Hybrid incompatibility caused by an epiallele

Abstract

Hybrid incompatibility resulting from deleterious gene combinations is thought to be an important step toward reproductive isolation and speciation. Here, we demonstrate involvement of a silent epiallele in hybrid incompatibility. In Arabidopsis thaliana accession Cvi-0, one of the two copies of a duplicated histidine biosynthesis gene, HISN6A, is mutated, making HISN6B essential. In contrast, in accession Col-0, HISN6A is essential because HISN6B is not expressed. Owing to these differences, Cvi-0 × Col-0 hybrid progeny that are homozygous for both Cvi-0 HISN6A and Col-0 HISN6B do not survive. We show that HISN6B of Col-0 is not a defective pseudogene, but a stably silenced epiallele. Mutating HISTONE DEACETYLASE 6 (HDA6), or the cytosine methyltransferase genes MET1 or CMT3, erases HISN6B's silent locus identity, reanimating the gene to circumvent hisn6a lethality and hybrid incompatibility. These results show that HISN6-dependent hybrid lethality is a revertible epigenetic phenomenon and provide additional evidence that epigenetic variation has the potential to limit gene flow between diverging populations of a species.gene silencing | epigenetic inheritance | DNA methylation | histone deacetylation | hybrid incompatibility M utations that accumulate in separate subpopulations of a species can facilitate reproductive isolation by engendering hybrid incompatibility, a reduction in fitness observed among hybrid progeny at the F1 or F2 generation (1-3). Bateson (4), Dobzhansky (5), and Muller (6) independently proposed that gene mutations made benign by compensatory mutations in interacting genes within isolated subpopulations prove deleterious when subpopulations or ecotypes interbreed, thereby contributing to speciation by reducing gene flow. Examples of this include the lethal consequences of a Saccharomyces cerevisiae protein directing improper splicing of essential Saccharomyces bayanus mRNAs in S. cerevisiae × S. bayanus hybrids (3) or the hybrid necrosis that results from expression of incompatible innate immune receptors in Arabidopsis thaliana (1).Lynch and Force (7) envisioned an alternative scenario by which hybrid incompatibilities might arise, as a result of gene duplication. Gene duplication initially results in gene redundancy, thereby relaxing constraints on sequence and functional divergence, but mutations most often transform one paralog into a nonfunctional pseudogene (8-10). Lynch and Force recognized that asymmetric resolution of gene duplicates in this manner could result in either paralog becoming the sole operational copy in different subpopulations of a species, such that hybrid progeny inheriting nonfunctional alleles of both subpopulations would suffer reduced fitness (7).Nonmutational (epigenetic) gene silencing could potentially contribute to hybrid incompatibility via the scenario envisioned by Lynch and Force. In plants, silent epialleles segregating in Mendelian fashion can be stably inherited over many generations, and are known to affect a number of well-studied traits, includin...

Genome‐wide identification of EMBRYO‐DEFECTIVE (EMB) genes required for growth and development in Arabidopsis

“…The robustness of these collections is sufficient to begin addressing questions about what remaining members represent promising candidates for undiscovered EMB genes, and what factors enable knockouts of other members to complete embryo development. In the case of histidine biosynthesis, different members of a recent gene duplication (HISN6A; HISN6B) are either silenced or inactivated in different accessions, resulting in hybrid incompatibility when those accessions are crossed (Bikard et al, 2009;Blevins et al, 2017).…”

“…Null mutations that disrupt only the product of the long transcript, which is targeted to plastids, exhibit defects in seedling pigmentation, whereas those that disrupt the product of the short transcript, which performs a different function in the cytosol, exhibit embryo lethality. Mutant phenotypes can also vary depending on genetic background (Parker et al, 2014;Blevins et al, 2017), a phenomenon frequently encountered in maize genetics.…”

Ability of the endangered species Papaver fauriei to produce hybrids with a cultivated poppy (Papaver sp.)

“…; Blevins et al . ). More than 98% of the seeds germinated from the F 1 generation of the crosses between P. fauriei and the cultivated poppy (Table ), indicating that most of the hybrid seeds were viable.…”

Dose‐dependent interactions between two loci trigger altered shoot growth in BG‐5 × Krotzenburg‐0 (Kro‐0) hybrids of Arabidopsis thaliana

“…The different mechanisms underlying F 1 hybrid incompatibilities provide fascinating insights into the evolutionary forces contributing to reproductive isolation in plants. Much of the work on A. thaliana post‐zygotic F 1 incompatibilities has focused on activation of immune responses as a cause (Bomblies et al ., ; Alcazar et al ., , ; Chae et al ., ; Todesco et al ., ; Swiadek et al ., ), with only a few studies investigating other mechanisms (Smith et al ., ; Blevins et al ., ; Plötner et al ., ). Here, we present the first example of altered inflorescence architecture being linked to F 1 hybrid incompatibility.…”