Thresholds for persistent leaf photochemical damage predict plant drought resilience in a tropical rainforest.

drought embolism resistance hydraulics photochemistry recovery rehydration tropical

Journal

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

Informations de publication

Date de publication:
07 2023
Historique:
received: 13 01 2023
accepted: 12 04 2023
medline: 15 6 2023
pubmed: 24 5 2023
entrez: 24 5 2023
Statut: ppublish

Résumé

Water stress can cause declines in plant function that persist after rehydration. Recent work has defined 'resilience' traits characterizing leaf resistance to persistent damage from drought, but whether these traits predict resilience in whole-plant function is unknown. It is also unknown whether the coordination between resilience and 'resistance' - the ability to maintain function during drought - observed globally occurs within ecosystems. For eight rainforest species, we dehydrated and subsequently rehydrated leaves, and measured water stress thresholds for declines in rehydration capacity and maximum quantum yield of photosystem II (F

Identifiants

pubmed: 37222272
doi: 10.1111/nph.18973
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

576-591

Informations de copyright

© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.

Références

Abid M, Tian Z, Ata-Ul-Karim ST, Wang F, Liu Y, Zahoor R, Jiang D, Dai T. 2016. Adaptation to and recovery from drought stress at vegetative stages in wheat (Triticum aestivum) cultivars. Functional Plant Biology 43: 1159-1169.
Aguilos M, Stahl C, Burban B, Hérault B, Courtois E, Coste S, Wagner F, Ziegler C, Takagi K, Bonal D. 2019. Interannual and seasonal variations in ecosystem transpiration and water use efficiency in a tropical rainforest. Forests 10: 14.
Anderegg WRL, Anderegg LDL, Berry JA, Field CB. 2014. Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off. Oecologia 175: 11-23.
Anderegg WRL, Schwalm C, Biondi F, Camarero JJ, Koch G, Litvak M, Ogle K, Shaw JD, Shevliakova E, Williams AP et al. 2015. Pervasive drought legacies in forest ecosystems and their implications for carbon cycle models. Science 349: 528-532.
Arend M, Brem A, Kuster TM, Günthardt-Goerg MS. 2013. Seasonal photosynthetic responses of European oaks to drought and elevated daytime temperature: photosynthetic responses to drought and elevated temperature. Plant Biology 15: 169-176.
Bartlett MK, Detto M, Pacala SW. 2019. Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade-offs among plant hydraulic traits. Ecology Letters 22: 67-77.
Bartlett MK, Scoffoni C, Ardy R, Zhang Y, Sun S, Cao K, Sack L. 2012a. Rapid determination of comparative drought tolerance traits: using an osmometer to predict turgor loss point. Methods in Ecology and Evolution 3: 880-888.
Bartlett MK, Scoffoni C, Sack L. 2012b. 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.
Bartlett MK, Klein T, Jansen S, Choat B, Sack L. 2016a. 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, Zhang Y, Yang J, Kreidler N, Sun S-W, Lin L, Hu Y-H, Cao K-F, Sack L. 2016b. Drought tolerance as a driver of tropical forest assembly: resolving spatial signatures for multiple processes. Ecology 97: 503-514.
Binks O, Meir P, Rowland L, Costa ACL, Vasconcelos SS, Oliveira AAR, Ferreira L, Christoffersen B, Nardini A, Mencuccini M. 2016. Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytologist 211: 477-488.
Blackman CJ, Brodribb TJ, Jordan GJ. 2009. Leaf hydraulics and drought stress: response, recovery and survivorship in four woody temperate plant species. Plant, Cell & Environment 32: 1584-1595.
Brodribb T, Brodersen CR, Carriqui M, Tonet V, Rodriguez Dominguez C, McAdam S. 2021. Linking xylem network failure with leaf tissue death. New Phytologist 232: 68-79.
Brodribb TJ, Bowman DJMS, Nichols S, Delzon S, Burlett R. 2010. Xylem function and growth rate interact to determine recovery rates after exposure to extreme water deficit. New Phytologist 188: 533-542.
Brodribb TJ, Skelton RP, McAdam SAM, Bienaimé D, Lucani CJ, Marmottant P. 2016. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209: 1403-1409.
Buckley RC, Corlett RT, Grubb PJ. 1980. Are the xeromorphic trees of tropical upper montane rain forests drought-resistant? Biotropica 12: 124.
Burlett R, Parise C, Capdeville G, Cochard H, Lamarque LJ, King A, Delzon S. 2022. Measuring xylem hydraulic vulnerability for long-vessel species: an improved methodology with the flow centrifugation technique. Annals of Forest Science 79: 5.
Burnham KP, Anderson DR. 2010. Model selection and multimodel inference: a practical information-theoretic approach. New York, NY, USA: Springer.
Campos H, Trejo C, Peña-Valdivia CB, García-Nava R, Conde-Martínez FV, Cruz-Ortega MR. 2014. Stomatal and non-stomatal limitations of bell pepper (Capsicum annuum L.) plants under water stress and re-watering: delayed restoration of photosynthesis during recovery. Environmental and Experimental Botany 98: 56-64.
Carpenter B, Gelman A, Hoffman MD, Lee D, Goodrich B, Betancourt M, Brubaker M, Guo J, Li P, Riddell A. 2017. stan: a probabilistic programming language. Journal of Statistical Software 76: 1.
Duffy PB, Brando P, Asner GP, Field CB. 2015. Projections of future meteorological drought and wet periods in the Amazon. Proceedings of the National Academy of Sciences, USA 112: 13172-13177.
Fan X-W, Li F-M, Song L, Xiong Y-C, An L, Jia Y, Fang X-W. 2009. Defense strategy of old and modern spring wheat varieties during soil drying. Physiologia Plantarum 136: 310-323.
Fletcher LR, Scoffoni C, Farrell C, Buckley TN, Pellegrini M, Sack L. 2022. Testing the association of relative growth rate and adaptation to climate across natural ecotypes of Arabidopsis. New Phytologist 236: 413-432.
Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S. 2011. Functional and phylogenetic diversity as predictors of biodiversity-ecosystem-function relationships. Ecology 92: 1573-1581.
Forner A, Aranda I, Granier A, Valladares F. 2014. Differential impact of the most extreme drought event over the last half century on growth and sap flow in two coexisting Mediterranean trees. Plant Ecology 215: 703-719.
Galbraith D, Malhi Y, Affum-Baffoe K, Castanho ADA, Doughty CE, Fisher RA, Lewis SL, Peh KS-H, Phillips OL, Quesada CA et al. 2013. Residence times of woody biomass in tropical forests. Plant Ecology & Diversity 6: 139-157.
Gould KS, Vogelmann TC, Han T, Clearwater MJ. 2002. Profiles of photosynthesis within red and green leaves of Quintinia serrata. Physiologia Plantarum 116: 127-133.
Gourlet-Fleury S, Guehl J-M, Laroussinie O, ECOFOR (Group), eds. 2004. Ecology and management of a Neotropical rainforest: lessons drawn from Paracou, a long-term experimental research site in French Guiana. Paris, France: Elsevier.
Granier A. 1987. Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiology 3: 309-320.
Guadagno CR, Ewers BE, Speckman HN, Aston TL, Huhn BJ, DeVore SB, Ladwig JT, Strawn RN, Weinig C. 2017. Dead or alive? Using membrane failure and chlorophyll a fluorescence to predict plant mortality from drought. Plant Physiology 175: 223-234.
Guan K, Pan M, Li H, Wolf A, Wu J, Medvigy D, Caylor KK, Sheffield J, Wood EF, Malhi Y et al. 2015. Photosynthetic seasonality of global tropical forests constrained by hydroclimate. Nature Geoscience 8: 284-289.
Guan X-K, Song L, Wang T-C, Turner NC, Li F-M. 2015. Effect of drought on the gas exchange, chlorophyll fluorescence and yield of six different-era spring wheat cultivars. Journal of Agronomy and Crop Science 201: 253-266.
Iqbal N, Hussain S, Raza MA, Yang C-Q, Safdar ME, Brestic M, Aziz A, Hayyat MS, Asghar MA, Wang XC et al. 2019. Drought tolerance of soybean (Glycine max L. Merr.) by improved photosynthetic characteristics and an efficient antioxidant enzyme activities under a split-root system. Frontiers in Physiology 10: 786.
John GP, Henry C, Sack L. 2018. Leaf rehydration capacity: associations with other indices of drought tolerance and environment. Plant, Cell & Environment 41: 2638-2653.
Johnson KM, Jordan GJ, Brodribb TJ. 2018. Wheat leaves embolized by water stress do not recover function upon rewatering. Plant, Cell & Environment 41: 2704-2714.
Kaiser WM. 1987. Effects of water deficit on photosynthetic capacity. Physiologia Plantarum 71: 142-149.
Kannenberg SA, Novick KA, Alexander MR, Maxwell JT, Moore DJP, Phillips RP, Anderegg WRL. 2019. Linking drought legacy effects across scales: from leaves to tree rings to ecosystems. Global Change Biology 25: 2978-2992.
Lamont BB, Lamont HC. 2000. Utilizable water in leaves of 8 arid species as derived from pressure-volume curves and chlorophyll fluorescence. Physiologia Plantarum 110: 64-71.
Lee J-E, Frankenberg C, van der Tol C, Berry JA, Guanter L, Boyce CK, Fisher JB, Morrow E, Worden JR, Asefi S et al. 2013. Forest productivity and water stress in Amazonia: observations from GOSAT chlorophyll fluorescence. Proceedings of the Royal Society B: Biological Sciences 280: 20130171.
Levionnois S, Ziegler C, Jansen S, Calvet E, Coste S, Stahl C, Salmon C, Delzon S, Guichard C, Heuret P. 2020. Vulnerability and hydraulic segmentations at the stem-leaf transition: coordination across Neotropical trees. New Phytologist 228: 512-524.
Loubry D. 1994. La phénologie des arbres caducifoliés en forêt guyanaise (5° de latitude nord): illustration d'un déterminisme à composantes endogène et exogène. Canadian Journal of Botany 72: 1843-1857.
Manzi OJL, Bellifa M, Ziegler C, Mihle L, Levionnois S, Burban B, Leroy C, Coste S, Stahl C. 2022. Drought stress recovery of hydraulic and photochemical processes in Neotropical tree saplings. Tree Physiology 42: 114-129.
Maréchaux I, Bonal D, Bartlett MK, Burban B, Coste S, Courtois EA, Dulormne M, Goret J, Mira E, Mirabel A et al. 2018. Dry-season decline in tree sapflux is correlated with leaf turgor loss point in a tropical rainforest. Functional Ecology 32: 2285-2297.
Maréchaux I, Saint-André L, Bartlett MK, Sack L, Chave J. 2020. Leaf drought tolerance cannot be inferred from classic leaf traits in a tropical rainforest. Journal of Ecology 108: 1030-1045.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2010. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33: 453-467.
Molino J-F, Sabatier D. 2001. Tree diversity in tropical rain forests: a validation of the intermediate disturbance hypothesis. Science 294: 1702-1704.
Moran JF, Becana M, Iturbe-Ormaetxe I, Frechilla S, Klucas RV, Aparicio-Tejo P. 1994. Drought induces oxidative stress in pea plants. Planta 194: 346-352.
Munné-Bosch S, Jubany-Marí T, Alegre L. 2001. Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant, Cell & Environment 24: 1319-1327.
Murphy L. 2015. likelihood: methods for maximum likelihood estimation [WWW document] URL https://cran.r-project.org/web/packages/likelihood/index.html [accessed 15 May 2023].
Oppenheimer HR, Leshem B. 1966. Critical thresholds of dehydration in leaves of Nerium oleander L. Protoplasma 61: 302-321.
Pineda-García F, Paz H, Meinzer FC. 2012. Drought resistance in early and late secondary successional species from a tropical dry forest: the interplay between xylem resistance to embolism, sapwood water storage and leaf shedding. Plant, Cell & Environment 36: 405-418.
Ploughe LW, Jacobs EM, Frank GS, Greenler SM, Smith MD, Dukes JS. 2019. Community Response to Extreme Drought (CRED): a framework for drought-induced shifts in plant-plant interactions. New Phytologist 222: 52-69.
Saglam A, Saruhan N, Terzi R, Kadioglu A. 2011. The relations between antioxidant enzymes and chlorophyll fluorescence parameters in common bean cultivars differing in sensitivity to drought stress. Russian Journal of Plant Physiology 58: 60-68.
Sancho-Knapik D, Álvarez-Arenas TG, Peguero-Pina JJ, Fernández V, Gil-Pelegrín E. 2011. Relationship between ultrasonic properties and structural changes in the mesophyll during leaf dehydration. Journal of Experimental Botany 62: 3637-3645.
Saveyn A, Steppe K, Lemeur R. 2007. Drought and the diurnal patterns of stem CO2 efflux and xylem CO2 concentration in young oak (Quercus robur). Tree Physiology 27: 365-374.
Silva EN, Silveira JAG, Ribeiro RV, Vieira SA. 2015. Photoprotective function of energy dissipation by thermal processes and photorespiratory mechanisms in Jatropha curcas plants during different intensities of drought and after recovery. Environmental and Experimental Botany 110: 36-45.
Skelton RP, Brodribb TJ, McAdam SAM, Mitchell PJ. 2017. Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland. New Phytologist 215: 1399-1412.
Song Y, Sterck F, Zhou X, Liu Q, Kruijt B, Poorter L. 2022. Drought resilience of conifer species is driven by leaf lifespan but not by hydraulic traits. New Phytologist 235: 978-992.
Souza RP, Machado EC, Silva JAB, Lagôa AMMA, Silveira JAG. 2004. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environmental and Experimental Botany 51: 45-56.
Stahl C, Burban B, Bompy F, Jolin ZB, Sermage J, Bonal D. 2010. Seasonal variation in atmospheric relative humidity contributes to explaining seasonal variation in trunk circumference of tropical rain-forest trees in French Guiana. Journal of Tropical Ecology 26: 393-405.
Stahl C, Burban B, Wagner F, Goret J-Y, Bompy F, Bonal D. 2013. Influence of seasonal variations in soil water availability on gas exchange of tropical canopy trees. Biotropica 45: 155-164.
Stan Development Team. 2018. rstan: the R interface to stan. R package v.2.21.8. [WWW document] URL https://mc-stan.org/ [accessed 15 May 2023].
Sterck F, Markesteijn L, Schieving F, Poorter L. 2011. Functional traits determine trade-offs and niches in a tropical forest community. Proceedings of the National Academy of Sciences, USA 108: 20627-20632.
Trifilò P, Petruzzellis F, Abate E, Nardini A. 2021. The extra-vascular water pathway regulates dynamic leaf hydraulic decline and recovery in Populus nigra. Physiologia Plantarum 172: 29-40.
Trueba S, Pan R, Scoffoni C, John GP, Davis SD, Sack L. 2019. Thresholds for leaf damage due to dehydration: declines of hydraulic function, stomatal conductance and cellular integrity precede those for photochemistry. New Phytologist 223: 134-149.
Trugman AT, Detto M, Bartlett MK, Medvigy D, Anderegg WRL, Schwalm C, Schaffer B, Pacala SW. 2018. Tree carbon allocation explains forest drought-kill and recovery patterns. Ecology Letters 21: 1552-1560.
Vollenweider P, Menard T, Arend M, Kuster TM, Günthardt-Goerg MS. 2016. Structural changes associated with drought stress symptoms in foliage of Central European oaks. Trees 30: 883-900.
Wagner F, Hérault B, Stahl C, Bonal D, Rossi V. 2011. Modeling water availability for trees in tropical forests. Agricultural and Forest Meteorology 151: 1202-1213.
Wagner F, Rossi V, Stahl C, Bonal D, Hérault B. 2012. Water availability is the main climate driver of Neotropical tree growth. PLoS ONE 7: e34074.
Wagner F, Rossi V, Stahl C, Bonal D, Hérault B. 2013. Asynchronism in leaf and wood production in tropical forests: a study combining satellite and ground-based measurements. Biogeosciences 10: 7307-7321.
Xiong D, Nadal M. 2020. Linking water relations and hydraulics with photosynthesis. The Plant Journal 101: 800-815.
Yang H, Ciais P, Wang Y, Huang Y, Wigneron J, Bastos A, Chave J, Chang J, Doughty C, Fan L et al. 2021. Variations of carbon allocation and turnover time across tropical forests. Global Ecology and Biogeography 30: 1271-1285.
Yang Y, Saatchi SS, Xu L, Yu Y, Choi S, Phillips N, Kennedy R, Keller M, Knyazikhin Y, Myneni RB. 2018. Post-drought decline of the Amazon carbon sink. Nature Communications 9: 3172.
Yuan W, Zheng Y, Piao S, Ciais P, Lombardozzi D, Wang Y, Ryu Y, Chen G, Dong W, Hu Z et al. 2019. Increased atmospheric vapor pressure deficit reduces global vegetation growth. Science Advances 5: eaax1396.
Zhang F-J, Zhang K-K, Du C-Z, Li J, Xing Y-X, Yang L-T, Li Y-R. 2015. Effect of drought stress on anatomical structure and chloroplast ultrastructure in leaves of sugarcane. Sugar Tech 17: 41-48.
Zhu S-D, Chen Y-J, Ye Q, He P-C, Liu H, Li R-H, Fu P-L, Jiang G-F, Cao K-F. 2018. Leaf turgor loss point is correlated with drought tolerance and leaf carbon economics traits. Tree Physiology 38: 658-663.
Ziegler C, Coste S, Stahl C, Delzon S, Levionnois S, Cazal J, Cochard H, Esquivel-Muelbert A, Goret J-Y, Heuret P et al. 2019. Large hydraulic safety margins protect Neotropical canopy rainforest tree species against hydraulic failure during drought. Annals of Forest Science 76: 115.
Zwieniecki MA, Brodribb TJ, Holbrook NM. 2007. Hydraulic design of leaves: insights from rehydration kinetics. Plant, Cell & Environment 30: 910-921.

Auteurs

Claire Fortunel (C)

AMAP (Botanique et Modélisation de l'Architecture des Plantes et des Végétations), Université de Montpellier, CIRAD, CNRS, INRAE, IRD, 34000, Montpellier, France.

Clément Stahl (C)

INRAE, UMR EcoFoG, CNRS, CIRAD, AgroParisTech, Université des Antilles, Université de Guyane, 97310, Kourou, France.

Sabrina Coste (S)

INRAE, UMR EcoFoG, CNRS, CIRAD, AgroParisTech, Université des Antilles, Université de Guyane, 97310, Kourou, France.

Camille Ziegler (C)

INRAE, UMR EcoFoG, CNRS, CIRAD, AgroParisTech, Université des Antilles, Université de Guyane, 97310, Kourou, France.
Université de Lorraine, AgroParisTech, INRAE, UMR Silva, 54000, Nancy, France.

Géraldine Derroire (G)

CIRAD, UMR EcoFoG (AgroParistech, CNRS, INRAE, Université des Antilles, Université de la Guyane), Campus Agronomique, 97310, Kourou, French Guiana.

Sébastien Levionnois (S)

AMAP (Botanique et Modélisation de l'Architecture des Plantes et des Végétations), Université de Montpellier, CIRAD, CNRS, INRAE, IRD, 34000, Montpellier, France.
INRAE, UMR EcoFoG, CNRS, CIRAD, AgroParisTech, Université des Antilles, Université de Guyane, 97310, Kourou, France.

Isabelle Maréchaux (I)

AMAP (Botanique et Modélisation de l'Architecture des Plantes et des Végétations), Université de Montpellier, CIRAD, CNRS, INRAE, IRD, 34000, Montpellier, France.

Damien Bonal (D)

Université de Lorraine, AgroParisTech, INRAE, UMR Silva, 54000, Nancy, France.

Bruno Hérault (B)

CIRAD, UPR Forêts et Sociétés, Yamoussoukro, Côte d'Ivoire.
Forêts et Sociétés, Univ Montpellier, CIRAD, 34000, Montpellier, France.
Institut National Polytechnique Félix Houphouët-Boigny, INP-HB, Yamoussoukro, Côte d'Ivoire.

Fabien H Wagner (FH)

Institute of Environment and Sustainability, University of California, Los Angeles, CA, 90095, USA.
Jet Propulsion Laboratory, California Institute of Technology, 4800 Oak Grove, Pasadena, CA, 91109, USA.

Lawren Sack (L)

Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, 90095, USA.

Jérôme Chave (J)

CNRS, Université Toulouse 3 Paul Sabatier, IRD, UMR 5174 Evolution et Diversité Biologique (EDB), 31062, Toulouse, France.

Patrick Heuret (P)

AMAP (Botanique et Modélisation de l'Architecture des Plantes et des Végétations), Université de Montpellier, CIRAD, CNRS, INRAE, IRD, 34000, Montpellier, France.

Steven Jansen (S)

Institute of Botany, Ulm University, Albert-Einstein-Allee 11, 89081, Ulm, Germany.

Grace John (G)

Department of Biology, University of Florida, Gainesville, FL, 32611, USA.

Christine Scoffoni (C)

Department of Biological Sciences, California State University, Los Angeles, CA, 90032, USA.

Santiago Trueba (S)

Université de Bordeaux, INRAE, UMR BIOGECO, Pessac, 33615, France.

Megan K Bartlett (MK)

Department of Viticulture and Enology, University of California, Davis, CA, 95616, USA.

Articles similaires

Genome, Viral Ralstonia Composting Solanum lycopersicum Bacteriophages
Semiconductors Photosynthesis Polymers Carbon Dioxide Bacteria
Fragaria Light Plant Leaves Osmosis Stress, Physiological
India Carbon Sequestration Environmental Monitoring Carbon Biomass

Classifications MeSH