Hybrid incompatibility caused by an epiallele

Blevins, Todd; Wang, Jing; Pflieger, David; Pontvianne, Frédéric; Pikaard, Craig S.

doi:10.1101/099317

Cited by 16 publications

(27 citation statements)

References 54 publications

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“…1). This result allowed Blevins et al (8) to conclude that HISN6B in Col represents a true epiallele, and that its epigenetic state is responsible for the hybrid incompatibility.…”

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confidence: 91%

“…14). In the case discussed here, both epialleles are also stable: The silent one in Col did not lose DNA methylation for over 30 generations (15,16), but remained active after passage through the silencing mutants for at least three generations (8) of silencing could restore a Cvi-compatible version of Col HISN6B, in contrast to mutants that interfere with the establishment of silencing by RNA-directed DNA methylation (8).…”

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confidence: 99%

“…However, it is assumed that incompatibility is not exclusively caused by genetic features (6), and there is evidence for the involvement of epigenetic factors connected with rearranged gene structures (7). In PNAS, Blevins et al (8) describe an example where hybrid incompatibility is caused by differences in epigenetic information that would be undetected by a search only for sequence differences. Combining genetic analysis with the availability of natural variation in the model plant Arabidopsis thaliana, the authors demonstrate that an epigenetically inactivated gene necessary for histidine biosynthesis (HISN6B) (9) causes hybrid incompatibility if combined with mutated copies of its duplicated version HISN6A.…”

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confidence: 99%

“…In Col, only HISN6A is expressed, whereas the HISN6B copies are epigenetically silent. Blevins et al (8) show that the lack of expression is associated with increased cytosine methylation at the promoter. They used the availability of several mutants in the Col background that lead to loss of DNA methylation: either directly due to lack of the methyltransferase, MET1 or CMT3, responsible for methylation at CG or CHG sites or indirectly by eliminating the histone deacetylase, HDA6, which, in turn, reduces DNA methylation.…”

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confidence: 99%

“…Promoter methylation of HISN6B is lost, and the gene is expressed in the mutants. Blevins et al (8) crossed the Col hda6 mutant with wild-type (wt) Col and identified segregating progeny homozygous for wt HDA6 that expressed HISN6B. These reactivated alleles remained expressed upon further propagation and were used to test whether they could circumvent the hybrid incompatibility upon combination with the mutated HISN6A.…”

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confidence: 99%

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Epigenetic contribution to diversification

Bente

Scheid

2017

Proc. Natl. Acad. Sci. U.S.A.

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“…1). This result allowed Blevins et al (8) to conclude that HISN6B in Col represents a true epiallele, and that its epigenetic state is responsible for the hybrid incompatibility.…”

mentioning

confidence: 91%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Epigenetic contribution to diversification

Bente

Scheid

2017

Proc. Natl. Acad. Sci. U.S.A.

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Natural variation in DNA methylation homeostasis and the emergence of epialleles

Zhang

Wendte

Ji³

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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In plants and mammals, DNA methylation plays a critical role in transcriptional silencing by delineating heterochromatin from transcriptionally active euchromatin. A homeostatic balance between heterochromatin and euchromatin is essential to genomic stability. This is evident in many diseases and mutants for heterochromatin maintenance, which are characterized by global losses of DNA methylation coupled with localized ectopic gains of DNA methylation that alter transcription. Furthermore, we have shown that genome-wide methylation patterns inArabidopsis thalianaare highly stable over generations, with the exception of rare epialleles. However, the extent to which natural variation in the robustness of targeting DNA methylation to heterochromatin exists, and the phenotypic consequences of such variation, remain to be fully explored. Here we describe the finding that heterochromatin and genic DNA methylation are highly variable among 725A. thalianaaccessions. We found that genic DNA methylation is inversely correlated with that in heterochromatin, suggesting that certain methylation pathway(s) may be redirected to genes upon the loss of heterochromatin. This redistribution likely involves a feedback loop involving the DNA methyltransferase, CHROMOMETHYLASE 3 (CMT3), H3K9me2, and histone turnover, as highly expressed, long genes with a high density of CMT3-preferred CWG sites are more likely to be methylated. Importantly, although the presence of CG methylation in genes alone may not affect transcription, genes containing CG methylation are more likely to become methylated at non-CG sites and silenced. These findings are consistent with the hypothesis that natural variation in DNA methylation homeostasis may underlie the evolution of epialleles that alter phenotypes.

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Additive and non-additive epigenetic signatures of natural hybridization between fish species with different mating systems

et al. 2022

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Hybridization is a major source of evolutionary innovation. In plants, epigenetic mechanisms can help to stabilize hybrid genomes and contribute to reproductive isolation, but the relationship between genetic and epigenetic changes in animal hybrids is unclear. We analysed the relationship between genetic background and methylation patterns in natural hybrids of two genetically divergent fish species with different mating systems, Kryptolebias hermaphroditus (self-fertilizing) and K. ocellatus (outcrossing). Co-existing parental species displayed highly distinct genetic (SNPs) and methylation patterns (37,000 differentially methylated cytosines). Hybrids had predominantly intermediate methylation patterns (88.5% of the sites) suggesting additive effects, as expected from hybridization between genetically distant species. The large number of differentially methylated cytosines between hybrids and parental species (n = 5,800) suggests that hybridization may play a role in increasing genetic and epigenetic variation. Although most of the observed epigenetic variation was additive and had a strong genetic component, we also found a small percentage of non-additive, potentially stochastic, methylation differences that might act as an evolutionary bet-hedging strategy and increase fitness under environmental instability.

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Hybrid incompatibility caused by an epiallele

Cited by 16 publications

References 54 publications

Epigenetic contribution to diversification

Epigenetic contribution to diversification

Natural variation in DNA methylation homeostasis and the emergence of epialleles

Additive and non-additive epigenetic signatures of natural hybridization between fish species with different mating systems

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