Viewing leaf structure and evolution from a hydraulic perspective

More than 40 000 km year of water flows through the intricate hydraulic pathways inside leaves. This water not only sustains terrestrial productivity, but also constitutes nearly70%of terrestrial evapotranspiration, thereby influencing both global and local climate (Chapin et al. 2002). Thus, the central role played by leaf vascular systems in terrestrial biology provides an important context for research into the function and evolution of water transport in leaves. Significant progress has been made recently towards understanding the linkages between anatomy and water transport efficiency in leaves, and these discoveries provide a novel perspective to view the evolution of land plants. Additional keywords: photosynthesis, vein density, xylem. Leaf hydraulics and gas exchange Photosynthesis in air affords considerable benefits over photosynthesis in the aquatic zone because CO2 diffuses into and through the leaf 10 000 times faster in air than in water (Nobel 2005). However, the cost of rapid CO2 diffusion into the leaf is a counter-flowofwater vapour from the leaf to atmosphere, exposing photosynthetic tissue to potentially lethal desiccation. Vascular plants offset the risk of drying out by investing in a hydraulic system – the xylem – that irrigates the photosynthetic tissue to limit the development of damaging water deficits during photosynthetic gas exchange. However, because the capacity of xylem to supply water is finite and the synthesis of xylem tissue is costly (6.5 and 11.8mmol glucose per g of cellulose and lignin, respectively (Lambers and Poorter 1992)) selection should favour plants that tailor hydraulic investment to fit the likely evaporational demand of a leaf (Sperry 2003). Clear evidence of the adaptive link between the gas-exchange capacity and hydraulic efficiency comes from studies of leaves (Sack et al. 2003; Brodribb et al. 2005), stems (Brodribb and Feild 2000; Santiago et al. 2004), roots (Becker et al. 1999) and whole plants (Sperry 2000; Meinzer 2002). The contrasting functional and architectural demands upon these different plant organs affect the way evolution has moulded the structure of their water transport systems. The following discussion focuses on the hydraulic systems in leaves, examining how different configurations of hydraulic and photosynthetic tissue are able to satisfy the competing demands of water delivery, light capture and economic cost. Leaf hydraulics and water supply to the photosynthetic surface Leaves not only create the demand for water transport in plants, but also represent a major resistor in plant hydraulic system (Tyree 2002). The fact that the water transport pathway in leaves constitutes at least 30% (Sack and Holbrook 2006) of the whole-plant resistance to water flow (while representing only a very small fraction of the whole-plant transport distance) indicates the inherent complexity of irrigating a surface at which evaporation is occurring. Once water enters from the stem into the leaf lamina, there is a dramatic shift in functional and architectural demands upon the hydraulic system. Unlike stems, the hydraulic transport distances in leaves are typically relatively short, but hydraulic transport is complicated by the fact that most leaves are highly flattened to optimise light harvesting efficiency (Smith et al. 1997). As a result, leaf hydraulic systems are generally required to uniformly irrigate a flat surface that is often complex in shape. Maximum hydraulic transport capacity would be achieved by a network of irrigation whereby xylem tubes were plumbed directly into all transpiring cells. Such an extravagant investment in xylem tissue never occurs because the cost to the plant in terms of construction and displacement of photosynthetic tissue would always exceed the benefits in photosynthetic performance. An evolutionary trade-off between the antagonistic demands of maximising photosynthesis relative to structural investment has yielded a great diversity in the hydraulic and morphological character of leaves. Here we will demonstrate how, amidst this diversity, a limited set of optimal CSIRO PUBLISHING Review www.publish.csiro.au/journals/fpb Functional Plant Biology, 2010, 37, 488–498 CSIRO 2010 10.1071/FP1001