DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids

Abstract

Summary Allopolyploidization, which entails interspecific hybridization and whole genome duplication (WGD), is associated with emergent genetic and epigenetic instabilities that are thought to contribute to adaptation and evolution. One frequent genomic consequence of nascent allopolyploidization is homoeologous exchange (HE), which arises from compromised meiotic fidelity and generates genetically and phenotypically variable progenies. Here, we used a genetically tractable synthetic rice segmental allotetraploid system to interrogate genome‐wide DNA methylation and gene expression responses and outcomes to the separate and combined effects of hybridization, WGD and HEs. Progenies of the tetraploid rice were genomically diverse due to genome‐wide HEs that affected all chromosomes, yet they exhibited overall methylome stability. Nonetheless, regional variation of cytosine methylation states was widespread in the tetraploids. Transcriptome profiling revealed genome‐wide alteration of gene expression, which at least in part associates with changes in DNA methylation. Intriguingly, changes of DNA methylation and gene expression could be decoupled from hybridity and sustained and amplified by HEs. Our results suggest that HEs, a prominent genetic consequence of nascent allopolyploidy, can exacerbate, diversify and perpetuate the effects of allopolyploidization on epigenetic and gene expression variation, and hence may contribute to allopolyploid evolution.

Gossypium Genomics: Trends, Scope, and Utilization for Cotton Improvement

“…For example, half of the MIXTAs, 40% of the CESAs, and 34% of CSL genes were highly expressed during fiber development of cultivated tetraploid cotton compared with wild species [13]. Polyploidy and domestication are associated with some epigenetic modifications (e.g., DNA methylation, miRNA, and siRNA biogenesis), which facilitate the increased transcripts of some key genes in fiber development [33][34][35]. The enrichment and high expression of fiber-related genes might contribute synergistically to fiber development.…”

Current research frontiers in plant epigenetics: an introduction to a Virtual Issue

“…Without directly altering the underlying DNA sequence, epigenetic signals such as histone modifications, DNA methylation and RNA interference (RNAi) can be specific to particular internal or external conditions and they can have phenotypic implications (e.g. Alonso et al , 2019b; Ding et al , 2019; Gehring, 2019; Li et al , 2019; Zhao et al , 2019). Epigenetics was first addressed in New Phytologist in 2003 in the context of genomic changes after whole genome doubling (Soltis et al , 2003).…”

“…Given their prevalence, disentangling the effects of hybridization and polyploidy from one another promises to improve our knowledge about plant genome evolution. Li et al (2019) report a large‐scale methylome stability across several rice accessions, including diploid parents, diploid F 1 hybrids and allotetraploids. However, they observed in the allopolyploids considerable but regional re‐patterning in the DNA methylation landscape that was missing in the diploid hybrid genomes, indicating that in this system hybridity can exacerbate, only in combination with polyploidy, a rewiring of epigenetic and gene expression landscape.…”

Replaying the evolutionary tape to investigate subgenome dominance in allopolyploid Brassica napus

“…Given that gene expression level dominance occurs instantly following the initial hybridization event (15) , resynthesized allopolyploids are the ideal system to investigate the establishment and escalation of subgenome dominance. Few studies have used multiple independently derived resynthesized allopolyploids to investigate the variability of subgenome dominance (21)(22)(23)(24)(25)(26) . Thus it remains unclear the extent to which the emergence of subgenome dominance is a result of pre-existing characteristics of the diploid progenitors or due to independent and non-recurrent events during polyploid formation.…”