The Underlying Nature of Epigenetic Variation: Origin, Establishment, and Regulatory Function of Plant Epialleles

Abstract

In plants, the gene expression and associated phenotypes can be modulated by dynamic changes in DNA methylation, occasionally being fixed in certain genomic loci and inherited stably as epialleles. Epiallelic variations in a population can occur as methylation changes at an individual cytosine position, methylation changes within a stretch of genomic regions, and chromatin changes in certain loci. Here, we focus on methylated regions, since it is unclear whether variations at individual methylated cytosines can serve any regulatory function, and the evidence for heritable chromatin changes independent of genetic changes is limited. While DNA methylation is known to affect and regulate wide arrays of plant phenotypes, most epialleles in the form of methylated regions have not been assigned any biological function. Here, we review how epialleles can be established in plants, serve a regulatory function, and are involved in adaptive processes. Recent studies suggest that most epialleles occur as byproducts of genetic variations, mainly from structural variants and Transposable Element (TE) activation. Nevertheless, epialleles that occur spontaneously independent of any genetic variations have also been described across different plant species. Here, we discuss how epialleles that are dependent and independent of genetic architecture are stabilized in the plant genome and how methylation can regulate a transcription relative to its genomic location.

Unveiling the Mysteries of Non-Mendelian Heredity in Plant Breeding

“…It also has practical implications for plant breeding, where understanding the non-Mendelian inheritance of epialleles can help to develop crops that are better adapted to changing environmental conditions and exhibit improved yield potential through epigenetic recombinant inbred lines (epiRILs) ( Figure 2 ) [ 113 , 114 ]. The use of epiRILs allows breeders to employ the function of epigenetic modifications in gene expression and phenotypic variation in a controlled genetic background, reducing the confounding effects of genetic variation [ 107 , 115 ].…”

“…Such epialleles can occur due to the activation of transposable elements (TEs) and their reinsertion into distant loci, determined by chromatin properties and the nature of the target sequence (CG content). The scheme was adapted from Srikant and Tri Wibowo [ 115 ] and was created by using BioRender.com.…”

“…The resulting epiRILs are then genotyped and phenotyped to identify genetic and epigenetic factors that contribute to phenotypic variation. Indeed, by genotyping and phenotyping epiRILs, it can be identified regions of the genome that are associated with phenotypic variation and epigenetic modifications [ 115 ]. This can lead to the identification of epigenetic modifications that are associated with specific phenotypes and can be used to develop crops that are better adapted to changing environmental conditions [ 107 , 116 ].…”

Epigenetic Changes Occurring in Plant Inbreeding

“…The first known epiallele is clark-kent (clk) in Arabidopsis , which is an epiallele of the SUPERMAN (SUP) gene. DNA hypermethylation in the body of the SUP gene was associated with the abnormal development of floral whorls [ 127 , 128 ], but this modification was not stable. In Linaria vulgaris , a stable epimutation was observed, which was associated with the hypermethylation of the Lcyc gene promoter, resulting in a different flower symmetry (radial symmetry) compared to wild-type plants (bilateral symmetry) [ 3 ].…”

Partial redundancy buffers deleterious effects of mutatingDNA methyltransferase 1-1(MET1-1) in polyploid wheat

“…Changes to methylation status can result in the production of stable epialleles which cause transcriptional and phenotypic alterations across generations. Epialleles affecting diverse traits have been identified, including alterations in floral morphology, fruit ripening, plant height and climate adaptation in a range of plant species (Cubas et al, 1999;Manning et al, 2006;He et al, 2018;Srikant & Tri Wibowo, 2021). The deliberate induction of stable epialleles has been demonstrated through epiRIL populations generated genetically by the use of met1 and ddm1 (Decreased DNA Methylation 1) mutants in Arabidopsis (Johannes et al, 2009;Reinders et al, 2009;Zhang et al, 2013;Catoni & Cortijo, 2018).…”