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First published online June 7, 2007; 10.1104/pp.107.101352 Plant Physiology 144:1890-1898 (2007) © 2007 American Society of Plant Biologists OPEN ACCESS ARTICLE
Leaf Maximum Photosynthetic Rate and Venation Are Linked by Hydraulics1,[W],[OA]Department of Plant Sciences, University of Tasmania, Hobart, Tasmania 7001, Australia (T.J.B., G.J.J.); and Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37996 (T.S.F.)
Leaf veins are almost ubiquitous across the range of terrestrial plant diversity, yet their influence on leaf photosynthetic performance remains uncertain. We show here that specific physical attributes of the vascular plumbing network are key limiters of the hydraulic and photosynthetic proficiency of any leaf. Following the logic that leaf veins evolved to bypass inefficient water transport through living mesophyll tissue, we examined the hydraulic pathway beyond the distal ends of the vein system as a possible limiter of water transport in leaves. We tested a mechanistic hypothesis that the length of this final traverse, as water moves from veins across the mesophyll to where it evaporates from the leaf, governs the hydraulic efficiency and photosynthetic carbon assimilation of any leaf. Sampling 43 species across the breadth of plant diversity from mosses to flowering plants, we found that the post-vein traverse as determined by characters such as vein density, leaf thickness, and cell shape, was strongly correlated with the hydraulic conductivity and maximum photosynthetic rate of foliage. The shape of this correlation provided clear support for the a priori hypothesis that vein positioning limits photosynthesis via its influence on leaf hydraulic efficiency.
Leaves have sustained virtually all terrestrial ecosystems over the last 400 million years (Kenrick and Crane, 1991  ; Boyce et al., 2002; Boyce, 2005). Over this period land plants have evolved an enormous diversity of leaf structure; diversity that marks phylogenetic relations among clades and constrains the functional performance and climatic associations of plant species (Givnish, 1987; Wing and Greenwood, 1993; Smith et al., 1997; Osborne et al., 2004; Sack and Holbrook, 2006). Leaf veins are at the core of this structural diversity, forming the transport network for water, nutrients, and carbon for nearly all plants. While our knowledge of the molecular and developmental processes that guide leaf vein development and patterning grows at an ever-increasing rate (Kang and Dengler, 2004; Fleming, 2005; Scarpella et al., 2006; Sieburth and Deyholos, 2006), the underlying physical principles that connect vein pattern with leaf productivity remain unresolved. Discovering the specific mechanisms that link leaf venation to fundamental global processes such as photosynthetic rate and evapotranspiration is a prerequisite for understanding how leaf form has responded to, or perhaps driven, changes in atmospheric conditions through geological time (Volk, 1989; Osborne et al., 2004; Beerling, 2005).
The adaptive significance of efficient water transport (i.e. the mass of water transported per unit pressure gradient) is evident throughout the history of vascular plants. Evolutionary innovations in xylem structure that increase hydraulic efficiency while maintaining the continuity of the water column have been crucial to the success of the vascular plants (Carlquist, 1975
Here we evaluate a new hypothesis that explicitly links the structural properties of the leaf vein system to functional processes of water transport and photosynthetic capacity across the entire range of terrestrial plant diversity. Our a priori hypothesis was that the length of mesophyll tissue that must be traversed as the transpiration stream passes from a vein ending to site of evaporation will reflect both the hydraulic and coupled photosynthetic performance of any leaf. The hydraulic component of this hypothesis is based on the knowledge that resistance to water flow through living leaf mesophyll is very high compared with the hydraulic resistance of vein xylem. Hence it follows that the distance water must flow through the mesophyll before evaporating (as determined by the positioning of leaf minor veins) should profoundly influence the hydraulic efficiency of the leaf. Leaf photosynthetic performance was hypothesized to become involved based upon the well supported observation that maximum net assimilation rate is coupled to the capacity of the leaf vascular system to supply water to photosynthesizing mesophyll cells (Brodribb et al., 2005 In this study we examine how the water transport and photosynthetic carbon assimilation rates of leaves are related to the spatial arrangement of veins in the leaf mesophyll. By sampling a large number of species spanning the breadth of plant complexity and phylogenetic diversity from mosses to angiosperms we sought to understand whether this hydraulic principle was fundamental or variable among plant groups.
Hydraulic and Photosynthetic Capacity
Across the diverse range of land plant diversity sampled, an intimate association between light-saturated net CO2 assimilation rate (Amax) and the hydraulic conductance (Kleaf) of whole leaves was found (Fig. 1A
). A single regression accurately described the dependence of Amax upon Kleaf in all 43 species, including mosses, ferns, lycopods, gymnosperms, and angiosperms. At values of Kleaf < 10 mmol m–2 s–1 MPa–1 mean Amax was highly sensitive to increasing Kleaf, but this sensitivity decreased as Amax in the tropical angiosperm species approached the upper limits for C3 photosynthesis in woody plants (Larcher, 1995
Anatomical Determinants of Leaf Hydraulics
Leaf vein architecture and xylem anatomy was extremely diverse in our species sample (Supplemental Table S1), yet the response of Kleaf to mean maximum mesophyll path length (Dm) fell into two distinct groups. In the larger group (34 out of 43 species), a single highly significant regression (r2 = 0.97; P < 0.001) described the relationship between 1/Kleaf and Dm (Fig. 1B). Regressions fitted independently to each phylogenetic category (mosses, ferns, conifers, and angiosperms) within this group were all highly significant and not different to the regression for the pooled data set. Also, we did not find any significant differences between regressions based upon grouping species as single-vein or multivein leaves (Fig. 1B). The second group of species (circled in Fig. 1C) demonstrated a very different association between Dm and Kleaf. These species included conifers and cycads that were specifically selected because they possessed specialized conductive tissue (accessory transfusion tissue; Griffith, 1957
In single-vein leaves, Dm was the product of both the thickness (vein to epidermis) and width (vein to stomata) of leaves (Fig. 2, C and D), while in multivein leaves the vein density and leaf thickness (vein to epidermis) combined to determine the Dm (Fig. 2, A and B). Species mean Kleaf was extremely sensitive to Dm (excepting gymnosperms with leaf sclereids). Increasing Dm led to a decline in Kleaf proportional to Dm–1.2 (Fig. 1C). The slope of this relationship was slightly higher than that proportionality expected (Dm–1) if path length was independently controlling Kleaf, i.e. if the resistance to hydraulic flow through the leaf was uniquely controlled by the length of the mesophyll pathway. However, for gymnosperms that possessed lignified accessory transfusion tissues in the leaf mesophyll, there was only weak correlation within this group between Kleaf and Dm. Typically the Kleaf values of these gymnosperms were nearly an order of magnitude higher than other species with equivalent Dm (Fig. 1C).
Combining the observed relationships between Dm, Kleaf, and Amax enabled us to model how the width of single-veined leaves influences leaf photosynthetic capacity (Fig. 3 ). Among single-veined species, only those with narrow scale or needle leaves were able to attain high photosynthetic rates characteristic of sun-adapted species (Fig. 3A), while broader leaves were associated with low photosynthetic rates (and typically shady, low evaporative demand environments). A similar analysis on multiveined leaves illustrates the impact of vein density on Kleaf and Amax (Fig. 3B). With leaf thickness held constant it would be expected that Amax should respond positively to increasing vein density, with a gradual plateau in slope as vein density reached the upper limits for our angiosperm sample (15.8 mm mm–2). It should be noted that vein density was not found to be strongly correlated with either Kleaf or Amax in our sample of multivein leaves presumably due to the large range of vein-epidermal thickness in this morphologically diverse species sample (T.J. Brodribb, unpublished data). This is understandable viewed in the context of Figure 3B showing that the modeled effect of increasing leaf thickness was to reduce the impact of vein density upon Amax. In our sample of multiveined leaves, we found little overlap between the vein density of ferns and the higher vein density in angiosperms (Fig. 3B).
We found that the photosynthetic capacity of leaves in terrestrial plants is strongly correlated with proximity of veins to the evaporative surfaces of the leaf. The close relationship between these two parameters supports our a priori hypothesis that the length of hydraulic pathway through the mesophyll should exert a controlling influence over Kleaf and secondarily over Amax. This influence of vein placement over leaf physiology was found to transcend the enormous phylogenetic, ecological, and functional variation represented in our species sample. The data presented here suggest that throughout the evolutionary history of terrestrial plants, the hydraulic properties of the leaf tissue have played a fundamental role in linking leaf construction with photosynthetic capacity (Fig. 1).
Previously it has been suggested that vein density was related to photosynthetic function because the vein surface area is thought to limit photosynthate transport away from the leaf (Amiard et al., 2005
The first of these two processes is explained by the fact that water flow through the leaf is analogous to current flow in an electrical circuit (Cowan, 1972
The second mechanism that coordinates leaf vein arrangement and leaf photosynthetic potential is the tendency for the leaves of terrestrial C3 plants to produce a conservative CO2/water exchange ratio (Cowan and Farquhar, 1977
High CO2 assimilation rates in plants where water is supplied to leaves through internal conducting cells should, according to our data, be associated with either very narrow leaves (in the case of single-vein leaves), or high vein densities (Fig. 3). However, the impact of leaf thickness on Kleaf and Amax is likely to be more complicated due to the interaction of palisade thickness and the proximity of the vein to the stomatal surface of the leaf. We found here that increasing the vertical distance from the vein to the stomatal epidermis should reduce hydraulic and photosynthetic performance (Fig. 3B), but other studies have shown positive correlations between leaf and palisade thickness and Kleaf (Aasamaa et al., 2001
A fundamental implication of the relationship shown here between Kleaf and vein proximity (Fig. 1B) is that the hydraulic conductivity of the cell matrix comprising the mesophyll tissue of the leaf is consistently low among terrestrial plants. While it is likely that there is variation between species in the hydraulic conductivity of leaf tissue due to cell anatomy and packing (possibly contributing to the variability in the angiosperm data and the fact that Kleaf was not exactly related to Dm–1), this was outweighed by the influence of path length on the hydraulic conductance of the mesophyll pathway. However, many gymnosperms possess obvious modifications to the mesophyll tissue apparently used to increase the post-venous hydraulic conductivity of their leaves. These plants have water-filled lignified cells (Fig. 2, E and F) that are highly pitted and generally elongated in the plane of water movement from the vein to the leaf margin (Brodribb and Holbrook, 2005
The presence of highly pitted lignified tissue in the mesophyll of gymnosperms leaves has been formally noted in the conifer family Podocarpaceae and the cycad genus Cycas (Griffith, 1957
Considering that the total length of the transpiration pathway can exceed 100 m, it is remarkable that the last few tens of microns should reveal fundamental physiological information about the photosynthetic and hydraulic performance of the individual plant. Despite all the myriad of variation and adaptation in xylem anatomy to improve long-distance transport, the hydraulic conductivity of the mesophyll appears as a unifying limitation to maximum leaf photosynthesis. This result indicates that leaf structure, as it relates to the hydraulic performance, contains important information about how plants have evolved higher yielding leaves. Considering the substantial cost to plants of leaf vein differentiation, the data presented here provide a basis for evaluating the structural costs associated with increasing leaf photosynthetic rate, and the resultant impact on plant productivity.
Plant Material
Measurements of maximum photosynthetic rate, leaf hydraulic conductance, and leaf anatomy were carried out on 43 C3 species carefully selected to represent the breadth of land plant evolutionary diversity (Table I
). A mixture of tropical and temperate species were sampled primarily from their natural habitats and included representatives from three major phylogenetic categories (angiosperms, gymnosperms, and ferns), while mosses and lycopods were collected only from temperate regions. Species were chosen to represent the range of vein architecture within major groups. Our sampling included eight species of gymnosperms known to possess lignified transfusion tissue or sclereids in the mesophyll (Griffith, 1957
Leaf Photosynthetic and Hydraulic Capacity
Kleaf was measured on excised leaves allowed to reach a transpirational steady state while attached to a flowmeter measuring the transpirational flux (Sack et al., 2002 Amax was measured on 10 healthy, mature leaves of each species using a portable gas analyzer (Li-COR 6400) to quantify CO2 uptake under conditions of saturating light and water availability. All species were measured on plants in the field under conditions of high soil water availability. During all measurements a high flow rate (500 mL min–1) through the cuvette was maintained such that conditions in the cuvette approximated ambient temperature, vapor-pressure difference, and CO2 (which ranged from 364–375 µmol mol–1). The resultant temperature in the leaf chamber remained between 25°C and 33°C and the leaf to air vapor pressure deficit was less than 2 kPa. Leaves were measured from the same plants used for hydraulic measurements, and all measurements were carried out between 8 AM and 11 AM when CO2 uptake was maximal. Light intensities of either 1,800 or 1,000 µmol quanta m–1 s–1 were used depending on the saturating photosynthetic photon flux density of the species (as determined by a light response curve made on one individual per species); the lower photosynthetic photon flux density was used in species with low Amax to avoid oversaturation with light.
The xylem pathway through the leaf mesophyll was quantified by measuring the linear path length from the minor veins to stomata and then calculating the hydraulic path length assuming water moved in the cell apoplast, and that mesophyll cells were uniform capsules of known aspect ratio (measured for each species). Multiple measurements were made on each leaf by dividing leaves into grids of either 200 x 200 µm or 500 x 500 µm depending on leaf thickness and vein density. For each grid cell the maximum distance between neighboring veins and between the vein and the epidermis was recorded. Maximum rather than mean distance was used because it was easily measured and scales with average distance if stomata are distributed relatively homogenously across the leaf. Calculation of a mean (maximum) linear mesophyll path length for each leaf required measurements to be made along two axes; first, the lateral distances between veins were measured (termed the x axis; Fig. 2B) and second, the perpendicular distance from the vein to the epidermis (termed the y axis; Fig. 2A). A mean value for maximum x and y distance was calculated from 30 to 40 subsamples per leaf in each of three to four leaves previously sampled for Kleaf. Paradermal sections were used to visualize the x axis distance between adjacent minor veins, or to the most distant adjacent stomata for single-vein leaves (Fig. 2, B and D), and cross sections allowed determination of the y axis distance from the vein endings to the stomatal gas exchange epidermis (Fig. 2A). Randomly spaced windows in the epidermis were cut with a razor, and then cleared in 1 M KOH. After clearing, veins were stained with toluidine blue to highlight xylem lignin. In the case of bryophytes and some conifers, sulforhodamine-B was infused into the xylem of transpiring leaves and leaves viewed using a fluorescence microscope (Axiophot, Carl Zeiss) to clearly visualize the water-conducting tissue. Thirty images of vein architecture under 10x magnification were captured from three leaves of each species using a digital camera attached to a compound microscope and the largest distance between adjacent veins measured in all veins. In the case of single-vein leaves or parallel venation, measurements were made using a digital ruler in Image-J (National Institutes of Health, available online). In leaves with reticulate venation, the center of the areole was found by tracing the veins in each field of view in Image-J and increasing the pen size until no white space remained in the areole. The last point of white space remaining was the center of the areole, and this maximum pen size was converted back to a linear distance. Vertical (y axis) distance from the vein to the epidermis was measured from leaf sections cut from the same leaves used for leaf clearing. Ten sections from three to four leaves per species were cut and stained with toluidine blue. Minor veins or vein endings were identified by their distinctive morphology (paradermal sections allowed clear identification of the types of tracheids that characterized vein endings, typically thin-walled large lumen cells) and these were photographed. Ten images of leaf cross sections were used to measure the distance from the vein xylem to the gas-exchange epidermis (the stomata-bearing surface in tracheophytes and the abaxial leaf surface in bryophytes). Only one amphistomatic leaf was included in our sample (Eucalyptus globulus) and in this species leaves were isobilateral, so measurements were made equally on both sides of the leaf. Cross-section images were also used to measure the dimensions of mesophyll cells along the same two axes described above. A sample of 100 cells located between the vein and the site of evaporation were measured for x and y dimensions for each species.
We assumed that the majority of water flowed apoplastically in the mesophyll (Steudle, 1994
Finally, Dm was taken as the hypotenuse of a right-angled triangle produced by these x and y dimensions: Dm =
In leaves where cells were elongated such that Cy > Cx (such as E. globulus), X and Y distances were calculated as follows: X = v/Cx(
The effects of leaf width and vein density on Amax were modeled by combining empirical relationships between Kleaf and Amax and Dm and Kleaf (regression equations from Fig. 1, A and C). Combining these two equations allowed Amax to be solved empirically as a function of Dm. In single-vein species the x dimension in leaves is equivalent to the leaf width (from vein to furthest adjacent stomata in single-vein leaves; Fig. 2D), hence the effect of leaf width on Amax was modeled while holding vein-epidermis thickness at a constant value of 70 µm and using a uniform cell aspect ratio of 1:1.4 (the mean value for all species). In multivein leaves it is the vein density that influences the x dimension in leaves (Fig. 2B); hence, we were able to model the effect of increasing vein density on Amax. Vein density was simplified to a square network and vein-epidermal thicknesses of 70, 100, and 130 µm were imposed. This range corresponded to the observed range in the angiosperm sample.
Our a priori hypothesis was that Kleaf should be related to 1/Dm, so the logarithm of Kleaf was regressed on the logarithm of Dm, then tested to see if the slope was equal to –1. Regression analysis was used to test for variation in slopes and intercepts between single- and multiveined leaves, among major phylogenetic groups, and between species with and without sclereids in the mesophyll. All analyses except the latter excluded species with sclereids in the mesophyll. Model fitting for the regression between Amax and Kleaf was empirical and based on a polynomial best fit. All analyses were performed with SAS (SAS Institute).
The following materials are available in the online version of this article.
We acknowledge helpful comments from two reviewers. Received April 21, 2007; accepted May 23, 2007; published June 7, 2007.
1 This work was supported by the National Geographic Society (grant no. 7475–03), the Australian Research Council (grant no. DP0559266), and an Australian Research Fellowship (to T.J.B.).  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Tim J. Brodribb (timothyb{at}utas.edu.au).
[W] The online version of this article contains Web-only data.
[OA] Open Access articles can be viewed online without a subscription. www.plantphysiol.org/cgi/doi/10.1104/pp.107.101352 * Corresponding author; e-mail timothyb{at}utas.edu.au; fax 61–362262698.
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Cy/2] and Y = t/Cy (
(X2 + Y2). 
