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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

C. rubella × C. grandiflora hybrid embryos are viable, revealing a major role of endosperm defects in hybrid seed incompatibility.(A) C. rubella × C. grandiflora hybrid seeds at 13 days after pollination (DAP). (B) Section through seeds derived from crosses of C. rubella × C. rubella (left) and C. rubella × C. grandiflora (right) at 13 DAP. The sections reveal that hybrid embryos reach the torpedo stage at which development arrests. (C) Comparison of adult plants of all crosses (C. grandiflora × C. grandiflora (Cg), C. grandiflora × C. rubella (Cg × Cr), C. rubella × C. grandiflora (Cr × Cg), C. rubella × C. rubella (Cr)). Flower phenotypes of the respective genotypes are shown on top.
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pgen.1005295.g003: C. rubella × C. grandiflora hybrid embryos are viable, revealing a major role of endosperm defects in hybrid seed incompatibility.(A) C. rubella × C. grandiflora hybrid seeds at 13 days after pollination (DAP). (B) Section through seeds derived from crosses of C. rubella × C. rubella (left) and C. rubella × C. grandiflora (right) at 13 DAP. The sections reveal that hybrid embryos reach the torpedo stage at which development arrests. (C) Comparison of adult plants of all crosses (C. grandiflora × C. grandiflora (Cg), C. grandiflora × C. rubella (Cg × Cr), C. rubella × C. grandiflora (Cr × Cg), C. rubella × C. rubella (Cr)). Flower phenotypes of the respective genotypes are shown on top.

Mentions: Delayed or complete block of endosperm cellularization has been correlated with embryo arrest [15]. We therefore tested whether abortion of hybrid C. rubella × C. grandiflora seeds is a consequence of abnormal endosperm development or rather caused by an embryo defect. To distinguish between both possibilities we isolated hybrid embryos at 13 DAP, when the endosperm was already completely collapsed, but the embryo was still viable (Fig 3A and 3B). Of 14 isolated embryos 9 developed normally and based on flower size the F1 plants were clearly recognized as hybrids (Fig 3C). C. grandiflora × C. rubella hybrids were easily obtained and resembled in flower size the reciprocal hybrid (Fig 3C). Together we conclude that abortion of C. rubella × C. grandiflora hybrid seeds is a consequence of abnormal endosperm development and most likely endosperm cellularization failure, which can be bypassed by embryo rescue.


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)

C. rubella × C. grandiflora hybrid embryos are viable, revealing a major role of endosperm defects in hybrid seed incompatibility.(A) C. rubella × C. grandiflora hybrid seeds at 13 days after pollination (DAP). (B) Section through seeds derived from crosses of C. rubella × C. rubella (left) and C. rubella × C. grandiflora (right) at 13 DAP. The sections reveal that hybrid embryos reach the torpedo stage at which development arrests. (C) Comparison of adult plants of all crosses (C. grandiflora × C. grandiflora (Cg), C. grandiflora × C. rubella (Cg × Cr), C. rubella × C. grandiflora (Cr × Cg), C. rubella × C. rubella (Cr)). Flower phenotypes of the respective genotypes are shown on top.
© Copyright Policy
Related In: Results  -  Collection

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

pgen.1005295.g003: C. rubella × C. grandiflora hybrid embryos are viable, revealing a major role of endosperm defects in hybrid seed incompatibility.(A) C. rubella × C. grandiflora hybrid seeds at 13 days after pollination (DAP). (B) Section through seeds derived from crosses of C. rubella × C. rubella (left) and C. rubella × C. grandiflora (right) at 13 DAP. The sections reveal that hybrid embryos reach the torpedo stage at which development arrests. (C) Comparison of adult plants of all crosses (C. grandiflora × C. grandiflora (Cg), C. grandiflora × C. rubella (Cg × Cr), C. rubella × C. grandiflora (Cr × Cg), C. rubella × C. rubella (Cr)). Flower phenotypes of the respective genotypes are shown on top.
Mentions: Delayed or complete block of endosperm cellularization has been correlated with embryo arrest [15]. We therefore tested whether abortion of hybrid C. rubella × C. grandiflora seeds is a consequence of abnormal endosperm development or rather caused by an embryo defect. To distinguish between both possibilities we isolated hybrid embryos at 13 DAP, when the endosperm was already completely collapsed, but the embryo was still viable (Fig 3A and 3B). Of 14 isolated embryos 9 developed normally and based on flower size the F1 plants were clearly recognized as hybrids (Fig 3C). C. grandiflora × C. rubella hybrids were easily obtained and resembled in flower size the reciprocal hybrid (Fig 3C). Together we conclude that abortion of C. rubella × C. grandiflora hybrid seeds is a consequence of abnormal endosperm development and most likely endosperm cellularization failure, which can be bypassed by embryo rescue.

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