How Stress Facilitates Phenotypic Innovation Through Epigenetic Diversity

Abstract

Climate adaptation through phenotypic innovation will become the main challenge for plants during global warming. Plants exhibit a plethora of mechanisms to achieve environmental and developmental plasticity by inducing dynamic alterations of gene regulation and by maximizing natural variation through large population sizes. While successful over long evolutionary time scales, most of these mechanisms lack the short-term adaptive responsiveness that global warming will require. Here, we review our current understanding of the epigenetic regulation of plant genomes, with a focus on stress-response mechanisms and transgenerational inheritance. Field and laboratory-scale experiments on plants exposed to stress have revealed a multitude of temporally controlled, mechanistic strategies integrating both genetic and epigenetic changes on the genome level. We analyze inter- and intra-species population diversity to discuss how methylome differences and transposon activation can be harnessed for short-term adaptive efforts to shape co-evolving traits in response to qualitatively new climate conditions and environmental stress.

Keywords: abiotic stress; energy stress; epigenetics (DNA methylation); epigenomics; methylome diversity; natural variation in plants; plant engineering; transposable element.

FIGURE 1

Illustrating the differences between methylation and methylome diversity at the population, strain and species-levels. Taking the example of heat stress, physiological changes often occur as an immediate response to acute changes in temperature before epigenetic pathways and transgenerationally stable changes in epigenetic landscapes fall into place (A). When the stress is chronic, populations belonging to a strain (B) non-native to the harsh temperature change often exhibit low survival rates, as they have rather homogenous methylation patterns and can rely only on rapid epigenetic/epigenomic changes for rapid stress-response mechanisms. Between strains however (C), methylome diversity is high and this may enable survival for plants harboring heat-resistant epialleles and modified methyltransferases. At the species-level (D), plants exhibit high levels of methylation and methylome diversity, due to evolutionary fixation of genetic and epigenetic marks, thereby providing an edge for heat-primed species to adapt with greater ease.

FIGURE 2

A conceptual model for transposable element and methylation dynamics illustrated in three different stress scenarios. The cartoons represent a genomic locus that houses a stress-response gene and a methylation-silenced transposable element (TE). When a stress is constantly applied over generations (A), hypomethylation at the TE locus can result in activation and re-insertion proximal to a stress-response associated/stress-response repressor gene, eventually recruiting methylation marks to fix a new regulatory mechanism for long-term stability. When a stress increases in magnitude during the lifetime of a plant (B), epialleles are first created to moderately regulate gene expression. To enable stronger gene expression changes, additional methylation changes are driven by activated TEs and their re-insertion. In situations where stress occurs repeatedly for short intervals (C), plants might require epigenetic switches that can be easily tuned. This can be facilitated by the presence of a distal regulatory element flanking a TE, which can also be hypomethylated upon TE activation, thus altering expression of a gene detrimental for stress-response. When TE activation is brief and does not involve copy number increase, small RNAs are recruited for methylation (through the RdDM pathway) and can spread to the neighboring element, thus switching ‘off’ the regulation once again when the stress is absent.