Coordination between water relations strategy and carbon investment in leaf and stem in six fruit tree species
Ismael Piña A , Marco Garrido-Salinas B * , Oscar Seguel C , Ismael Opazo D , Carlos Faúndez-Urbina E , Nicolás Verdugo-Vásquez F and Emilio Villalobos-Soublett GA
B
C
D
E
F
G
Abstract
The water relation strategy is a key issue in climate change. Given the difficulty of determining water relations strategy, there is a need for simple traits with a solid theoretical basis to estimate it. Traits associated with resource allocation patterns along a ‘fast-slow’ plant economics spectrum are particularly compelling, reflecting trade-offs between growth rate and carbon allocation. Avocado (Persea americana), fig tree (Ficus carica), mandarin (Citrus reticulata), olive (Olea europaea), pomegranate (Punica granatum), and grapevine (Vitis vinifera) were characterised in terms of iso-anisohydric strategy through stomatal behaviour, water potential at the turgor loss point (TLP), and hydroscape area. Additionally, the association of these metrics with leaf mass per area (LMA) and wood density (WDen) was explored. We observed high coordination between LMA and WDen, and both traits were related to metrics of water relation strategy. More anisohydric species tended to invest more carbon per unit leaf area or unit stem volume, which has implications for hydraulic efficiency and water stress tolerance. WDen and TLP were the most powerful traits in estimating the water relation strategy for six fruit species. These traits are easy to measure, time-cost efficient, and appear central to coordinating multiple traits and behaviours along the water relations strategies.
Keywords: carbon economic spectrum, fruit trees, hydraulics, isohydrism, leaf mass per area, stomatal conductance, water potential, wood density.
References
Aasamaa K, Sõber 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. Functional Plant Biology 28(8), 765-774.
| Crossref | Google Scholar |
Arroyo-García R, Ruiz-Garcia L, Bolling L, Ocete R, López MA, Arnold C, et al. (2006) Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms. Molecular Ecology 15(12), 3707-3714.
| Crossref | Google Scholar | PubMed |
Barotto AJ, Monteoliva S, Gyenge J, Martinez-Meier A, Fernandez ME (2018) Functional relationships between wood structure and vulnerability to xylem cavitation in races of Eucalyptus globulus differing in wood density. Tree Physiology 38(2), 243-251.
| Crossref | Google Scholar | PubMed |
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 113, 13098-13103.
| Crossref | Google Scholar |
Besnard G, Bervillé A (2000) Multiple origins for Mediterranean olive (Olea europaea L. ssp. europaea) based upon mitochondrial DNA polymorphisms. Comptes Rendus de l’Académie des Sciences - Series III - Sciences de la Vie 323(2), 173-181.
| Crossref | Google Scholar |
Boehm J (1893) Capillarität und saftsteigen. Berichte der Deutschen Botanischen Gesellschaft 11, 14-23.
| Google Scholar |
Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144(4), 1890-1898.
| Crossref | Google Scholar | PubMed |
Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV (2014) Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences 111(40), 14489-14493.
| Crossref | Google Scholar |
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(1), 68-79.
| Crossref | Google Scholar | PubMed |
Buckley TN (2005) The control of stomata by water balance. New Phytologist 168(2), 275-292.
| Crossref | Google Scholar | PubMed |
Chandra R, Jadhav VT, Sharma J (2010) Global scenario of pomegranate (Punica granatum L.) culture with special reference to India. Fruit, Vegetable and Cereal Science and Biotechnology 4, 7-18.
| Google Scholar |
Chen Z, Zhang Y, Yuan W, Zhu S, Pan R, Wan X, Liu S (2021) Coordinated variation in stem and leaf functional traits of temperate broadleaf tree species in the isohydric–anisohydric spectrum. Tree Physiology 41(9), 1601-1610.
| Crossref | Google Scholar | PubMed |
Dayer S, Lamarque LJ, Burlett R, Bortolami G, Delzon S, Herrera JC, Cochard H, Gambetta GA (2022) Model-assisted ideotyping reveals trait syndromes to adapt viticulture to a drier climate. Plant Physiology 190(3), 1673-1686.
| Crossref | Google Scholar | PubMed |
de Mendiburu F (2021) agricolae: statistical procedures for agricultural research. R package version 1.3-5. Available at https://CRAN.R-project.org/package=agricolae
Dixon H (1894) On the ascent of sap. Annals of Botany os-8, 468-470.
| Crossref | Google Scholar |
Essa YH, Hirschi M, Thiery W, El-Kenawy AM, Yang C (2023) Drought characteristics in Mediterranean under future climate change. npj Climate and Atmospheric Science 6, 133.
| Crossref | Google Scholar |
Fajardo A, Piper FI, García-Cervigón AI (2022) The intraspecific relationship between wood density, vessel diameter and other traits across environmental gradients. Functional Ecology 36, 1585-1598.
| Crossref | Google Scholar |
Fu X, Meinzer FC (2019) Metrics and proxies for stringency of regulation of plant water status (iso/anisohydry): a global data set reveals coordination and trade-offs among water transport traits. Tree Physiology 39(1), 122-134.
| Crossref | Google Scholar |
Galindo-Tovar ME, Ogata-Aguilar N, Arzate-Fernández AM (2008) Some aspects of avocado (Persea americana Mill.) diversity and domestication in Mesoamerica. Genetic Resources and Crop Evolution 55, 441-450.
| Crossref | Google Scholar |
Garreaud RD, Boisier JP, Rondanelli R, Montecinos A, Sepúlveda HH, Veloso-Aguila D (2020) The Central Chile Mega Drought (2010–2018): a climate dynamics perspective. International Journal of Climatology 40, 421-439.
| Crossref | Google Scholar |
Garrido MI, Vergara S (2022) Lack of tradeoff between leaf hydraulic efficiency and safety across six contrasting water-stress tolerant fruit tree species. Agronomy 12(10), 2351.
| Crossref | Google Scholar |
Graves S, Piepho H-P, Dorai-Raj S, Selzer L (2023) multcompView: visualizations of paired comparisons. R package version 0.1-9. Available at https://CRAN.R-project.org/package=multcompView
Gray EF, Wright IJ, Falster DS, Eller ASD, Lehmann CER, Bradford MG, Cernusak LA (2019) Leaf:wood allometry and functional traits together explain substantial growth rate variation in rainforest trees. AoB PLANTS 11(3), plz024.
| Crossref | Google Scholar |
Gutschick VP, Wiegel FW (1988) Optimizing the canopy photosynthetic rate by patterns of investment in specific leaf mass. The American Naturalist 132(1), 67-86.
| Crossref | Google Scholar |
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126, 457-461.
| Crossref | Google Scholar | PubMed |
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26(6), 689-701.
| Crossref | Google Scholar | PubMed |
Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni C, Sack L (2019) A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Communications 10(1), 3398.
| Crossref | Google Scholar | PubMed |
Hochberg U, Rockwell FE, Holbrook NM, Cochard H (2018) Iso/anisohydry: a plant–environment interaction rather than a simple hydraulic trait. Trends in Plant Science 23(2), 112-120.
| Crossref | Google Scholar | PubMed |
Klein T (2014) The variability of stomatal sensitivity to leaf water potential across tree species indicates a continuum between isohydric and anisohydric behaviours. Functional Ecology 28(6), 1313-1320.
| Crossref | Google Scholar |
Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist 190(3), 709-723.
| Crossref | Google Scholar | PubMed |
Martínez-Vilalta J, Poyatos R, Aguadé D, Retana J, Mencuccini M (2014) A new look at water transport regulation in plants. New Phytologist 204(1), 105-115.
| Crossref | Google Scholar | PubMed |
McDowell NG, Allen CD (2015) Darcy’s law predicts widespread forest mortality under climate warming. Nature Climate Change 5, 669-672.
| Crossref | Google Scholar |
McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, et al. (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytologist 178(4), 719-739.
| Crossref | Google Scholar | PubMed |
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.
| Crossref | Google Scholar |
Meinzer FC, Woodruff DR, Marias DE, Smith DD, McCulloh KA, Howard AR, Magedman AL (2016) Mapping ‘hydroscapes’ along the iso- to anisohydric continuum of stomatal regulation of plant water status. Ecology Letters 19(11), 1343-1352.
| Crossref | Google Scholar | PubMed |
Meinzer FC, Smith DD, Woodruff DR, Marias DE, McCulloh KA, Howard AR, Magedman AL (2017) Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status. Plant, Cell & Environment 40, 1618-1628.
| Crossref | Google Scholar | PubMed |
Niinemets U, Cescatti A, Rodeghiero M, Tosens T (2005) Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species. Plant, Cell & Environment 28, 1552-1566.
| Crossref | Google Scholar |
Opazo I, Pimentel P, Salvatierra A, Ortiz M, Toro G, Garrido-Salinas M (2024) Water stress tolerance is coordinated with water use capacity and growth under water deficit across six fruit tree species. Irrigation Science 42, 493-507.
| Crossref | Google Scholar |
Orians GH, Solbrig OT (1977) A cost-income model of leaves and roots with special reference to arid and semiarid areas. The American Naturalist 111(980), 677-690.
| Crossref | Google Scholar |
Poorter L, Bongers F (2006) Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87, 1733-1743.
| Crossref | Google Scholar | PubMed |
Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, et al. (2008) Are functional traits good predictors of demographic rates? Evidence from five neotropical forests. Ecology 89, 1908-1920.
| Crossref | Google Scholar | PubMed |
Pratt RB, Jacobsen AL, Ewers FW, Davis SD (2007) Relationships among xylem transport, biomechanics and storage in stems and roots of nine Rhamnaceae species of the California chaparral. New Phytologist 174, 787-798.
| Crossref | Google Scholar |
Ratzmann G, Meinzer FC, Tietjen B (2019) Iso/anisohydry: still a useful concept. Trends in Plant Science 24(3), 191-194.
| Crossref | Google Scholar | PubMed |
Reich PB (2014) The world-wide ‘fast–slow’ plant economics spectrum: a traits manifesto. Journal of Ecology 102(2), 275-301.
| Crossref | Google Scholar |
RStudio Team (2020) RStudio: integrated development for R. Rstudio Team, PBC, Boston, MA, USA. Available at http://www.rstudio.com
Sack L, Cornwell WK, Santiago LS, Barbour MM, Choat B, Evans JR, et al. (2010) A unique web resource for physiology, ecology and the environmental sciences: PrometheusWiki. Functional Plant Biology 37(8), 687-693.
| Crossref | Google Scholar |
Salvi AM, Gosetti SG, Smith DD, Adams MA, Givnish TJ, McCulloh KA (2022) Hydroscapes, hydroscape plasticity and relationships to functional traits and mesophyll photosynthetic sensitivity to leaf water potential in Eucalyptus species. Plant, Cell & Environment 45(9), 2573-2588.
| Crossref | Google Scholar | PubMed |
Schloerke B, Cook D, Larmarange J, Briatte F, Marbach M, Thoen E, Elberg A, Crowley J (2021) GGally: Extension to ‘ggplot2’. R package version 2.1.2. Available at https://CRAN.R-project.org/package=GGally
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9(7), 671-675.
| Crossref | Google Scholar | PubMed |
Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148(3668), 339-346.
| Crossref | Google Scholar | PubMed |
Scora RW (1975) On the history and origin of Citrus. Bulletin of the Torrey Botanical Club 102, 369-375.
| Crossref | Google Scholar |
Simonneau T, Lebon E, Coupel-Ledru A, Marguerit E, Rossdeutsch L, Ollat N (2017) Adapting plant material to face water stress in vineyards: which physiological targets for an optimal control of plant water status? OENO One 51, 167-179.
| Crossref | Google Scholar |
Skelton RP, West AG, Dawson TE (2015) Predicting plant vulnerability to drought in biodiverse regions using functional traits. Proceedings of the National Academy of Sciences 112(18), 5744-5749.
| Crossref | Google Scholar |
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 Phytologist 229, 1955-1969.
| Crossref | Google Scholar | PubMed |
Sperry JS, Love DM (2015) What plant hydraulics can tell us about responses to climate-change droughts. New Phytologist 207(1), 14-27.
| Crossref | Google Scholar | PubMed |
Swenson NG, Enquist BJ (2007) Ecological and evolutionary determinants of a key plant functional trait: wood density and its community-wide variation across latitude and elevation. American Journal of Botany 94(3), 451-459.
| Crossref | Google Scholar | PubMed |
Tardieu F, Simonneau T (1998) Variability among species of stomatal control under fluctuating soil water status and evaporative demand: modelling isohydric and anisohydric behaviours. Journal of Experimental Botany 49, 419-432.
| Crossref | Google Scholar |
Torres-Ruiz JM, Cochard H, Mencuccini M, Delzon S, Badel E (2016) Direct observation and modelling of embolism spread between xylem conduits: a case study in Scots pine. Plant, Cell & Environment 39(12), 2774-2785.
| Crossref | Google Scholar | PubMed |
Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23(1), 267-282.
| Crossref | Google Scholar |
Volschenk T (2021) Effect of water deficits on pomegranate tree performance and fruit quality – a review. Agricultural Water Management 246, 106499.
| Crossref | Google Scholar |
Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, et al. (2004) The worldwide leaf economics spectrum. Nature 428(6985), 821-827.
| Crossref | Google Scholar | PubMed |