Coordination of stem and leaf traits define different strategies to regulate water loss and tolerance ranges to aridity.

SurEau model drought embolism resistance intraspecific variation leaf economic spectrum plant hydraulics tree mortality

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
04 2021
Historique:
received: 12 08 2020
accepted: 31 12 2020
pubmed: 17 1 2021
medline: 15 5 2021
entrez: 16 1 2021
Statut: ppublish

Résumé

Adaptation to drought involves complex interactions of traits that vary within and among species. To date, few data are available to quantify within-species variation in functional traits and they are rarely integrated into mechanistic models to improve predictions of species response to climate change. We quantified intraspecific variation in functional traits of two Hakea species growing along an aridity gradient in southeastern Australia. Measured traits were later used to parameterise the model SurEau to simulate a transplantation experiment to identify the limits of drought tolerance. Embolism resistance varied between species but not across populations. Instead, populations adjusted to drier conditions via contrasting sets of trait trade-offs that facilitated homeostasis of plant water status. The species from relatively mesic climate, Hakea dactyloides, relied on tight stomatal control whereas the species from xeric climate, Hakea leucoptera dramatically increased Huber value and leaf mass per area, while leaf area index (LAI) and epidermal conductance (g

Identifiants

pubmed: 33452823
doi: 10.1111/nph.17185
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

497-509

Informations de copyright

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.

Références

Aranda I, Bahamonde HA, Sanchez-Gomez D. 2017. Intra-population variability in the drought response of a beech (Fagus sylvatica L.) population in the southwest of Europe. Tree Physiology 37: 938-949.
Ay J-S, Guillemot J, Martin-StPaul N, Doyen L, Leadley P. 2017. The economics of land use reveals a selection bias in tree species distribution models. Global Ecology and Biogeography 26: 65-77.
Bartlett MK, Klein T, Jansen S, Choat B, Sack L. 2016. The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proceedings of the National Academy of Sciences, USA 113: 13098-13103.
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. Ecology Letters 15: 393-405.
Benito Garzón M, Alía R, Robson TM, Zavala MA. 2011. Intra-specific variability and plasticity influence potential tree species distributions under climate change. Global Ecology and Biogeography 20: 766-778.
Blackman CJ, Brodribb TJ. 2011. Two measures of leaf capacitance: insights into the water transport pathway and hydraulic conductance in leaves. Functional Plant Biology 38: 118-126.
Blackman CJ, Creek D, Maier C, Aspinwall MJ, Drake JE, Pfautsch S, O’Grady A, Delzon S, Medlyn BE, Tissue DT et al. 2019. Drought response strategies and hydraulic traits contribute to mechanistic understanding of plant dry-down to hydraulic failure. Tree Physiology 39: 910-924.
Blackman CJ, Li X, Choat B, Rymer PD, De Kauwe MG, Duursma RA, Tissue DT, Medlyn BE. 2019. Desiccation time during drought is highly predictable across species of Eucalyptus from contrasting climates. New Phytologist 224: 632-643.
Brodribb TJ, Holbrook NM, Edwards EJ, Gutiérrez MV. 2003. Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant, Cell & Environment 26: 443-450.
Brodribb TJ, Powers J, Cochard H, Choat B. 2020. Hanging by a thread? Forests and drought. Science 368: 261-266.
Cano FJ, López R, Warren CR. 2014. Implications of the mesophyll conductance to CO2 for photosynthesis and water-use efficiency during long-term water stress and recovery in two contrasting Eucalyptus species. Plant, Cell & Environment 37: 2470-2490.
Cardillo M, Weston PH, Reynolds ZKM, Olde PM, Mast AR, Lemmon EM, Lemmon AR, Bromham L. 2017. The phylogeny and biogeography of Hakea (Proteaceae) reveals the role of biome shifts in a continental plant radiation. Evolution 71: 1928-1943.
Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. 2009. Towards a worldwide wood economics spectrum. Ecology Letters 12: 351-366.
Choat B, Brodribb TJ, Brodersen CR, Duursma RA, López R, Medlyn BE. 2018. Triggers of tree mortality under drought. Nature 558: 531-539.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
Christoffersen BO, Gloor M, Fauset S, Fyllas NM, Galbraith DR, Baker TR, Kruijt B, Rowland L, Fisher RA, Binks OJ. 2016. Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS v.1-Hydro). Geoscientific Model Development Discussions 9: 4227-4255.
Cochard H, Damour G, Bodet C, Tharwat I, Poirier M, Améglio T. 2005. Evaluation of a new centrifuge technique for rapid generation of xylem vulnerability curves. Physiologia Plantarum 124: 410-418.
Cochard H, Pimont F, Ruffault J, Martin-StPaul N. 2020. SurEau.c: a mechanistic model of plant water relations under extreme drought. bioRxiv. doi: 10.1101/2020.05.10.086678.
Duursma RA, Blackman CJ, Lopéz R, Martin-StPaul NK, Cochard H, Medlyn BE. 2019. On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytologist 221: 693-705.
Duursma R, Choat B. 2017. fitplc - an R package to fit hydraulic vulnerability curves. Journal of Plant Hydraulics 4: e002.
Farquhar GD, Von Caemmerer SV, Berry J. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78-90.
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb TJ, Bucci SJ, Cao KF et al. 2016. Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species. New Phytologist 209: 123-136.
Groom PK, Lamont BB. 1997. Xerophytic implications of increased sclerophylly: interactions with water and light in Hakea psilorrhyncha seedlings. New Phytologist 136: 231-237.
Holtta T, Cochard H, Nikinmaa E, Mencuccini M. 2009. Capacitive effect of cavitation in xylem conduits: results from a dynamic model. Plant, Cell & Environment 32: 10-21.
IPCC. 2014. AR5 synthesis report: climate change 2014. Geneva, Switzerland: IPCC. [WWW document] URL https://www.ipcc.ch/report/ar5/syr/
Jarvis PG, Monteith JL, Weatherley PE. 1976. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philosophical Transactions of the Royal Society of London B: Biological Sciences 273: 593-610.
Journé V, Barnagaud J-Y, Bernard C, Crochet P-A, Morin X. 2020. Correlative climatic niche models predict real and virtual species distributions equally well. Ecology 101: e02912.
Lamont BB, Groom PK, Cowling RM. 2002. High leaf mass per area of related species assemblages may reflect low rainfall and carbon isotope discrimination rather than low phosphorus and nitrogen concentrations. Functional Ecology 16: 403-412.
Lamont BB, Groom PK, Williams M, He T. 2015. LMA, density and thickness: recognizing different leaf shapes and correcting for their nonlaminarity. New Phytologist 207: 942-947.
Lamont BB, He T, Lim SL. 2016. Hakea, the world’s most sclerophyllous genus, arose in southwestern Australian heathland and diversified throughout Australia over the past 12 million years. Australian Journal of Botany 64: 77-88.
Lanning M, Wang L, Novick KA. 2020. The importance of cuticular permeance in assessing plant water-use strategies. Tree Physiology 40: 425-432.
Lens F, Picon-Cochard C, Delmas CE, Signarbieux C, Buttler A, Cochard H, Jansen S, Chauvin T, Doria LC, Del Arco M et al. 2016. Herbaceous angiosperms are not more vulnerable to drought-induced embolism than angiosperm trees. Plant Physiology 172: 661-667.
Li L, McCormack ML, Ma C, Kong D, Zhang Q, Chen X, Zeng H, Niinemets Ü, Guo D. 2015. Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecology Letters 18: 899-906.
Limousin J-M, Rambal S, Ourcival J-M, Rodríguez-Calcerrada J, Pérez-Ramos IM, Rodríguez-Cortina R, Misson L, Joffre R. 2012. Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought. Oecologia 169: 565-577.
López R, López de Heredia U, Collada C, Cano FJ, Emerson BC, Cochard H, Gil L. 2013. Vulnerability to cavitation, hydraulic efficiency, growth and survival in an insular pine (Pinus canariensis). Annals of Botany 111: 1167-1179.
López R, Nolf M, Duursma RA, Badel E, Flavel RJ, Cochard H, Choat B. 2018. Mitigating the open vessel artefact in centrifuge-based measurement of embolism resistance. Tree Physiology 39: 143-155.
López R, Rodríguez-Calcerrada J, Gil L. 2009. Physiological and morphological response to water deficit in seedlings of five provenances of Pinus canariensis: potential to detect variation in drought-tolerance. Trees- Structure and Function 23: 509-519.
Martinez-Vilalta J, Cochard H, Mencuccini M, Sterck F, Herrero A, Korhonen JF, Llorens P, Nikinmaa E, Nole A, Poyatos R et al. 2009. Hydraulic adjustment of Scots pine across Europe. New Phytologist 184: 353-364.
Martin-StPaul N, Delzon S, Cochard H. 2017. Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20: 1437-1447.
Martin-StPaul NK, Limousin JM, Vogt-Schilb H, Rodriguez-Calcerrada J, Rambal S, Longepierre D, Misson L. 2013. The temporal response to drought in a Mediterranean evergreen tree: comparing a regional precipitation gradient and a throughfall exclusion experiment. Global Change Biology 19: 2413-2426.
Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR. 2009. Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Functional Ecology 23: 922-930.
Mencuccini M, Grace J. 1995. Climate influences the leaf area/sapwood area ratio in Scots pine. Tree Physiology 15: 1-10.
Mencuccini M, Rosas T, Rowland L, Choat B, Cornelissen H, Jansen S, Kramer K, Lapenis A, Manzoni S, Niinemets Ü. 2019. Leaf economics and plant hydraulics drive leaf: wood area ratios. New Phytologist 224: 1544-1556.
Mitchell PJ, Veneklaas EJ, Lambers H, Burgess SS. 2008. Leaf water relations during summer water deficit: differential responses in turgor maintenance and variation in leaf structure among different plant communities in south-western Australia. Plant, Cell & Environment 31: 1791-1802.
Nardini A, Casolo V, Dal Borgo A, Savi T, Stenni B, Bertoncin P, Zini L, McDowell NG. 2016. Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant, Cell & Environment 39: 618-627.
Parmesan C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution, and Systematics 37: 637-669.
Peters JMR, Gauthey A, Lopez R, Carins-Murphy MR, Brodribb TJ, Choat B. 2020. Non-invasive imaging reveals convergence in root and stem vulnerability to cavitation across five tree species. Journal of Experimental Botany 71: 6623-6637.
Petherick L, Bostock H, Cohen TJ, Fitzsimmons K, Tibby J, Fletcher M-S, Moss P, Reeves J, Mooney S, Barrows T. 2013. Climatic records over the past 30 ka from temperate Australia-a synthesis from the Oz-INTIMATE workgroup. Quaternary Science Reviews 74: 58-77.
Pfautsch S, Harbusch M, Wesolowski A, Smith R, Macfarlane C, Tjoelker MG, Reich PB, Adams MA. 2016. Climate determines vascular traits in the ecologically diverse genus Eucalyptus. Ecology Letters 19: 240-248.
Pivovaroff AL, Pasquini SC, De Guzman ME, Alstad KP, Stemke JS, Santiago LS. 2016. Multiple strategies for drought survival among woody plant species. Functional Ecology 30: 517-526.
Pivovaroff AL, Sack L, Santiago LS. 2014. Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis. New Phytologist 203: 842-850.
Pockman WT, Sperry JS. 2000. Vulnerability to xylem cavitation and the distribution of Sonoran desert vegetation. American Journal of Botany 87: 1287-1299.
Powell TL, Koven CD, Johnson DJ, Faybishenko B, Fisher RA, Knox RG, McDowell NG, Condit R, Hubbell SP, Wright SJ. 2018. Variation in hydroclimate sustains tropical forest biomass and promotes functional diversity. New Phytologist 219: 932-946.
Powell TL, Wheeler JK, de Oliveira AAR, da Costa ACL, Saleska SR, Meir P, Moorcroft PR. 2017. Differences in xylem and leaf hydraulic traits explain differences in drought tolerance among mature Amazon rainforest trees. Global Change Biology 23: 4280-4293.
R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/.
Rambal S, Lempereur M, Limousin J, Martin-StPaul N, Ourcival J, Rodríguez-Calcerrada J. 2014. How drought severity constrains gross primary production (GPP) and its partitioning among carbon pools in a Quercus ilex coppice? Biogeosciences 11: 6855-6869.
Ramírez-Valiente JA, Sánchez-Gómez D, Aranda I, Valladares F. 2010. Phenotypic plasticity and local adaptation in leaf ecophysiological traits of 13 contrasting cork oak populations under different water availabilities. Tree Physiology 30: 618-627.
Reich PB. 2014. The world-wide ‘fast-slow’plant economics spectrum: a traits manifesto. Journal of Ecology 102: 275-301.
Reich PB, Wright I, Cavender-Bares J, Craine J, Oleksyn J, Westoby M, Walters M. 2003. The evolution of plant functional variation: traits, spectra, and strategies. International Journal of Plant Sciences 164(S3): S143-S164.
Rodríguez-Calcerrada J, Li M, López R, Cano FJ, Oleksyn J, Atkin OK, Pita P, Aranda I, Gil L. 2017. Drought-induced shoot dieback starts with massive root xylem embolism and variable depletion of nonstructural carbohydrates in seedlings of two tree species. New Phytologist 213: 597-610.
Rosas T, Mencuccini M, Barba J, Cochard H, Saura-Mas S, Martínez-Vilalta J. 2019. Adjustments and coordination of hydraulic, leaf and stem traits along a water availability gradient. New Phytologist 223: 632-646.
Sack L, Tyree MT. 2005. Leaf hydraulics and its implications in plant structure and function. Vascular transport in plants. San Diego, CA, USA: Elsevier, 93-114.
Savolainen O, Pyhäjärvi T, Knürr T. 2007. Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution, and Systematics 38: 595-619.
Specht R, Specht A. 1989. Canopy structure in Eucalyptus-dominated communities in Australia along climatic gradients. Acta oecologica. Oecologia plantarum 10: 191-213.
Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR. 2015. Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiology 167: 40-43.
Tyree M, Hammel H. 1972. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23: 267-282.
Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH, Hulshof C, Jung V, Messier J. 2012. The return of the variance: intraspecific variability in community ecology. Trends in ecology & evolution 27: 244-252.
Warren CR, Aranda I, Cano FJ. 2011. Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant, Cell & Environment 34: 1609-1629.
West AG, Dawson TE, February EC, Midgley GF, Bond WJ, Aston TL. 2012. Diverse functional responses to drought in a Mediterranean-type shrubland in South Africa. New Phytologist 195: 396-407.
Westoby M. 1998. The relationship between local and regional diversity: comment. Ecology 79: 1825-1827.
Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM. 2013. Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant, Cell & Environment 36: 1938-1949.
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M. 2004. The worldwide leaf economics spectrum. Nature 428: 821.
Wright IJ, Westoby M. 2002. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist 155: 403-416.
Xu X, Medvigy D, Powers JS, Becknell JM, Guan K. 2016. Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests. New Phytologist 212: 80-95.

Auteurs

Rosana López (R)

Departamento de Sistemas y Recursos Naturales, Universidad Politécnica de Madrid, Madrid, 28040, Spain.

Francisco Javier Cano (FJ)

Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia.

Hervé Cochard (H)

Université Clermont-Auvergne, INRA, PIAF, Clermont-Ferrand, 63000, France.

Brendan Choat (B)

Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia.

Articles similaires

Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Animals Dietary Fiber Dextran Sulfate Mice Disease Models, Animal
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria
Fragaria Light Plant Leaves Osmosis Stress, Physiological

Classifications MeSH