Immediate Genetic and Epigenetic Changes in F1 Hybrids Parented by Species with Divergent Genomes in the Rice Genus (Oryza)

Abstract

BackgroundInter-specific hybridization occurs frequently in higher plants, and represents a driving force of evolution and speciation. Inter-specific hybridization often induces genetic and epigenetic instabilities in the resultant homoploid hybrids or allopolyploids, a phenomenon known as genome shock. Although genetic and epigenetic consequences of hybridizations between rice subspecies (e.g., japonica and indica) and closely related species sharing the same AA genome have been extensively investigated, those of inter-specific hybridizations between more remote species with different genomes in the rice genus, Oryza, remain largely unknown.Methodology/Principal FindingsWe investigated the immediate chromosomal and molecular genetic/epigenetic instability of three triploid F1 hybrids produced by inter-specific crossing between species with divergent genomes of Oryza by genomic in situ hybridization (GISH) and molecular marker analysis. Transcriptional and transpositional activity of several transposable elements (TEs) and methylation stability of their flanking regions were also assessed. We made the following principle findings: (i) all three triploid hybrids are stable in both chromosome number and gross structure; (ii) stochastic changes in both DNA sequence and methylation occurred in individual plants of all three triploid hybrids, but in general methylation changes occurred at lower frequencies than genetic changes; (iii) alteration in DNA methylation occurred to a greater extent in genomic loci flanking potentially active TEs than in randomly sampled loci; (iv) transcriptional activation of several TEs commonly occurred in all three hybrids but transpositional events were detected in a genetic context-dependent manner.Conclusions/SignificanceArtificially constructed inter-specific hybrids of remotely related species with divergent genomes in genus Oryza are chromosomally stable but show immediate and highly stochastic genetic and epigenetic instabilities at the molecular level. These novel hybrids might provide a rich resource of genetic and epigenetic diversities for potential utilization in rice genetic improvements.

Drosophila Interspecific Hybridization Causes a Deregulation of the piRNA Pathway Genes

“…zuc and spnE are the only genes that displayed higher inter-individual variability in hybrids compared to both parental species (see Supplementary file 6). However, because hybrids are known by their high genome instability, these differences could be due to stochastic genetic and epigenetic changes that do not involve the meiotic process, as suggested by other authors [54]. These results are in concordance with previous studies in hybrids showing high individual and cross heterogeneity in transposition [22] and expression rates [25] of the retrotransposon Osvaldo.…”

Plasticity of Mitochondrial DNA Inheritance and Its Impact on Nuclear Gene Transcription in Yeast Hybrids

“…were common between the two mitotypes and, therefore, likely to be caused by the hybridisation event itself, for example, fitness changes would lead to impaired growth rates and concomitant transcriptional changes [33,34]. Transcriptional shock upon hybridisation has been documented in various plants and animals, and is interestingly associated with differentiation of phenotypic traits in a wide range of environments [35][36][37][38]. However, for those genes whose expression was significantly different between the two mitotypes (when compared to parents), we performed an enrichment analysis to determine the key molecular pathways that are affected by the mitochondrial DNA (Table S4).…”

Genome-scale transcriptional study of hybrid effects and regulatory divergence in an F1 hybrid Ruellia (Wild Petunias: Acanthaceae) and its parents

“…This may in part be explained by responses to genetic and epigenetic instabilities in resultant homoploid or allopolyploid hybrids, a phenomenon known as genome shock [38, 39]. For example, alterations to DNA replication and perturbation of chromatin structures may induce the release of transposons and aberrant RNA transcripts, and DEGs enriched in pathways that maintain the stability of novel transcripts and degrade aberrant transcripts may be necessary for hybrid function [40, 41].

Fig.

…”