization of land (Sperry, 2003; Franks & Brodribb, 1996; Raven & Edwards, 2004). Nonetheless, the issue of 2005). In addition to the cell wall, the key innovations that which Charophytic group is most closely related to terrestrial allowed plants to maintain hydration and adequate rates of gas plants remains somewhat controversial primarily because of exchange on land were the cuticle, the stomata and the evolu- different approaches to gene and taxon sampling (Qiu et al., tion of vascular tissue. The functional significance, evolution- 2006, Qiu, 2008; McCourt et al., 2004; Gensel, 2008; see ary history and developmental elements of these traits will be also Turmel et al., 2007). addressed below. Despite the progress in elucidating the phylogenetic rela- tionships of the green algae and their affinities to land plants, the shared physiological and biochemical elements of dessica- The green algae: earth’s first land plants tion tolerance have attracted less attention (Graham & Gray, The connection between land plants and green algae (Chloro- 2001). This comes despite Raven’s early efforts to provide phyta) has been apparent since centuries before Darwin’s such a context for the evolution of Charophytes and his mis- time, and there is no doubt that embryophytic land plants are givings about the suitability of Charales to life on land based descendants of freshwater green algae (Graham, 1993; on latter group’s physiology and morphology (Raven, 1977). Graham et al., 2000; Lewis & McCourt, 2004; McCourt Perhaps, the plasticity of algal forms (Bhattacharya & Medlin, et al., 2004). Specifically, it is believed that for the Charophy- 1998), combined with the antiquity of the Charophyte tic green algae lacking bicarbonate pumps, competition for to embryophyte divergence, hopelessly complicates such a

CO2 may have been the driving force behind their venture mapping exercise (Graham & Gray, 2001) but it could onto land (Graham, 1993). Clearly, the photosynthetic nonetheless inform the plausibility of current evolutionary benefits of fourfold increased CO2 diffusivity and higher light scenarios because environmental water stress exerts some of levels outweighed the costs of exposure to UV radiation and the strongest selective pressures on terrestrial (and marine) dessication (Denny, 1993; Graham, 1993). A complete dis- biota (Yancey et al., 1982). cussion of the morphological, biochemical and reproductive Graham & Gray (2001) argue that the closest Charophytic adaptations predisposing Charophytic algae to life on land is ancestors of land plants would have been dessication-tolerant beyond the scope of this review, but excellent treatments can and occupied ephemeral, ‘variably unfavourable’ aquatic habitats. be found in Graham (1993), Graham et al. (2009), Gensel These habitats acted as sites of strong evolutionary pressures (2008) and Gensel & Edwards (2001). Because the fossil related to the effects of water deficit, and thus provided record of the green algae is fragmentary and incomplete the Charophytes with an impetus towards terrestrialization (Graham, 1993), the discussion will be limited to recent pro- (Graham & Gray, 2001). Consequently, the water status of gress regarding the algal ancestry of land plants. terrestrial Charophyceans would have fluctuated in response The green algae display a surprising array of cellular and to water availability (so-called poikilohydry), and the evolution colonial morphologies, and some species such as Chara of desiccation tolerance would have been essential in allowing braunii, may superficially resemble plants (McCourt et al., them to recover from otherwise fatal (80–90%) protoplasmic 2004). Although green algae are typically associated with water loss. Dessication tolerance is a common phenomenon aquatic ecosystems, they can also be indigenous and highly in basal plant lineages characterized by small-statured pheno- speciose elements of desert soil microbiotic communities types such as the algae, bryophytes and some ferns (Proctor & (Evans & Johansen, 1999). Although the most widely recog- Tuba, 2002). This trait has been lost, however, in more

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Fig. 1 The phylogeny of land plants in the context of palaeoclimate and clade radiations over Phanero- zoic time, updated from Sperry (2003). The graph indicates modelled atmospheric CO2 concentrations according to Berner (2006), as well as correspond- ing large-scale climatic patterns (Zachos et al., 2001; Willis & McElwain, 2002; Berner, 2005; Huey & Ward, 2005; Brezinski et al., 2008; Trotter et al., 2008). The phylogeny is from Sperry (2003) with updates from Burleigh & Mathews (2004) and Qiu (2008). Important morphological features relevant to the evolution of plant water relations are indi- cated on the phylogeny according to Sperry (2003) with several updates (Proctor, 1981; Franks & Farquhar, 2007; VanAller Hernick et al., 2008). Presence in the fossil record is denoted by thick black line. Relative tracheophyte abundances were estimated or re-drawn from Niklas (1992, 1997), Willis & McElwain (2002), Singh (2004) and Montanez et al. (2007). There is good fossil evidence to suggest that liverworts may have been present as early as the Late Ordovician (dotted line; Wellman et al., 2003). derived plants due to structural constraints that prevent the cuticle, the stomata and water-conducting tissues – allowed collapse and refilling of cells, as well as the high cost of solute plants to resolve these conflicting requirements. Of these production required to minimize drought injury to cell three traits, the cuticle is the oldest. We currently know noth- membranes and metabolic components (Beck et al., 2007). ing about the evolution of the cuticle, except that it is a syna- pomorphy of land plants, the earliest fragments of which were found in the Ordovician (Wellman et al., 2003). Neverthe- The significance of the plant cuticle less, one can neither discuss the evolution of plant homoihydry Although multicellularity reduces water loss by reducing total (that is the ability to maintain hydration over a range of exter- surface to volume ratios, it is unlikely that an algal colony nal conditions of water availability; Raven & Edwards, 2004; larger than few hundred cells could have maintained adequate Raven, 1984) nor the plant fossil record (Willis & McElwain, hydration for long periods of time without a means of restrict- 2002; Wellman et al., 2003; Taylor et al., 2009) without ing water loss, or efficiently replacing lost water. Additionally, mentioning this feature. because a water film represents a significant barrier to CO2 The 1 to 15 lm thick cuticle covers most of the aerial diffusion, such a simple multicellular arrangement may have elements of land plants where it protects the shoot from significantly constrained photosynthesis (Franks & Brodribb, herbivory, UV-induced damage and water loss (Edwards 2005). All land plants must then reconcile two opposing bio- et al., 1996; McElwain & Chaloner, 1996; Raven & Edwards, physical constraints. On the one hand, photosynthesis 2004). The cuticle is essentially a waxy layer on the external requires large surface areas to facilitate light capture and CO2 cell walls of the epidermis (Bargel et al., 2004, 2006), in diffusion, whereas on the other, water conservation favours which cutin forms the highest fraction and acts as a matrix for low surface:volume ratios. Three critical innovations – the the deposition of fatty acids, alkanes and waxes. Because the

2010 Blackwell Publishing Ltd 116 J. PITTERMANN cuticle can significantly restrict water loss, it is unlikely that mosses exhibit what appear to be proto- or pseudo-stomata the colonization of land by plants would have occurred with- but as the function of these pores in gas exchange is unclear out the evolution of this layer (Niklas, 1992; Raven & (see below; Duckett et al., 2009; Proctor, 1981), they may be Edwards, 2004). Waxes are the key constituents of the cuticle unsuitable candidates for stomatal precursors. Hence, true barrier but it is the cutin fraction that is most resilient to stomata are currently accepted to be monophyletic, with their degradation and thus best conserved in the fossil record origins in the hornworts (Raven, 2002). (Schreiber & Riederer, 1996). It is noteworthy that some Unfortunately, the fossil record is silent with regard to Charophytic algae can synthesize a wax-free extracellular layer changes in epidermal cells that may have led to the formation that may allow a limited amount of water and CO2 diffusion of stomata, but simple perforations are apparent in the cuticles (Graham, 1993; Edwards et al., 1996). of taxonomically mysterious taxa such as Spongiophyton Historically, the usefulness of fossilized cuticle lay primarily (Gensel et al., 1991) and Nematothallus from the Lower in the patterns of preserved stomatal impressions whose size, Devonian (Edwards et al., 1998; Taylor et al., 2009). These distribution and abundance are used to infer palaeo-atmo- organisms had thick cuticles, so epidermal pores would have spheric CO2 concentrations (McElwain & Chaloner, 1996; significantly reduced resistance for gaseous diffusion. Similar McElwain et al., 1999; Royer et al., 2001; Retallack, 2001; perforations found on the thalli of the extant liverwort, Kouwenberg et al., 2003). Unfortunately, cuticle thickness Conocephalum conicum probably function in gas exchange alone is a poor predictor of species’ drought tolerance because (Proctor, 1981; Raven & Edwards, 2004), but it is unlikely cuticle permeability and thickness may not be related that they exert dynamic control over water loss. Without (Edwards et al., 1996; McElwain & Chaloner, 1996). How- active regulation courtesy of the guard cells, these plants ever, emerging work has shown that cuticle alkanes record the passively and continually lose water in response to the atmo- deuterium isotope signatures (¶D) of meteoric water and can spheric vapour pressure deficit. serve as a accurate biomarkers for palaeoclimatic reconstruc- The oldest unequivocal stomatal specimens have been tion, particularly if isotopic models take into account the described from unidentified cuticle and tissue fragments from relationships between leaf wax ¶D patterns and latitude, plant the Pridoli epoch (Upper Silurian, 416–418.7 Mya, Upper form and photosynthetic pathway (Sachse et al., 2004; Liu & Silurian, Edwards et al., 1996, 1998). In these samples, the Yang, 2008). Because deuterium enrichment is also partially stomatal apparatus appears nearly circular, consisting of two controlled by transpiration and soil evaporation, n-alkanes thick guard cells that create a lenticular pore. Perhaps due to may also be useful in constraining estimates of transpiration or poor preservation and small fragment size, there is no evapotranspiration from well-preserved fossil material (Smith evidence for a substomatal chamber and in several of these & Freeman, 2006). Silurian samples, epidermal cells appear to underlie the guard cells. Small substomatal cavities are found, however, in sam- ples of pro-tracheophytes such as Rhynia gwynne-vaughanii, The evolution of stomata Aglaophyton major, Horneophyton lignieri and the lycophyte The cuticle imposes a high degree of resistance on gaseous dif- Asteroxylon mackiei from the Lower Devonian (397.5– fusion, so it must be perforated in order for CO2 to enter. 416 Mya; Edwards et al., 1998). These taxa generally have These perforations take the form of stomata, the 30- to 80-lm low stomatal frequencies, and some such as Asteroxylon have long epidermal pores that are formed by the aperture of two sunken stomata –features that are consistent with the idea that adjacent elongated guard cells and found on surfaces of most water stress was the key abiotic variable acting on early terres- photosynthetic tissue (Hetherington & Woodward, 2003; trial vegetation (Gray et al., 1985). Taylor et al., 2009). It is the turgor-mediated opening and Based on our understanding of stomatal behaviour in closing of the guard cells in response to leaf hydration, light modern taxa, it has long been accepted that the evolutionary levels, atmospheric CO2, abscissic acid and soil water availabil- pressures that drove water conservation strategies favoured ity that controls the diffusion of CO2 and water vapour the coupling of the cuticle with stomata (Raven, 2002; Franks between the leaf and the atmosphere (Davies & Zhang, 1991; & Brodribb, 2005). However, the underlying assumption Assmann & Wang, 2001; Buckley, 2005; Messinger et al., that the regulation of water loss was the impetus for the evolu- 2006; Ainsworth & Rogers, 2007). Stomatal conductance is tion of stomata (especially in early land plants) has recently tightly coupled to hydraulic transport in land plants (Jones & been challenged by Duckett et al. (2009) who argue that the Sutherland, 1991; Brodribb & Holbrook, 2004), so stomatal ‘pseudostomata’ of the Sphagnum moss evolved to facilitate evolution may have occurred closely in time with the vascular dehydration in sporophytic capsules, rather than conserve system (Kenrick & Crane, 1997; Sperry, 2003). water. In this plant, it is dehiscence and collapse of guard cells The position of stomata on the land plant phylogeny is that opens the stomatal aperture, rather than an increase in decided by the placement of ancestral taxa such as liverworts guard cell pressure, as typically observed in higher land plants. and bryophytes, the standing of which has been called into Duckett et al.’s results leave the evolution of stomata open to question (Raven, 2002). Some species of liverworts and interpretation. One could argue that stomata initially

2010 Blackwell Publishing Ltd The evolution of water transport in plants 117 appeared in mosses for the purpose of dehydration and were Lastly, increased water use efficiency may have been the subsequently adapted for gas exchange in higher plants, but driving force behind selection for presumably ‘optimized’, alternatively stomata could have evolved to facilitate gas i.e. rapid, stomatal responses of angiosperms to short-term exchange on land, but were co-opted by the mosses for the changes in CO2, relative to conifers and ferns (Brodribb purpose of dehydration. A final option is that, in Sphagnum,the et al., 2009). Considering that water use efficiency positively stomata fulfil both functions over time (Duckett et al., 2009). affects species’ reproductive output (Farris & Lechowicz, Duckett et al.’s study changes our perspective on the evo- 1990; Dudley, 1996; Ackerly et al., 2000), one could argue lution of stomata and will undoubtedly motivate future work that the evolution of stomata single-handedly provided on stomatal structure and function in modern taxa. Despite ancestral land plants with a competitive advantage, and thus the fact that stomatal design has remained fundamentally helped transform the terrestrial landscape into a three- unchanged, notable differences in size, density, shape and dimensional mosaic of vegetation, rather than a dense film of ornamentation are apparent across the major plant groups liverworts. (Ziegler, 1987; Franks & Beerling, 2009a,b). The functional significance of some of this variation apparently lies in the The transition to plant vascular tissue tempo of stomatal movements whereby the derived, dumbell- shaped stomata of grasses open and close much faster than With the cuticle and the stomata in place, the evolution of the classical kidney-shaped stomata of older lineages (Franks water-conducting cells completed the basic bauplan needed & Farquhar, 2007). The authors argue that faster response for plant homoiohydry (Raven & Edwards, 2004). What are times of graminoid stomata may have increased water-use the transitional steps from undifferentiated mesophyll cells to efficiency during the global aridification that peaked 45 to a bundle of directionally aligned hollow tubes, and what are 30 Mya, and thus conferred the grasses with a competitive the biotic and abiotic signals responsible for this pattern in the advantage. first place? Understanding vascular tissue ontogeny may Others have applied finite element analysis to explore the inform our interpretation of fossil material and its relevance to relationships between stomatal structure and function to show the evolution of xylem. that sunken stomata, a cuticular lining, small substomatal Our current outlook on the differentiation of unspecified chamber size and reduced stomatal aperture, each have the plant cells into elongated tracheary elements is shaped by potential to greatly decrease stomatal conductance (Roth-Ne- model systems such as Zinnia, Arabidopsis and Populus belsick, 2007). How variation in the size of the substomatal (Tuskan et al., 2006; Turner et al., 2007). In plants with chamber relates to stomatal size is empirically unknown, as are a meristematic, procambial region, cambial cells are pro- the consequences of this allometry for photosynthesis, but grammed to differentiate into either phloem or vascular tissue. Roth-Nebelsick’s model suggests that transpiration estimates However, under appropriate culture conditions, mesophyll based solely on fossil stomatal density and aperture size may cells can also be made to de-differentiate and develop into overestimate stomatal conductance. tracheary elements (Fig. 2). Auxin, the newly discovered xylo- Along these lines, the gas-exchange response of Rhyniophy- gen hormone and other signalling compounds control these tic plants has received considerable attention because the changes and much progress has been made in elucidating the morphological detail of their tissues is well preserved, and genetic regulation of cell differentiation (Roberts & McCann, their terrestial habit represents the beginning of the evolution 2000; Chaffey, 2002). What makes this particularly relevant in of modern plant physiology. It appears that Rhyniophytes col- an evolutionary context is that the totipotency of plant cells onized diverse habitats with variations in temperature can be so easily manipulated with the appropriate signalling (Edwards et al., 2001) and water availability due to periodic compounds, most of which are produced by neighbouring flooding (Rice et al., 2002; Trewin et al., 2003), thereby pro- cells (Nieminen et al., 2004). In other words, the design of viding the context in which the ecophysiology of these taxa even the most basic of vascular systems belonging to liver- can be examined. The cuticle of Rhyniophytic taxa is charac- worts (Ligrone & Duckett, 1996) and bryophytes (Proctor & terized by low stomatal densities suggesting that in the CO2- Tuba, 2002) required little more than the appropriate signal rich climate of the Lower Devonian, these plants would have to upregulate a suite of genes that control cell differentiation. exhibited high water-use efficiencies (Edwards et al., 1998). One of the critical steps to the formation of vascular tissue Computer simulations suggest that transpiration and photo- may have been the establishment of a polar auxin gradient synthesis were greatest in Nothia aphylla, a ‘leafy’ Rhynio- because auxin stimulates the differentiation, patterning and phyte with relatively high stomatal densities (El-Saadawy & elongation of tracheary elements (McCann, 1997; Sieburth & Lacey, 1979), when compared with the more conservative Deyholos, 2006). An auxin gradient can also arise due to Rhynia and Aglaophyton (Konrad et al., 2000; Roth-Nebel- wounding, and generate a response characterized by cell sick & Konrad, 2003). The stricter water-use strategies of the rotation in the new tissue formed near the injury (Kramer latter two taxa probably reflect the absence of a well-devel- et al., 2008). Interestingly, evidence for this rotated cell oped root system (Roth-Nebelsick & Konrad, 2003). arrangement was recently discovered in secondary vascular tis-

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Fig. 2 The differentiation of mesophyll and procambial cells into vascular conduits according to Turner et al. (2007). Different combinations of hormones may act on the procambial or mesophyll cells to initiate the formation of tracheary elements or conduits. Conduit expansion and elongation is followed by the deposition of the secondary wall and followed by cell death and digestion of cell endwalls. Lignification completes this developmental sequence. sue belonging to an Archeopteris (upper Devonian, 375 Mya; Following cell differentiation, the process of expansion is Rothwell & Lev-Yadun, 2005) as well as in wood of tree-sized driven by mechanical forces that are a function of osmotic pres- fossil equisetophytes and arborescent lycophytes belonging to surization, which in mature plant cells can generate pressures different lineages (Rothwell et al., 2008). In these plants, the ranging from 0.1 to 3 MPa (Somerville et al., 2004; Taiz & independent origins of secondary vascular tissue suggest a role Zeiger, 2006). Brassinosteroid hormones are thought to play for the parallel evolution of regulation by auxin in each clade a role in the complex co-ordination of the simultaneous expan- (Rothwell et al., 2008). sion of multiple cells, although several auxin-mediated There is evidence that vascular tissue differentiation is a enzymes acidify and loosen the fibrous, cellulose cell wall homologous phenomenon in land plants. Indeed, molecular matrix (Wang & He, 2004; Turner et al., 2007). Importantly, data indicate that auxin metabolic pathways are present in a class of proteins known as expansins regulates the loosening basal plant lineages such as the Charales, liverworts and bryo- of the cell wall (Cosgrove, 2005; Popper, 2008). Expansins phytes (Cooke et al., 2002). Of further interest are computer are not only ubiquitous across the land plant taxa, but also models showing close correspondence between predicted thought to be integral to the development of xylem and evolu- procambial vascular patterns based on theoretical input auxin tion of the plant vascular system (Popper, 2008). The genetic concentrations, and their close correspondence to actual toolbox required for cell wall expansion is present in algae, stelar patterns observed in the Early Devonian Psilophyton so the only other key innovation in the evolution of plant and several members of the pro-gymnosperm group, the vascular tissue would have been the development of the cellu- Aneurophytales (Stein, 1993). Altogether, there is growing losic secondary cell wall for increased rigidity. In plants, this sec- evidence for the contribution of auxin to the evolution of vas- ondary wall is deposited interior to the primary cell wall cular plants, and the subsequent diversification of Silurian and following cell expansion, but excluded from the vessel endwall Devonian plant lineages. and the pitted regions of the conduit that allow water to move

2010 Blackwell Publishing Ltd The evolution of water transport in plants 119 from one cell to another (Somerville et al., 2004; Choat et al., 2006; Berner et al., 2007). In the proposed sequence of

2008). events, a rise in O2 levels due to photosynthesis facilitated The rigidification of cell walls with polyphenols probably lignification, which in turn supported the evolution of occurred synchronously, or nearly so with the evolution of arborescence, further increasing photosynthetic biomass in a early plant vascular systems (see next section). Developmen- feedforward cycle. Interestingly, some would argue that lignin tally, the deposition of lignin or its precursors such as lignan is not even a prerequisite for conferring stiffness to the plant into the cellulose, pectin and protein wall matrix of the sec- body per se and is merely a secondary requirement for arbores- ondary wall is the final step towards increasing the stiffness cence because non-lignified tissues can impart rigidity to the and compressive resistance of the conducting cell as well as its plant body (Rowe & Speck, 2004), thereby eliminating the impermeamility to water (Niklas, 1992; Lewis, 1999; Koehler necessity for the role of oxygen in the first place. However, lig- & Telewski, 2006). For example, Arabidopsis and Nicotiana nin is essential to preventing cell implosion at the negative mutants with disrupted lignin synthesis not only exhibit mal- water potentials that can occur at the tops of trees as a result of formed vasculature, but also show a high frequency of gravity (Koch et al., 2004; Domec et al., 2008), so modern crimped or collapsed conduits (Turner & Somerville, 1997; trees would probably have not evolved beyond a height of Piquemal et al., 1998; Jones et al., 2001). 5 m without this phenolic (Niklas, 1992). It is unlikely that The complex genetic and chemical components of lignifica- selection would favour a combination of weak xylem and non- tion have been identified (Boerjan et al., 2003; Peter & Neale, lignifed support tissue when the economy of modern wood 2004) so a solid grasp of the functional implications of the yields higher dividends courtesy of simultaneous canopy process on plant hydraulics is in the near future. Recently, 12 support and water transport. Whether O2 facilitated this genes were targeted as the probable candidates of vascular lig- streamlining of plant form and function cannot be directly nification in Arabidopsis (Raes et al., 2003) whereas the Black tested, but a quantitative model, although limited, may Cottonwood genome-sequencing project uncovered a high provide us with useful insights. number of gene families responsible for ligno-cellulosic wall formation (Tuskan et al., 2006). However, the genetics of The transport advantages of conducting tissue herbaceous model systems such as those of Arabidopsis and Zinnia are easily manipulated (McCann, 1997; Roberts & With the basic blueprint for the vascular network in place, the McCann, 2000) so, at this point in time, we know more about next step in the evolution of xylem was to maximize the trans- tracheary element formation from these plants than from port gains of this low resistance pathway. Indeed, the need to woody taxa. Interestingly, evidence from the Zinnia model of reliably move water and solutes throughout the plant body tracheary element formation suggests that lignification follows selected for the evolution of vascular tissue in even the most cell death, which means that surrounding parenchyma tissue primitive plants such as liverworts (Ligrone & Duckett, 1996; may be responsible for the synthesis and release of lignin VanAller Hernick et al., 2008). Furthermore, the near simul- precursors (Turner et al., 2007). Certainly, once the digestion taneous appearance of vascular systems and stomata during of cell contents begins, cell growth has ceased so lignin depo- the Mid-Silurian suggests that selection not only favoured the sition is the logical, final stage of creating a functioning, but functional coupling between these traits (Sperry, 2003; Raven dead water-filled xylem conduit. & Edwards, 2004), but also their co-ordinated optimization Lignins were generally thought to be absent from the algae, to maximize photosynthesis (Brodribb, 2009). but the cell walls of the Charophyte Coleochaete were found to The frictional resistance to water transport is significantly contain lignin-like compounds, adding further support for reduced when water travels through microscopic, hollow their close association with land plants (Delwiche et al., channels rather than the nanoscopic pathways that character- 1989). True lignin was recently discovered in the flexible, ize symplastic water movement. Not surprisingly, water joint-like tissue, the red algae Calliarthron, prompting the transport through elongated, hollow single cells is 106 times suggestion that lignin biosynthetic pathways may have had an more efficient than transport through parenchymal tissue via early function in biomechanics, in addition to protecting cells plasmodesmatal channels (Raven, 1977). Similarly, ectohydric from microbial attack and UV damage (Martone et al., 2009; water transport, which describes the wicking of water through see also Niklas, 1992). Both studies indicate that the funda- external capillary structures, is common in both terrestrial mental pathways of lignin biosynthesis are deeply conserved, Charophycean algae and bryophytes (Proctor & Tuba, 2002; so the lignification of xylem was essentially a function of time Franks & Brodribb, 2005) but is insufficient for taller plants. and increased tissue specificity. Both pathways present such high degrees of resistance that On a final note, the biosynthesis of lignin is dependent on plants exclusively relying on non-vascular water transport oxygen, leading some workers to speculate that elevated O2 rarely exceed heights of a few centimetres and are typically produced by the abundant land plants during the Mid-Devo- poikilohydric (Niklas, 1992; Proctor & Tuba, 2002). nian to the Early Carboniferous, may have spurred the evolu- The hydraulic advantage of wide, hollow conduits over nar- tion of xylem lignification (Graham et al., 1995; Berner, row channels is evident in the context of the Hagen–Poiseuille

2010 Blackwell Publishing Ltd 120 J. PITTERMANN equation, which predicts water-transport efficiency through Fig. 4) to the nearly 500-lm wide vessels of extant tropical smooth-walled capillaries. Here, the flow rate of water, Q, vines and lianas (Ewers, 1985). with a viscosity g, passing through a capillary with a diameter of D is proportional to the pressure gradient dP ⁄ dx driving PART II: VASCULAR PLANTS IN THE FOSSIL the flow such that, RECORD pD4 dP Q ¼ : ð1Þ 128g dx Conducting tissue in protracheophytes and early vascular plants Equation 1 demonstrates that hydraulic efficiency is propor- tional to the conduit diameter raised to the fourth power, so a The Late Silurian to the Early Devonian represent a period of modest increase in conduit diameter leads to significant gains remarkable terrestrial plant speciation as well as exploration of in transport (Tyree et al., 1994; Tyree & Zimmermann, different forms of vascular structure. Geochemically based

2002). Single conduit measurements of hydraulic efficiency models suggest that elevated atmospheric CO2 coupled with agree with the predictions of the Hagen–Poiseuille equation 2–4 C warmer sea surface temperatures characterized the (Zwieniecki et al., 2001). Functionally, this means that all else climate during this initial phase of plant diversification (Berner, being equal, 16 conduits with a 20-lm diameter are required 2006; Came et al., 2007). Some of the extinct taxa from this to achieve the hydraulic efficiency of one 40-lm vessel period may well be the ancestors of certain bryophytic lineages (Fig. 3). or true vascular land plants, while others were early experi- The higher area-specific conductivity of larger conduits ments in the homoihydric lifestyle. The most well-studied confers several advantages, an important one being that a (though neither the oldest nor most ancestral) plants of this plant can invest less carbon in transport tissue, particularly as period are from the Early Devonian Rhynie Chert (398– the conduits are dead. Secondly, the lower transport resistance 396 Mya). This group has traditionally occupied the position associated with large conduits reduces the pressure drop that of the simplest vascular plants but this perspective has changed is required to move water from the roots to the leaves. Very as it became clear that Rhyniophytes share features of both negative water potentials can predispose the xylem to dysfunc- bryophytes and vascular plants (Kenrick & Crane, 1997; tion (see Part III) and stress the leaf tissue, both of which can Taylor et al., 2009). Kenrick & Crane (1997) provide the most lead to reductions in gas exchange. Lastly, high transport widely accepted cladistic treatment of the evolution of early efficiencies characteristic of xylem with large conduits can sup- land plants, using among other character traits, the anatomy of port increased transpiration rates, which in turn allow higher vascular tissue to decide placement on the phylogeny. What rates of photosynthesis (Brodribb & Feild, 2000; Brodribb emerges is a trend towards xylem comprised of progressively et al., 2002; Santiago et al., 2004). Predictably, plants have larger tracheids with an increasingly complex and mechanically exploited the relationship between diameter and efficiency robust wall anatomy (Kenrick & Crane, 1991, 1997; Edwards, such that there has been a 60-fold increase in conduit diame- 2003; Taylor et al., 2009) presumably reflecting selection for ter since the evolution of the early 5- to 8-lm wide Cooksonian efficient vascular transport and conduit support under negative tracheids from the upper Silurian (416 Mya; Niklas, 1992; xylem pressures. The evolution of angiosperm vessels and

Fig. 3 All else being equal, 16 conduits (vessels) with a 20-lm diameter (A: Populus sp., diffuse- porous wood) are required to achieve the hydraulic efficiency of one 40-lm diameter conduits (B: AB Quercus sp., ring-porous wood). Note that the vessels are embedded in a matrix of fibres.

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Fig. 4 Tracheid diameters increased almost 18-fold from 8 lm during the Upper Silurian, to a maximum of 140 lm in the Upper Devonian (Niklas, 1985; courtesy of Blackwell Publishing) representing substantial gains in hydraulic efficiency.

fibres for water transport and support respectively represents confirm that vascular tissue may have been present in this the pinnacle of vascular specialization in woody plants. Infor- extinct species, although the authors do not discuss this possi- mative photographs and detailed commentary of the taxa bility (VanAller Hernick et al., 2008; Fig. 5). It is not unlikely described in this section can be found in Taylor et al. (2009), however, that M. sharonae may represent one of the earliest Edwards (2003), Kenrick & Crane (1991), Stewart & Roth- experiments in the design of transport tissue as both the well (1993) and Kenrick & Crane (1997). extant Symphyogyna and this fossil liverwort are ascribed to the Liverworts occupy the basal position in the land plant phy- order Metzgeriales. logeny so the nearest analogue to the most primitive form of The oldest macrofossil vascular land plants are the cookson- vascular tissue probably resides in the gametophyte of the ioids of the Mid-Silurian (Wenlockian, 428–422 Mya) repre- extant, stomatalless liverwort Symphyogyna brasiliensis and its sented by Cooksonia (Edwards & Feehan, 1980), and similar relatives in the Pallaviciniineae. Non-lignified, elongate water- fossils such as Tortilicaulis (Edwards, 1996; Bateman et al., conducting cells with thickened secondary walls are packed 1998; Boyce, 2008). Early land plants from the Silurian and together in the central regions of Symphyogyna’s thallus in Early Devonian form a diverse group with nebulous evolu- what may ostensibly be the most primitive vascular bundle. tionary affinities, but currently accepted hypotheses suggest Water travels from one cell to another via plasmodesmatal that, despite its antiquity in the fossil record, Cooksonia is pores and perforated, primary wall regions along the length of derived from the protracheophytes, and belongs between the the cell (Ligrone & Duckett, 1996; Ligrone et al., 2000). rhyniopsids and the lycophytes (Kenrick & Crane, 1997). Close examination of the recently discovered fossil liverwort Efforts to confidently place Cooksonia on the land plant phy- Metzgeriothallus sharonae (Mid-Devonian, 390 Mya) could logeny are also hampered by limited and partially preserved

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Fig. 5 Fossils of the liverwort, Metzgeriothallus sharonae from the Middle Devonian of eastern New York, USA (VanAller Hernick et al., 2008; courtesy of Elsevier Press). A single vein is evident in each lobe of the gametophyte thallus (A: 10· mag- nification). The elongate cells present in the vein closely resemble vascular tissue (B: 120· magnifica- ABtion). fossil material which may or may not actually by Cooksonia in stele), parenchyma with intercellular air spaces, a cuticle and the strict sense (Boyce, 2008). stomata (Edwards et al., 1998; Taylor et al., 2009). Aglaophy- Cooksonioids were probably only a few centimetres tall, ton’s conducting tissue is composed of smooth, thin and with erect, bifurcating axial stems that ranged in diameter thick-walled cells of variable diameter (18–50 lm; Edwards, from <100 lm to 1.5 mm (Boyce, 2008). Lacking roots 2003) and is understood to be much more primitive than that and leaves, the shoots of these simple plants terminated in of Cooksonia. Indeed, this is one of several reasons why Aglao- sporangia. Although Cooksonia is accepted as the first phyton is placed with the protracheophytes, a group more clo- vascular plant (Taylor et al., 2009), the actual contribution sely allied with the mosses rather than true vascular plants of the limited vascular tissue to water transport is question- (Edwards, 1986; Kenrick & Crane, 1997; Edwards, 2003). able because the conduits are so narrow (<5 lm; Boyce, Similarly, Horneophyton lignieri, an abundant and well-docu- 2008). Close examination has shown that the conduits of mented 20-cm tall species from the Rhynie Chert, has also Cooksonia pertonii exhibit thick annual and spiral wall rings, been grouped with the protracheophytes (Kenrick & Crane, when compared with the thinner primary wall thickenings 1997; Wellman et al., 2004). found in modern protoxylem (Edwards, 2003). These rings The tracheids of more advanced rhynioids such as Senni- rigidify an otherwise highly perforated and what appears to caulis, Stockmanesella, Huvenia, Sciadophyton and Rhynia be a mechanically weak conduit wall. Despite their small gwynne-vaughanii are typically <25 lm in diameter, and size, Cooksonia’s conduits may have adequately delivered reveal increasing complexity and ornamentation in the form water to axial tissues in order to maintain the necessary of helical thickenings and spongy tissue layers (Kenrick & turgor pressure for an erect stature (Bateman et al., Crane, 1991; Edwards, 2003; Taylor et al., 2009). These 1998). Cooksonia possessed stomata, but they were low in plants represent the first tracheophytes (Kenrick & Crane, frequency and occurred primarily in the vicinity of the 1997). The so-called G- and P-type tracheids found in eutra- sporangia, prompting the suggestion that their role was to cheophytes and euphyllophytes respectively, range from 30 to facilitate nutrient transport via transpiration-driven water 80 lm in diameter and may exhibit scalariform (ladder-like)

flow rather than increase CO2 diffusion for photosynthesis pitting and a decay-resistant inner layer that covers the pit (Edwards et al., 1996, 1998; Boyce, 2008). apertures (Kenrick & Crane, 1991, 1997; Edwards, 2003). At The younger, more derived flora of the famous Rhynie first glance, the P-tracheid xylem of the euphyllophyte Chert has provided an abundance of specimens that reveal the Psilophyton resembles that of ferns, thereby representing the diversity of conducting tissues in early land plants (Taylor most modern conduit anatomy of Lower Devonian taxa. et al., 2009). The cherts, which were formed in a hot-spring Taken together, the general impression from the fossil environment, preserve a terrestrial and freshwater floodplain record is that vascular tissue in the earliest land plants became habitat containing numerous species of early land plants (Rice progressively more efficient due to selection for larger lumen et al., 2002; Trewin et al., 2003). Of these, one the best diameters. Simultaneously, tracheids became increasingly understood is Aglaophyton major, an 18-cm tall plant consist- more robust as evidenced by the helical and annular thicken- ing of bifurcating, stomatiferous, cylindrical axes that lie ings in S- and G-type tracheids, relative to the smooth, thin- loosely on the substrate surface and function as rhizomes walled conduits of Aglaophyton. Such fortified conduits would (Taylor et al., 2009). Aglaophyton lacked a root system and have withstood the negative xylem pressures associated with leaves, but possessed a central bundle of vascular tissue (proto- water stress, rather than collapsed. Implosion-resistant, and

2010 Blackwell Publishing Ltd The evolution of water transport in plants 123 perhaps to some extent lignified vasculature may have allowed Zimmermann, 2002; Pittermann et al., 2006a). According Early Devonian taxa to exploit periodically drier environ- to the classic scenario of Bailey & Tupper (1918) the subse- ments. Concurrently, increased perforation of the conduit quent evolution of tracheids into the fibres and vessel walls allowed water to move from one conduit to another, elements of angiosperm xylem capitalized on the functional which not only increased transport efficiency, but also main- specialization of each cell type. Fibres are short and thick- tained transport continuity should one or several conduits walled, providing the necessary strength for increasingly become dysfunctional. lateral canopies while the large vessel elements reduce True tracheids are a key synapomorphy of the tracheophytic resistance to water transport. land plants, but the first appearance of lignin in the vascular Not surprisingly, competition for light and the need for plant fossil record is equivocal (Friedman & Cook, 2000; Boy- effective spore dispersal prompted the evolution of arbores- ce et al., 2002). However, the recent use of novel micro-ana- cence (Niklas, 1985, 1992; Mosbrugger, 1990), well before lytical techniques to analyse fossil material has lead to the appearance of secondary xylem, that is wood. In fact, the breakthroughs in our understanding of lignification and thus evolution of secondary xylem is not even a requirement for the structure and function of tracheophytes from both fossil elevated canopies assuming that other tissues such as a and extant lineages. Specifically, soft X-ray carbon spectromi- hypodermal sterome, thick external periderm or cortex tissue croscopy combined with isotope ratio mass spectrometry has provide structural support (Niklas, 1997; Rowe & Speck, proved useful in analysing the wall chemistry of conducting 2004, 2005). This means that during the Devonian, the tree tissues belonging to fossil plant material (Boyce et al., 2002, habit was free to arise independently and more or less 2003). Because lignin has a carbon isotopic signal that is 4&– simultaneously in ferns, lepidophytes, horsetails and progym- 8& lighter than cellulose within the same plant, it is possible nosperms (Mosbrugger, 1990). to test for tissue lignification by comparing the 13C signal of Modern and extinct tree ferns lack secondary xylem so taphonomically equivalent fossils that possess lignified tissue structural support comes from abundant schlerenchymatous with those whose tissue chemistry is unknown. Concurrent X- (i.e. lignifed) fibres, support roots, numerous thin axes and ray spectroscopy can identify the presence of aromatic carbon other plant matter that makes up the false trunk (Mosbrugger, compounds that are characteristic of lignin. 1990; Taylor et al., 2009). The Mid-Cretaceous fern, Temp- These microanalytical techniques allowed Boyce et al. skya is a good example of this strategy as its main axis looks dis- (2003) to demonstrate that the vascular strand of Aglaophyton proportionately large relative to the size of the emerging major lacked lignified water-conducting cells unlike the ring fronds due to the accumulation of roots, fibres and plant deb- of lignified fibrous cells just beneath the epidermis. These ris (Taylor et al., 2009). Modern ferns, such as those in the fibres probably served a mechanical function that rigidified genera Dicksonia and Cyathea rarely exceed heights of 10 m, Aglaophyton’s narrow, cortex-filled stems (Bateman et al., but the reasons for this height limit have not been examined. 1998; Boyce et al., 2003). By contrast, more derived taxa such Buckling is unlikely to occur given the compressive strength as Rhynia gwynne-vaughnii exhibited lightly lignified xylem, of fern trunks (Mosbrugger, 1990; Niklas, 1997). Although with significant lignification evident in the tracheids of Aste- hydraulic limits in ferns may arise from limited conduit size roxylon mackiei (see also Kenrick & Crane, 1991). The greater and conduit density (Gibson et al., 1984) it may be that there xylem fraction, and perhaps to some degree, the greater stiff- is little to gain by growing tall in a light-limited environment ness afforded to taxa with progressively more lignified tissue is already dominated by tall angiosperms with expansive cano- consistent with Rhynia’s and Asteroxylon’s tendency towards pies. increased height and horizontal branching (Boyce et al., The evolution of the vascular cambium (the axial meristem 2003). New methods, such as X-ray carbon spectromicrosco- that gives rise to secondary xylem) relaxed the restrictions on py, are exciting and may offer greater insight into the hydraulic axial height and girth imposed by primary xylem. Fossil and mechanical properties of the first vascular plants, particu- evidence suggests that the vascular cambium originated early larly those with equivocal phylogenetic affinities. in the evolution of land plants and may have evolved in response to strong selective pressure for increased plant size. The primitive progymnosperm group Aneurophytales were Vascular tissue in advanced land plants the first to show limited secondary xylem by the Mid-Devo- For nearly 300 million years, tracheid-based xylem remained nian, but by the Late Devonian, secondary xylem was present the most prevalent transport tissue in the plant kingdom. in representatives of nearly all major plant groups including The ornate tracheids of the Early Devonian tracheophytes Lepidodendrales, horsetails, seed ferns, progymnosperms and eventually led to the hydraulically efficient, large-diameter, perhaps even in the Cladoxylopsids (fern affiliates), although scalariform tracheids of more derived groups such as the the vascular patterns of these fern allies are highly variable even horsetails and ferns, and eventually to the thick-walled within a specimen (Niklas, 1997; Taylor et al., 2009). tracheids that provided a biomechanical and a transport func- Of the three types of vascular cambia that evolved in plants, tion in progymnosperms, gingkos and conifers (Tyree & the bifacial and monocot ‘etagen’ cambia are present in mod-

2010 Blackwell Publishing Ltd 124 J. PITTERMANN ern taxa, while the unifacial vascular cambium disappeared all modern trees. As its name implies, the bifacial cambium after the Late Devonian (Esau, 1943; Niklas, 1997). The produces secondary xylem towards the inside of the stem axis, unifacial vascular cambium was present in Sphenophyllum and phloem to the outside. Its primary advantage lies in the (relatives of horsetails), and Sigillaria and Lepidodendron, capacity of the cambial initials to divide both anticlinally and both representatives of Carboniferous arborescent Lycopods periclinally such that each year, new cells are added in a man- (Thomas & Watson, 1976; Taylor et al., 2009). Lepidodon- ner that allows for the indeterminate expansion of the stem dron was a dominant element of the swampy Carboniferous axis as well as the addition of branches. Of the two cambial landscape, whereas Sigillaria may have occupied drier sites strategies discussed thus far, selection has favoured the bifacial (Phillips & DiMichele, 1992; Stewart & Rothwell, 1993; vascular cambium because it successfully combines water Taylor et al., 2009). Because the unifacial cambium was transport with mechanical support of the canopy (Rowe & capable of only producing new xylem cells to the interior of Speck, 2004, 2005). the main axis (periclinal division), and unable to divide radially The monocot ‘etagen’ cambium is recently derived in the to generate new cambial initial cells (anticlinal division), the angiosperm monocots (Lower Cretaceous; Herendeen & girth of these plants was thought to be determinate and Crane, 1995) and produces lignified fibres in well-ordered, established early in their development by a large number of discrete vascular bundles containing both xylem and phloem fusiform initials (Eggert, 1961; Cichan, 1985a,b). Conse- (Esau, 1943; Rudall, 1995; Tomlinson, 2006). There is no quently, lateral expansion of the secondary xylem as well as the secondary xylem in monocots. Arborescent monocots such as stem axis in Sphenophyllum and the tree like Lycopods could palms are unusual in the plant world because most of the stem only be achieved by the progressive, centrifugal enlargement volume is occupied by primary vascular tissue that is thought of the cambial initials rather than an increase in the number to remain fully functional over the life of the plant (Tyree & cambial cells (Cichan, 1985a,b). Zimmermann, 2002; Tomlinson, 2006). Despite the limited cambial expansion of these early trees, On the whole, the evolutionary trajectory of plant vascular they often reached heights of 40 m and their basal diameters systems has selected for some combination of increasing exceeded 2 m. Reconstructions suggest that Sigillaria and hydraulic efficiency and biomechanical support. The evalua- Lepidodendron were characterized by vertical, monopodial tion of Murray’s law in the context of different wood types axes that lacked side-branches but terminated in a large, pro- now serves as a classic example of the support structure versus fusely branched crown of leafy twigs (Phillips & DiMichele, hydraulic efficiency trade-off. Murray’s law was originally 1992; Taylor et al., 2009). With greater height, girth and leaf developed for cardiovascular design, and states that for a fixed area presumably became a higher demand for water. The investment in blood and vessel volume, the optimal transport increased length and diameter of the lateral tracheids (25 mm arrangement equalizes the sum of conduit radii cubed along long, 120 lm diameter) relative to the central tracheids the flow path. Interestingly, this axiom also applies to vascular (14 mm long, 85 lm diameter) of the main axis (Cichan, plants but only if the support requirement is entirely separate 1985a,b) may have adequately supplied this demand, albeit in from the transport function, as in the xylem of leaves, ring- a limited capacity. Simple predictions using the Hagen– porous species (see Fig. 3), vines and some ferns (McCulloh Poiseuille equation suggest that hydraulic transport in the et al., 2003; McCulloh & Sperry, 2005). Significant deviation periphery of a Lepidodendron stem may have been over four- from Murray’s law occurs when vascular tissue increasingly fold higher (on a cell basis) than in the interior of the axis. performs a structural function, as in the case of conifers However, the trunks of arborescent lycopods contained a (McCulloh et al., 2004). Murray’s law has not been evaluated high fraction of cortex tissue (Mosbrugger, 1990), so a deter- in extinct taxa such as the Sphenophyllum or Lepidodenron, but minate meristem producing only a limited amount of xylem it is unlikely that the unifacial cambium compromised the may have been the transport bottleneck failing to deliver water transport in tissue that was largely decoupled from can- enough water to both maintain turgor and support gas opy support. In other words, transport efficiency is likely to exchange during drought. This is consistent with the idea have selected for adherence to Murray’s law even in morpho- that arborescent lycopods disappeared in response to a drier logically complex, although extinct taxa, but this hypothesis climate in the Late Carboniferous (Phillips & DiMichele, remains to be tested. 1992). Concurrently, the apparent developmental inflexibility Because the structural and hydraulic performance of fossil of the unifacial cambium may have limited structural diversity taxa is impossible to examine directly, the remaining option is and branching, which also would have placed these early trees to uncover the biophysical priciples that underlie modern at a competitive disadvantage for resources and perhaps con- plant structure and function, and to apply them to ancient tributed to their demise (Rowe & Speck, 2005). Alas, this taxa, or towards models of new morphologies. Indeed, the ‘nascent innovation’ was successful for only 50 million years. theoretical approach has yielded a vast array of spectacularly By constrast, the bifacial vascular cambium first character- diverse, yet realistic plant ‘morphospace’ that accurately ized by the Mid-Devonian progymnosperms Archaeopteris describes both modern and fossil flora (Niklas, 1997, 2004). (Beck, 1960, 1970; Meyer-Berthaud et al., 1999) is found in Because the plant vascular system reflects the overall construc-

2010 Blackwell Publishing Ltd The evolution of water transport in plants 125 tion of a broad array of plant life forms including herbaceous, thought to reflect a more optimized vascular strategy that cap- woody, lianecescent and mococot plants, we can utilize the italizes on the division of labour to efficiently deliver water structure–function relationships of modern xylem to generate through the vessels and while relegating storage and mechani- reasonable hypotheses about the physiology and habitat of cal requirements to the fibres. ancient plants. In conifers as well as in angiosperms, water moves from one conduit to another via perforations in the cell wall, also known as bordered pits (Fig. 6; Choat et al., 2008). These pits are PART III: THE FUNCTIONAL ANATOMY OF composed of a water-permeable, cellulosic pit membrane that MODERN PLANT VASCULAR TISSUE – THE is surrounded on either side by the overarching secondary cell HYDRAULIC TRADE-OFFS OF RESISTANCE TO wall, the pit border. The perforated cell wall provides an aper- ABIOTIC STRESS ture through which water can pass from one conduit to A good grasp of anatomy is useful to correctly interpret the another through the pit membrane. relationships between xylem structure and function. This is Significant progress has been made in our understanding of because the transport characteristics of the xylem impose the evolution of xylem structure and function, and the trade- physical constraints on the rate at which water can be supplied offs that accompany pit structure, conduit length and conduit to the leaves, and on the maximum transpiration rates allowed diameter in conifers and angiosperms (Tyree et al., 1994; by stomata (Tyree & Sperry, 1989; Sperry et al., 1998; Comstock & Sperry, 2000; Sperry et al., 2006). Specifically, Brodribb, 2009). The following discussion will focus on we now have a quantitative grasp of the functional conse- conifers and woody angiosperms simply because most vascular quences of wood bearing either vessels or tracheids, and are in structure function work has been performed on woody better position to consider the vascular performance of fossil species. However, there is no apparent reason why the plants. principles derived from this research should not apply equally It is intuitive that conduit lumen diameter and conduit well to non-woody plants. length highly impact conducting efficiency and that as such, selection has favoured the evolution of larger conduits (Fig. 4). Indeed, this perspective has been emphasized in the The structure of conifer and angiosperm xylem literature effectively arguing that angiosperm wood, with its Conifer wood is homogenous, meaning that it is composed longer and wider vessels, is inherently more hydraulically entirely of overlapping individual cells referred to as tracheids. efficient that the homoxylous, tracheid-based wood of coni- Modern conifer tracheids range in size from about 0.5 to fers (Tyree & Zimmermann, 2002). Broadly speaking, the nearly 4 mm in length and 8–80 lm in diameter (Panshin & hydraulic properties of both plant forms are thought to have de Zeeuw, 1980; Pittermann & Sperry, 2003; Pittermann significant implications for their resource competition, fitness et al., 2006a) and their size depends on, among other factors, and ecological dominance (Bond, 1989). However, this their location within the tree and whether or not they function perspective has recently shifted because on closer inspection, in supporting the canopy. In general, root tracheids tend to the transport issue is not just one of conduit volume but of be longer and wider with thinner conduit walls rather than overall conduit structure: aside from length, the biggest differ- stem tracheids (Pittermann et al., 2006b). This is because ence between vessels and tracheids resides in the endwalls of root tissue is optimized for the delivery of water to the canopy these conduits where the interconduit pits are located. whereas stem tissue must compromise between water trans- Conifers possess intertracheid pits that are composed of port and structural support (Sperry et al., 2006; Pittermann two distinct regions: the outer margo region is rather porous et al., 2006a,b). with micron-scale openings and thus offers minimal resistance Angiosperm xylem is slightly more complex than that of to water flow whereas the inner, thickened torus region is conifers and exhibits a greater capacity for variation. Water impermeable. By contrast, the intervessel pit membranes of transport occurs through multicellular conduits known as ves- angiosperms are composed of a homogenous, tightly woven sels. Vessels are composed of two or more single-celled vessel mesh of microfibrils. Pore sizes range from 5 to 420 nm and elements that are stacked one on top of the other to form an the membrane lacks a central thickening (Choat et al., 2008). elongated tube that may be up to 0.5 mm in diameter and The functional ramifications of this differing pit structure on 2 m in length. Unlike in the tracheids, the distal regions of the water transport are profound because the pit resistance to individual vessel elements (known as endwalls) are digested water flow is almost 60· lower in conifer pit membranes ) away either entirely, or in a scalariform pattern with the (6 ± 1 MPa s m 1) than in those of angiosperms ) end-result resembling an elongated pipe that offers a low resis- (336 ±81 MPa s m 1). This reduction in pit resistance is tance pathway for water movement from the root to the can- equivalent to an almost eightfold increase in tracheid length, opy (Ewers, 1985; Schulte & Castle, 1993; Ellerby & Ennos, and thus hydraulically compensates for the otherwise 1998). The vessels are embedded in a matrix of short, thick- increased resistance that would be associated with greater walled fibres (Fig. 3). Consequently, angiosperm xylem is number of endwall crossings due to short tracheids. By

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Fig. 6 A diagram describing the events of freeze– thaw and air-seeding cavitation in conifers (see text). Shaded tracheids are water filled and under

negative xylem pressure (PX), clear tracheids are air

filled and at atmospheric pressure (P0). In functional tracheids, the thickened torus region of the pit membrane is centrally located within the pit cham- ber. When a neighbouring tracheid is air-filled, the pit membrane deflects against the pit border and the torus is pressed against the pit aperture, thereby isolating the dysfunctional tracheid. Air seeding occurs when the torus becomes dislodged from its sealing position. In angiosperms, air seeding occurs through the largest pore in the deflected, homoge- nous pit membrane (see Choat et al., 2008 for details). contrast, the greater length of the angiosperm vessel counter- vesselless angiosperms show hydraulic conductivities that are acts the increased hydraulic resistance offered by the homoge- much higher than predicted, and surprisingly similar to the nous pit membrane. The end result is that conifer and xylem conductivities of conifers (Hacke et al., 2007). angiosperm xylem exhibits similar hydraulic efficiency at an How can we employ these structure–function relationships equivalent conduit diameter (Pittermann et al., 2005; Sperry in the context of plant palaeo-physiology? Xylem is preserved et al., 2006). extremely well in the fossil record so it is possible with good The ancestral condition of tracheid-based wood relies on sampling and sectioning techniques to re-construct hydraulic homogenous pit membranes rather than the more efficient transport in extinct taxa, or at the very least get a sense of it. torus–margo arrangement for the interconduit flow of water. However, it is important to acknowledge the implicit assump- This suggests that these ancestral tracheids may have been up tion here, which is that xylem structure–function relationships to 38-fold less efficient than tracheids of equivalent size that have been conserved over time. This is doubtful because many bear the more derived torus–margo membrane arrangement extinct taxa combine suites of vascular traits that have no living (Sperry et al., 2006). Furthermore, it has been shown that analogue. Archaeopteris, the Devonian pro-gymnosperm is across a broad sampling of conifers and angiosperms, the end- just such a case because its xylem employs tracheids with an wall contribution to conduit resistance is 64 ± 4% and unusual clustered arrangement of intertracheid pits that lack a 56 ± 2% in conifer tracheids and eudicot vessels respectively torus–margo membrane (Beck, 1970; Meyer-Berthaud et al., (Wheeler et al., 2005; Pittermann et al., 2006b). Since 1999; Taylor et al., 2009). Although it is currently impossible cycads, ferns and the basal vesselless angiosperms possess to directly measure hydraulic efficiency in fossil xylem, it is tracheids without a torus–margo pit membrane, how does pit possible to construct and test a scaled, physical model much in resistance scale with lumen resistance in these more primitive the way that Lancashire & Ennos (2002) used glycerine and taxa? So far, this has only been examined across a broad toy truck tyres to evaluate the resistance of interconduit pits. sampling of vesselless angiosperms. Interestingly, vesselless Perhaps the most simplistic way of retrodicting water- angiosperms exhibit pit resistances that are much closer to transport efficiency is to use the Hagen–Poiseuille relation- )1 those of conifers than angiosperms (16 ± 2 MPa s m ) ship to calculate the lumen conductivity (ks) on a xylem area despite having a homogenous membrane (Hacke et al., (A) basis, 2007). On average, pit resistance accounted for 77 ± 2% of P p D4 the total vessel hydraulic resistance. Scanning electron ks ¼ ; ð2Þ A128g microscopy revealed that these pit membranes are much more porous than those of eudicots, thereby presenting a relatively where A is the area represented by the sum of D4 or the total lower resistance to water transport. Consequently, the xylem area. It is important to keep in mind that scalariform

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perforation plates in vessels, as well as interconduit pits reduce hydraulic resistance (RCA,thatis1⁄ K) into its constituent the actual conductivity by well over 40% of what the Hagen– resistances, those being the conduit lumen resistance (RL)

Poiseuille relationship predicts (see discussion above, Sperry and the endwall resistance (RW) not unlike resistors in series et al., 2006; Schulte & Castle, 1993). Similarly, the helical (eqn 4; for model details, see Lancashire & Ennos, 2002; and annular thickenings found in the protoxylem of extant Sperry & Hacke, 2004; Pittermann et al., 2006a,b; Wilson plants, and the tracheids of Cooksonia and Sennicaulis can et al., 2008). reduce the effective diameter of the conduits, and thus reduce RW ¼ RL þ RW; ð4Þ ks (Jeje & Zimmermann, 1979). The endwall resistance can be broken down into The Hagen–Poiseuille method may be most readily applica- 2R ble in a broadly comparative study of well-classified plants that R ¼ pit ; ð5Þ W N fall clearly into either the woody coniferous or woody angio- pits sperm category, where we can assume that pit membranes are where Npits represents the number of pits per endwall. Pit likely to constitute a fraction of hydraulic resistance that is resistance, Rpit is described by the addition of the pit aperture comparable to their living relatives. However, equation 2 can and pit membrane resistances, both of which can be separated also be applied to taxa where pit membranes have not broadly into their constituents including the porosity of the pit been examined such as in the cycads and ferns, but with much membrane, the size of the pit membrane pores, the thickness less certainty. For example, Calkin et al. (1986) determined of the membrane microfibrils, and the depth and width of the that digestion of pit membranes with cellulase increased pit aperture (described in detail in Sperry & Hacke, 2004; hydraulic conductivity by 66% in Pteris vittata. Modelling fern Wilson et al., 2008). xylem may be challenging particularly in taxa that harbour ves- Lastly, the inverse of the Hagen–Poiseuille equation esti- sels in addition to the more commonly observed tracheids mates flow across half of a tube’s length, (Carlquist & Schneider, 2007). 64gL However, another interesting exercise is to model fluid flow R ¼ ; ð6Þ L pD4 in extinct taxa with xylem anatomy that is no longer found in where L represents tracheid length. modern plants. Cichan (1986) was one of the first to recog- Wilson et al. (2008) applied a more complete version of nize the value of this approach, and thus applied the Hagen– the above model to investigate the hydraulic resistance of Poiseuille relationship to tracheids in the secondary xylem of Medullosa, Cordaites and a Pinus species. This choice of living Carboniferous pteridophytic and progymnosperm taxa in and extinct plants allowed the authors to compare the struc- order to estimate the comparative hydraulic performance of ture and function of tracheids with and without torus–margo these extinct plants. In his survey, tracheid diameters ranged pitting. Interestingly, Medullosa and Cordaites have tracheids from a minimum of 36 lm in the Sphenophyte (i.e. horsetail) that have angiosperm-like, homogenous pit membranes, Arthropitys communis to a maximum of 174 lm in the seed presumably a suboptimal combination of conduit size and fern Medullosa noei. The tracheid size of Medullosan wood is pitting that is expected to produce a substantial drop in exceptional by today’s standards because the largest conduits hydraulic efficiency (on a sapwood area basis) relative to in extant plants are found in the lianas, with vessels (not trac- equivalently sized tracheids with torus–margo pitting heids) commonly in excess of 150 lm (Ewers, 1985; Cichan, (Pittermann et al., 2005). However, the conduit-specific 1986). As expected, predicted k was the highest in plants s conductivity of Medullosa was calculated to be over two with the largest tracheid diameters such as M. noei and Spheno- magnitudes higher than that of extant conifers, a reflection of phyllum plurifoliatum, reaching or exceeding the k of extant s the unusually wide and long tracheids that constitute this vines and lianas (Cichan, 1986). Clearly, these extinct plants species’ xylem (Wilson et al., 2008). The authors suggest exploited a morphospace that was quite different from today’s that the vasculature and hydraulic performance of these fossil forms. plants is similar to angiosperm lianas, whose climbing habit However, given what we know about pit resistance in eliminates any need for the xylem to perform canopy support woody plants, we can build upon Cichan’s method to achieve function. This is consistent with the climbing hooks and a higher level of precision in our transport models. In practice, tendrils present on the branches and pinnae of Medullosa hydraulic conductance (K) quantifies the efficiency of water specimens (Krings et al., 2003). transport through xylem, and is measured as the flow rate of Because water transport sets the upper limit for transpira- liquid water (Q) for a given pressure gradient (DW) driving tion, the relatively high hydraulic efficiency of Medullosan flow: xylem is in line with its large leaves and high leaf stomatal den- Q K ¼ : ð3Þ sities (Wilson et al., 2008). This plant probably required large DW amounts of water to support photosynthesis, which may have However, K cannot be measured directly on fossil material, narrowed its habitat to humid tropical floodplains (DiMichele so an alternative approach for estimating K is to separate et al., 2006).

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The approach to partitioning resistances in fossil angio- sperm xylem can be accomplished in manner similar to that of Wilson et al. (2008) but it could prove to be more challenging because vessels may be longer than tracheids by several orders of magnitude and the vessel network may be tortuous, with complex pitting patterns (Tyree & Zimmermann, 2002; Kitin et al., 2004). We can however turn to the structure–function relationships derived from extant angiosperms to find simple, anatomically based correlates of hydraulic efficiency. Again, vessel diameter may prove to be the most useful metric because it scales well with length and the pitted endwall area, and thus correlates strongly with xylem transport capacity (Wheeler et al., 2005; Sperry et al., 2006).

Lastly, the RCA of conifer tracheids with torus–margo pitting can be inferred from the following summary equation, Fig. 7 The per cent loss of conductivity (PLC) and cavitation pressure (P50)in 128g r D response to either a combination of freeze–thaw and water stress, or water P 2; RCA ¼ 2 þ 2 ðÞ1 þ C ð7Þ stress alone at the range of xylem pressures in stems of Utah Juniper (from pD FPL Pittermann & Sperry, 2005). 2 where RL and RW are described by [128g ⁄ (pD )] and 2 [rPD ⁄ (FPL )] respectively (Pittermann et al., 2006b). Essen- the entire conduit to create an embolism, which blocks water tially, mean RCA is determined by conduit lumen diameter transport in that cell (Fig. 6). Because embolism reduces the (D), the length of the conduit (L), intertracheid pit resistance number of functional conduits, water must subsequently on an area basis (rP), the fraction of the tracheid wall area travel from the root to the leaf at progressively more negative occupied by pits (FP) and the ratio of the tracheid double wall xylem pressures through a higher resistance pathway. Under thickness to lumen diameter (C) (Pittermann et al., 2006b; increasing drought conditions, these higher tensions predis-

Sperry et al., 2006). The average intertracheid rP is pose the xylem to further cavitation events that can potentially ) 6±1MPasm 1 but some degree of variation exists in the lead to the dangerous situation of runaway embolism and north temperate conifer clades that may reflect tracheid loca- plant death (Tyree & Sperry, 1988; Hacke & Sperry, 2001; tion within the plant as well as species’ drought resistance and Tyree & Zimmermann, 2002; Choat et al., 2008). habitat preference (Mayr et al., 2002; Burgess et al., 2006; Species’ cavitation resistance is typically presented in the Pittermann et al., 2006b; Domec et al., 2008). form of vulnerability curves, which express the per cent loss of hydraulic conductivity due to embolism in response to more negative water potentials (Fig. 7; Hacke & Sperry, 2001). Relationships between xylem anatomy, and drought and Vulnerability curves can be generated from almost any portion freeze–thaw induced cavitation of a plant such as roots, stems and leaves. The xylem pressure Not only can wood anatomy be used to describe species’ at which a segment exhibits 50% loss of hydraulic conductivity hydraulic efficiency but it can also help identify species’ limits is referred to as the P50, or the ‘cavitation pressure’, and can to water transport. This is because the vascular features that be used to compare cavitation resistance between plant organs allow us to model conductivity can also capture the suscepti- or species. bility of xylem to hydraulic failure caused by drought or Despite the looming threat of a hydraulic catastrophe, freeze–thaw induced cavitation. In this way, wood anatomy plants are only as cavitation resistant as their environment can potentially serve as an additional indicator of a fossil requires them to be. This is because there are several costs plant’s access to water and ⁄ or palaeoclimate. associated with embolism resistance, namely carbon invest- Water transport by the C–T mechanism works remarkably ment and reduced transport efficiency. Progressively negative well but it is not without its limitations. When leaf transpira- water potentials can threaten xylem conduits with implosion tion exceeds the transport capacity of the xylem such as during because the tension exerted on the water column exposes the a drought, the pressure in the water column can become nega- conduit walls to a combination of hoop and bending stresses tive enough to allow the phase change of water from a liquid (Hacke et al., 2001). Hence, xylem conduits must be suffi- to a vapour state. This transition is known as cavitation or ciently, but not overly reinforced to withstand wall collapse. air-seeding, and it is caused by the aspiration of air into the Anatomically, this translates to a tight, positive correlation transpiration stream through the pit membrane. If the pull of between the ratio of conduit double wall thickness (t)to the transpiration stream creates sufficient tension in the sap, hydraulic mean lumen diameter, that is the empty space con- 2 the air bubble expands and the conduit is simultaneously fined by the inner walls of the conduit [b;(t ⁄ b)h ] and species’ drained of water. Ultimately, a mixture of air and vapour fills cavitation pressure (Fig. 8; Kolb & Sperry, 1999; Hacke

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Fig. 9 The relationship between species cavitation pressure and conduit diam- Fig. 8 Species’ cavitation pressure as a function of the wall thickness to lumen eter (data from Sperry et al., 2006; J. Pittermann, unpublished data). diameter ratio (data from Hacke et al., 2001; Pittermann et al., 2006a,b; Pratt et al., 2007, J. Pittermann, unpublished data). Archaeopteris cavitation pressure was estimated from fossil root and stem material (courtesy of D. occur through the largest pore on a pit membrane, the likeli- Erwin). hood of an air seeding event rises with increasing pit area (Wheeler et al., 2005; Sperry et al., 2006; Choat et al., 2008). et al., 2001; Hacke & Sperry, 2001; Pittermann et al., 2006a; Intervessel pit area scales with vessel diameter, thus providing Jacobsen et al., 2007). Consequently, the greater investment an explanation for the weak, although consistent relationship in xylem wall content is reflected in higher wood densities as between vessel diameter and vulnerability to cavitation. well as improved mechanical strength, and thus represents the In conifers, air seeding is also thought to occur through the carbon cost of cavitation resistance (Hacke et al., 2001; Baas pit membrane but no relationship exists between the pit area et al., 2004; Jacobsen et al., 2007; Pratt et al., 2007). and cavitation pressure (Pittermann et al., 2006b). In water However, the thickness:span relationship is driven by variation filled tracheids, water moves from one tracheid to another in conduit diameter rather than wall thickness, which explains through the porous margo region of the pit membrane. the general trend for reduced hydraulic conductivity with Should one tracheid become embolized, surface tension in increased resistance to cavitation (Hacke et al., 2006; Pitter- the margo deflects the pit membrane such that the torus is mann et al., 2006a; Sperry et al., 2006). Although conduit appressed against the pit aperture and air is prevented from diameter is also coupled with species’ cavitation pressure, entering the neighbouring, functional tracheid. Air seeding there is much variation in this relationship and a broad occurs when the xylem pressure is negative enough to dis- sampling is required to achieve adequate resolution (Fig. 9). lodge the torus from its sealing position (Fig. 6). Conse- 2 Hence, conduit (t ⁄ b)h serves a much better structural quently, it is the ratio of the torus diameter to the pit aperture correlate with cavitation pressure than conduit diameter. diameter that is thought to control air seeding in conifers,

Unlike angiosperm xylem which features fibres for struc- while the progressive reductions in pit aperture with P50 may tural support and vessels for water transport, conifer xylem is represent the pit-level hydraulic cost of cavitation resistance homoxylous, meaning that its tracheids serve both a transport (Burgess et al., 2006; Domec et al., 2008; Hacke & Jansen, as well as a support role. This means that on average, stem 2009). 2 tracheids exhibit greater (t ⁄ b)h than vessels at a given cavita- Lastly, hydraulic dysfunction may also be caused by freeze– tion pressure (Fig. 8; Sperry et al., 2006; Hacke et al., 2001). thaw cavitation, a common phenomenon in plants inhabiting To achieve improved cavitation resistance, an increase in seasonal or high elevation climates. When xylem sap freezes, 2 tracheid (t ⁄ b)h is accomplished by shrinking the tracheid dissolved gases are coalesced into bubbles during ice forma- lumen diameter rather than increasing tracheid wall thickness. tion. This is because air is insoluble in ice. The bubbles remain Consequently, conifer xylem exhibits a 46-fold range in hydrau- inert while the sap is frozen, but may expand as it melts and lic conductivity – a significant strength versus transport efficiency tensions are re-introduced into the xylem. If xylem pressures trade-off (Pittermann et al., 2006a; Sperry et al., 2006). are sufficiently negative during thawing, the largest of these A similar cavitation safety versus efficiency trade-off is bubbles may expand and nucleate an embolism (Figs 6 and 7). evident in angiosperms but unlike in the conifers, it may be The likelihood of freeze–thaw induced embolism is described more tightly coupled to the process of air seeding at the pit by a modification of the capillary equation, such that the xylem level. The recently proposed ‘pit area hypothesis’ suggests that pressure (PX) must be more negative than the critical freeze– vulnerability to air seeding is related to the intervessel pit area thaw cavitation pressure (PXF) in order for the bubble to on a conduit. As air seeding in angiosperms is thought to expand and embolism to occur,

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2T relationship that should exist between conduit diameter and PXF ¼ ; ð8Þ rb P50. However, the relationship between vessel diameter and vulnerability to freezing-induced cavitation in oaks is generally where T is the surface tension of water and rb is the radius of consistent with theory (Sperry & Sullivan, 1992; Davis et al., the largest bubble. Hence, the larger the bubble, the less 1999; Cavender-Bares et al., 2005). negative the PXF required for bubble expansion (Davis et al., 1999; Pittermann & Sperry, 2003). In contrast to drought-induced embolism, conduit diame- The relationship between stomatal conductance and the structure and function of xylem ter is explicitly linked to species’ vulnerability to freezing induced embolism. This is because rb is a function of radial air The guiding principle of effective water transport is that the content, which is directly proportional to conduit diameter hydraulic supply of water must meet the transpirational (Pittermann & Sperry, 2003, 2005). Practically, this means demands of the leaves (Sperry et al., 1998; Sperry, 2000). that species with an average conduit diameter >30 lm are Not surprisingly, the stomata play a key role because should highly susceptible to freeze–thaw cavitation, even under the water supply become compromised, or transpiration mildly negative xylem tensions. By contrast, plants with exceed the plant’s hydraulic capacity, stomatal closure is the narrow conduit diameters are largely protected from this form first line of defence against desiccation. However, stomatal of stress because the smaller bubbles that are produced upon conductance (gs) must also be well regulated because an inap- freezing have a greater tendency to shrink and redissolve propriately low gs will impose a carbon limitation on photo- during the thaw (Pittermann & Sperry, 2005). Hence, taxa synthesis. Hence, photosynthesis and stomatal conductance with narrow conduits such as alpine conifers are freeze–thaw are closely coupled in what was probably the first of an cavitation resistant but at the cost of reduced hydraulic integrated sequence of adaptations that transformed the conductance, while the opposite is true of plants with gas-exchange characteristics of plants during their coloniza- large-diameter conduits. tion of land (Hetherington & Woodward, 2003; Franks & The interdependence between xylem pressure and conduit Brodribb, 2005; Franks & Beerling, 2009a,b). Stomatal diameter was examined in conifer wood, and used to roughly distributions have been used to infer palaeoclimates from approximate the freeze–thaw vulnerability curves from a fossil leaves but can leaf stomatal distributions lead us to an tracheid diameter distribution according to, improved understanding of plant palaeophysiology? The close coupling between stomatal conductance and P ¼ 120D1:53; ð9Þ XF f water transport is well documented and several studies have where Df is the critical cavitation diameter, which is the shown that alterations in stem water transport can cause either conduit diameter that will embolize due to freezing and thaw- stomatal closure or stomatal opening. Stomatal behaviour is ing at a pressure PXF (Pittermann & Sperry, 2005). Whether governed by the vapour pressure deficit between the leaf inte- equation 9 applies to angiosperm wood is currently unknown. rior and ambient atmosphere, water status, the leaf boundary Although the relationships between wood anatomy layer, soil-to-leaf water transport and chemical signals such as and resistance to drought and freeze-thaw stress are well abscisic acid. However, it is the leaf water status that encapsu- developed and could potentially be applied to fossil material, lates the holistic effect of these factors on stomatal conduc- it is important that any inferences about species’ habitat or tance because leaf water potential regulates the turgor microhabitat based on xylem anatomy be approached with pressure of both stomatal guard cells as well as the subsidiary caution. If possible, conclusions should consider the evolu- cells surrounding the stomata (Meinzer & Grantz, 1990; tionary lineage, the overall plant form, and leaf venation Saliendra et al., 1995; Buckley, 2005). Not surprisingly, the patterns, which are coupled to species hydraulic and photo- leaf water potential is to a large extent, controlled by the synthetic capacity (Sack & Frole, 2006; Brodribb et al., 2007; transport capacity of the xylem and its ability to recharge water Brodribb, 2009), and may also be related to habitat (Royer lost by transpiration. Indeed, an artificial reduction of xylem et al., 2008). For example, inferences about species’ resistance transport rapidly induces stomatal closure and reduces transpi- to drought-induced cavitation based on diameter alone may ration, whereas root pressurization restores leaf water poten- be erroneous, because conduit diameter can be weakly linked tial and induces stomatal opening (Saliendra et al., 1995; to cavitation in angiosperms (Wheeler et al., 2005; Sperry Hubbard et al., 2001). Alternatively, partial de-foliation of et al., 2006) but may be influenced by evolutionary lineage in the plant canopy increases the supply of water relative to the both angiosperms and conifers (Cavender-Bares & Holbrook, demand, thereby inducing an increase in stomatal conduc- 2001; Pittermann et al., 2006a,b). We know that despite tance (Oren et al., 2001). having xylem with large diameter conduits, ring-porous spe- A strong relationship exists between stem hydraulic cies such as oaks, are actually resistant to drought-induced conductance and photosynthesis suggesting that leaf gas cavitation and exhibit low water potentials in situ (Cochard exchange is proportional to, or constrained by vascular sup- et al., 1992) and may thus deviate from the seemingly simple ply (Brodribb & Feild, 2000; Hubbard et al., 2001; Santi-

2010 Blackwell Publishing Ltd The evolution of water transport in plants 131 ago et al., 2004; Maherali et al., 2008; Brodribb, 2009). was well over 50% lower than that of the 340 ppm grown These findings are corroborated by extensive work docu- plants. A similar response was observed across eight species of menting the coupling between leaf vasculature, stomatal conifers grown at 280 and 800 ppm (J. Pittermann, unpub- conductance and gas exchange across a variety of plant life lished data, Fig. 10). These results imply that plants may have forms (Brodribb et al., 2003, 2005). Because at least 25% of been predisposed to a high degree of water stress during peri- the total resistance to plant water flow resides in the leaves, ods of low CO2 such as the Pleistocene glacial periods. leaves may exert a disproportionately high degree of control Increased susceptibility to drought stress combined with over plant water relations (Sack et al., 2003). It may also be reduced water use efficiency may have been a contributing fac- that the leaf stomatal and vascular performance may affect tor to the reduced vegetation cover during the Pleistocene the structure and function of ‘upstream’ stem xylem, (Cowling & Sykes, 1999). although that possibility has not previously been discussed. If we accept that the apparent changes in stomatal densities

Certainly, such a co-ordinated response would require some are consistent with the fluctuating CO2 levels of the Mid-to- degree of phenotypic plasticity in both the leaves and the Late Phanerozoic, then atmospheric CO2 may have had a pro- xylem in the short term, but it may also have significant found effect on the whole plant conductance to water. For long-term or even deep-time evolutionary implications on example, the ‘topdown’ stomatal response to CO2 may have the structure and function of xylem. at various times selected for plant hydraulic architecture that

Atmospheric CO2 levels may have constrained the struc- was better equipped to mine water via deeper and more com- ture and function relationships of soil-to-leaf hydraulic trans- plex root systems. Such plants may have also been more effi- port in just such a manner. There is much geological, cient at transporting water by allocating a greater proportion biological and theoretical evidence to suggest that atmo- of resources to xylem, or by increasing the transport efficiency spheric CO2 levels have fluctuated dramatically over time of their xylem tissue. Hence, under periods of good water

(Zachos et al., 2001; Beerling, 2002; Berner, 2006; Fletcher availability and low atmospheric CO2, it is tempting to specu- et al., 2008). Indeed, CO2 levels are thought to have reached late that selection may have favoured the presence of more highs well over 4000 ppm during the Devonian and lows efficient, large-diameter conduits or a greater fraction of tissue below 500 ppm during the Carboniferous (Fig. 1). Interest- devoted to water transport, in order to meet the increased ingly, much of the evidence for deep-time atmospheric CO2 transpirational demands inherent to leaves with high stomatal fluctuations has either been derived from or corroborated by densities. measures of the leaf stomatal response. Specifically, it has The alternative hypothesis is that reduced atmospheric CO2 been shown that across a broad sampling of plants from the levels may have imposed a carbon limitation on growth in a angiosperms and conifers, stomatal density increases in manner that reduced leaf area, such that whole-plant transpi- response to low atmospheric CO2 whereas the opposite is ration scaled with reduced plant size. Consequently, xylem true under elevated levels of CO2 (Woodward, 1987; area ⁄ leaf area, leaf-specific hydraulic efficiency and conduit McElwain et al., 1999; Royer et al., 2001; Retallack, 2001; diameter would remain unchanged. Indeed, several studies Beerling, 2002; Kouwenberg et al., 2003). Data derived have shown smaller leaf areas in plants grown under subambi- from the stomatal index, a more refined measure of the ent CO2 (Dippery et al., 1995; Cowling & Sage, 1998). stomatal response that controls for leaf expansion, also However, the data do indicate that transpiration rates indicate that in some taxa, CO2 is a developmental driver of continue to be higher in these plants than those grown at leaf stomatal distributions (Lake et al., 2002). The discovery ambient CO2 levels (Ward et al., 1999), suggesting that on a that stomatal abundance is related to atmospheric CO2 aug- whole-plant scale, the increased water loss may also impose a mented our understanding of palaeoclimates because CO2 0.6 ) could be retrodicted from leaves much older than ice cores. –1 800 ppm grown s

–2 280 ppm grown In this way, stomatal density in combination with isotope and 0.5 palaeosol signals serves as a reasonable CO2 proxy with which 0.4 to evaluate the accuracy of climate models. We know, however, that stomata play a dual role in regulat- 0.3 ing water loss as much as CO2 uptake, yet the effect of vacillat- 0.2 ing CO levels on the palaeo-physiology, especially water 2 0.1 relations of the sampled plants have attracted less attention. Stomatal conductance (g, mol m Stomatal conductance (g, The effect that increasing stomatal densities may have on leaf 0 Larix Sequoia Pinus Pinus Taxodium water loss was apparent to Woodward (1987) who showed Metasequoia elliottiiPseudotsuga occidentalis menziesii ponderosa distichumsempervirensSequoiadendron that the stomatal conductance of Acer pseudoplatanus seed- glyptostroboides giganteum lings grown under 225 ppm of CO was twice as high as that 2 Fig. 10 The stomatal conductance of Cupressaceaous and Pinaceous conifer of seedlings grown under 340 ppm. Functionally, this meant seedlings grown at 280 and 800 ppm in growth cabinets (mean ± SD; J. Pitter- that the water-use efficiency of the 225 ppm-grown seedlings mann, unpublished data).

2010 Blackwell Publishing Ltd 132 J. PITTERMANN significant physiological limitation. Lastly, an increase or area. Such a transport response would require the co-ordina- decrease in the pressure gradients within the xylem may alter tion between the vascular cambium and stomatal patterning the flow rates such that transpirational demands are effectively during leaf development, and there is evidence to suggest that met without a need for anatomical changes in the xylem tissue in some species, stomatal development is labile and thus

(Fig. 11). This response, would however predispose the plants responsive to atmospheric CO2 (Lake et al., 2002; Beerling, to a greater possibility of cavitation caused by air seeding. 2005) but whether this couples to vascular development

We can begin to explore the impact of atmospheric CO2 on remains unknown. Alternatively, xylem anatomy may exhibit plant water relations by returning to some basic relationships limited phenotypic plasticity, and thus impose fundamental between xylem transport, anatomy and stomatal conductance. limits on leaf gas exchange as appears to be the case in diffuse

The relationship between gs and leaf-specific hydraulic and ring porous angiosperm trees (Bush et al., 2008). conductance (Kl) can be described such that, If a link does indeed exist between atmospheric CO2, stoma- tal conductance, stomatal density and vascular design, it is DW tempting to speculate that the 70 million years during the gs ¼ K1 ; ð10Þ VPD Mid-Devonian to Early Carboniferous provided atmospheric where DW is the water potential difference between the soil conditions that supported the evolution of secondary xylem and the leaves (Wsoil ) Wleaf) driving water movement and (wood). Climate models suggest that this period of the Phan- VPD represents the vapour pressure deficit between the leaf erozoic was characterized by CO2 levels that are thought to interior and the ambient air (Bond & Kavanagh, 1999; have been at least as low or lower than those of today, and

Hubbard et al., 2001). Kl is a measure of hydraulic efficiency which may have stimulated not only an increase in stomatal on a whole-plant basis (Bond & Kavanagh, 1999; Sperry, densities but also the appearance of large leaves (Beerling

2000; Hubbard et al., 2001). If we assume that ks scales with et al., 2001; Osborne et al., 2004). Furthermore, it is at this

Kl (certainly ks scales with leaf-specific conductivity, Kl; J. Pit- time that elevated atmospheric oxygen levels are thought to termann, unpublished data), then substituting equation 2 for have supported an increase in xylem lignification and possibly

Kl in equation 10 yields the final relationship, selection for woody taxa (Graham et al., 1995; Berner, 2005; Berner et al., 2007). A concurrent argument is that low CO2 ðÞDW pRD4 selected for high stomatal densities, which in turn increased g 1 : ð11Þ s A128gVPD evaporative cooling thereby releasing leaves from the con- straints of overheating. This is also consistent with survey Equation 11 expresses a theoretical correlation between results from the fossil record showing a 25-fold enlargement of stomatal conductance and the theoretical maximal transport leaf areas during this time (Osborne et al., 2004). In any case, capacity of the xylem, as constrained by conduit diameter. if atmospheric CO2 precipitated changes in leaf size and stoma-

Simplistically, equation 11 implies that an overall rise in gs tal density, then we might expect a co-ordinated response from requires an increase in conduit diameter, for a given xylem the vascular system designed to increase transport efficiency.

A

B

Fig. 11 Some theoretical relationships between xylem structure and function in response to low and

high ambient CO2.

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PART IV: CONCLUDING REMARKS cies is useful, incorporating pit resistance into fossil plant transport models will allow us to broaden our understanding Plant water transport and climate of xylem function in extinct plants, as well as the significance of evolutionary transitions from one conduit type to another Plant water transport irrevocably changed our planet. Even such as in the case of the Rhyniophytic plants. As we do this the earliest transpiring plants would have subtly modified their however, comparative studies of xylem structure and function local water regime, whereas the Devonian forests were proba- in modern taxa need to develop within a broader evolutionary bly key players in the formation of soils, carbon sequestration framework. For example, we know little about the relation- and climate change (Retallack, 1997; Algeo & Scheckler, ships between cavitation resistance, pit resistance and hydrau- 1998; Berner, 2005; Berner et al., 2007) Xylem function cer- lic efficiency in monocots and Gnetales. tainly impacts atmospheric moisture, and the Amazon rainfor- Aside from the extensive descriptive work documenting the est is a dramatic, modern day example of how large-scale anatomy of fern xylem, not much is currently known about water transport controls continental climates as nearly 50% of the comparative hydraulics of ferns, and the homogenous fern global precipitation is recycled from forests (Malhi et al., intertracheid pit membrane in particular (Carlquist & Schnei- 2008). Deep roots extract and potentially re-distribute the soil der, 2007). This is important information because tracheids water that is ultimately transpired back to the atmosphere, a with homogenous pit membranes represent the ancestral state phenomenon that is critical to maintaining hydration when of xylem in leafy tracheophytes (Euphyllophytes; Kenrick & high evaporative demand and reduced rainfall conspire to Crane, 1997). However, new data collected from across the reduce stomatal conductance, such as during the dry season fern lineage show that fern xylem is as efficient on an (Oliveira et al., 2005). Consequently, extensive deforestation area basis as that of angiosperms and conifers (J. Pittermann tends to lower evapotranspiration, cloud formation and rain- & E. Limm, unpublished data), suggesting that the large fall by a feedforward effect that progressively reduces ecosys- tracheid size in combination with what appears to be a highly tem water cycling. Model projections suggest that the permeable pit membrane (Carlquist & Schneider, 2007) combine removal of 30–40% of the Amazonian forest could drive the to ramp up water transport in an otherwise seemingly subopti- region into a permanently drier climate regime (Oyama & mal combination of vascular traits (Pittermann et al., 2005). Nobre, 2003). Regional meteorological phenomena will also We can also exploit our current understanding of the rela- be affected by alteration of the forest canopy boundary effects tionship between pit area and pit structure in angiosperms and so, taken together, there is indisputable evidence that plant conifers respectively, to gain more insight into the drought water transport is a key element of large-scale ecosystem sta- resistance of early land plants. The pit area hypothesis holds bility (Betts et al., 2004). across angiosperms of different evolutionary lineages, Evapotranspiration is a common metric of area-based although membrane porosity may also variably affect resis- terrestrial water loss but recent work suggests that transpi- tance to cavitation (Jarbeau et al., 1995; Hacke et al., 2006, ration alone can modify continental hydrology. Extensive 2007; see also Choat et al., 2008). Assuming that pit mem- field studies have shown that elevated CO2 reduces stoma- branes are well preserved in fossil specimens, perhaps the best tal conductance and transpiration, an effect that generally approach may be to examine the pit membrane size, scaling improves the water balance of terrestrial vegetation (Korn- and porosity in a comparative manner, sampling taxa across er, 2003). However, the suppression of transpiration leads the land plant phylogeny. to greater water retention in soils and ultimately higher Understanding the structure and function of xylem can water discharge into rivers, a phenomenon referred to as inform us not only about the physiological limits of plant ‘physiological forcing’ (Betts et al., 2007). How would this water transport and the constraints it places on photosynthe- scenario play out under low CO2 conditions, which typically sis, but this information also has potential to augment models give rise to increased stomatal conductance? Given the of palaeocommunity assembly. For instance, the Devonian uncertainties of climate modelling, a simple answer may and Carboniferous are characterized by significantly different not exist but all things being equal, a reasonable guess may climatic patterns than those of today, as well as changes in the be that increased transpiration would lower soil moisture, relative positions of land masses and tremendous diversifica- and thus impact terrestrial water levels. tion of the terrestrial flora (DiMichele & Gastaldo, 2008). Plant distributions in these ancient and unfamiliar landscapes will, to some extent, be determined by xylem efficiencies and Future directions drought resistance. Altogether, this is an excellent time to Plant vascular tissue is one of potential drivers of plant diversi- fruitfully study the evolution of plant water transport across a fication (Donoghue, 2005), so much insight can be gained multitude of scales, ranging from the molecular, organismal into the evolution of plants by applying a neontological and and up to the ecosystem level. Certainly, the intersection of quantitative approach to fossil wood. Although the Hagen– plant physiology and palaeobotany offer much opportunity Poiseuille method of computing theoretical hydraulic efficien- for truly novel discoveries.

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ACKNOWLEDGMENTS Beerling DJ (2002) Low atmospheric CO2 levels during the Permo- Carboniferous glaciation inferred from fossil lycopsids. Proceedings I am very grateful to the three anonymous reviewers of the National Academy of Sciences 99, 12567–12571. whose thoughtful comments and copious advice dramatically Beerling DJ (2005) Leaf evolution: gases, genes and geochemistry. Annals of Botany 96, 345–352. improved this manuscript. Also, many thanks to David Beerling DJ, Berner RA (2002) Feedbacks and the coevolution of

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