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Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids.

ABSTRACT: As a major agent of rapid speciation, interspecific hybridization has played an important role in plant evolution. When hybridization involves species that exhibit self-incompatibility (SI), this prezygotic barrier to self-fertilization must be overcome or lost to allow selfing. How SI, a normally dominant trait, is lost in nascent hybrids is not known, however. Here we demonstrate that hybrid self-fertility can result from epigenetic changes in expression of the S-locus genes that determine specificity in the SI response. We analyzed loss of SI in synthetic hybrids produced by crossing self-fertile and self-incompatible species in each of two crucifer genera. We show that SI is lost in the stigmas of A. thaliana-lyrata hybrids and their neo-allotetraploid derivatives and in the pollen of C. rubella-grandiflora hybrids and their homoploid progenies. Aberrant processing of S-locus receptor kinase gene transcripts as detected in Arabidopsis hybrids and suppression of the S-locus cysteine-rich protein gene as observed in Capsella hybrids are two reversible mechanisms by which SI might break down upon interspecific hybridization to generate self-fertile hybrids in nature.

SUBMITTER: Nasrallah JB

PROVIDER: S-EPMC1855105 | biostudies-literature | 2007 Apr

REPOSITORIES: biostudies-literature

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Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids.

Nasrallah June B JB Liu Pei P Sherman-Broyles Susan S Schmidt Renate R Nasrallah Mikhail E ME

Genetics 20070121 4

As a major agent of rapid speciation, interspecific hybridization has played an important role in plant evolution. When hybridization involves species that exhibit self-incompatibility (SI), this prezygotic barrier to self-fertilization must be overcome or lost to allow selfing. How SI, a normally dominant trait, is lost in nascent hybrids is not known, however. Here we demonstrate that hybrid self-fertility can result from epigenetic changes in expression of the S-locus genes that determine spe ...[more]

PMID: 17237505

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Project description:The Piwi-interacting RNA (piRNA) pathway defends the germline of animals from the deleterious activity of selfish transposable elements (TEs) through small-RNA mediated silencing. Adaptation to novel invasive TEs is proposed to occur by incorporating their sequences into the piRNA pool that females produce and deposit into their eggs, which then propagates immunity against specific TEs to future generations. In support of this model, the F1 offspring of crosses between strains of the same Drosophila species sometimes suffer from germline derepression of paternally inherited TE families, caused by a failure of the maternal strain to produce the piRNAs necessary for their regulation. However, many protein components of the Drosophila piRNA pathway exhibit signatures of positive selection, suggesting that they also contribute to the evolution of host genome defense. Here we investigate piRNA pathway function and TE regulation in the F1 hybrids of interspecific crosses between D. melanogaster and D. simulans and compare them with intraspecific control crosses of D. melanogaster. We confirm previous reports showing that intraspecific crosses are characterized by derepression of paternally inherited TE families that are rare or absent from the maternal genome and piRNA pool, consistent with the role of maternally deposited piRNAs in shaping TE silencing. In contrast to the intraspecific cross, we discover that interspecific hybrids are characterized by widespread derepression of both maternally and paternally inherited TE families. Furthermore, the pattern of derepression of TE families in interspecific hybrids cannot be attributed to their paucity or absence from the piRNA pool of the maternal species. Rather, we demonstrate that interspecific hybrids closely resemble piRNA effector-protein mutants in both TE misregulation and aberrant piRNA production. We suggest that TE derepression in interspecific hybrids largely reflects adaptive divergence of piRNA pathway genes rather than species-specific differences in TE-derived piRNAs.

Dataset Information

Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids.

Publications

Epigenetic mechanisms for breakdown of self-incompatibility in interspecific hybrids.

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