Abstract
The tradeoffs between carbon assimilation and hydraulic efficiencies and drought-tolerance traits on different scales are considered a central tenet in plant ecophysiology; however, no clear tradeoff between these traits has emerged in previous studies using woody angiosperms or grasses by investigating several hydraulic tolerance and gas exchange efficiency and/or water transport efficiency traits. In this study, we measured numerous efficiency, resistance, and leaf anatomical traits, including light-saturated gas exchange, leaf hydraulic vulnerability curves, pressure–volume curves, and leaf anatomical traits, in seven species with diverse drought tolerance. A substantial variation in photosynthetic rate, stomatal conductance, mesophyll conductance, maximum leaf hydraulic conductance (Kmax), mesophyll anatomical traits, and leaf vein density across species was observed. Both mesophyll conductance and Kmax were related to leaf anatomical traits, but other gas exchange traits were decoupled from Kmax. Although the efficiency and tolerance traits varied widely across estimated species, no clear trade-off between safety traits and efficiency traits was observed. These findings suggested that postulated leaf-level drought tolerance-carbon assimilation and hydraulic efficiency tradeoff does not exist among distant species and that the fact that different leaf anatomical traits determine efficiency and tolerance capacity might contribute to the lack of such tradeoffs.
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References
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
Binks O, Meir P, Rowland L, da Costa AC, Vasconcelos SS, de Oliveira AA, 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 Phytol 211:477–488
Blackman CJ, Brodribb T, 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
Blonder B, Buzzard V, Simova I, Sloat L, Boyle B, Lipson R, Aguilar-Beaucage B, Andrade A, Barber B, Barnes C, Bushey D, Cartagena P, Chaney M, Contreras K, Cox M, Cueto M, Curtis C, Fisher M, Furst L, Gallegos J, Hall R, Hauschild A, Jerez A, Jones N, Klucas A, Kono A, Lamb M, Matthai JD, McIntyre C, McKenna J, Mosier N, Navabi M, Ochoa A, Pace L, Plassmann R, Richter R, Russakoff B, Aubyn HS, Stagg R, Sterner M, Stewart E, Thompson TT, Thornton J, Trujillo PJ, Volpe TJ, Enquist BJ (2012) The leaf-area shrinkage effect can bias paleoclimate and ecology research. Am J Bot 99:1756–1763
Brodribb T, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898
Brodribb T, Bienaimé D, Marmottant P (2016) Revealing catastrophic failure of leaf networks under stress. Proc Natl Acad Sci USA 113:4865–4869
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
Buckley TN, John GP, Scoffoni C, Sack L (2015) How does leaf anatomy influence water transport outside the xylem? Plant Physiol 168:1616–1635
Buckley TN, John GP, Scoffoni C, Sack L (2017) The sites of evaporation within leaves. Plant Physiol 173:1763–1782
Caringella MA, Bongers FJ, Sack L (2015) Leaf hydraulic conductance varies with vein anatomy across Arabidopsis thaliana wild-type and leaf vein mutants. Plant, Cell Environ 38:2735–2746
Desclaux D, Roumet P (1996) Impact of drought stress on the phenology of two soybean (Glycine max L. Merr) cultivars. Field Crop Res 46:61–70
Domec JC, Noormets A, King JS, Sun GE, McNulty SG, Gavazzi MJ, Boggs JL, Treasure EA (2009) Decoupling the influence of leaf and root hydraulic conductances on stomatal conductance and its sensitivity to vapour pressure deficit as soil dries in a drained loblolly pine plantation. Plant Cell Environ 32:980–991
Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell Environ 27:137–153
Evans JR, Kaldenhoff R, Genty B, Terashima I (2009) Resistances along the CO2 diffusion pathway inside leaves. J Exp Bot 60:2235–2248
Farrell C, Szota C, Arndt SK (2017) Does the turgor loss point characterize drought response in dryland plants? Plant, Cell Environ 40:1500–1511
Gago J, Carriquí M, Nadal M, Clemente-Moreno MJ, Coopman RE, Fernie AR, Flexas J (2019) Photosynthesis optimized across land plant phylogeny. Trends Plant Sci 24:947–958
Gleason SM, Westoby M, Jansen S, Choat B, Hacke UG, Pratt RB, Bhaskar R, Brodribb T, Bucci SJ, Cao KF, Cochard H, Delzon S, Domec JC, Fan ZX, Feild TS, Jacobsen AL, Johnson DM, Lens F, Maherali H, Martinez-Vilalta J, Mayr S, McCulloh KA, Mencuccini M, Mitchell PJ, Morris H, Nardini A, Pittermann J, Plavcova L, Schreiber SG, Sperry JS, Wright IJ, Zanne AE (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209:123–136
Grassi G, Magnani F (2005) Stomatal, mesophyll conductance and biochemical limitations to photosynthesis as affected by drought and leaf ontogeny in ash and oak trees. Plant Cell Environ 28:834–849
Harley PC, Loreto F, Di Marco G, Sharkey TD (1992) Theoretical considerations when estimating the mesophyll conductance to CO2 flux by analysis of the response of photosynthesis to CO2. Plant Physiol 98:1429–1436
Kagotani Y, Nishida K, Kiyomizu T, Sasaki K, Kume A, Hanba YT (2016) Photosynthetic responses to soil water stress in summer in two Japanese urban landscape tree species (Ginkgo biloba and Prunus yedoensis): effects of pruning mulch and irrigation management. Trees 30:697–708
Kotula L, Ranathunge K, Steudle E (2009) Apoplastic barriers effectively block oxygen permeability across outer cell layers of rice roots under deoxygenated conditions. roles of apoplastic pores and of respiration. New Phytol 184:909–917
Kumar D, Hassan MA, Miguel AN, Veena A, Monica B, Oscar V (2017) Effects of salinity and drought on growth, ionic relations, compatible solutes and activation of antioxidant systems in oleander (Nerium oleander L.). PLoS ONE 12:e0185017
Lê S, Josse J, Husson F (2008) FactoMineR : an R package for multivariate analysis. J Stat Soft 25:18
Lenzi A, Pittas L, Martinelli T, Lombardi P, Tesi R (2009) Response to water stress of some oleander cultivars suitable for pot plant production. Sci Hortic 122:426–431
Li D, Liu H, Qiao Y, Wang Y, Cai Z, Dong B, Shi C, Liu Y, Li X, Liu M (2013) Effects of elevated CO2 on the growth, seed yield, and water use efficiency of soybean (Glycine max (L.) Merr.) under drought stress. Agric Water Manag 129:105–112
Liu H, Ye Q, Gleason SM, He P, Yin D (2021) Weak tradeoff between xylem hydraulic efficiency and safety: climatic seasonality matters. New Phytol 229:1440–1452
Lo Gullo MA, Nardini A, Trifilò P, Salleo S (2003) Changes in leaf hydraulics and stomatal conductance following drought stress and irrigation in Ceratonia siliqua (Carob tree). Physiol Plant 117:186–194
Nadal M, Flexas J (2018) Chapter 17 - Mesophyll conductance to CO2 diffusion: Effects of drought and opportunities for improvement. In: García-Tejero IF, Zuazo VH (eds) Water scarcity and sustainable agriculture in semiarid environment. Academic Press, Amsterdam, pp 403–438
Nadal M, Flexas J (2019) Variation in photosynthetic characteristics with growth form in a water-limited scenario: implications for assimilation rates and water use efficiency in crops. Agric Water Manag 216:457–472
Nadal M, Flexas J, Gulías J (2018) Possible link between photosynthesis and leaf modulus of elasticity among vascular plants. a new player in leaf traits relationships? Ecol Lett 21:1372–1379
Nardini A, Pedà G, La Rocca N (2012) Trade-offs between leaf hydraulic capacity and drought vulnerability: morpho-anatomical bases, carbon costs and ecological consequences. morpho-anatomical bases, carbon costs and ecological consequences. New Phytol 196:788–798
Nardini A, Qunapuu-Pikas E, Savi T (2014) When smaller is better. leaf hydraulic conductance and drought vulnerability correlate to leaf size and venation density across four Coffea arabica genotypes. Funct Plant Biol 41:972–982
Niinemets Ü, Portsmuth A, Truus L (2002) Leaf structural and photosynthetic characteristics, and biomass allocation to foliage in relation to foliar nitrogen content and tree size in three Betula species. Ann Bot 89:191–204
Ocheltree TW, Nippert JB, Prasad PV (2016) A safety vs efficiency trade-off identified in the hydraulic pathway of grass leaves is decoupled from photosynthesis, stomatal conductance and precipitation. New Phytol 210:97–107
Onoda Y, Wright IJ, Evans JR, Hikosaka K, Kitajima K, Niinemets Ü, Poorter H, Tosens T, Westoby M (2017) Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytol 214:1447–1463
Powell TL, Wheeler JK, de Oliveira AA, da Costa AC, Saleska SR, Meir P, Moorcroft PR (2017) Differences in xylem and leaf hydraulic traits explain differences in drought tolerance among mature Amazon rainforest trees. Glob Change Biol 23:4280–4293
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ranathunge K, Steudle E, Lafitte R (2005) Blockage of apoplastic bypass-flow of water in rice roots by insoluble salt precipitates analogous to a Pfeffer cell. Plant Cell Environ 28:121–133
Rockwell FE, Holbrook NM, Stroock AD (2014) The competition between liquid and vapor transport in transpiring leaves. Plant Physiol 164:1741–1758
Roig-Oliver M, Nadal M, Clemente-Moreno MJ, Bota J, Flexas J (2020) Cell wall components regulate photosynthesis and leaf water relations of Vitis vinifera cv. Grenache acclimated to contrasting environmental conditions. J Plant Physiol 244:153084
Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87:483–491
Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381
Sack L, Pasquet-Kok J (2011) Leaf pressure-volume curve parameters. PrometheusWiki /tiki-pagehistory.php?page=Leaf pressure-volume curve parameters&preview=16:(Accessed March 29, 2020).
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 Environ 26:1343–1356
Sade N, Shatil-Cohen A, Attia Z, Maurel C, Boursiac Y, Kelly G, Granot D, Yaaran A, Lerner S, Moshelion M (2014) The role of plasma membrane aquaporins in regulating the bundle sheath-mesophyll continuum and leaf hydraulics. Plant Physiol 166:1609–1620
Scoffoni C, Rawls M, McKown AD, 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, McKown AD, Rawls M, Sack L (2012) Dynamics of leaf hydraulic conductance with water status. quantification and analysis of species differences under steady state. J Exp Bot 63:643–658
Scoffoni C, Vuong C, Diep S, Cochard H, Sack L (2014) Leaf shrinkage with dehydration: coordination with hydraulic vulnerability and drought tolerance. coordination with hydraulic vulnerability and drought tolerance. Plant Physiol 164:1772–1788
Scoffoni C, Albuquerque C, Brodersen CR, Townes SV, John GP, Cochard H, Buckley TN, McElrone AJ, Sack L (2016a) Leaf vein xylem conduit diameter influences susceptibility to embolism and hydraulic decline. New Phytol 213:1076–1092
Scoffoni C, Chatelet DS, Pasquet-Kok J, Rawls M, Donoghue MJ, Edwards EJ, Sack L (2016b) Hydraulic basis for the evolution of photosynthetic productivity. Nature Plants 2:16072
Scoffoni C, Albuquerque C, Brodersen CR, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L (2017) Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiol 173:1197–1210
Secchi F, Zwieniecki MA (2014) Down-regulation of plasma intrinsic protein1 aquaporin in poplar trees is detrimental to recovery from embolism. Plant Physiol 164:1789–1799
Sorek Y, Greenstein S, Netzer Y, Shtein I, Jansen S, Hochberg U (2021) An increase in xylem embolism resistance of grapevine leaves during the growing season is coordinated with stomatal regulation, turgor loss point and intervessel pit membranes. New Phytol 229:1955–1969
Steudle E (2000) Water uptake by roots. Effects of water deficit. J Exp Bot 51:1531–1542
Tomás M, Flexas J, Copolovici L, Galmes J, Hallik L, Medrano H, Ribas-Carbo M, Tosens T, Vislap V, Niinemets Ü (2013) Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: quantitative limitations and scaling up by models. quantitative limitations and scaling up by models. J Exp Bot 64:2269–2281
Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, Talts E, Tomás M, Hanba Y, Niinemets Ü, Flexas J (2016) The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol 209:1576–1590
Trifiló P, Raimondo F, Savi T, Lo Gullo MA, Nardini A (2016) The contribution of vascular and extra-vascular water pathways to drought-induced decline of leaf hydraulic conductance. J Exp Bot 67:5029–5039
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 Phytol 223:134–149
Tschaplinski TJ, Norby RJ (1991) Physiological indicators of nitrogen response in a short rotation sycamore plantation. I. CO2 assimilation, photosynthetic pigments and soluble carbohydrates. Physiol Plant 82:117–126
Tyree MT, Jarvis PG (1982) Water in tissues and cells. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology II water relations and carbon assimilation. Springer, Berlin Heidelberg, pp 35–77
Ullah I, Rahman M, Ashraf M, Zafar Y (2008) Genotypic variation for drought tolerance in cotton (Gossypium hirsutum L.): leaf gas exchange and productivity. Flora 203:105–115
Viger M, Smith HK, Cohen D, Dewoody J, Trewin H, Steenackers M, Bastien C, Taylor G (2016) Adaptive mechanisms and genomic plasticity for drought tolerance identified in European black poplar (Populus nigra L.). Tree Physiol 36:909–928
Wang X, Du T, Huang J, Peng S, Xiong D (2018) Leaf hydraulic vulnerability triggers the decline in stomatal and mesophyll conductance during drought in rice (Oryza sativa). J Exp Bot 69:4033–4045
Wang X, Zhao J, Huang J, Peng S, Xiong D (2022) Evaporative flux method of leaf hydraulic conductance estimation: sources of uncertainty and reporting format recommendation. Plant Methods 18:63
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M, Flexas J, Garnier E, Groom PK, Gulías J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Xiong D, Flexas J (2018) Leaf economics spectrum in rice: leaf anatomical, biochemical and physiological trait trade-offs. J Exp Bot 69:5599–5609
Xiong D, Flexas J (2021) Leaf anatomical characteristics are less important than leaf biochemical properties in determining photosynthesis responses to nitrogen top-dressing. J Exp Bot 72:5709–5720
Xiong D, Yu T, Zhang T, Li Y, Peng S, Huang J (2015) Leaf hydraulic conductance is coordinated with leaf morpho-anatomical traits and nitrogen status in the genus Oryza. J Exp Bot 66:741–748
Xiong D, Flexas J, Yu T, Peng S, Huang J (2017) Leaf anatomy mediates coordination of leaf hydraulic conductance and mesophyll conductance to CO2 in Oryza. New Phytol 213:572–583
Xiong D, Douthe C, Flexas J (2018) Differential coordination of stomatal conductance, mesophyll conductance, and leaf hydraulic conductance in response to changing light across species. Plant, Cell Environ 41:436–450
Acknowledgements
We thank Dr. Meisha-Marika Holloway-Phillps, Dr. Tom Buckley, Dr. Christine Scoffoni and Prof. Lawren Sack for helpful insights in interpreting Kleaf vulnerability curves data; and Dr. Cyril Douthe for his critical comments on the study design.
Funding
DX was funded by the National Natural Science Foundation of China (No. 32022060). JF was funded by project PGC2018-093824-B-C41 from the Ministerio de Ciencia, Innovación y Universidades and the ERDF (FEDER).
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DX and JF: conceived and designed the experiments. DX: performed the experiments. DX and JF: analyzed the data. DX: wrote the manuscript; JF: provided editorial advice.
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Communicated by Kouki Hikosaka.
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Xiong, D., Flexas, J. Safety–efficiency tradeoffs? Correlations of photosynthesis, leaf hydraulics, and dehydration tolerance across species. Oecologia 200, 51–64 (2022). https://doi.org/10.1007/s00442-022-05250-4
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DOI: https://doi.org/10.1007/s00442-022-05250-4