Summary
In most terrestrial ecosystems, water availability is the principal governor of primary productivity. Vascular plants can only sustain high rates of photosynthetic activity by transporting enormous quantities of water from reserves in the soil to the sites of gas exchange in leaves to prevent desiccation of photosynthetic tissues. This demand for water requires plants to invest in a vascular system that begins as a simple pipe system in roots and branches and terminates in a sophisticated network of veins in the leaf. This chapter will examine the tight linkage between photosynthesis and the efficiency of water transport in leaves, explaining how plants use a non-living network of xylem to deliver water under high tension to evaporating cells. We explore how plants achieve high efficiency in water delivery by developing an intricately branched system of leaf veins as a means of piping water close to the stomatal layer, and how evolution has shaped the venation of higher plant species as densely reticulated networks.
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Abbreviations
- ∆ψ :
-
difference in water potential
- ABA:
-
abscisic acid
- F :
-
flux rate of water
- K :
-
hydraulic conductance
- K leaf :
-
hydraulic conductance of the leaf
- K ox :
-
Definition
- K x :
-
Definition
- MPa:
-
megapascals
- ψ :
-
water potential
References
Aasamaa K, Sober A, Rahi M (2001) Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Aust J Plant Physiol 28:765–774
Aasamaa K, Niinemets U, Sober A (2005) Leaf hydraulic conductance in relation to anatomical and functional traits during Populus tremula leaf ontogeny. Tree Physiol 25:1409–1418
Adams WW III, Watson AM, Mueh KE, Amiard V, Turgeon R, Ebbert V, Demmig-Adams B (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynth Res 94:455–466
Andrade LJ, Meinzer CF, Goldstein G, Holbrook MN, Cavelier J, Jackson P, Silvera K (1998) Regulation of water flux through trunks, branches, and leaves in trees of a lowland tropical forest. Oecologia 115:463–471
Angeles G, Bond B, Boyer J, Brodribb T, Brooks J, Burns M, Comstock J (2004) The cohesion-tension theory. New Phytol 163:451–452
Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405
Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123
Blackman CJ, Brodribb TJ (2011) Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Funct Plant Biol 38:118–126
Blonder B, Violle C, Bentley LP, Enquist BJ (2011) Venation networks and the origin of the leaf economics spectrum. Ecol Lett 14:91–100
Blonder B, Violle C, Enquist BJ (2013) Assessing the causes and scales of the leaf economics spectrum using venation networks in Populus tremuloides. J Ecol 101:981–989
Boyce CK, Cody GD, Fogel ML, Hazen RM, Alexander CMD, Knoll AH (2003) Chemical evidence for cell wall lignification and the evolution of tracheids in early Devonian plants. Intl J Plant Sci 164:691–702
Boyce CK (2005) Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31:117–140
Boyce CK (2008) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34:179–194
Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. P Roy Soc Lond Series B Bio 276:1771–1776
Boyce CK, Zwieniecki MA (2012) Leaf fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm evolution. Proc Natl Acad Sci U S A 109:10403–10408
Brodribb T, Feild T, Jordan G (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898
Brodribb TJ, Hill RS (1999) The importance of xylem constraints in the distribution of conifer species. New Phytol 143:365–372
Brodribb TJ, Feild TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant Cell Environ 23:1381–1388
Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173
Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139–1146
Brodribb TJ, Holbrook NM, Zwieniecki MA, Palma B (2005) Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima. New Phytol 165:839–846
Brodribb TJ, Holbrook NM (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant Cell Environ 29:2205–2215
Brodribb TJ (2009) Xylem hydraulic physiology: the functional backbone of terrestrial plant productivity. Plant Sci 177:245–251
Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecol Lett 13:175–183
Brodribb TJ, Jordan GJ (2011) Water supply and demand remain balanced during leaf acclimation of Nothofagus cunninghamii trees. New Phytol 192:437–448
Brodribb TJ, McAdam SAM (2011) Passive origins of stomatal control in vascular plants. Science 331:582–585
Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytol 199:559–570
Brodribb TJ, Skelton RP, McAdam SA, Bienaimé D, Lucani CJ, Marmottant P (2016) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytol 209:1403–1409
Buckley TN, Sack L, Gilbert ME (2011) The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiol 156:962–973
Buckley TN (2015) The contributions of apoplastic, symplastic and gas phase pathways for water transport outside the bundle sheath in leaves. Plant Cell Environ 38:7–22
Carafa A, Duckett JG, Knox JP, Ligrone R (2005) Distribution of cell-wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants. New Phytol 168:231–240
Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28:1082–1089
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, . . . Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 7426: 752--755, 491
Cochard H, Coll L, Le Roux X, Ameglio T (2002) Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol 128:282–290
Cochard H, Froux F, Mayr S, Coutard C (2004a) Xylem wall collapse in water-stressed pine needles. Plant Physiol 134:401–408
Cochard H, Nardini A, Coll L (2004b) Hydraulic architecture of leaf blades: where is the main resistance? Plant Cell Environ 27:1257–1267
Cochard H, Venisse JS, Barigah TS, Brunel N, Herbette S, Guilliot A, Sakr S (2007) Putative role of aquaporins in variable hydraulic conductance of leaves in response to light. Plant Physiol 143:122–133
Cowan IR, Farquhar GD (1977) Stomatal function in relation to leaf metabolism and environment. Symp Soc Exp Biol 31:471–505
Darwin F (1898) Observations on stomata. P Roy Soc Lond Series B Biol 63:413–417
Diefendorf AF, Mueller KE, Wing SL, Koch PL, Freeman KH (2010) Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proc Natl Acad Sci U S A 107:5738–5743
Dixon HH, Joly J (1895) On the ascent of sap. Philos T Roy Soc Lond 186:563–576
Edwards D (2003) Xylem in early tracheophytes. Plant Cell Environ 26:57–72
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
Feild TS, Upchurch GR, Chatelet DS, Brodribb TJ, Grubbs KC, Samain MS, Wanke S (2011) Fossil evidence for low gas exchange capacities for early cretaceous angiosperm leaves. Paleobiology 37:195–213
Feild TS, Brodribb TJ (2013) Hydraulic tuning of vein cell microstructure in the evolution of angiosperm venation networks. New Phytol 199:720–726
Fiorin L, Brodribb TJ, Anfodillo T (2015) Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves. New Phytol 209:216–227
Franks PJ (2006) Higher rates of leaf gas exchange are associated with higher leaf hydrodynamic pressure gradients. Plant Cell Environ 29:584–592
Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philos T Ro Soc Lond B 367:537–546
Givnish T (1986) Optimal stomatal conductance, allocation of energy between leaves and roots, and the marginal cost of transpiration. In: Givnish TJ (ed) On the economy of plant form and function. Cambridge University Press, New York, pp 171–214
Hao G-Y, Hoffmann WA, Scholz FG, Bucci SJ, Meinzer FC, Franco AC, Goldstein G (2007) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155:405–415
Heinen RB, Ye Q, Chaumont F (2009) Role of aquaporins in leaf physiology. J Exp Bot 60:2971–2985
Henzler T, Waterhouse NR, Smyth JA, Carvajal M, Cooke TD, Schäffner RA, Clarkson TD (1999) Diurnal variations in hydraulic conductivity and root pressure can be correlated with the expression of putative aquaporins in the roots of Lotus japonicus. Planta 210:50–60
Hubbard RM, Ryan MG, Stiller V, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24:113–121
Jones HG, Sutherland RA (1991) Stomatal control of xylem embolism. Plant Cell Environ 14:607–612
Katifori E, Szöllősi GJ, Magnasco MO (2010) Damage and fluctuations induce loops in optimal transport networks. Phys Rev Lett 104:048704
Kim YX, Steudle E (2007) Light and turgor affect the water permeability (aquaporins) of parenchyma cells in the midrib of leaves of Zea mays. J Exp Bot 58:4119–4129
Knipfer T, Eustis A, Brodersen C, Walker AM, McElrone AJ (2015) Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure. Plant Cell Environ 38:1503–1513
Komatsu K, Suzuki N, Kuwamura M, Nishikawa Y, Nakatani M, Ohtawa H, Sakata Y (2013) Group a PP2Cs evolved in land plants as key regulators of intrinsic desiccation tolerance. Nat Commun 4:2219
Körner C, Farquhar GD, Roksandic Z (1988) A global survey of carbon isotope discrimination in plants from high altitude. Oecologia 74:623–632
Lehmann P, Or D (2015) Effects of stomata clustering on leaf gas exchange. New Phytol 207:1015–1025
Li L, McCormack ML, Ma C, Kong D, Zhang Q, Chen X, Guo D (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906
Li S, Zhang Y-J, Sack L, Scoffoni C, Ishida A, Chen Y-J, Cao K-F (2013) The heterogeneity and spatial patterning of structure and physiology across the leaf surface in giant leaves of Alocasia macrorrhiza. PLoS One 8:e66016
Ligrone R, Vaughn KC, Renzaglia KS, Knox PJ, Duckett JG (2002) Diversity in the distribution of polysaccharide and glycoprotein epitopes in the cell walls of bryophytes: new evidence for the multiple evolution of water-conducting cells. New Phytol 156:491–508
Ligrone R, Duckett JG, Renzaglia KS (2012) Major transitions in the evolution of early land plants: a bryological perspective. Ann Bot 109:851–871
Maherali H, Sherrard ME, Clifford MH, Latta RG (2008) Leaf hydraulic conductivity and photosynthesis are genetically correlated in an annual grass. New Phytol 180:240–247
McAdam SAM, Brodribb TJ (2012) Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24:1510–1521
McAdam SA, Brodribb TJ (2015) The evolution of mechanisms driving the stomatal response to vapor pressure deficit. Plant Physiol 167: 833—843
Meinzer FC, Grantz DA (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity. Plant Cell Environ 13:383–388
Muller O, Cohu CM, Stewart JJ, Protheroe JA, Demmig-Adams B, Adams WW III (2014) Association between photosynthesis and contrasting features of minor veins in leaves of summer annuals loading phloem via symplastic versus apoplastic routes. Physiol Plant 152:174–183
Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing xylem cavitation? Trees 15:14–24
Nardini A, Tyree MT, Salleo S (2001) Xylem cavitation in the leaf of Prunus laurocerasus L. and its impact on leaf hydraulics. Plant Physiol 125:1700–1709
Nardini A, Salleo S, Andri S (2005) Circadian regulation of leaf hydraulic conductance in sunflower (Helianthus annuus). Plant Cell Environ 28:750–759
Noblin X, Mahadevan L, Coomaraswamy IA, Weitz DA, Holbrook NM, Zwieniecki MA (2008) Optimal vein density in artificial and real leaves. Proc Natl Acad Sci U S A 105:9140–9144
Nolf M, Creek D, Duursma R, Holtum J, Mayr S, Choat B (2015) Stem and leaf hydraulic properties are finely coordinated in three tropical rain forest tree species. Plant Cell Environ 38:2652–2661
Oren R, Sperry JS, Katul G, Pataki DE, Ewers BE, Phillips N, Schäfer KVR (1999) Survey and synthesis of intra- and inter specific variation in stomatal sensitivity to vapor pressure deficit. Plant Cell Environ 22:1515–1526
Parent B, Hachez C, Redondo E, Simonneau T, Chaumont F, Tardieu F (2009) Drought and abscisic acid effects on aquaporin content translate into changes in hydraulic conductivity and leaf growth rate: a trans-scale approach. Plant Physiol 149:2000–2012
Peak D, Mott KA (2011) A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant Cell Environ 34:162–178
Pressel S, Goral T, Duckett JG (2014) Stomatal differentiation and abnormal stomata in hornworts. J Bryol 36:87–103
Raschke K, Resemann A (1986) The midday depression of CO2 assimilation in leaves of Arbutus unedo L.: diurnal changes in photosynthetic capacity related to changes in temperature and humidity. Planta 168:546–558
Raven JA (1977) Evolution of vascular land plants in relation to supracellular transport processes. Adv Bot Res 5:153–219
Reich PB (2014) The worldwide ‘fast–slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301
Rockwell FE, Holbrook NM, Stroock AD (2014) The competition between liquid and vapor transport in transpiring leaves. Plant Physiol 164:1741–1758
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. J Exp Bot 53:2177–2184
Sack L, Streeter C, Holbrook NM (2004) Hydraulic analysis of water flow through sugar maple and red oak. Plant Physiol 134:1824–1833
Sack L, Tyree MT, Holbrook NM (2005) Leaf hydraulic architecture correlates with regenreration irradiance in tropical rainforest trees. New Phytol 167:403–413
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology 87:483–491
Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Physiol Mol Biol 57:361–381
Sack L, Scoffoni C (2013) Leaf venation: structure, function, development, evolution, ecology and applications in the past, present and future. New Phytol 198:983–1000
Sack L, Scoffoni C, John GP, Poorter H, Mason CM, Mendez-Alonzo R, Donovan LA (2013) How do leaf veins influence the worldwide leaf economic spectrum? Review and synthesis. J Exp Bot 64:4053–4080
Saliendra N, Sperry J, Comstock J (1995) Influence of leaf water status on stomatal response to humidity, hydraulic conductance, and soil drought in Betula occidentalis. Planta 196:357–366
Scoffoni C, Rawls M, McKown A, Cochard H, Sack L (2011) Decline of leaf hydraulic conductance with dehydration: relationship to leaf size and venation architecture. Plant Physiol 156:832–843
Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. Plant Physiol 164:1772–1788
Skelton RP, Brodribb TJ, Choat B (2017) Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation. New Phytol 214:561–569
Sperry JS, Adler FR, Campbell GS, Comstock JP (1998) Limitation of plant water use by rhizosphere and xylem conductance: results from a model. Plant Cell Environ 21:347–359
Tyree MT, Cruiziat P, Benis M, Lo Gullo MA, Salleo S (1981) The kinetics of rehydration of detached sunflower leaves from different initial water deficits. Plant Cell Environ 4:309–317
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Physiol Plant Mol Biol 40:19–38
Tyree MT, Sinclair B, Lu P, Granier A (1993) Whole shoot hydraulic resistance in Quercus species measured with a new high-pressure flowmeter. Ann Forest Sci 50:417–423
Tyree MT, Sobrado MA, Stratton LJ, Becker P (1999) Diversity of hydraulic conductance in leaves of temperate and tropical species: possible causes and consequences. J Trop For Sci 11:47–60
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, Berlin
Wan X, Steudle E, Hartung W (2004) Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. J Exp Bot 55:411–422
Wong SC, Cowan IR, Farquhar GD (1979) Stomatal conductance correlates with photosynthetic capacity. Nature 282:424–426
Zhang Y-J, Rockwell FE, Wheeler JK, Holbrook NM (2014) Reversible deformation of transfusion tracheids in Taxus baccata is associated with a reversible decrease in leaf hydraulic conductance. Plant Physiol 165:1557–1565
Zhu C, Schraut D, Hartung W, Schäffner AR (2005) Differential responses of maize MIP genes to salt stress and ABA. J Exp Bot 56:2971–2981
Zimmermann MH (1983) Xylem structure and the ascent of sap. Springer, Berlin
Zwieniecki MA, Brodribb TJ, Holbrook NM (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environ 30:910–921
Acknowledgments
Authors gratefully acknowledge the support of the Australian Research Council who supported TJB with a Future Fellowship during the period of writing this chapter.
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Brodribb, T.J., Buckley, T.N. (2018). Leaf Water Transport: A Core System in the Evolution and Physiology of Photosynthesis. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_4
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