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Evolution of environmental stress responses in plants

2020; Wiley; Volume: 43; Issue: 12 Linguagem: Inglês

10.1111/pce.13922

1365-3040

Zhong‐Hua Chen, Pamela S. Soltis,

Allelopathy and phytotoxic interactions

Green plants (Viridiplantae) have been impacted by environmental stress throughout their approximately 500 million years of evolution. Diverse sources of environmental pressure have shaped the adaptation, the diversification and the extinction of green plant lineages, ultimately influencing agriculture and human health. Environmental stress factors include temperature, drought, salinity, flooding, quantity and quality of light, concentration of atmospheric CO2, soil nutrient and heavy metal content; all have been major topics for agricultural, ecological and environmental research in recent decades. Environmental stress responses in green plants have been studied for decades, using lab-based experimentation of biochemistry and genetics, physiological studies in controlled environmental facilities, field-based ecological surveys, broad phylogenetically based studies, or a combination of these approaches (Bromham, Hua, & Cardillo, 2016; De Storme & Geelen, 2014; Mizoguchi, Ichimura, & Shinozaki, 1997; Zhao et al., 2019). However, most studies are limited to a single or a small number of plant species. When and how did green plants evolve the adaptive mechanisms to respond to diverse environmental stresses? Addressing these questions will require application of advanced research tools coupled with a firm understanding of Viridiplantae morphology and evolution. This is a multi-disciplinary endeavour, combining expertise in plant systematics, phylogenetics, phylogenomics, molecular biology, physiology and ecology to decipher the underlying mechanisms (Figure 1). Below we give an overview of the content of the Special Issue of Plant, Cell & Environment on "Evolution of Environmental Stress Responses in Plants." We will begin at a broad ecological-evolutionary scale, and then focus more on the fine scale adaptations involved in stress tolerance. The review article by Bromham and co-authors present a comprehensive overview of "macro-evoeco" studies—that is, macroevolutionary and macroecological analyses and their potential utilization for investigating the evolution of environmental stress response in Viridiplantae (Bromham, Hua, & Cardillo, 2020). Macroevolutionary and macroecological analyses from many different species introduce a new perspective on environmental stress shaping plant evolution and the distribution of biodiversity. The authors tested the evolution of salt tolerance as a case study that illustrates a macroevolutionary approach to the evolution of environmental stress tolerances. The authors mapped the phylogenetic distribution of salt tolerance of 200 known halophytes across a phylogenetic tree of 2,684 grasses (Edwards & Smith, 2010) and found the distribution of salt-tolerant species is uneven. Interestingly, many salt-tolerant species occur in clades with few or no other halophytes, indicating many independent origins of salt tolerance in the grass family (Bromham et al., 2020). The authors then provide three explanations of this "tippy" phylogenetic distribution of a stress tolerance trait that can be produced by very different mechanisms: (a) repeated evolution in response to recent environmental change, (b) overall frequent gain and frequent loss (reversal), (c) frequent gain and a high extinction rate. The authors concluded that salt tolerance in grasses is not "hard to evolve." Instead, salt tolerance plants arise presumably due to the competitive advantage of the adaptation in saline conditions where other salt-sensitive species cannot grow. Three macroecological models (Specialists colonize, Locals adapt, Generalists disperse) were discussed in detail for the formation of species assemblages in areas of high environmental stress (Bromham et al., 2020). Some potential future applications of macroevolutionary and macroecological analyses of large clades of plants were proposed to facilitate better prediction of current stress tolerance on the plant species to adapt to changing environmental stresses. Flowering plants (angiosperms) are the largest land plant lineage with over 304,419 accepted species classified in 405 families and 14,559 genera (http://www.theplantlist.org). The tremendous diversity of flowering plants was greatly enhanced by their ability to adapt to broad ranges of stressful environmental conditions, which may be linked, in part, to the frequent occurrence of whole-genome duplication (WGD) events (Caperta, Rois, Teixeira, Garcia-Caparros, & Flowers, 2020; One Thousand Plant Transcriptomes Initiative, 2019; Soltis & Soltis, 2000; Zhang et al., 2020). Zhang and colleagues review ancient polypoidization events and summarize the possible role of WGD for facilitation of adaptation to environmental stress (Zhang et al., 2020). Growing evidence indicates that multiple ancient polyploidy events occurred around 100–120 million years ago during the Cretaceous, and drove the early diversification of major clades of angiosperms. These events were the gamma WGD in the common ancestor of core eudicots, the tau WGD of monocots, the lambda WGD of magnoliids and the pi WGD in Nymphaeales. Although these ancient WGDs occurred independently, they have contributed to the expansion of many stress-related genes in these lineages which may have been utilized by plants to adapt to global environmental changes in the Cretaceous. The authors also reviewed evidence for the possible contributions of WGD and gene duplications may have made to the adaptation of heat shock transcription factor (HSFs) for high temperatures, the C-repeat binding factor transcription factors (CBFs) for low temperature, and the Arabidopsis response regulators (ARRs) for light stress (Zhang, Wu, et al., 2020). The review by Viudes and colleagues aimed at the under-studied field of myxodiaspory evolution, indicating the release of a polysaccharidic mucilage upon water imbibition of seeds (myxospermy) or fruits (myxocarpy) of myxodiasporous species may have potential roles in plant response to environmental stresses (Viudes, Burlat, & Dunand, 2020). A deep characterization of the molecular actors revealed the mucilage secretory cell (MSC) toolbox that underpins seed mucilage establishment in Arabidopsis thaliana (Francoz, Ranocha, Burlat, & Dunand, 2015). Recent studies reported that 94 genes (a majority of them transcription factors) of the MSC toolbox participate in seed mucilage production and release in A. thaliana (Francoz et al., 2015; Viudes et al., 2020). The authors showed that key genes transparent testa glabra 1 (TTG1) and basic helix–loop–helix (bHLH) have strong sequence and functional conservation across flowering plants. Recent advances on three main aspects of myxodiaspory were also summarized. First of all, it represents a combination of highly diverse traits, ranging from the evolution of mucilage secretory cells to diverse polysaccharidic composition and ultrastructural organization of mucilage. Secondly, an asymmetrical selection pressure is exerted on myxospermy-related genes in A. thaliana. Thirdly, newly identified myxodiaspory ecological functions indicate new perspectives in the control of soil microorganisms and establishment support of plants. Thus, the evolution of seed mucilage is a wide-spread capacity in angiosperms providing multiple ecological functions including higher germination efficiency under diverse environmental stresses (Viudes et al., 2020). The global impact of climatic shifts during the Miocene (23–5.3 million years ago) had dramatic implications for today's flora and fauna. Global cooling and aridification in the Miocene promoted the evolution of modern terrestrial biomes on a global basis, including the expansion of grasslands, deserts, as well as arctic-alpine habitats (Folk, Siniscalchi, & Soltis, 2020; Herbert et al., 2016). Global cooling and aridification during the mid-Miocene promoted the radiation of many extreme-adapted flowering plants (Folk et al., 2019; Sun et al., 2020). Folk and co-authors provide a broad synthesis from an evolutionary/phylogenetic perspective, linking stress response to plant physiological traits, morphology and genomic diversity of flowering plants. The authors summarize the diverse physiological and structural traits and the phylogenetic distribution of the adaptations to cold and drought. The authors also describe the recurring association of these changes with rapid diversification events of flowering plants that occurred in multiple lineages since the Miocene (Folk et al., 2020). Across the three-fold facets of dry-cold correlation (traits, phylogeny and time), the authors highlight the amazing diversity of solutions flowering plants have developed in the face of extreme environments. Significantly, they note the broad correlation between cold and dry adaptations that in some cases "may hint at deep common origins." Moreover, they suggest that cold and drought adaptations have numerous parallels that fall along three levels: (a) many shared traits from the cell level to general habit, (b) close phylogenetic relationships among radiations in freezing- and drought-prone habitats and (c) a similar timing of those historical climatic shifts that gave rise to modern cold and dry habitats (Folk et al., 2020). A certain level of drought tolerance and/or avoidance has been key to survival for most land plants since their colonization of terrestrial landscapes roughly 500 million years ago (Komatsu, Takezawa, & Sakata, 2020; Zhao et al., 2019). Among the plant hormones, abscisic acid (ABA) is fundamental for land plant adaptation to drought conditions and the core components of angiosperm ABA signalling are soluble ABA receptors (PYR/PYL/RCAR), group A protein phosphatase type 2C (PP2C) and SNF1-related protein kinase2 (SnRK2) (Geiger et al., 2009; Gosti et al., 1999; Ma et al., 2009; Park et al., 2009). Komatsu and colleagues reviewed the functional genomics studies and uncovered the ABA core modules in streptophyte algae (Komatsu et al., 2020; One Thousand Plant Transcriptomes Initiative, 2019; Zhao et al., 2019). The authors describe recent discoveries involving the ABA core module in non-angiosperm green plants, tracing the origin of ABA as a phytohormone. They also discuss the origin of ABA signalling from an evolutionary perspective, suggesting that the core ABA signalling pathway was present in the common ancestor of land plants well before the angiosperm lineage diverged (Komatsu et al., 2020). Identification of an ABA receptor PYL ortholog in Zygnema supports the phylogenomic placement of Zygnematales as the closest streptophyte algal relatives of land plants. Evidence also suggests that laterally transferred PYR/PYL/RCAR co-opted a pre-existing signalling cascade in streptophyte algae through inhibition of PP2C activity without ABA-binding activity. This step would have been a key evolutionary event for establishing ABA signalling and providing the opportunity for a foothold on land. In the common ancestor of land plants, PYR/PYL/RCAR evolved to bind ABA, marking the emergence of ABA receptors to interact with PP2C-A in an ABA-dependent manner (Komatsu et al., 2020; Sun et al., 2019). It was also speculated that molecular evolution of PYR/PYL/RCAR in land plants, which can repress PP2C-A in an ABA-dependent manner, enabled land plants to tolerate desiccation. Molecular techniques such as transformation of streptophyte algae and bryophytes should be employed to examine the role of the prototype of streptophyte algal ABA signalling and the complex drought tolerance during land plant evolution (Komatsu et al., 2020). In a research article of this Special Issue, De La Harpe and colleagues studied the adaptive radiation of flowering plants in Bromeliaceae (pineapple family) to xeric (heat/drought) conditions using phylogenomic approaches, whole-genome sequencing, RNA-sequencing and metabolite profiling (De La Harpe et al., 2020). Evolutionary analyses of sequencing data suggest that evolution of Crassulacean acid metabolism (CAM) is associated with changes to different pathways mediating xeric adaptation in Bromeliaceae. C3/CAM shifts were accompanied by gene expansion of XAP5 Circadian Timekeeper homologs, regulating sugar- and light-dependent growth and development. This links carbohydrate flux to drought hormone ABA-mediated response to heat/drought stresses via differential gene expression of ABF2/ABF3 transcription factor homologs and adaptive sequence evolution of an ENO2/LOS2 enolase homolog (De La Harpe et al., 2020). Based on the results, the authors indicated that the correlated trait shifts are triggered by relatively few changes at pleiotropic regulators, rather than genomic clustering of adaptive mutations. The repeated trait shifts may be due to convergent evolution or early evolutionary events at the onset of the radiation of the Bromeliaceae (De La Harpe et al., 2020), which requires further investigations. Salinity is a major threat to biodiversity, ecosystems and global food security (Munns et al., 2020). In this Special Issue, three groups of scientists present systematic reviews of their understanding of the evolution of plant salinity tolerance at ecological, physiological, cellular and molecular levels (Caperta et al., 2020; Kotula, Garcia Caparros, Zorb, Colmer, & Flowers, 2020; Liu et al., 2020). Secretory structures (e.g., mucilage secretion, salt glands) are found in all angiosperm clades, with the potential to influence plant microenvironments, nutrient balance and stress tolerance (Galloway, Knox, & Krause, 2020; Viudes et al., 2020). Caperta and co-authors studied the link between secretory structures and salt tolerance in plants using the Plumbaginaceae family, which is adapted to a wide range of arid and saline habitats with at least 45 salt-tolerant species. All the halophytic members of Plumbaginaceae have salt glands, but these structures are absent in salt-tolerant members of the sister family Polygonaceae. Only 74 of 524 the euhalophytes (plants that can tolerate at least 200 mM NaCl) are reported to have salt glands—with the Amaranthaceae, Poaceae and Plumbaginaceae accounting for 80% of these species, allowing their successful colonization of saline habitats (Caperta et al., 2020). Improvement of salt tolerance is needed to maintain global food production because most crop species are sensitive to salinity (Munns et al., 2020). Kotula and colleagues summarize successes and failures of transgenic approaches in improving salt tolerance in crop species. They first presented a conceptual model of coordinated physiological and molecular mechanisms in roots and shoots required for salt tolerance. A total of 48 out of 51 transformations overexpressing genes of key proteins contributing to Na+ exclusion (H+-ATPase, salt overly sensitive [SOS1] antiporter and high affinity K+ transporter [HKT1]), Na+ compartmentation in vacuoles (Vacular H+ATPase, Vacular H+PPase, and Na+/H+ antiporter [NHX]), aquaporins and dehydrins showed improvements in salt tolerance on a basis of biomass of transgenic plants. Of these 51 transformations, 26 involved crop species, but with limited tests in field conditions (Kotula et al., 2020; Munns et al., 2012; Schilling et al., 2014). Moreover, 13 transformations involved genes that were cloned from halophytes of the flowering plant families Aizoaceae, Amaranthaceae, Brassicaceae, Iridaceae, Plumbaginaceae, Tamaricaceae and Zygophyllaceae, but the number of genes is too small for a useful systematic analysis. Thus, there is little advantage in using halophytes as a gene donor species when compared with a non-halophyte. The authors also suggest that biotechnological approaches of multiple salt tolerance genes should be attempted (Kotula et al., 2020). Efforts to breed crops for salt tolerance should explore the potential arising from increased understanding of the energy cost of adaptation and from halophytic traits that have passed the "evolution test" (Liu et al., 2020; Munns et al., 2020). One of these traits is an ability to maintain redox balance and efficient reactive oxygen species (ROS) signalling mechanisms. At the molecular and cellular levels, plants rely on ROS-mediated signalling networks, such as the NADPH oxidase encoded by respiratory burst oxidase homologs (RBOHs), that operate upstream of many physiological and genetic processes to adapt to salt stress (Foreman et al., 2003; Liu et al., 2020). Liu and co-authors conducted an evolutionary bioinformatics analysis to link the kinetics of ROS signalling with the abundance and/or structure of NADPH oxidases across 50 contrasting halophytic and glycophytic species as well as species of the major green plant lineages. Predicted RBOH proteins were identified in all the tested plant lineages except some algae species from the Streptophyta, Chlorophyta and Rhodophyta. Interestingly, the authors reported that the number of RBOH copies correlates negatively with salinity stress tolerance in the glycophytic group. Instead, RBOHs in halophytes have evolved additional phosphorylation target sites at the N-termini of the proteins, allowing more control over their function for more efficient ROS signalling and adaptation to saline conditions (Liu et al., 2020). Heavy metals and metalloids are toxic to plants at high concentrations (Meharg, 1994). Some plant species are heavy metal hyperaccumulators; and yet they tolerate and accommodate high amounts of toxic metal without symptoms of toxicity. Manara and colleagues reviewed the genetic evidence for the evolution of heavy metal hyper-tolerance and hyper-accumulation traits. The authors discuss the most updated concepts regarding the evolution of hyperaccumulation and hyper-tolerance, highlighting the ecological context for the plant populations (Manara, Fasani, Furini, & DalCorso, 2020). Metal hyper-tolerance and hyperaccumulation involve plant interaction with different soil types, plant integration within ecological niches and the plant co-evolution with herbivores and pathogens. There are three theories underlying the evolution of hyperaccumulation of metals: allelopathy, induced protection of other abiotic stresses such as drought, and defensive enhancement against herbivores and pathogens. Therefore, studying the evolution of hyperaccumulating plants should focus on joint effects and trade-offs between different forms of defence in natural populations and adaptation to the environment, influencing the genome and epigenome of plants towards evolutionary success (Manara et al., 2020). In summary, this Special Issue of Plant, Cell and Environment represents an interdisciplinary collection of articles addressing some important questions regarding the evolution of abiotic stress response in a broad range of plant species across a broad range of scales. We hope that the questions raised in these articles, their findings and the new hypotheses arising will inspire scientists to conduct exciting research work on this topic in the near future. The research outcomes are likely to contribute new fundamental knowledge and offer practical applications towards the sustainability of the environment, agriculture, food and health.