Altered chromatin compaction and histone methylation drive non-additive gene expression in an interspecific Arabidopsis hybrid

Abstract

BackgroundThe merging of two diverged genomes can result in hybrid offspring that phenotypically differ greatly from both parents. In plants, interspecific hybridization plays important roles in evolution and speciation. In addition, many agricultural and horticultural species are derived from interspecific hybridization. However, the detailed mechanisms responsible for non-additive phenotypic novelty in hybrids remain elusive.ResultsIn an interspecific hybrid between Arabidopsis thaliana and A. lyrata, the vast majority of genes that become upregulated or downregulated relative to the parents originate from A. thaliana. Among all differentially expressed A. thaliana genes, the majority is downregulated in the hybrid. To understand why parental origin affects gene expression in this system, we compare chromatin packing patterns and epigenomic landscapes in the hybrid and parents. We find that the chromatin of A. thaliana, but not that of A. lyrata, becomes more compact in the hybrid. Parental patterns of DNA methylation and H3K27me3 deposition are mostly unaltered in the hybrid, with the exception of higher CHH DNA methylation in transposon-rich regions. However, A. thaliana genes enriched for the H3K27me3 mark are particularly likely to differ in expression between the hybrid and parent.ConclusionsIt has long been suspected that genome-scale properties cause the differential responses of genes from one or the other parent to hybridization. Our work links global chromatin compactness and H3K27me3 histone modification to global differences in gene expression in an interspecific Arabidopsis hybrid.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1281-4) contains supplementary material, which is available to authorized users.

Epigenetic perspectives on the evolution and domestication of polyploid plant and crops

“…This suggests differential epigenetic modifications between two subgenomes within the allotetraploid, which is consistent with genome-wide dominance of A. arenosa genes over A. thaliana ones [61••]. A recent study in the interspecific hybrid between A. thaliana and A. lyrata also found overall down-regulation of A. thaliana genes compared to A. lyrata genes, which correlates with A. thaliana chromatin that is more compact than A. lyrata chromatin [83], and the A. thaliana genes that are associated with histone H3K27me3 marks tend to alter their expression in the interspecific hybrid.…”

Extensive allele‐level remodeling of histone methylation modification in reciprocal F1 hybrids of rice subspecies

“…Collectively, our results suggest that although histone modification (H3K4me3 and H3K27me3) remodeling contributes to the overall non‐additive gene expression in rice F 1 hybrids, DNA methylation does not seem to play a major role. This is consistent with recent findings in Arabidopsis intra‐ and interspecific F 1 hybrids that DNA methylation remodeling does not directly impact gene expression (Greaves et al ., ; Zhu et al ., ).…”

“…Gene expression in an F 1 hybrid is regulated by the independent actions, as well as interactions, of its subgenomes. Epiallelic interactions and remodeling may play a major role in orchestrating the unique gene expression profile of a hybrid (Groszmann et al ., ; Shi et al ., ; Zhang et al ., ; Zhu et al ., ; Ding and Chen, ). We profiled transcriptomes in leaf and root of the reciprocal F 1 hybrids and their parent cultivars (NPB and 93‐11).…”

“…Indeed, accumulated studies in several plants, including A. thaliana (Greaves et al ., ; Yang et al ., ; Zhu et al ., ), rice (He et al ., ; Zhao and Zhou, ; Chen and Zhou, ), maize (Springer and Stupar, ; Zhao et al ., ) and sorghum (Zhang et al ., ) have shown that DNA methylation undergoes extensive repatterning in F 1 hybrids. It was found that substantial proportions of genomic regions in parental alleles with either the same or different DNA methylation levels may undergo repatterning in a hybrid, culminating to non‐additive levels (Greaves et al ., ; Guo et al ., ; Zhang et al ., ,; Zheng et al ., ).…”

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

“…A second key result of this study is that, notwithstanding the overall methylome stability among the genomically divergent and recombinant allopolyploid rice lines, locus‐specific DNA methylation repatterning occurred extensively, and that this effect appears to be caused by the combination of WGD and HEs, rather than by hybridization per se. In this aspect, we note that several previous studies in a wide spectrum of plant taxa including A. thaliana (Greaves et al ., ; Yang et al ., ; Zhu et al ., ), rice (He et al ., ; Chodavarapu et al ., ; Zhao & Zhou, ; Chen & Zhou, ) and maize (Springer & Stupar, ; Zhao et al ., ) have shown that DNA methylation may undergo extensive repatterning in F1 hybrids. However, our results indicate that the effect of hybridization on DNA methylation alteration pales when compared with that of WGD and HEs.…”