Evolution of the stomatal regulation of plant water content · 2017. 4. 12. · 1 1 Research Update 2 Evolution of the stomatal regulation of plant water content. 3 Timothy J. Brodribb

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Research Update 1

Evolution of the stomatal regulation of plant water content. 2 Timothy J. Brodribb & Scott A.M. McAdam 3

*both authors contributed equally to this work 4

Abstract 5

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

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Why is stomatal evolution important? 14

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

Stomatal evolution has become a focus of some debate in recent years (Brodribb et al., 2009; 32 Brodribb and McAdam, 2011; Chater et al., 2011; Ruszala et al., 2011; Franks and Britton-Harper, 33 2016), largely initiated by evidence that although the stomata of ancient lineages of vascular plants 34 opened similarly to angiosperms in response to light and CO2, they close differently. In particular, the 35 observation that stomatal conductance and transpiration of ferns and lycophytes does not decline 36 significantly in response to ABA (Brodribb and McAdam, 2011), led to the theory that stomatal 37 closure during water stress originated in early vascular plants as a passive response of guard cells to 38 dehydration, and that the “active” closure mechanism, mediated by ABA, evolved much later in seed 39

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

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

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

Developmental homology but functional divergence? 69

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



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

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

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

Ancient stomatal opening driven by photosynthesis in the guard cells 117

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



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

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



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

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

Although a role for stomatal opening seems apparent across all land plants, the role and process of 175 stomatal closure seems much less uniform, particularly if basal plants are considered. In vascular 176 plants however, a primary stomatal function is the action to close the pore during water stress to 177 reduce transpiration and maintain plant hydration and avoid damage to the plant vascular system 178 (Fig. 2). The possible selective pressures driving the evolution of stomatal closure in the light is 179 typically cited as; (1) being a mechanism for increasing water use efficiency (during stomatal closure 180 at low humidity) or (2) as a means of protecting tissues from desiccation. It is hard to understand 181 how selection for efficient water use can operate at the level of the individual plant due to the fact 182 that water conservation inevitably provides more water for competitors (Cowan, 2002). The 183 alternative, protective role, provides a much more convincing selective advantage to plants, and 184 seems likely to underpin the evolution of stomatal responses in the light (Wolf et al., 2016). However, 185 as mentioned above, several lines of evidence suggest that this action may not be an ancestral 186 character in stomatal evolution, including the widespread capacity for desiccation-tolerance 187 (Peñuelas and Munné-Bosch, 2010) in bryophytes and the fact that ancestral stomata probably aided 188 rather than inhibited desiccation (of sporangia) in basal land plants (Caine et al., 2016). Desiccation-189 tolerance obviates the need to control evaporation from leaves, but was likely to be incompatible 190 with the evolution of massive plants that began to dominate forests during the radiation of land 191 plants (Kenrick and Crane, 1997). The reason for this is that the internal water transport system in all 192 plants becomes cavitated during acute water stress causing leaves to be cut off from water in the 193 soil (Tyree and Sperry, 1989). This type of damage can be easily repaired in small plants where 194 capillary action can redissolve air embolisms in the vascular system after rain (Rolland et al., 2015), 195 but larger woody plants are unable to repair cavitated xylem tissues by capillarity or root pressure 196 (Charrier et al., 2016), and therefore xylem becomes irreversibly damaged during water stress 197 (Brodribb and Cochard, 2009; Cochard and Delzon, 2013). Stomatal closure to protect the xylem 198 from cavitation must have thus been an evolutionary prerequisite for the increase in plant size that 199 occurred during the radiation of vascular plants. Indeed it has been demonstrated that the stomata 200 of early vascular plants such as ferns close before the decline in hydraulic function associated with 201 desiccation (Brodribb and Holbrook, 2003). New techniques that visualize the process of xylem 202 cavitation, clearly demonstrate that a similar role of stomatal closure in protecting the xylem from 203 cavitation during water stress (Fig. 2) is also common to gymnosperms and angiosperms (Brodribb et 204 al., 2016; Hochberg et al., 2017). There are good examples of interaction between opening and 205 closing signals to stomata during the early onset of plant desiccation, for example the opening of 206 stomata at high VPD by exposure to low CO2 (Bunce, 2006). However the closure mechanism during 207 drying appears to override all other signals as plants approach turgor loss (Aasamaa and Sõber, 2011; 208 Bartlett et al., 2016), and subsequent xylem cavitation (Hochberg et al., 2017). 209



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

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

Metabolically controlled stomatal closure in response to leaf water deficit 237

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



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

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

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

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



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

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

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

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



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

On-going questions in the field of stomatal evolution 351

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

There are a number of environmental signals regulating stomatal aperture that have not been 370 discussed in this review for which either we have little regulatory understanding of, like inverted 371 stomatal rhythms in CAM plants (Ting, 1987), or little functional understanding of, like stomatal 372 responses to phytohormones other than ABA (Dodd, 2003). Future work to resolve these questions 373 and place these responses in the context of evolution is essential. There remains much debate in 374 the literature on the evolution of the stomatal response to CO2 (Brodribb et al., 2009; Franks and 375 Britton-Harper, 2016). A common feature of all studies in this area is a conserved tendency to 376 respond to CO2, particularly low CO2, which likely reflects a common photosynthetic signalling in all 377 stomata (Brodribb et al., 2009; Franks and Britton-Harper, 2016). However, major differences across 378 lineages in the way stomata instantaneously respond to CO2 in the dark (Doi and Shimazaki, 2008; 379 Brodribb and McAdam, 2013) as well as the influence of ABA on the sensitivity of stomata to CO2 380 (McAdam et al., 2011) reflect, as yet undescribed and potentially important, mechanistic differences 381



10

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

Figure Legends 384

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

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

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

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



11

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

430



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Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang PG, Poretsky E, Belknap TF, Waadt R, Alemán F, Schroeder JI (2015)Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4: e03599


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Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms.New Phytol 162: 663-670


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http://www.ncbi.nlm.nih.gov/pubmed?term=Aasamaa K%2C S�ber A %282011%29 Responses of stomatal conductance to simultaneous changes in two environmental factors%2E Tree Physiology 31%3A 855%2D864&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Aasamaa K, S�ber A (2011) Responses of stomatal conductance to simultaneous changes in two environmental factors. Tree Physiology 31: 855-864http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Aasamaa&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Responses of stomatal conductance to simultaneous changes in two environmental factors&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Responses of stomatal conductance to simultaneous changes in two environmental factors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Aasamaa&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Apostolakos P%2C Livanos TL%2C Nikolakopoulou TL%2C Galatis B %282010%29 Callose implication in stomatal opening and closure in the fern Asplenium nidus%2E New Phytologist 186%3A 623%2D635&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Apostolakos P, Livanos TL, Nikolakopoulou TL, Galatis B (2010) Callose implication in stomatal opening and closure in the fern Asplenium nidus. New Phytologist 186: 623-635http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Apostolakos&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Callose implication in stomatal opening and closure in the fern Asplenium nidus&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Callose implication in stomatal opening and closure in the fern Asplenium nidus&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Apostolakos&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Baer A%2C Wheeler JK%2C Pittermann J %282016%29 Not dead yet%3A the seasonal water relations of two perennial ferns during California%27s exceptional drought%2E New Phytologist 210%3A 122%2D132&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Baer A, Wheeler JK, Pittermann J (2016) Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought. New Phytologist 210: 122-132http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Baer&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Not dead yet: the seasonal water relations of two perennial ferns during California's exceptional drought&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Baer&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Bartlett MK%2C Klein T%2C Jansen S%2C Choat B%2C Sack L %282016%29 The correlations and sequence of plant stomatal%2C hydraulic%2C and wilting responses to drought%2E Proc Natl Acad Sci U S A 113%3A 13098%2D13103&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Bartlett MK, Klein T, Jansen S, Choat B, Sack L (2016) The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proc Natl Acad Sci U S A 113: 13098-13103http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bartlett&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bartlett&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Bauerle WL%2C Whitlow TH%2C Setter TL%2C Vermeylen FM %282004%29 Abscisic acid synthesis in Acer rubrum L%2E leaves?a vapor%2Dpressure%2Ddeficit%2Dmediated response%2E Journal of the American Society for Horticultural Science 129%3A 182%2D187&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Bauerle WL, Whitlow TH, Setter TL, Vermeylen FM (2004) Abscisic acid synthesis in Acer rubrum L. leaves?a vapor-pressure-deficit-mediated response. Journal of the American Society for Horticultural Science 129: 182-187http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bauerle&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Abscisic acid synthesis in Acer rubrum L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Abscisic acid synthesis in Acer rubrum L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bauerle&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Boyce CK %282008%29 How green was Cooksonia%3F The importance of size in understanding the early evolution of physiology in the vascular plant lineage%2E Paleobiology 34%3A 179%2D194&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Boyce CK (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34: 179-194http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Boyce&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=How green was Cooksonia&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=How green was Cooksonia&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Boyce&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brandt B%2C Brodsky DE%2C Xue S%2C Negi J%2C Iba K%2C Kangasj�rvi J%2C Ghassemain M%2C Stephan AB%2C Hu H%2C Schroeder JI %282012%29 Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action%2E Proc%2E Natl%2E Acad%2E Sci%2E U%2ES%2EA%2E 109%3A 10593%2D10598&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brandt B, Brodsky DE, Xue S, Negi J, Iba K, Kangasj�rvi J, Ghassemain M, Stephan AB, Hu H, Schroeder JI (2012) Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action. Proc. Natl. Acad. Sci. U.S.A. 109: 10593-10598http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brandt&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Reconstruction of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatse action&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brandt&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brandt B%2C Munemasa S%2C Wang C%2C Nguyen D%2C Yong T%2C Yang PG%2C Poretsky E%2C Belknap TF%2C Waadt R%2C Alem�n F%2C Schroeder JI %282015%29 Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells%2E eLife 4%3A e03599&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brandt B, Munemasa S, Wang C, Nguyen D, Yong T, Yang PG, Poretsky E, Belknap TF, Waadt R, Alem�n F, Schroeder JI (2015) Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells. eLife 4: e03599http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brandt&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brandt&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brodribb TJ%2C Cochard H %282009%29 Hydraulic Failure Defines the Recovery and Point of Death in Water%2DStressed Conifers%2E Plant Physiology 149%3A 575%2D584&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brodribb TJ, Cochard H (2009) Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers. Plant Physiology 149: 575-584http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brodribb&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Hydraulic Failure Defines the Recovery and Point of Death in Water-Stressed Conifers&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brodribb&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brodribb TJ%2C Holbrook NM %282003%29 Stomatal closure during leaf dehydration%2C correlation with other leaf physiological traits%2E Plant Physiol 132%3A 2166%2D2173&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132: 2166-2173http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brodribb&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Stomatal closure during leaf dehydration, correlation with other leaf physiological traits&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Stomatal closure during leaf dehydration, correlation with other leaf physiological traits&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brodribb&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brodribb TJ%2C Holbrook NM %282004%29 Stomatal protection against hydraulic failure%3A a comparison of coexisting ferns and angiosperms%2E New Phytol 162%3A 663%2D670&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytol 162: 663-670http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brodribb&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brodribb&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brodribb TJ%2C Jordan GJ%2C Carpenter RJ %282013%29 Unified changes in cell size permit coordinated leaf evolution%2E New Phytologist 199%3A 559%2D570&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytologist 199: 559-570http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brodribb&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Unified changes in cell size permit coordinated leaf evolution&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Unified changes in cell size permit coordinated leaf evolution&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brodribb&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brodribb TJ%2C McAdam SAM %282011%29 Passive origins of stomatal control in vascular plants%2E Science 331%3A 582%2D585&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. 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Chater C, Kamisugi Y, Movahedi M, Fleming A, Cuming AC, Gray JE, Beerling DJ (2011) Regulatory mechanism controlling stomatalbehavior conserved across 400 million years of land plant evolution. Current biology 21: 1025-1029


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http://www.ncbi.nlm.nih.gov/pubmed?term=Chen Z%2DH%2C Chen G%2C Dai F%2C Wang Y%2C Hills A%2C Ruan Y%2DL%2C Zhang G%2C Franks PJ%2C Nevo E%2C Blatt MR %282016%29 Molecular evolution of grass stomata%2E Trends in Plant Science doi%3A 10%2E1016%2Fj%2Etplants%2E2016%2E09%2E005&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Chen Z-H, Chen G, Dai F, Wang Y, Hills A, Ruan Y-L, Zhang G, Franks PJ, Nevo E, Blatt MR (2016) Molecular evolution of grass stomata. Trends in Plant Science doi: 10.1016/j.tplants.2016.09.005http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Chen&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Molecular evolution of grass stomata.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Molecular evolution of grass stomata.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Chen&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Chen Z%2DH%2C Hills A%2C Baetz U%2C Amtmann A%2C Lew V%2C Blatt MR %282012%29 Systems dynamic modelling of the stomatal guard cell predicts emergent behaviours in transport%2C signalling and volume control%2E Plant Physiol%2E%3A doi%3A 10%2E1104%2Fpp%2E1112%2E197350&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Chen Z-H, Hills A, Baetz U, Amtmann A, Lew V, Blatt MR (2012) Systems dynamic modelling of the stomatal guard cell predicts emergent behaviours in transport, signalling and volume control. Plant Physiol.: doi: 10.1104/pp.1112.197350http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Chen&hl=en&c2coff=1http://scholar.

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Evolution of the stomatal regulation of plant water content · 2017. 4. 12. · 1 1 Research Update 2 Evolution of the stomatal regulation of plant water content. 3 Timothy J. Brodribb