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

Ying Wu,Jie Wang,Bao Liu,Kun Shen,Xiuyun Lin,Tingting Jiang,Shuai Sun,Shuai Cao,Jinsong Pang,Samuel Manthi Josiah,Yue Sun,Khalil Kashkush

doi:10.1371/journal.pone.0132911

Ying Wu, Jie Wang + Show 10 more

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https://doi.org/10.1371/journal.pone.0132911

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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.

Highlights

Interspecific hybridization and its attendant whole genome doubling are important evolutionary players in higher plants [1,2,3,4]
We 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
These rapid genomic changes are diverse in scope, including nucleotide base changes, activation of transposable elements (TEs), and cytosine methylation alterations, which are often causally linked to changes in gene expression, function and new phenotypes [19,20,21,22]

Summary

Introduction

Interspecific hybridization and its attendant whole genome doubling (allopolyploidization) are important evolutionary players in higher plants [1,2,3,4]. Recent genetic and genomic studies have revealed a range of rapid genetic and epigenetic changes associated with nascent hybridization and polyploidization in many plant taxa including Arabidopsis [5, 6], wheat [7,8,9,10,11], Brassica [12, 13], Spartina [14, 15], and others [16, 17] These findings have lent strong supports to the “genome shock” theory proposed by McClintock nearly 30 years ago [18]. 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.

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