Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between <i>Mimulus</i> species

Garner, Austin G.; Kenney, Amanda M.; Fishman, Lila; Sweigart, Andrea L.

doi:10.1111/nph.13897

Cited by 65 publications

(87 citation statements)

References 90 publications

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“…This difference could be because of genetic variation between natural populations, consistent with our data showing that the genetic basis of A. lyrata × A. arenosa hybrid seed lethality differs among A. arenosa populations. The presence of distinct incompatibility loci in A. arenosa populations suggests a recent intraspecific diversification of those loci and therefore a fast evolving genetic basis of hybrid incompatibility, similar to that proposed for other species (38,44,45). Genomic imprinting, the epigenetic phenomenon by which genes are expressed in a parent-of-origin manner, has been causally linked to endosperm-based hybridization barriers and is disturbed in interspecific hybrid seeds (24,(46)(47)(48).…”

Section: Discussionsupporting

confidence: 55%

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

Lafon‐Placette

Johannessen

Hornslien

et al. 2017

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

113

128

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Based on the biological species concept, two species are considered distinct if reproductive barriers prevent gene flow between them. In Central Europe, the diploid species Arabidopsis lyrata and Arabidopsis arenosa are genetically isolated, thus fitting this concept as "good species." Nonetheless, interspecific gene flow involving their tetraploid forms has been described. The reasons for this ploidy-dependent reproductive isolation remain unknown. Here, we show that hybridization between diploid A. lyrata and A. arenosa causes mainly inviable seed formation, revealing a strong postzygotic reproductive barrier separating these two species. Although viability of hybrid seeds was impaired in both directions of hybridization, the cause for seed arrest differed. Hybridization of A. lyrata seed parents with A. arenosa pollen donors resulted in failure of endosperm cellularization, whereas the endosperm of reciprocal hybrids cellularized precociously. Endosperm cellularization failure in both hybridization directions is likely causal for the embryo arrest. Importantly, natural tetraploid A. lyrata was able to form viable hybrid seeds with diploid and tetraploid A. arenosa, associated with the reestablishment of normal endosperm cellularization. Conversely, the defects of hybrid seeds between tetraploid A. arenosa and diploid A. lyrata were aggravated. According to these results, we hypothesize that a tetraploidization event in A. lyrata allowed the production of viable hybrid seeds with A. arenosa, enabling gene flow between the two species.interspecies hybrid seed failure | Arabidopsis | reproductive isolation | endosperm cellularization | EBN

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Section: Discussionsupporting

confidence: 55%

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

Lafon‐Placette

Johannessen

Hornslien

et al. 2017

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

113

128

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“…Triploid endosperm interactions refer to seed failure as a result of abnormal endosperm development, often caused by alterations in expression of imprinted genes (see Gutierrez-Marcos et al 2003), whereas maternal-zygote incompatibilities are incompatibilities between paternally inherited alleles and the maternal factors that initiate development (e.g., Josefsson et al 2006). F1 hybrid seed inviability due to incompatibilities involving abnormal endosperm development and imprinted genes has been found between several closely related species (Josefsson et al 2006;Rebernig et al 2015;Garner et al 2016). Such seed inviability would reduce germination as found here.…”

Section: Other Sources Of Risupporting

confidence: 58%

Cytonuclear incompatibility contributes to the early stages of speciation

Barnard‐Kubow

Galloway

2016

Evolution

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Genetic incompatibility is a hallmark of speciation. Cytonuclear incompatibilities are proposed to be among the first genetic barriers to arise during speciation. Accordingly, reproductive isolation (RI) within species should be heavily influenced by interactions between the organelle and nuclear genomes. However, there are few clear examples of cytonuclear incompatibility within a species. Here, we show substantial postzygotic RI in first-generation hybrids between differentiated populations of an herbaceous plant (up to 92% reduction in fitness). RI was primarily due to germination and survival, with moderate RI for pollen viability. RI for survival was asymmetric and caused by cytonuclear incompatibility, with the strength of incompatibility linearly related to chloroplast genetic distance. This cytonuclear incompatibility may be the result of a rapidly evolving plastid genome. Substantial asymmetric RI was also found for germination, but was not associated with cytonuclear incompatibility, indicating endosperm or maternal-zygote incompatibilities. These results demonstrate that cytonuclear incompatibility contributes to RI within species, suggesting that initial rates of speciation could be influenced by rates of organelle evolution. However, other genetic incompatibilities are equally important, indicating that even at early stages, speciation can be a complex process involving multiple genes and incompatibilities.

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“…Seed inviability appears to be caused by genes with parent‐of‐origin effects, including imprinted genes, in both Mimulus (Garner et al. ) and Arabidopsis (Wolff et al. ).…”

Section: Discussionmentioning

confidence: 99%

Genomic imprinting, disrupted placental expression, and speciation

2016

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The importance of regulatory incompatibilities to the early stages of speciation remains unclear. Hybrid mammals often show extreme parent-of-origin growth effects that are thought to be a consequence of disrupted genetic imprinting (parent-specific epigenetic gene silencing) during early development. Here we test the long-standing hypothesis that abnormal hybrid growth reflects disrupted gene expression due to loss of imprinting (LOI) in hybrid placentas, resulting in dosage imbalances between paternal growth factors and maternal growth repressors. We analyzed placental gene expression in reciprocal dwarf hamster hybrids that show extreme parent-of-origin growth effects relative to their parental species. In massively enlarged hybrid placentas, we observed both extensive transgressive expression of growth-related genes and bi-allelic expression of many genes that were paternally silenced in normal sized hybrids. However, the apparent widespread disruption of paternal silencing was coupled with reduced gene expression levels overall. These patterns are contrary to the predictions of the LOI model and indicate that hybrid misexpression of dosage sensitive genes is caused by other regulatory mechanisms in this system. Collectively, our results support a central role for disrupted gene expression and imprinting in the evolution of mammalian hybrid inviability, but call into question the generality of the widely invoked LOI model.

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Genetic loci with parent‐of‐origin effects cause hybrid seed lethality in crosses between Mimulus species

Cited by 65 publications

References 90 publications

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

Cytonuclear incompatibility contributes to the early stages of speciation

Genomic imprinting, disrupted placental expression, and speciation

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