An Epigenetic Alphabet of Crop Adaptation to Climate Change

Abstract

Crop adaptation to climate change is in a part attributed to epigenetic mechanisms which are related to response to abiotic and biotic stresses. Although recent studies increased our knowledge on the nature of these mechanisms, epigenetics remains under-investigated and still poorly understood in many, especially non-model, plants, Epigenetic modifications are traditionally divided into two main groups, DNA methylation and histone modifications that lead to chromatin remodeling and the regulation of genome functioning. In this review, we outline the most recent and interesting findings on crop epigenetic responses to the environmental cues that are most relevant to climate change. In addition, we discuss a speculative point of view, in which we try to decipher the “epigenetic alphabet” that underlies crop adaptation mechanisms to climate change. The understanding of these mechanisms will pave the way to new strategies to design and implement the next generation of cultivars with a broad range of tolerance/resistance to stresses as well as balanced agronomic traits, with a limited loss of (epi)genetic variability.

Zebularine, a DNA Methylation Inhibitor, Activates Anthocyanin Accumulation in Grapevine Cells

“…In most cases, a high methylation level at the promoter in all sequence contexts is associated with a reduced gene expression [ 35 ], although in a few cases the reverse situation was demonstrated, as for example for the Arabidopsis ROS1 gene [ 36 , 37 ]. Moreover, transcriptional regulation through DNA methylation has been shown to play important roles during plant development and in response to environmental changes [ 38 , 39 , 40 , 41 ]. Interestingly, the genes whose expression regulation involves DNA methylation include a number of genes related to plant metabolism and in particular to plant secondary metabolism.…”

Epigenetic variation: A major player in facilitating plant fitness under changing environmental conditions

“…Notably, phenotypic plasticity patterns do not always follow the principles of Mendelian genetics ( Foust et al, 2016 ; Yi and Goodisman, 2021 ; Guarino et al, 2022 ) and instead are shown to be supported largely by epigenetic mechanisms that generally originate as combinatorial effects of the interactions of genotypes with the environment (Genotype x Environment, abbreviated as GxE) ( Peltier et al, 2018 ). The classic example showing that epigenetic mechanisms generate phenotypic variability came from studies in Linaria vulgaris ( Cubas et al, 1999 ).…”

“…In recent decades, emerging epigenetic processes have been highlighted as promising mechanisms to facilitate the generation of the first tier of rapid phenotypic diversity required to improve the fitness and adaptive responses in the natural populations of plants ( Bräutigam et al, 2013 ; Amaral et al, 2020 ; Ashe et al, 2021 ). A survey of published literature shows that a large number of research investigations wherein the epigenetic route has been shown to deploy rapid phenotypic plasticity for adaptation and evolution have come from studies in model plant and crop species ( Ding et al, 2018 ; Guarino et al, 2022 ; Varotto et al, 2022 ) which is primarily due to the availability of large genomic resources accumulated in this group of plants. The advancement in sequencing technologies and their cost effectiveness, has lately facilitated the availability of genomic resources in natural populations of non-model species as well.…”

“…Plants being stationary get exposed to various periodic (such as seasonal variations) or sudden (such as biotic stresses or climate factors) environmental changes. Epigenetic mechanisms help plants in generating plastic responses to stressful environments ( Lämke and Bäurle 2017 ; Ashapkin et al, 2020 ; Yi and Goodisman, 2021 ; Guarino et al, 2022 ). The plants may remember the past stress(es) and use their past responses’ memory to mitigate the recurring stress(es) by generating a more pronounced and/or faster response through a phenomenon known as ‘defense priming’ or ‘stress priming’ ( Lämke and Bäurle, 2017 ; Liu et al, 2022 ).…”

“…Stress exposure cascades a response-signaling cycle in plants that along with genetic modifications leads to many epigenetic changes routed through mechanisms such as chromatin remodeling, DNA methylation, histone modification, and non-coding RNAs ( Turcotte et al, 2022 ). These epigenetic mechanisms have resulted in novel epialleles associated with morphological, metabolic, and developmental traits in plants ( Tirnaz and Batley 2019 ) that can be exploited for developing new climate-resilient crop varieties to mitigate the challenges of changing environments ( Springer and Schmitz, 2017 ; Kawakatsu and Ecker, 2019 ; Varotto et al, 2020 ; Kakoulidou et al, 2021 ; Guarino et al, 2022 ) and help in crop domestication by targeting epigenetic diversity to engineer crop plants for optimal crop production ( Ding and Chen, 2018 ).…”