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.

Xenobiotic detoxification is a common trait of all living organisms, necessary for developmental plasticity and stress tolerance. The gene set involved in this biological process is dubbed the xenome (i.e. involved in drug metabolism in mammals, degradation of allelochemicals and environmental pollutants by bacteria and plant communities). Recently, we found that allopolyploidy increased tolerance to xenobiotics (phenanthrene) in Spartina. To decipher the molecular mechanisms underlying this process, we examined how interspecific hybridization and genome doubling impact miRNAs expression under xenobiotic induced stress. In this work we used a deep sequencing approach, and analyzed the parental species S. alterniflora and S. maritima, their F1 hybrid S. x townsendii and the allopolyploid S. anglica under phenanthrene exposure. We found that hybridization and genome doubling reprogrammed a myriad of miRNAs under phenanthrene-induced stress. Hence, to identify the master miRNAs involved in phenanthrene tolerance, we performed experimental functional validation of phenanthrene-responsive Spar-miRNAs using Arabidopsis T-DNA mutant lines inserted in homologous MIR genes, 39 knock out T-DNA Arabidopsis mutants, tagged in the most conserved miRNAs genes in vascular plants were screened. Development of MIR159 and MIR156 mutants was significantly affected under phenanthrene-induced stress. Subsequently, we performed in planta experimental validation to confirm the interaction between these miRNAs and their targets. These analyses suggest that MIR159 and MIR156 regulatory modules were targeted to induce the xenome relaxation and impact developmental plasticity responses in phylogenetically distant species under xenobiotic-induced stress. Graphical abstract