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Tree Physiology 31, 1039–1040 doi:10.1093/treephys/tpr100 Commentary Stomatal (mis)behaviour T.J. Brodribb1 and S.A.M. McAdam School of Plant Science, University of Tasmania, Bag 55, Hobart 7001, Australia; 1Corresponding author ([email protected]) Received August 5, 2011; accepted August 28, 2011; published online September 24, 2011; handling Editor Danielle Way When stomata first evolved they initiated the greening of terrestrial earth, and now more than 400 million years later these simple bi-cellular valves in the leaf surface regulate global fluxes of water and carbon. Despite their importance and super ficial simplicity, the behaviour of stomata remains a great challenge to understand. Different approaches to studying stomatal control have yielded rather disparate models for how stomata respond to environmental stimuli. Much of this discord arises from the diversity of mechanisms apparently involved in changing guard cell turgor and hence the aperture of the stomatal pore. On the one hand, the physical tension produced by dragging water from the soil through the xylem to the leaves directly influences leaf and guard cell turgor, while on the other hand, phytohormone levels (most importantly abscisic acid), light, photosynthesis and atmospheric gases induce active changes in guard cell turgor by triggering ionic pumping. Each stomatal control mechanism has its own champion and no model has ever successfully integrated all components. In such an environment there is great value in examining how different parts of the stomatal control network interact, particularly the competition between ‘hydraulic’ signals related to leaf water content and ‘metabolic’ signals related to ambient photosynthetic conditions. A paper by Aasamaa and Sõber in Tree Physiology (Aasamaa and Sõber 2011a) makes a novel attempt to describe how competing influences from metabolic and hydraulic stimuli interact to produce net stomatal responses. Focusing on a group of woody angiosperms, the Aasamaa and Sõber paper shows that when stomata are subjected to opposing influences of metabolism (by changing light or CO2) and hydraulics (by drying soil or changing humidity) the hydraulic signal dominates. This result is supported by other studies of leaf (Aasamaa and Sõber 2011b) and whole-tree gas exchange (Oren et al. 1999) and is perhaps not surprising when the origins of stomatal control systems are considered. The first stomata to evolve as unequivocal regulators of photosynthesis and water loss (unlike the stomata in some bryophytes) can be traced back to the lycophyte and fern ancestors (Figure 1), and recent studies show that extant members of this clade have weak or absent responses to CO2, abscisic acid (ABA) and blue light (Doi et al. 2006, Doi and Shimazaki 2008, Brodribb and McAdam 2011, Ruszala et al. 2011). Examining the behaviour of these early stomata shows that in planta they function as light-activated hydraulic valves, responding only to leaf hydration in the light (Brodribb and McAdam 2011). This hydrau- lic priority in stomatal control makes perfect sense considering the fundamental importance of stomatal closure as a means of preventing lethal plant desiccation, and Aasamaa and Sõber show that hydraulic priority is maintained through the vascular plant phylogeny despite the evolution of additional components in the stomatal control programme. In today’s research environment where the great bulk of physiological investigation into stomatal control has moved onto Petri dishes and into molecular laboratories, studies like Aasamaa and Sõber’s are critical for improving our understanding of the way that stomata perform in diverse taxa under realistic environmental conditions. Molecular research suggests that stomatal development and function are relatively conservative across vascular plants (Peterson et al. 2010), yet studies of stomatal behaviour in planta indicate considerable functional diversity between closely related species (Aasamaa and Sõber 2011a), and broad systematic variation in the way that stomata of early- and late-diverging vascular plants behave (Brodribb et al. 2009). The reason for this disparity is that stomata perceive the external environment through the lens of the wholeplant system, and hence are just as sensitive to intrinsic © The Author 2011. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected] 1040 Brodribb and Mcadam Figure 1. A phylogenetic reconstruction of stomatal evolution in land plants shows how stomatal function is first unequivocally associated with plant hydration and photosynthesis in the spore-bearing vascular plants (blue shading shows hydraulic control signals, red shading shows metabolic control signals and grey shading represents uncertain responses). Studies of gas exchange in the ancestors of the first vascular plants (ferns and lycophytes) indicate that stomata act as passive hydraulic valves, only sensitive to leaf water status in the light. The divergence of seed plants appears to coincide with the evolution of stomata that respond strongly to a suite of metabolic signals, yet hydraulic control remains prioritized even in higher plants (Aasamaa and Sõber, 2011a), as shown by black bars. The ‘high CO2’ response in seed plants is not shown in bold because only angiosperms have strong closure responses to elevated CO2. properties of the hydraulic and photosynthetic systems of the plant as they are to extrinsic factors such as light, soil and atmospheric water content, and CO2 concentrations. Only by integrating molecular- and cell-level physiology with leaf and whole-plant studies can we move forward in developing a model of stomatal behaviour that applies generally across species and environments. Such a model is desperately needed if we hope to understand or modify the way in which plants interact with the atmosphere. References Aasamaa, K. and A. Sõber. 2011a. Responses of stomatal conductance to simultaneous changes in two environmental factors. Tree Physiol. 31:855–864. Aasamaa, K. and A. Sõber. 2011b. Stomatal sensitivities to changes in leaf water potential, air humidity, CO2 concentration and light intensity, and the effect of abscisic acid on the sensitivities in six temperate deciduous tree species. Environ. Exp. Bot. 71:72–78. Brodribb, T.J. and S.A.M. McAdam. 2011. Passive origins of stomatal control in vascular plants. Science 331:582–585. Tree Physiology Volume 31, 2011 Brodribb, T.J., S.A.M. McAdam, G.J. Jordan and T.S. Field. 2009. Evolution of stomatal responsiveness to CO2 and optimization of water-use efficiency among land plants. New Phytol. 183:839–847. Doi, M. and K.I. Shimazaki. 2008. The stomata of the fern Adiantum capillus-veneris do not respond to CO2 in the dark and open by photosynthesis in guard cells. Plant Physiol. 147:922–930. Doi, M., M. Wada and K. Shimazaki. 2006. The fern Adiantum capillus-veneris lacks stomatal responses to blue light. Plant Cell Physiol. 47:748–755. Oren, R., J.S. Sperry, G. Katul, D.E. Pataki, B.E. Ewers, N. Phillips and K.V.R. Schäfer. 1999. Survey and synthesis of intra- and inter specific variation in stomatal sensitivity to vapor pressure deficit. Plant Cell Environ. 22:1515–1526. Peterson, K.M., A.L. Rychel and K.U. Torii. 2010. Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22:296–306. Ruszala, E.M., D.J. Beerling, P.J. Franks, C. Chater, S.A. Casson, J.E. Gray and A.M. Hetherington. 2011. Land plants acquired active stomatal control early in their evolutionary history. Curr. Biol. 21:1–6. Wei, C.F., M.T. Tyree and E. Steudle. 1999. Direct measurement of xylem pressure in leaves of intact maize plants. A test of the cohesion-tension theory taking hydraulic architecture into consideration. Plant Physiol. 121:1191–1205.