Viewing leaf structure and evolution from a hydraulic perspective
Tim J. Brodribb A E , Taylor S. Feild B D and Lawren Sack CA 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.
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 |
Altalib KH, Torrey JG
(1961) Sclereid distribution in leaves of Pseudotsuga under natural and experimental conditions. American Journal of Botany 48, 71–79.
| Crossref |
Arzee T
(1953) Morphology and ontogeny of foliar sclereids in Olea europaea. 1. Distribution and structure. American Journal of Botany 40, 680–687.
| Crossref |
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 |
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 |
Berner RA
(1994) GEOCARB II: a revised model of atmospheric CO2 over Phanerozoic time. American Journal of Science 294, 56–91.
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 |
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 |
Boyer JS
(1985) Water transport. Annual Review of Plant Physiology 36, 473–516.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Brodribb TJ, Feild TS
(2008) Evolutionary significance of a flat-leaved Pinus in Vietnamese rainforest. New Phytologist 178, 201–209.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
Farquhar GD, Raschke K
(1978) Resistance to transpiration of sites of evaporation within leaf. Plant Physiology 61, 1000–1005.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
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 |
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 |
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 |
Foard DE
(1959) Pattern and control of sclereid formation in the leaf of Camellia japonica. Nature 184, 1663–1664.
| Crossref | GoogleScholarGoogle Scholar |
Foster AS
(1946) Ontogeny of the foliar sclereids in Mouriria huberi Cogn. American Journal of Botany 33, 820.
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 |
Foster AS
(1956) Plant idioblasts – remarkable examples of cell specialization. Protoplasma 46, 184–193.
| Crossref | GoogleScholarGoogle Scholar |
Franceschinelli EV, Yamamoto K
(1993) Taxonomic use of leaf anatomical characters in the genus Simarouba (Simaroubaceae). Flora 188, 117–123.
Givnish TJ
(1987) Comparative-studies of leaf form – assessing the relative roles of selective pressures and phylogenetic constraints. New Phytologist 106, 131–160.
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 |
Goldberg D,
Wildova R, Herben T
(2008) Consistency vs. contingency of trait-performance linkages across taxa. Evolutionary Ecology 22, 477–481.
| Crossref | GoogleScholarGoogle Scholar |
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 |
Griffith MM
(1957) Folar ontogeny of Podocarpus macrophyllus with special reference to transfusion tissue. American Journal of Botany 44, 705–715.
| Crossref | GoogleScholarGoogle Scholar |
Heinen RB,
Ye Q, Chaumont F
(2009) Role of aquaporins in leaf physiology. Journal of Experimental Botany 60, 2971–2985.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
van den Honert TH
(1948) Water transport in plants as a catenary process. Discussions of the Faraday Society 3, 146–153.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
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 |
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 |
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 |
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 |
Meidner H
(1976) Water vapor loss from a physical model of a substomatal cavity. Journal of Experimental Botany 27, 691–694.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
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 |
Rao AN, Singaray M
(1968) Controlled differentiation of foliar sclereids in Fagraea fragrans. Experientia 24, 298–299.
| Crossref | GoogleScholarGoogle Scholar |
Rao TA,
Nayak P, Chakraborti S
(1985) Foliar sclereids in Persoonia R.Br. ex Knight (Proteaceae). Current Science 54, 350–353.
Raven JA
(1977) Evolution of vascular land plants in relation to supracellular transport processes. Advances in Botanical Research 5, 153–219.
| Crossref | GoogleScholarGoogle Scholar |
Roth A,
Mosbrugger V,
Belz G, Neugebauer HJ
(1995) Hydrodynamic modelling study of angiosperm leaf venation types. Botanica Acta 108, 121–126.
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 |
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 |
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 |
Sack L, Holbrook NM
(2006) Leaf hydraulics. Annual Review of Plant Physiology and Molecular Biology 57, 361–381.
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 |
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 |
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 |
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 |
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 |
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 |
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 |
Smith WK,
Vogelmann TC,
DeLucia EH,
Bell DT, Shepherd KA
(1997) Leaf form and photosynthesis. Bioscience 47, 785–793.
| Crossref | GoogleScholarGoogle Scholar |
Sperry JS
(2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.
| Crossref | GoogleScholarGoogle Scholar |
Sperry JS
(2003) Evolution of water transport and xylem structure. International Journal of Plant Sciences 164, S115–S127.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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.
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 |
Vogel S
(2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytologist 183, 13–26.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wagner WH
(1979) Reticulate veins in the systematics of modern ferns. Taxon 28, 87–95.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
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 |
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 |
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 |
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 |
Wylie RB
(1952) The bundle sheath extension in leaves of dicotyledons. American Journal of Botany 39, 645–651.
| Crossref | GoogleScholarGoogle Scholar |
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 |
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 |
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 |
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 |
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 |