Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
EVOLUTIONARY REVIEW

Viewing leaf structure and evolution from a hydraulic perspective

Tim J. Brodribb A E , Taylor S. Feild B D and Lawren Sack C
+ Author Affiliations
- Author Affiliations

A School of Plant Science, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia.

B Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA.

C UCLA Ecology and Evolutionary Biology, 621 Charles E. Young Drive South, Los Angeles, CA 90095-1606, USA.

D Present address: School of Biological Sciences, Monash University, Clayton, Vic. 3800, Australia.

E Corresponding author. Email: timothyb@utas.edu.au

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 37(6) 488-498 https://doi.org/10.1071/FP10010
Submitted: 12 January 2010  Accepted: 6 March 2010   Published: 20 May 2010

Abstract

More than 40 000 km3 year–1 of water flows through the intricate hydraulic pathways inside leaves. This water not only sustains terrestrial productivity, but also constitutes nearly 70% 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.


Acknowledgements

Support from the Australian Research Council in the form of a fellowship to TJB is gratefully acknowledged. TSF was supported by US National Science Foundation grant (IOB-0714156) and LS by NSF Grant IOB-0546784.


References


Abrams MD, Kubiske ME (1990) Leaf structural characteristics of 31 hardwood and conifer tree species in central Wisconsin: influence of light regime and shade-tolerance rank. Forest Ecology and Management 31, 245–253.
Crossref | GoogleScholarGoogle Scholar | open url image1

Altalib KH, Torrey JG (1961) Sclereid distribution in leaves of Pseudotsuga under natural and experimental conditions. American Journal of Botany 48, 71–79.
Crossref |
open url image1

Arzee T (1953) Morphology and ontogeny of foliar sclereids in Olea europaea. 1. Distribution and structure. American Journal of Botany 40, 680–687.
Crossref |
open url image1

Becker P, Tyree MT, Tsuda M (1999) Hydraulic conductances of angiosperms versus conifers: similar transport efficiency at the whole-plant level. Tree Physiology 19, 445–452.
PubMed |
open url image1

Beerling DJ (2002) Low atmospheric CO2 levels during the Permo-Carboniferous glaciation inferred from fossil lycopsids. Proceedings of the National Academy of Sciences of the United States of America 99, 12567–12571.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Berner RA (1994) GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 294, 56–91. open url image1

Boyce CK (2005) Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31, 117–140.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society of London. Series B. Biological Sciences 276, 1771–1776.
Crossref | GoogleScholarGoogle Scholar | open url image1

Boyer JS (1985) Water transport. Annual Review of Plant Physiology 36, 473–516.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brodribb TJ, Feild TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant, Cell & Environment 23, 1381–1388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brodribb TJ, Feild TS (2008) Evolutionary significance of a flat-leaved Pinus in Vietnamese rainforest. New Phytologist 178, 201–209.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175–183.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132, 2166–2173.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb TJ, Holbrook NM (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant, Cell & Environment 27, 820–827.
Crossref | GoogleScholarGoogle Scholar | open url image1

Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiology 137, 1139–1146.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb TJ, Holbrook NM (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant, Cell & Environment 29, 2205–2215.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytologist 165, 839–846.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brodribb T, Feild T, Jordan G (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cavender-Bares J, Kozak KH, Fine PVA, Kembel SW (2009) The merging of community ecology and phylogenetic biology. Ecology Letters 12, 693–715.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chapin FS , Matson PA , Mooney HA (2002) ‘Principles of terrestrial ecosystem ecology.’ (Springer-Verlag: New York)

Cochard H, Froux F, Mayr S, Coutard C (2004) Xylem wall collapse in water-stressed pine needles. Plant Physiology 134, 401–408.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Tyree MT, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiology 143, 122–133.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Coomes DA, Heathcote S, Godfrey ER, Shepherd JJ, Sack L (2008) Scaling of xylem vessels and veins within the leaves of oak species. Biology Letters 4, 302–306.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cornwell WK, Ackerly DD (2009) Community assembly and shifts in plant trait distributions across an environmental gradient in coastal California. Ecological Monographs 79, 109–126.
Crossref | GoogleScholarGoogle Scholar | open url image1

Domec JC, Palmroth S, Ward E, Maier CA, Therezien M, Oren R (2009) Acclimation of leaf hydraulic conductance and stomatal conductance of Pinus taeda (loblolly pine) to long-term growth in elevated CO2 (free-air CO2 enrichment) and N fertilization. Plant, Cell & Environment 32, 1500–1512.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dunbar-Co S, Sporck MJ, Sack L (2009) Leaf trait diversification and design in seven rare taxa of the Hawaiian plantago radiation. International Journal of Plant Sciences 170, 61–75.
Crossref | GoogleScholarGoogle Scholar | open url image1

Edwards DS (1980) Evidence for the sporophytic status of the Lower Devonian plant Rhynia gwynne-vaughanii Kidston and Lang. Review of Palaeobotany and Palynology 29, 177–188.
Crossref | GoogleScholarGoogle Scholar | open url image1

Farquhar GD, Raschke K (1978) Resistance to transpiration of sites of evaporation within leaf. Plant Physiology 61, 1000–1005.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feild TS, Balun L (2008) Xylem hydraulic and photosynthetic function of Gnetum (Gnetales) species from Papua New Guinea. New Phytologist 177, 665–675.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ (2004) Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82–107.
Crossref | GoogleScholarGoogle Scholar | open url image1

Feild TS, Chatelet DS, Brodribb TJ (2009) Ancestral xerophobia: a hypothesis on the whole-plant ecophysiology of early angiosperms. Geobiology 7, 237–264.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Foard DE (1959) Pattern and control of sclereid formation in the leaf of Camellia japonica. Nature 184, 1663–1664.
Crossref | GoogleScholarGoogle Scholar | open url image1

Foster AS (1946) Ontogeny of the foliar sclereids in Mouriria huberi Cogn. American Journal of Botany 33, 820. open url image1

Foster AS (1947) Structure and ontogeny of the terminal sclereids in the leaf of Mouriria huberi Cogn. American Journal of Botany 34, 501–514.
Crossref | GoogleScholarGoogle Scholar | open url image1

Foster AS (1956) Plant idioblasts – remarkable examples of cell specialization. Protoplasma 46, 184–193.
Crossref | GoogleScholarGoogle Scholar | open url image1

Franceschinelli EV, Yamamoto K (1993) Taxonomic use of leaf anatomical characters in the genus Simarouba (Simaroubaceae). Flora 188, 117–123. open url image1

Givnish TJ (1986) Optimal stomatal conductance, allocation of energy between leaves and roots, and the marginal cost of transpiration. In ‘On the economy of plant form and function’. (Ed. TJ Givnish) pp. 171–231. (Cambridge University Press: Cambridge)

Givnish TJ (1987) Comparative-studies of leaf form – assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106, 131–160. open url image1

Glasspool IJ, Hilton J, Collinson ME, Wang S-J, Sen L-C (2004) Foliar physiognomy in Cathaysian gigantopterids and the potential to track Palaeozoic climates using an extinct plant group. Palaeogeography, Palaeoclimatology, Palaeoecology 205, 69–110.
Crossref | GoogleScholarGoogle Scholar | open url image1

Goldberg D, Wildova R, Herben T (2008) Consistency vs. contingency of trait-performance linkages across taxa. Evolutionary Ecology 22, 477–481.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gortan E, Nardini A, Gasco A, Salleo S (2009) The hydraulic conductance of Fraxinus ornus leaves is constrained by soil water availability and coordinated with gas-exchange rates. Tree Physiology 29, 529–539.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Griffith MM (1957) Folar ontogeny of Podocarpus macrophyllus with special reference to transfusion tissue. American Journal of Botany 44, 705–715.
Crossref | GoogleScholarGoogle Scholar | open url image1

Haberlandt G (1884) ‘Physiological plant anatomy.’ (Today & Tomorrows: New Delhi, India)

Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. Journal of Experimental Botany 60, 2971–2985.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

van den Honert TH (1948) Water transport in plants as a catenary process. Discussions of the Faraday Society 3, 146–153.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jacobsen AL, Pratt RB, Davis SD, Ewers FW (2008) Comparative community physiology: nonconvergence in water relations among three semi-arid shrub communities. New Phytologist 180, 100–113.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kaldenhoff R, Ribas-Carbo M, Flexas J, Lovisolo C, Heckwolf M, Uehlein N (2008) Aquaporins and plant water balance. Plant, Cell & Environment 31, 658–666.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kraft NJB, Valencia R, Ackerly DD (2008) Functional traits and niche-based tree community assembly in an amazonian forest. Science 322, 580–582.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lambers H, Poorter H (1992) Inherent variation in growth-rate between higher-plants – a search for physiological causes and ecological consequences. Advances in Ecological Research 23, 187–261.
Crossref | GoogleScholarGoogle Scholar | open url image1

Maherali H, Sherrard ME, Clifford MH, Latta RG (2008) Leaf hydraulic conductivity and photosynthesis are genetically correlated in an annual grass. New Phytologist 180, 240–247.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Maximov NA (1929) ‘The plant in relation to water.’ (Unwin Brothers: London)

McKown AD, Cochard H, Sack L (2010) Decoding leaf hydraulics with a spatially explicit model: principles of venation architecture and implications for its evolution. The American Naturalist 175, 447–460.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Meidner H (1976) Water vapor loss from a physical model of a substomatal cavity. Journal of Experimental Botany 27, 691–694.
Crossref | GoogleScholarGoogle Scholar | open url image1

Meinzer FC (2002) Co-ordination of vapour and liquid phase water transport properties in plants. Plant, Cell & Environment 25, 265–274.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nardini A, Salleo S (2003) Effects of the experimental blockage of the major veins on hydraulics and gas exchange of Prunus laurocerasus L. leaves. Journal of Experimental Botany 54, 1213–1219.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nardini A, Gortan E, Salleo S (2005) Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species. Functional Plant Biology 32, 953–961.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niinemets U, Portsmuth A, Tobias M (2006) Leaf size modifies support biomass distribution among stems, petioles and mid-ribs in temperate plants. New Phytologist 171, 91–104.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets U, Portsmuth A, Tena D, Tobias M, Matesanz S, Valladares F (2007a) Do we underestimate the importance of leaf size in plant economics? Disproportional scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100, 283–303.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niinemets U, Portsmuth A, Tobias M (2007b) Leaf shape and venation pattern alter the support investments within leaf lamina in temperate species: a neglected source of leaf physiological differentiation? Functional Ecology 21, 28–40.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niklas KJ (1992) ‘Plant biomechanics: an engineering approach to plant form and function.’ (University of Chicago Press: Chicago)

Nobel PS (2005) ‘Physicochemical and environmental plant physiology.’ 3rd edn. (Elsevier: Burlington, MA)

Noblin X, Mahadevan L, Coomaraswamy IA, Weitz DA, Holbrook NM, Zwieniecki MA (2008) Optimal vein density in artificial and real leaves. Proceedings of the National Academy of Sciences of the United States of America 105, 9140–9144.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pearcy RW, Osteryoung K, Randall D (1982) Carbon-dioxide exchange characteristics of C4 Hawaiian Euphorbia species native to diverse habitats. Oecologia 55, 333–341.
Crossref | GoogleScholarGoogle Scholar | open url image1

Pesacreta TC, Hasenstein KH (1999) The internal cuticle of Cirsium horridulum (Asteraceae) leaves. American Journal of Botany 86(7), 923–928.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rao AN, Singaray M (1968) Controlled differentiation of foliar sclereids in Fagraea fragrans. Experientia 24, 298–299.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rao TA, Nayak P, Chakraborti S (1985) Foliar sclereids in Persoonia R.Br. ex Knight (Proteaceae). Current Science 54, 350–353. open url image1

Raven JA (1977) Evolution of vascular land plants in relation to supracellular transport processes. Advances in Botanical Research 5, 153–219.
Crossref | GoogleScholarGoogle Scholar | open url image1

Roth A, Mosbrugger V, Belz G, Neugebauer HJ (1995) Hydrodynamic modelling study of angiosperm leaf venation types. Botanica Acta 108, 121–126. open url image1

Roth-Nebelsick A, Uhl D, Mosbrugger V, Kerp H (2001) Evolution and function of leaf architecture: a review. Annals of Botany 87, 553–566.
Crossref | GoogleScholarGoogle Scholar | open url image1

Royer DL, Sack L, Wilf P, Lusk CH, Jordan GJ , et al . (2007) Fossil leaf economics quantified: calibration, Eocene case study, and implications. Paleobiology 33, 574–589.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology 87, 483–491.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Physiology and Molecular Biology 57, 361–381. open url image1

Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53, 2177–2184.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26, 1343–1356.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sack L, Streeter C, Holbrook NM (2004) Hydraulic analysis of water flow through sugar maple and red oak. Plant Physiology 134, 1824–1833.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sack L, Dietrich EM, Streeter CM, Sanchez-Gomez D, Holbrook NM (2008) Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proceedings of the National Academy of Sciences of the United States of America 105, 1567–1572.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Saldaña A, Lusk CH, Gonzáles WL, Gianoli E (2007) Natural selection on ecophysiological traits of a fern species in a temperate rainforest. Evolutionary Ecology 21, 651–662.
Crossref | GoogleScholarGoogle Scholar | open url image1

Santiago LS, Goldstein G, Meinzer FC, Fisher JB, Machado K, Woodruff D, Jones T (2004) Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia 140, 543–550.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Scoffoni C, Pou A, Aasamaa K, Sack L (2008) The rapid light response of leaf hydraulic conductance: new evidence from two experimental methods. Plant, Cell & Environment 31, 1803–1812.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Smith WK, Vogelmann TC, DeLucia EH, Bell DT, Shepherd KA (1997) Leaf form and photosynthesis. Bioscience 47, 785–793.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS (2003) Evolution of water transport and xylem structure. International Journal of Plant Sciences 164, S115–S127.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tomlinson PB, Fisher JB (2005) Development of nonlignified fibers in leaves of Gnetum gnemon (Gnetales). American Journal of Botany 92, 383–389.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tyree MT (2002) ‘Xylem structure and the ascent of sap.’ (Springer-Verlag: Berlin)

Tyree MT, Yianoulis P (1980) The site of water evaporation from substomatal cavities, liquid path resistances and hydroactive stomatal closure. Annals of Botany 46, 175–193. open url image1

Uhl D, Mosbrugger V (1999) Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeography, Palaeoclimatology, Palaeoecology 149, 15–26.
Crossref | GoogleScholarGoogle Scholar | open url image1

Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytologist 183, 13–26.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wagner WH (1979) Reticulate veins in the systematics of modern ferns. Taxon 28, 87–95.
Crossref | GoogleScholarGoogle Scholar | open url image1

Westoby M, Wright IJ (2003) The leaf size-twig size spectrum and its relationship to other important spectra of variation among species. Oecologia 135, 621–628.
PubMed |
open url image1

Woodruff DR, Meinzer FC, Lachenbruch B (2008) Height-related trends in leaf xylem anatomy and shoot hydraulic characteristics in a tall conifer: safety versus efficiency in water transport. New Phytologist 180, 90–99.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Worsdell WC (1897) On ‘transfusion tissue’: its origin and function in the leaves of gymnospermous plants. Transactions of the Linnean Society London; Botanical Series II 5, 301–319.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al . (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wullschleger SD, Oosterhuis DM (1989) The occurrence of an internal cuticle in cotton (Gossypium hirsutum L.) leaf stomates. Environmental and Experimental Botany 29, 229–235.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wylie RB (1951) Principles of foliar organization shown by sun-shade leaves from 10 species of deciduous dicotyledonous trees. American Journal of Botany 38, 355–361.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wylie RB (1952) The bundle sheath extension in leaves of dicotyledons. American Journal of Botany 39, 645–651.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zhang W, Hu YX, Li ZY, Wang PS, Xu M (2009) Foliar sclereids in tea and its wild allies, with reference to their taxonomy. Australian Systematic Botany 22, 286–295.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zwieniecki MA, Boyce CK, Holbrook NM (2004a) Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape. Annals of Botany 94, 507–513.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zwieniecki MA, Boyce CK, Holbrook NM (2004b) Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant, Cell & Environment 27, 357–365.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zwieniecki MA, Stone HA, Leigh A, Boyce CK, Holbrook NM (2006) Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant, Cell & Environment 29, 803–809.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zwieniecki MA, Brodribb TJ, Holbrook NM (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant, Cell & Environment 30, 910–921.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1