Physiological Plasticity of Plants Facing Climate Change
Erola Fenollosa
Department of Evolutionary Biology, Ecology and Environmental Sciences, Universitat de Barcelona, Barcelona, Spain
Institute of Research in Biodiversity (IRBio-UB), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorSergi Munné-Bosch
Department of Evolutionary Biology, Ecology and Environmental Sciences, Universitat de Barcelona, Barcelona, Spain
Institute of Research in Biodiversity (IRBio-UB), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorErola Fenollosa
Department of Evolutionary Biology, Ecology and Environmental Sciences, Universitat de Barcelona, Barcelona, Spain
Institute of Research in Biodiversity (IRBio-UB), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorSergi Munné-Bosch
Department of Evolutionary Biology, Ecology and Environmental Sciences, Universitat de Barcelona, Barcelona, Spain
Institute of Research in Biodiversity (IRBio-UB), Universitat de Barcelona, Barcelona, Spain
Search for more papers by this authorAbstract
Plant plasticity is essential to provide plants with the most adequate physiological mechanisms to face climate stochasticity. Both biodiversity conservation and food security lie on our current understanding of physiological plasticity to project the impacts of climate change and establish mitigation strategies. In this article, we focus on the evolutionary role of plasticity, its costs and limits, molecular basis and the physiological mechanisms allowing the expression of the most adequate plant phenotype in response to the major current climate change drivers. Furthermore, we provide novel insights into the most common approaches and methods used to study and evaluate plasticity, using plant photoprotection as an example. It is concluded that much progress has been made in the role of plasticity in plant responses to climate change, although further insights into stress memory, sensory mechanisms, and the plant responses to multiple environmental stresses is still required to better understand plant responses to climate change.
References
- Aljazairi, S. and Arias, C. (2015). Carbon and nitrogen allocation and partitioning in traditional and modern wheat genotypes under pre-industrial and future CO2 conditions. Plant Biology 17: 647–659.
- Amthor, J.S. (2001). Effects of atmospheric CO2 concentration on wheat yield : review of results from experiments using various approaches to control CO2 concentration. Field Crops Research 73: 1–35.
- Anadon-Rosell, A., Dawes, M.A., Fonti, P. et al. (2018). Xylem anatomical and growth responses of the dwarf shrub Vaccinium myrtillus to experimental CO2 enrichment and soil warming at treeline. Science of the Total Environment 642: 1172–1183.
- Apel, K. and Hirt, H. (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55: 373–399.
- Asseng, S. (2015). Rising temperatures reduce global wheat production. Nature Climate Change 5: 143–147.
- Auge, G.A., Blair, L.K., Karediya, A., and Donohue, K. (2018). The autonomous flowering-time pathway pleiotropically regulates seed germination in Arabidopsis thaliana. Annals of Botany 121: 183–191.
- Avolio, M.L., Hoffman, A.M., and Smith, M.D. (2018). Linking gene regulation, physiology, and plant biomass allocation in Andropogon gerardii in response to drought. Plant Ecology 219: 1–15.
- Balao, F. (2018). Uncovering the contribution of epigenetics to plant phenotypic variation in Mediterranean ecosystems. Plant Biology 20: 38–49.
- Beaman, J.E., White, C.R., and Seebacher, F. (2016). Evolution of plasticity: mechanistic link between development and reversible acclimation. Trends in Ecology & Evolution 31: 237–249.
- Bigot, S., Buges, J., Gilly, L. et al. (2018). Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change. Global Change Biology 24 (12): 5573–5589.
- Blessing, C.H., Werner, R.A., Siegwolf, R., and Buchmann, N. (2015). Allocation dynamics of recently fixed carbon in beech saplings in response to increased temperatures and drought. Tree Physiology 35: 585–598.
- Borland, A.M., Zambrano, V.A.B., Ceusters, J., and Shorrock, K. (2011). The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytologist 191: 619–633.
- Bossdorf, O., Richards, C.L., and Pigliucci, M. (2008). Epigenetics for ecologists. Ecology Letters 11: 106–115.
- Brumos, J., Robles, L.M., Yun, J. et al. (2018). Local auxin biosynthesis is a key regulator of plant article local auxin biosynthesis is a key regulator of plant development. Developmental Cell 47: 306–318.e5.
- Buide, M.L., del Valle, J.C., Castilla, A.R., and Narbona, E. (2018). Sex expression variation in response to shade in gynodioecious-gynomonoecious species: Silene littorea decreases flower production and increases female flower proportion. Environmental and Experimental Botany 146: 54–61.
- Burggren, W. (2018). Developmental phenotypic plasticity helps bridge stochastic weather events associated with climate change. Journal of Experimental Biology 221: 1–9.
- Callahan, H.S., Dhanoolal, N., Ungerer, M.C., and Callahan, H.S. (2005). Plasticity genes and plasticity costs: a new approach using an Arabidopsis recombinant inbred population. New Phytologist 166: 129–140.
- Callahan, H.S., Maughan, H., and Steiner, U.K. (2008). Phenotypic plasticity, costs of phenotypes, and costs of plasticity toward an integrative view. Annals of the New York Academy of Sciences 1133: 44–66.
- Catoni, R., Gratani, L., and Varone, L. (2012). Physiological, morphological and anatomical trait variations between winter and summer leaves of Cistus species. Flora 207: 442–449.
- Chevin, L., Lande, R., and Mace, G.M. (2010). Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology 8 (4): e1000357.
- Choi, W., Toyota, M., Kim, S. et al. (2014). Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. PNAS 111: 6497–6502.
- Chun, Y.J. (2011). Phenotypic plasticity of introduced versus native purple loosestrife: univariate and multivariate reaction norm approaches. Biological Invasions 13: 819–829.
- Colautti, R.I. and Barrett, S.C.H. (2013). Rapid adaptation to climate facilitates range expansion of an invasive plant. Science 342: 364–366.
- Coté, I.M., Darling, E.S., and Brown, C.J. (2016). Interactions among ecosystem stressors and their importance in conservation. Proceedings of the Royal Society B 283: 1–9.
- Crisp, P.A., Ganguly, D., Eichten, S.R. et al. (2016). Reconsidering plant memory: intersections between stress recovery, RNA turnover, and epigenetics. Science Advances 2 (2): e1501340.
- Dalal, A., Attia, Z., and Moshelion, M. (2017). To produce or to survive: how plastic is your crop stress physiology? Frontiers in Plant Science 8: 1–8.
- Del Valle, C.J., Buide, M.L., Whittall, J.B., and Narbona, E. (2018). Phenotypic plasticity in light-induced flavonoids varies among tissues in Silene littorea (Caryophyllaceae). Environmental and Experimental Botany 153: 100–107.
- Demmig-Adams, B., Cohu, C.M., Muller, O., and William, W.A. (2012). Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynthesis Research 113: 75–88.
- Dodd, M.S., Papineau, D., Grenne, T. et al. (2017). Evidence for early life in Earth's oldest hydrothermal vent precipitates. Nature 543: 60–64.
- Dorn, L.A., Pyle, E.H., and Schmitt, J. (2000). Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs. Evolution 54: 1982–1994.
- Droste, T., Flory, S.L., and Clay, K. (2010). Variation for phenotypic plasticity among populations of an invasive exotic grass. Plant Ecology 207: 297–306.
- Du, C., Wang, X., Zhang, M. et al. (2019). Effects of elevated CO2 on plant C-N-P stoichiometry in terrestrial ecosystems: a meta-analysis. Science of the Total Environment 650: 697–708.
- Edelaar, P., Jovani, R., and Gomez-Mestre, I. (2017). Should I change or should I go? Phenotypic plasticity and matching habitat choice in the adaptation to environmental heterogeneity. The American Naturalist 190: 506–520.
- Ernande, B. and Dieckmann, U. (2004). The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics. Journal of Evolutionary Biology 17: 613–628.
- Fenollosa, E., Munné-bosch, S., and Pintó-marijuan, M. (2017). Contrasting phenotypic plasticity in the photoprotective strategies of the invasive species Carpobrotus edulis and the coexisting native species Crithmum maritimum. Physiologia Plantarum 160: 185–200.
- Fenollosa, E., Gámez, A., and Munné-bosch, S. (2018). Plasticity in the hormonal response to cold stress in the invasive plant Carpobrotus edulis. Journal of Plant Physiology 231: 202–209.
- Fischer, E.M., Beyerle, U., Schleussener, C.F. et al. (2018). Biased estimates of changes in climate extremes from prescribed SST simulations. Geophysical Research Letters 45: 8500–8509.
- Forrest, J.R.K. and Thomson, J.D. (2011). An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecological Monographs 81: 469–491.
- Forsman, A. (2015). Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115: 276–284.
- Franks, S.J., Weber, J.J., and Aitken, S.N. (2013). Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7: 123–139.
- Gabriel, W. (2005). How stress selects for reversible phenotypic plasticity. Journal of Evolutionary Biology 18: 873–883.
- Gagliano, M., Renton, M., Depczynski, M., and Mancuso, S. (2014). Experience teaches plants to learn faster and forget slower in environments where it matters. Behavioral Ecology 175: 63–72.
- Ghalambor, C.K., McKay, J.K., Carroll, S.P., and Reznick, D.N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new. Functional Ecology 21: 394–407.
- Gianoli, E. and Palacio-López, K. (2009). Phenotypic integration may constrain phenotypic plasticity in plants. Oikos 118: 1924–1928.
- Gianoli, E. and Valladares, F. (2012). Studying phenotypic plasticity: the advantages of a broad approach. Biological Journal of the Linnean Society 105: 1–7.
- Godoy, O. and Valladares, F. (2012). The relative importance for plant invasiveness of trait means, and their plasticity and integration in a multivariate framework. New Phytologist 195: 912–922.
- Hedrich, R., Salvador-recatalà, V., and Dreyer, I. (2016). Electrical wiring and long-distance plant communication. Trends in Plant Science 21: 376–387.
- Hendrey, G.R., Ellsworth, D.S., Lewin, K.F., and Nagy, J. (1999). A free-air enrichment system for exposing tall forest vegetation to elevated atmospheric CO2. Global Change Biology 5: 293–309.
- Herman, J.J. and Sultan, S.E. (2011). Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2: 1–10.
- Hughes, T.P., Kerry, J.T., Connolly, S.R. et al. (2019). Ecological memory modifies the cumulative impact of recurrent climate extremes. Nature Climate Change 9: 40–43.
- Jung, J., Domijan, M., Klose, C. et al. (2016). Phytochromes function as thermosensors in Arabidopsis. Science 354: 886–889.
- Knight, T.M., Steets, J.A., Vamosi, J.C. et al. (2005). Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36: 467–497.
- Koini, M.A., Alvey, L., Allen, T. et al. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription Factor PIF4. Current Biology 19: 408–413.
- Lande, R. (2009). Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22: 1435–1446.
- Latta, L.C., Weider, L.J., Colbourne, J.K., and Pfrender, M.E. (2012). The evolution of salinity tolerance in Daphnia: a functional genomics approach. Ecology Letters 15: 794–802.
- Legris, M., Klose, C., Burgie, E.S. et al. (2016). Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354: 897–900.
- Long, S.P., Ainsworth, E.A., Rogers, A., and Ort, D.R. (2004). Rising atmospheric carbon dioxide: plants FACE the future. Annual Review of Plant Biology 55: 591–628.
- Lüttge, U., Beck, E., and Bartels, D. (2011). Plant Desiccation Tolerance. Springer-Verlag.
10.1007/978-3-642-19106-0_3 Google Scholar
- Marchiori, P.E.R., Machado, E.C., Sales, C.R.G. et al. (2017). Physiological plasticity is important for maintaining sugarcane growth under water deficit. Frontiers in Plant Science 8: 1–12.
- Mathur, S. and Jajoo, A. (2014). Alterations in photochemical efficiency of photosystem II in wheat plant on hot summer day. Physiology and Molecular Biology of Plants 20: 527–531.
- Memmott, J., Craze, P.G., Waser, M., and Price, M.V. (2007). Global warming and the disruption of plant–pollinator interactions. Ecology Letters 10: 710–717.
- Menzel, A., Sparks, T.H., Estrella, N. et al. (2006). European phenological response to climate change matches the warming pattern. Global Change Biology 12: 1969–1976.
- Merilä, J. and Hendry, A.P. (2013). Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications 7: 1–14.
- Michmizos, D. and Hilioti, Z. (2019). A roadmap towards a functional paradigm for learning and memory in plants. Journal of Plant Physiology 232: 209–215.
- Mikolajewski, D.J., Johansson, F., Wohlfahrt, B., and Stoks, R. (2006). Invertebrate predation selected for the loss of a morphological antipredator trait. Evolution 60: 1306–1310.
- Miller, G., Schlauch, K., Tam, R. et al. (2009). The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Science Signaling 2: ra45.
- Mittler, R. (2006). Abiotic stress, the field environment and stress combination. Trends in Plant Science 11: 1360–1385.
- Munné-Bosch, S., Queval, G., and Foyer, C.H. (2013). The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiology 161: 5–19.
- Murren, C.J., Auld, J.R., Callahan, H. et al. (2015). Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity. Heredity 115: 293–301.
- Nakashima, S., Kebukawa, Y., Kitadai, N., and Igisu, M. (2018). Geochemistry and the origin of life: from extraterrestrial processes, chemical evolution on earth, fossilized life's records, to natures of the extant life. Life (Basel, Switzerland) 8: 1–21.
- Nakayama, H., Sinha, N.R., and Kimura, S. (2017). How do plants and phytohormones accomplish heterophylly, leaf phenotypic plasticity, in response to environmental cues. Frontiers in Plant Science 8: 1–7.
- Narayanan, S., Tamura, P.J., Roth, M.R. et al. (2016). Wheat leaf lipids during heat stress: high day and night temperatures result in major lipid alterations. Plant, Cell and Environment 39: 787–803.
- Nievola, C.C., Carvalho, C.P., Carvalho, V. et al. (2017). Rapid responses of plants to temperature changes. Temperature 4: 371–405.
10.1080/23328940.2017.1377812 Google Scholar
- Parker, I.M., Rodriguez, J., and Loik, M.E. (2003). An evolutionary approach to understanding the biology of invasions: local adaptation and general-purpose genotypes in the weed Verbascum thapsus. Conservation Biology 17: 59–72.
- Pei, Z., Murata, Y., Benning, G.J. et al. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406: 731–734.
- Pigliucci, M. (2005). Evolution of phenotypic plasticity: where are we going now? Trends in Ecology & Evolution 20: 481–486.
- de Pinto, M.C., Locato, V., Paradiso, A., and De Gara, L. (2015). Role of redox homeostasis in thermo-tolerance under a climate change scenario. Annals of Botany 116: 487–496.
- Price, T.D., Qvarnström, A., and Irwin, D.E. (2003). The role of phenotypic plasticity in driving genetic evolution. Proceedings of the Royal Society B: Biological Sciences 270: 1433–1440.
- Puglielli, G., Gratani, L., Catoni, R. et al. (2017). Short-term physiological plasticity: trade-off between drought and recovery responses in three Mediterranean Cistus species. Ecology and Evolution 7: 10880–10889.
- Ramel, F., Birtic, S., Ginies, C. et al. (2012). Carotenoid oxidation products are stress signals that mediate gene responses to singlet oxygen in plants. PNAS 109: 5535–5540.
- Raschke, K., Shabahang, M., and Wolf, R. (2003). The slow and the quick anion conductance in whole guard cells: their voltage-dependent alternation, and the modulation of their activities by abscisic acid and CO2. Planta 217: 639–650.
- Reich, P.B., Hobbie, S.E., Lee, T.D., and Pastore, M.A. (2018). Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment. Science 360: 317–320.
- Rentel, M.C., Knight, M.R., and Kingdom, U. (2004). Oxidative stress-induced calcium signaling. Plant Physiology 135: 1471–1479.
- Rezaei, E.E. (2018). Climate change effect on wheat phenology depends on cultivar change. Scientific Reports 8: 1–10.
- Richards, E.J. (2006). Inherited epigenetic variation: revisiting soft inheritance. Nature Reviews 7: 395–402.
- Rico, L., Ogaya, R., and Barbeta, A. (2014). Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biology 16: 419–427.
- Rubio de Casas, R., Vargas, P., Perez-Corona, E. et al. (2009). Variation in sclerophylly among Iberian populations of Quercus coccifera L. is associated with genetic differentiation across contrasting environments. Plant Biology 11: 464–472.
- Saidi, Y., Peter, M., Finka, A. et al. (2010). Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response. Plant Signalling and Behaviour 5: 1530–1533.
- Scheiner, S.M. (1993). Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 24: 35–68.
- Scheiner, S.M. and Holt, R.D. (2012). The genetics of phenotypic plasticity. X. Variation versus uncertainty. Ecology and Evolution 2: 751–767.
- Scheiner, S.M., Barfield, M., and Holt, R.D. (2017). The genetics of phenotypic plasticity. XV. Genetic assimilation, the Baldwin effect, and evolutionary rescue. Ecology 7: 8788–8803.
- Seal, C.E., Daws, M.I., Flores, J. et al. (2017). Thermal buffering capacity of the germination phenotype across the environmental envelope of the Cactaceae. Global Change Biology 23: 5309–5317.
- Sevanto, S. and Dickman, L.T. (2015). Where does the carbon go?—Plant carbon allocation under climate change. Tree Physiology 35: 581–584.
- Sheffield, J., Wood, E.F., and Roderick, M.L. (2012). Little change in global drought over the past 60 years. Nature 491: 435–438.
- Snell-rood, E.C. and Carolina, S. (2012). Integrative and comparative biology selective processes in development: implications for the costs and benefits of phenotypic plasticity. Integrative and Comparative Biology 52: 31–42.
- Sultan, S.E. and Spencer, H.G. (2002). Metapopulation structure factors plasticity over local adaptation. The American Naturalist 160: 271–283.
- Sultan, S.E., Barton, K., and Wilczek, A.M. (2009). Contrasting patterns of transgenerational plasticity in ecologically distinct congeners. Ecology 90: 1831–1839.
- Takahashi, S. and Badger, M.R. (2011). Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science 16: 53–60.
- Tonnabel, J., David, P., and Pannell, J.R. (2017). Sex-specific strategies of resource allocation in response to competition for light in a dioecious plant. Oecologia 185: 675–686.
- Tuba, Z. (2008). Notes on the poikilochlorophyllous desiccation-tolerant plants. Acta Biologica Szegediensis 52: 111–113.
- Turcotte, M.M. and Levine, J.M. (2016). Phenotypic plasticity and species coexistence. Trends in Ecology & Evolution 31: 803–813.
- Valladares, F., Sanchez-gomez, D., and Zavala, M.A. (2006). Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology 94: 1103–1116.
- Valladares, F., Gianoli, E., and Gómez, J.M. (2007). Ecological limits to plant phenotypic plasticity. New Phytologist 176: 749–763.
- Valladares, F., Bastias, C.C., Godoy, O. et al. (2015). Species coexistence in a changing world. Frontiers in Plant Science 6: 1–16.
- Van Heerwaarden, B. and Sgrò, C.M. (2017). The quantitative genetic basis of clinal divergence in phenotypic plasticity. Evolution 71: 2618–2633.
- Van Kleunen, M. and Fischer, M. (2004). Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytologist 166: 49–60.
- Van Tienderen, P.H. (1991). Evolution of generalists and specialists in spatially heterogeneous environments. Evolution 45: 1317–1331.
- Verma, V., Ravindran, P., and Kumar, P.P. (2016). Plant hormone-mediated regulation of stress responses. BMC Plant Biology 16: 86.
- Virdi, K.S., Laurie, J.D., Xu, Y. et al. (2015). Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nature Communications 6: 1–9.
- Wang, Z., Pang, X., and Lv, Y. (2012). A dynamic framework for quantifying the genetic architecture of phenotypic plasticity. Briefings in Bioinformatics 14: 82–95.
- Wei, Z., Du, T., Li, X. et al. (2018). Interactive effects of elevated CO2 and N fertilization on yield and quality of tomato grown under reduced irrigation regimes. Frontiers in Plant Science 9: 1–10.
- West-Eberhard, M.J. (2005). Developmental plasticity and the origin of species differences. PNAS 102: 6543–6549.
- Woodward, F.I. (2002). Potential impacts of global elevated CO2 concentrations on plants. Current Opinion in Plant Biology 5: 207–211.
- Woodward, F.I., Lake, J.A., and Quick, W.P. (2002). Stomatal development and CO2: ecological consequences. New Phytologist 153: 477–484.
- Zhao, X., Zhou, N., Lai, S. et al. (2019). Elevated CO2 improves lodging resistance of rice by changing physicochemical properties of the basal internodes. Science of the Total Environment 647: 223–231.
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