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The Evolution of Water Transport in Plants: an Integrated Approach J 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 Ó 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.
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