Plant phenotypic plasticity in a changing climate A.B. Nicotra', O.K. Atkin" S.P. Bonser2, A.M. Davidson" E.J. Finnegan3, U. Mathesius', P. Poot4, M.D. Purugganan5, C.L. Richards6, F. Valladares7 and M. van Kleunen8 1 Research School of Biology, The Australian National University, Canberra, ACT, Australia 2 Evolution and Ecology Research Centre & School of Biological, Earth and Environmental Sciences University of New South Wales Sydney, Australia 3 CSIRO Plant Industry, Canberra, ACT, Australia 4 School of Plant Biology, Faculty of Natural and Agricultural Sciences, University of Western Australia, Crawley, WA, Australia, and Science Division, Department of Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, WA, Australia 5 Department of Biology, Center for Genomics and Systems Biology, New York University, New York, NY, USA 6 Department of Integrative Biology, University of South Florida, Tampa, FL, USA 71nstituto de Recursos Naturales. CSIC, Madrid, Spain 8 Institute of Plant Sciences and Oeschger Centre, University of Bern, Bern, Switzerland Climate change is altering the availability of resources Glossary and the conditions that are crucial to plant performance. One way plants will respond to these changes is through Adaptive plasticity: Phenotypic plasticity that increases the global fitness of a genotype (Figure 2). environmentally induced shifts in phenotype (phenotyp­ Environmental sensing loci: Genes or gene regions that encode sensors, or ic plasticity). Understanding plastic responses is crucial receptors, for environmental signals, e.g. genes encoding photoreceptors or for predicting and managing the effects of climate receptors detecting microbial signals. Epialleles: Different forms or alleles of a gene that are identical in DNA change on native species as well as crop plants. Here, sequence but differ in epigenetic markers. These epigenetic differences are we provide a toolbox with definitions of key theoretical usually associated with differing expressions of the epialleles. The causes of elements and a synthesis of the current understanding of their formation are as yet poorly understood. Epigenetic: Includes the mechanisms of gene regulation that lead to heritable. the molecular and genetic mechanisms underlying plas­ but potentially reversible. changes in gene expression without changing the ticity relevant to climate change. By bringing ecological, DNA sequence of the gene (Box 1). evolutionary, physiological and molecular perspectives Fitness: The fitness of an individual is taken as the relative abundance and success of its genes (often measured as the number of surviving offspring) together, we hope to provide clear directives for future over multiple generations. In many cases, especially with large or long-lived research and stimulate cross-disciplinary dialogue on species, direct estimates of fitness are not feasible and total biomass, seed the relevance of phenotypic plasticity under climate number or biomass, survivorship or growth rates of a single generation are used as proxies. change. Genome plasticity: A change in genome structure or organization associated with environmental signals. leading to the evolution of new phenotypes. might Climate change and plant adaption result from mutational hotspots, genome expansion. transposable elements or somatic recombination. Climate change is altering the environments in which all Genotype: When we refer to a genotype we do so in a population genetic organisms develop. Plant species can adjust to these novel sense. not in reference to a molecular sequence of a single gene. but to the conditions through phenotypic plasticity (see Glossary), complete genome. Phenotype: The appearance or characteristics of an organism resulting adapt through natural selection or migrate to follow con­ from both genetic and environmental influences. In our terms, all organisms ditions to which they are adapted; these options are not have a phenotype not just those expressing a mutation in a given gene of mutually exclusive. For any given plant species or popula­ interest. Phenotypic plasticity: The range of phenotypes a single genotype can express tion, determining responses to environmental changes will as a function of its environment. require an understanding of the environmentally induced Plant functional traits: Quantitative traits related to the fitness and success of variation in the phenotype of individual plants. Once individuals in a given environment, they provide good indicators about species' ecologies (e.g. what growth rates they are likely to exhibit. what regarded as noise, phenotypic plasticity is now understood recruitment strategy they rely on) and are often related to competitive status, to be genetically controlled, heritable and of potential commonness/rarity or dominance in the community (Box 2). importance to species' evolution [1,2]. With mounting evi­ Plant functional types: Categorical assessments enabling plant species to be grouped according to functional position in a community or ecosystem. For dence from molecular and developmental biology, we are example, classifications can be based on growth form (e.g. herb, grass. shrub). now at the threshold of gaining a sophisticated under­ nitrogen fixing status. photosynthetic pathway or leaf longevity. Post-transcriptional and post-translational modifications: Chemical modifica­ standing of the mechanisms of plasticity, which will be tions to mRNA or proteins that are made after an mRNA or protein is crucial for predicting changes in species distributions, transcribed or translated. respectively (e.g. the phosphorylation of proteins). community composition and crop productivity under cli­ Regulatory gene transcription: The process of making mRNA of a regulatory gene. The RNA is subsequently translated to form a protein, the product of the mate change [3,4]. gene. Some authors have argued that plastic responses to Signaling cascades: These are cascades of events that mediate cellular rapid climate change are less important than adaptation responses to external signalS, for example the cascades of protein phosphor­ ylation and second messenger generation following the perception of a Signal by a receptor kinase. Corresponding author: Nicotra, A.B. ([email protected]). 684 (a) Epigenetic, transcriptional or post- Environment transcriptional regulation t / "\ Signal � Receptor � Signal cascade • Phenotype (e.g. light) (e.g. (e.g. induction of (e.g. synthesis of photoreceptor) transcription anthocyanin) factors) (b) ",,"",," � E* Phenotype Signal received e.g. Signal is transduced ,�"� '" regulated by by perceiving light into increased with enhanced enzyme G environment, with a photoreceptor transcription of genes, activity and products, e.g. GxE genotypes react e.g. of the ,�." .. __ ,M'" � similarly anthocyanin content in different biosynthesis pathway environment E No environmental Signal receptor may Mutation of Genotypes differ response be missing or mutated transcription factor, or constitutively in trait, <D 2 => G' genes encoding these no environmentally Cij > GxE proteins may be induced change silenced by epigenetic .� mechanisms. I- One genotype has One genotype Genotypes differ in E' Phenotype regulated by more sensitive increases amount of product G' environment, receptor than the transcription more in produced in response to GxE' genotypes react other response to signal environment, but both �3 differently. than the other show response � Env1 Env2 Env1 Env2 Figure 1. Anthocyanins are produced in leaves in response to excess light and temperature and osmotic extremes, and serve as a reversible plastic mechanism for the protection of photosynthetic machinery 186-88J. Here, we use an anthocyanin example to illustrate la) the points in the molecular machinery, which translate an environmental signal (excess light in this case) into a phenotype. (b) In the evolutionaryand ecological literature, these responses are commonly presented as reaction norms. Here, the blue and red lines indicate the reaction norms of two different genotypes responding to a change from a low light environment (Env1) to a high light one (Env2). The extent of phenotypic change in response to a signal is its phenotypic plasticity. Asterisks in the panels denote whether there is a significant effect of environment (EJ or genotype (GJ, and whether there is a significant genotype by environment interaction (G x E). (c) Likely examples of the mechanisms underlying the cases depicted in panels 1-3 are given separately for each point in the signal pathway. The leaves on the left and right represent the phenotypes in Env1 and Env2, respectively. or shifts in the geographic range of distribution [5,6], These Thus, we argue that, in the context of rapid climate change, studies argue that the failure to expand beyond current phenotypic plasticity can be a crucial determinant of plant limits demonstrates that a species' adaptive potential has responses, both short- and long-term. been largely exhausted, or argue that plasticity will be an Here, we provide a conceptual toolbox with definitions of unimportant factor because the cues that signaled the the key theoretical elements and a synthesis of the current plastic responses in the first place might no longer be understanding of the molecular and genetic mechanisms 'reliable' in changed climates [7], However, as we show underlying phenotypic plasticity, as relevant to climate below, plastic changes in seed longevity, phenology, leaf change. We discuss