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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

Molecular response to reciprocal hybridizations of C. rubella × C. grandiflora is similar to interploidy hybridizations in Arabidopsis.(A) Genes up- and downregulated in C. rubella × C. grandiflora reciprocal hybrid seeds compared to both parents overlap with genes deregulated in Arabidopsis interploidy seeds. The Arabidopsis osd1 mutant produces unreduced gametes, mimicking an interploidy hybridization when crossed with wild-type (WT). P values reflecting significance of overlap were calculated using a hypergeometric test. (B) Heatmap of expression log2 fold changes of selected AGL genes between samples. Capsella AGLs with several homologs in Arabidopsis are marked by small letters.
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pgen.1005295.g005: Molecular response to reciprocal hybridizations of C. rubella × C. grandiflora is similar to interploidy hybridizations in Arabidopsis.(A) Genes up- and downregulated in C. rubella × C. grandiflora reciprocal hybrid seeds compared to both parents overlap with genes deregulated in Arabidopsis interploidy seeds. The Arabidopsis osd1 mutant produces unreduced gametes, mimicking an interploidy hybridization when crossed with wild-type (WT). P values reflecting significance of overlap were calculated using a hypergeometric test. (B) Heatmap of expression log2 fold changes of selected AGL genes between samples. Capsella AGLs with several homologs in Arabidopsis are marked by small letters.

Mentions: The observed non-reciprocal defects in Capsella hybrid seeds resembled defects in response to interploidy hybridizations in Arabidopsis [13]. To test whether the similarity at the phenotypic level was also reflected at the molecular level, we generated genome-wide expression data of C. rubella and C. grandiflora parental seeds and reciprocal hybrid seeds. We filtered for genes exhibiting transgressive expression towards both parents, thus having either increased or decreased expression levels compared to both parents. For each gene we identified the closest homolog in Arabidopsis and analyzed the expression of those genes in interploidy hybrid seeds generated using the omission of second division1 (osd1) mutant [30,31]. Loss of OSD1 causes the formation of unreduced male and female gametes at high frequency [32], allowing to mimic interploidy hybridizations. A large proportion of genes were similarly deregulated in C. rubella × C. grandiflora hybrid seeds and seeds of paternal excess hybridizations in Arabidopsis (Fig 5A, S2 Table), while substantially fewer genes overlapped with deregulated genes in maternal excess seeds (S2 Fig). Conversely, in the reciprocal cross a substantial number of downregulated genes overlapped with downregulated genes in maternal excess hybridizations in Arabidopsis (Fig 5A, S2 Table), whereas the overlap with deregulated genes in paternal excess seeds was less pronounced (S2 Fig). These data reveal that interspecies and interploidy hybridizations cause a similar molecular response; while C. rubella × C. grandiflora hybrid seeds mimic a paternal excess phenotype, C. grandiflora × C. rubella hybrid seeds mimic a maternal excess phenotype. Notably, genes related to microtubular activity were enriched among downregulated genes in both C. rubella × C. grandiflora and Arabidopsis paternal excess hybrid seeds, while upregulated genes were enriched for genes involved in cell wall modification and specifically in glycosyl hydrolyzing activity (S3 Table). Microtubules are required in the phragmoplast for the transport of vesicles to construct a new cell wall [33], while glycosyl hydrolyzing enzymes can degrade pectin, which is assumed to be a key step in the deconstruction of plant cell walls [34]. Therefore, reduced expression of genes that are potentially required to build the phragmopast together with increased expression of genes that degrade cell walls correlates with the observed cellularization failure in interploidy and interspecies hybrid seeds (S3 Table). Conversely, in the reciprocal cross C. grandiflora × C. rubella, pectinesterase encoding genes were significantly downregulated, suggesting that inhibition of pectin degradation promotes cellularization.


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)

Molecular response to reciprocal hybridizations of C. rubella × C. grandiflora is similar to interploidy hybridizations in Arabidopsis.(A) Genes up- and downregulated in C. rubella × C. grandiflora reciprocal hybrid seeds compared to both parents overlap with genes deregulated in Arabidopsis interploidy seeds. The Arabidopsis osd1 mutant produces unreduced gametes, mimicking an interploidy hybridization when crossed with wild-type (WT). P values reflecting significance of overlap were calculated using a hypergeometric test. (B) Heatmap of expression log2 fold changes of selected AGL genes between samples. Capsella AGLs with several homologs in Arabidopsis are marked by small letters.
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pgen.1005295.g005: Molecular response to reciprocal hybridizations of C. rubella × C. grandiflora is similar to interploidy hybridizations in Arabidopsis.(A) Genes up- and downregulated in C. rubella × C. grandiflora reciprocal hybrid seeds compared to both parents overlap with genes deregulated in Arabidopsis interploidy seeds. The Arabidopsis osd1 mutant produces unreduced gametes, mimicking an interploidy hybridization when crossed with wild-type (WT). P values reflecting significance of overlap were calculated using a hypergeometric test. (B) Heatmap of expression log2 fold changes of selected AGL genes between samples. Capsella AGLs with several homologs in Arabidopsis are marked by small letters.
Mentions: The observed non-reciprocal defects in Capsella hybrid seeds resembled defects in response to interploidy hybridizations in Arabidopsis [13]. To test whether the similarity at the phenotypic level was also reflected at the molecular level, we generated genome-wide expression data of C. rubella and C. grandiflora parental seeds and reciprocal hybrid seeds. We filtered for genes exhibiting transgressive expression towards both parents, thus having either increased or decreased expression levels compared to both parents. For each gene we identified the closest homolog in Arabidopsis and analyzed the expression of those genes in interploidy hybrid seeds generated using the omission of second division1 (osd1) mutant [30,31]. Loss of OSD1 causes the formation of unreduced male and female gametes at high frequency [32], allowing to mimic interploidy hybridizations. A large proportion of genes were similarly deregulated in C. rubella × C. grandiflora hybrid seeds and seeds of paternal excess hybridizations in Arabidopsis (Fig 5A, S2 Table), while substantially fewer genes overlapped with deregulated genes in maternal excess seeds (S2 Fig). Conversely, in the reciprocal cross a substantial number of downregulated genes overlapped with downregulated genes in maternal excess hybridizations in Arabidopsis (Fig 5A, S2 Table), whereas the overlap with deregulated genes in paternal excess seeds was less pronounced (S2 Fig). These data reveal that interspecies and interploidy hybridizations cause a similar molecular response; while C. rubella × C. grandiflora hybrid seeds mimic a paternal excess phenotype, C. grandiflora × C. rubella hybrid seeds mimic a maternal excess phenotype. Notably, genes related to microtubular activity were enriched among downregulated genes in both C. rubella × C. grandiflora and Arabidopsis paternal excess hybrid seeds, while upregulated genes were enriched for genes involved in cell wall modification and specifically in glycosyl hydrolyzing activity (S3 Table). Microtubules are required in the phragmoplast for the transport of vesicles to construct a new cell wall [33], while glycosyl hydrolyzing enzymes can degrade pectin, which is assumed to be a key step in the deconstruction of plant cell walls [34]. Therefore, reduced expression of genes that are potentially required to build the phragmopast together with increased expression of genes that degrade cell walls correlates with the observed cellularization failure in interploidy and interspecies hybrid seeds (S3 Table). Conversely, in the reciprocal cross C. grandiflora × C. rubella, pectinesterase encoding genes were significantly downregulated, suggesting that inhibition of pectin degradation promotes cellularization.

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