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Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm.

Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C - PLoS Genet. (2015)

Bottom Line: Whether the change in mating system was accompanied by the evolution of additional reproductive barriers that enforced species divergence remained unknown.While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors resulted in complete seed abortion caused by endosperm cellularization failure, the reciprocal hybridization resulted in the formation of small seeds with precociously cellularized endosperm.These results provide strong support for the theory that crosses between plants of different mating systems will be unbalanced, with the outcrosser behaving like a plant of increased ploidy, evoking a response that resembles an interploidy-type seed failure.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center of Plant Biology, Uppsala, Sweden.

ABSTRACT
The transition to selfing in Capsella rubella accompanies its recent divergence from the ancestral outcrossing C. grandiflora species about 100,000 years ago. Whether the change in mating system was accompanied by the evolution of additional reproductive barriers that enforced species divergence remained unknown. Here, we show that C. rubella and C. grandiflora are reproductively separated by an endosperm-based, non-reciprocal postzygotic hybridization barrier. While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors resulted in complete seed abortion caused by endosperm cellularization failure, the reciprocal hybridization resulted in the formation of small seeds with precociously cellularized endosperm. Strikingly, the transcriptomic response of both hybridizations mimicked respectively the response of paternal and maternal excess hybridizations in Arabidopsis thaliana, suggesting unbalanced genome strength causes hybridization failure in both species. These results provide strong support for the theory that crosses between plants of different mating systems will be unbalanced, with the outcrosser behaving like a plant of increased ploidy, evoking a response that resembles an interploidy-type seed failure. Seed incompatilibity of C. rubella pollinated by C. grandiflora followed the Bateson-Dobzhansky-Muller model, involving negative genetic interaction of multiple paternal C. grandiflora loci with at least one maternal C. rubella locus. Given that both species only recently diverged, our data suggest that a fast evolving mechanism underlies the post-zygotic hybridization barrier(s) separating both species.

No MeSH data available.


Related in: MedlinePlus

Cross direction-dependent incompatibility affects development of Capsella rubella and C. grandiflora hybrid seeds.Percentage (A) and phenotypes (B) of aborted and non-aborted seeds of C. rubella, C. grandiflora and reciprocal hybrids of both species. Scale bars reflect 1 mm. (C) Percentage of germinated seeds of indicated crosses. (D) Seedlings of indicated crosses 10 days after germination. Seed area (E) and seed weight (F) of indicated crosses. Error bars show standard deviation. Significance was determined by t test analysis. * P < 0.05, ** P < 0.01 ns, not significant. In all graphs numbers on top of the bars correspond to number of analyzed seeds.
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pgen.1005295.g001: Cross direction-dependent incompatibility affects development of Capsella rubella and C. grandiflora hybrid seeds.Percentage (A) and phenotypes (B) of aborted and non-aborted seeds of C. rubella, C. grandiflora and reciprocal hybrids of both species. Scale bars reflect 1 mm. (C) Percentage of germinated seeds of indicated crosses. (D) Seedlings of indicated crosses 10 days after germination. Seed area (E) and seed weight (F) of indicated crosses. Error bars show standard deviation. Significance was determined by t test analysis. * P < 0.05, ** P < 0.01 ns, not significant. In all graphs numbers on top of the bars correspond to number of analyzed seeds.

Mentions: The recently diverged C. rubella and C. grandiflora species are reproductively separated by different mating systems [1,3,4]. However, whether there are additional reproductive barriers between both species has not yet been investigated. We therefore performed reciprocal crosses between C. grandiflora and C. rubella and analyzed the resulting seed set. Pollinations in both directions were successful and resulted in similar numbers of seeds per silique between reciprocal crosses and intra-species crosses, revealing that there were no pollen incompatibilities between C. rubella and C. grandiflora (S1 Table). However, hybrid seeds developed abnormally and aborted at different frequencies; while about 40% of seeds after crosses of C. grandiflora × C. rubella (female × male) were abnormal (Fig 1A and 1B), corresponding to a germination rate of about 60% (Fig 1C), in the reciprocal cross all seeds aborted (Fig 1A, 1B and 1C). Hybrid seedlings of the cross C. grandiflora × C. rubella were variable in size and germination time point (Fig 1D) but developed into fertile adult plants. Intra-species crosses resulted in seed abortion rates below 5% and germination rates above 80% (Fig 1A and 1C). The seeds of the parental species were similar in size and weight (Fig 1B, 1E and 1F; P > 0.1, t-test). Seeds of the cross C. rubella × C. grandiflora were significantly larger than C. rubella seeds but lighter compared to both parental seeds (Fig 1E and 1F; P < 0.05, t-test), while seeds of the reciprocal cross were significantly smaller and lighter (Fig 1E and 1F; P < 0.01, t-test).


Non-reciprocal Interspecies Hybridization Barriers in the Capsella Genus Are Established in the Endosperm.

Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C - PLoS Genet. (2015)

Cross direction-dependent incompatibility affects development of Capsella rubella and C. grandiflora hybrid seeds.Percentage (A) and phenotypes (B) of aborted and non-aborted seeds of C. rubella, C. grandiflora and reciprocal hybrids of both species. Scale bars reflect 1 mm. (C) Percentage of germinated seeds of indicated crosses. (D) Seedlings of indicated crosses 10 days after germination. Seed area (E) and seed weight (F) of indicated crosses. Error bars show standard deviation. Significance was determined by t test analysis. * P < 0.05, ** P < 0.01 ns, not significant. In all graphs numbers on top of the bars correspond to number of analyzed seeds.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4472357&req=5

pgen.1005295.g001: Cross direction-dependent incompatibility affects development of Capsella rubella and C. grandiflora hybrid seeds.Percentage (A) and phenotypes (B) of aborted and non-aborted seeds of C. rubella, C. grandiflora and reciprocal hybrids of both species. Scale bars reflect 1 mm. (C) Percentage of germinated seeds of indicated crosses. (D) Seedlings of indicated crosses 10 days after germination. Seed area (E) and seed weight (F) of indicated crosses. Error bars show standard deviation. Significance was determined by t test analysis. * P < 0.05, ** P < 0.01 ns, not significant. In all graphs numbers on top of the bars correspond to number of analyzed seeds.
Mentions: The recently diverged C. rubella and C. grandiflora species are reproductively separated by different mating systems [1,3,4]. However, whether there are additional reproductive barriers between both species has not yet been investigated. We therefore performed reciprocal crosses between C. grandiflora and C. rubella and analyzed the resulting seed set. Pollinations in both directions were successful and resulted in similar numbers of seeds per silique between reciprocal crosses and intra-species crosses, revealing that there were no pollen incompatibilities between C. rubella and C. grandiflora (S1 Table). However, hybrid seeds developed abnormally and aborted at different frequencies; while about 40% of seeds after crosses of C. grandiflora × C. rubella (female × male) were abnormal (Fig 1A and 1B), corresponding to a germination rate of about 60% (Fig 1C), in the reciprocal cross all seeds aborted (Fig 1A, 1B and 1C). Hybrid seedlings of the cross C. grandiflora × C. rubella were variable in size and germination time point (Fig 1D) but developed into fertile adult plants. Intra-species crosses resulted in seed abortion rates below 5% and germination rates above 80% (Fig 1A and 1C). The seeds of the parental species were similar in size and weight (Fig 1B, 1E and 1F; P > 0.1, t-test). Seeds of the cross C. rubella × C. grandiflora were significantly larger than C. rubella seeds but lighter compared to both parental seeds (Fig 1E and 1F; P < 0.05, t-test), while seeds of the reciprocal cross were significantly smaller and lighter (Fig 1E and 1F; P < 0.01, t-test).

Bottom Line: Whether the change in mating system was accompanied by the evolution of additional reproductive barriers that enforced species divergence remained unknown.While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors resulted in complete seed abortion caused by endosperm cellularization failure, the reciprocal hybridization resulted in the formation of small seeds with precociously cellularized endosperm.These results provide strong support for the theory that crosses between plants of different mating systems will be unbalanced, with the outcrosser behaving like a plant of increased ploidy, evoking a response that resembles an interploidy-type seed failure.

View Article: PubMed Central - PubMed

Affiliation: Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center of Plant Biology, Uppsala, Sweden.

ABSTRACT
The transition to selfing in Capsella rubella accompanies its recent divergence from the ancestral outcrossing C. grandiflora species about 100,000 years ago. Whether the change in mating system was accompanied by the evolution of additional reproductive barriers that enforced species divergence remained unknown. Here, we show that C. rubella and C. grandiflora are reproductively separated by an endosperm-based, non-reciprocal postzygotic hybridization barrier. While hybridizations of C. rubella maternal plants with C. grandiflora pollen donors resulted in complete seed abortion caused by endosperm cellularization failure, the reciprocal hybridization resulted in the formation of small seeds with precociously cellularized endosperm. Strikingly, the transcriptomic response of both hybridizations mimicked respectively the response of paternal and maternal excess hybridizations in Arabidopsis thaliana, suggesting unbalanced genome strength causes hybridization failure in both species. These results provide strong support for the theory that crosses between plants of different mating systems will be unbalanced, with the outcrosser behaving like a plant of increased ploidy, evoking a response that resembles an interploidy-type seed failure. Seed incompatilibity of C. rubella pollinated by C. grandiflora followed the Bateson-Dobzhansky-Muller model, involving negative genetic interaction of multiple paternal C. grandiflora loci with at least one maternal C. rubella locus. Given that both species only recently diverged, our data suggest that a fast evolving mechanism underlies the post-zygotic hybridization barrier(s) separating both species.

No MeSH data available.


Related in: MedlinePlus