Pivotal roles of environmental sensing and signaling mechanisms in plant responses to climate change

Abstract

Climate change reshapes the physiology and development of organisms through phenotypic plasticity, epigenetic modifications, and genetic adaptation. Under evolutionary pressures of the sessile lifestyle, plants possess efficient systems of phenotypic plasticity and acclimation to environmental conditions. Molecular analysis, especially through omics approaches, of these primary lines of environmental adjustment in the context of climate change has revealed the underlying biochemical and physiological mechanisms, thus characterizing the links between phenotypic plasticity and climate change responses. The efficiency of adaptive plasticity under climate change indeed depends on the realization of such biochemical and physiological mechanisms, but the importance of sensing and signaling mechanisms that can integrate perception of environmental cues and transduction into physiological responses is often overlooked. Recent progress opens the possibility of considering plant phenotypic plasticity and responses to climate change through the perspective of environmental sensing and signaling. This review aims to analyze present knowledge on plant sensing and signaling mechanisms and discuss how their structural and functional characteristics lead to resilience or hypersensitivity under conditions of climate change. Plant cells are endowed with arrays of environmental and stress sensors and with internal signals that act as molecular integrators of the multiple constraints of climate change, thus giving rise to potential mechanisms of climate change sensing. Moreover, mechanisms of stress-related information propagation lead to stress memory and acquired stress tolerance that could withstand different scenarios of modifications of stress frequency and intensity. However, optimal functioning of existing sensors, optimal integration of additive constraints and signals, or memory processes can be hampered by conflicting interferences between novel combinations and novel changes in intensity and duration of climate change-related factors. Analysis of these contrasted situations emphasizes the need for future research on the diversity and robustness of plant signaling mechanisms under climate change conditions.

Global Warming, Climate Change, and Environmental Pollution: Recipe for a Multifactorial Stress Combination Disaster

“…The accumulated impact of human life on our planet over the past several decades, and in particular the industrial revolution, resulted in a constant increase in greenhouse gas production (mainly CO 2 ) caused by the burning of fossil fuels ( Figure 1A; www.ipcc.ch/) [1][2][3][4][5][6][7][8][9]. The accumulation of CO 2 in the atmosphere traps the IR radiation emitted from the surface of the Earth following absorption of sunlight and heats our planet, driving an alarming trend of continual increase in global surface and ocean temperatures, termed global warming ( Figure 1A; www.ipcc.ch/, https://ourworldindata.org/owid-grapher, www.eea.europa.eu/) [1][2][3][4][5][6][7][8][9].…”

Element content and expression of genes of interest in guard cells are connected to spatiotemporal variations in stomatal conductance

“…This would result in a different perception and signalization between sides; for example, stomata of Gossypium barbadense (L.) have distinct sensitivity to light between sides linked with different pigment contents (Lu, Quiñones, & Zeiger, 1993). A different sensitivity between sides would lead to a diversity of gene expression (see Bigot et al, 2018), and element content in the guard cells, which may be a part of what we observed. A stronger gene expression on the adaxial side might be seen as the result of a more extreme condition on the side facing the light source.…”

“…Previously reported thermal and irradiance gradients between leaf surfaces of a few degrees (Buckley, John, Scoffoni, & Sack, ; Clum, ; Sheriff, ) could result in different perceived environmental conditions between leaf sides (e.g., light, VPD, and temperature), prompting different stomatal control, as was found on poplar clones in response to a change in light and VPD (Ceulemans, Hinckley, & Impens, ; Pallardy & Kozlowski, ). Differences in the intensity and nature of perceived stresses, such as evaporative demand, light, and heat (Urban, Ingwers, McGuire, & Teskey, ) may induce a distinct conjugation of stress between sides, which may affect the synergic or antagonistic response to environmental cues (Bigot et al, ). This would result in a different perception and signalization between sides; for example, stomata of Gossypium barbadense (L.) have distinct sensitivity to light between sides linked with different pigment contents (Lu, Quiñones, & Zeiger, ).…”

Roles of Organellar RNA-Binding Proteins in Plant Growth, Development, and Abiotic Stress Responses

“…A recent study has also demonstrated that chloroplast-localized SDP, which affects rRNA processing in chloroplasts under normal conditions, has positive effects on salt, heat, freezing, or UV stress tolerance, as it influences the stress-responsive genes in the nucleus [ 117 ]. Beyond organelles, it will be of great interest to investigate how nCMRBP-mediated organellar retrograde signaling (ORS) influences the reprogramming of the expression of stress-responsive nuclear genes, and the organellar and nuclear epigenetic modifications for stress priming and memory [ 101 , 118 , 119 , 120 , 121 ]. Although the study of organellar proteomics and metabolomics is far behind than those in the nucleus and cytoplasm, recent studies emphasize the importance of homeostasis between the nucleus and organelles in plant acclimation to environmental changes [ 122 , 123 , 124 , 125 ].…”