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Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia.

ABSTRACT: Self-incompatibility (SI) is the flowering plant reproductive system in which self pollen tube growth is inhibited, thereby preventing self-fertilization. SI has evolved independently in several different flowering plant lineages. In all Brassicaceae species in which the molecular basis of SI has been investigated in detail, the product of the S-locus receptor kinase (SRK) gene functions as receptor in the initial step of the self pollen-rejection pathway, while that of the S-locus cysteine-rich (SCR) gene functions as ligand. Here we examine the hypothesis that the S locus in the Brassicaceae genus Leavenworthia is paralogous with the S locus previously characterized in other members of the family. We also test the hypothesis that self-compatibility in this group is based on disruption of the pollen ligand-producing gene. Sequence analysis of the S-locus genes in Leavenworthia, phylogeny of S alleles, gene expression patterns, and comparative genomics analyses provide support for both hypotheses. Of special interest are two genes located in a non-S locus genomic region of Arabidopsis lyrata that exhibit domain structures, sequences, and phylogenetic histories similar to those of the S-locus genes in Leavenworthia, and that also share synteny with these genes. These A. lyrata genes resemble those comprising the A. lyrata S locus, but they do not function in self-recognition. Moreover, they appear to belong to a lineage that diverged from the ancestral Brassicaceae S-locus genes before allelic diversification at the S locus. We hypothesize that there has been neo-functionalization of these S-locus-like genes in the Leavenworthia lineage, resulting in evolution of a separate ligand-receptor system of SI. Our results also provide support for theoretical models that predict that the least constrained pathway to the evolution of self-compatibility is one involving loss of pollen gene function.

SUBMITTER: Chantha SC

PROVIDER: S-EPMC3653793 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia.

Chantha Sier-Ching SC Herman Adam C AC Platts Adrian E AE Vekemans Xavier X Schoen Daniel J DJ

PLoS biology 20130514 5

Self-incompatibility (SI) is the flowering plant reproductive system in which self pollen tube growth is inhibited, thereby preventing self-fertilization. SI has evolved independently in several different flowering plant lineages. In all Brassicaceae species in which the molecular basis of SI has been investigated in detail, the product of the S-locus receptor kinase (SRK) gene functions as receptor in the initial step of the self pollen-rejection pathway, while that of the S-locus cysteine-rich ...[more]

PMID: 23690750

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Project description:BackgroundMolecular lock-and-key systems are common among reproductive proteins, yet their evolution remains a major puzzle in evolutionary biology. In the Brassicaceae, the genes encoding self-incompatibility have been identified, but technical challenges currently prevent detailed analyses of the molecular interaction between the male and female components. In the present study, we investigate sequence polymorphism in the female specificity determinant SRK of Arabidopsis halleri from throughout Europe. Using a comparative approach based on published SRK sequences in A. lyrata and Brassica, we track the signature of frequency-dependent selection acting on these genes at the codon level. Using simulations, we evaluate power and accuracy of our approach and estimate the proportion of codon sites involved in the molecular interaction.ResultsWe identified several members of the S-gene family, together with 22 putative S-haplotypes. Linkage to the S-locus and the presence of a kinase domain were formally demonstrated for four and six of these haplotypes, respectively, and sequence polymorphism was extremely high. Twenty-five codons showed signs of positive selection in at least one species, and clustered significantly (but not exclusively) within hypervariable regions. We checked that this clustering was not an artifact due to variation in evolution rate at synonymous sites. Simulations revealed that the analysis was highly accurate, thus providing a reliable set of candidates for future functional analyses, but with an overall power not higher than 60 %. Assuming similar power, we infer from our results that about 23% of all codons in the S-domain may actually be involved in recognition. Interestingly, while simulations demonstrated that this comparison remained reliable even at very high levels of divergence, codons identified in Brassica had higher posterior rates of non-synonymous to synonymous substitutions than codons identified in A. halleri or A. lyrata, possibly suggesting more intense selection in Brassica.ConclusionThe signature of balancing selection can be identified reliably at the codon level even in cases of very high sequence divergence, provided that a sufficiently large set of sequences are analyzed. Altogether, our results indicate that a large proportion of codons may be involved in recognition and confirm the particular importance of hypervariable regions. The more intense signature of positive selection detected in Brassica suggests that allelic diversification in this genus was very recent, possibly following a recent demographic bottleneck.

Project description:Background and aimsThe evolution of interspecific reproductive barriers is crucial to understanding species evolution. This study examines the contribution of transitions between self-compatibility (SC) and self-incompatibility (SI) and genetic divergence in the evolution of reproductive barriers in Dendrobium, one of the largest orchid genera. Specifically, it investigates the evolution of pre- and postzygotic isolation and the effects of transitions between compatibility states on interspecific reproductive isolation within the genus.MethodsThe role of SC and SI changes in reproductive compatibility among species was examined using fruit set and seed viability data available in the literature from 86 species and ∼2500 hand pollinations. The evolution of SC and SI in Dendrobium species was investigated within a phylogenetic framework using internal transcribed spacer sequences available in GenBank.Key resultsBased on data from crossing experiments, estimations of genetic distance and the results of a literature survey, it was found that changes in SC and SI significantly influenced the compatibility between species in interspecific crosses. The number of fruits produced was significantly higher in crosses in which self-incompatible species acted as pollen donor for self-compatible species, following the SI × SC rule. Maximum likelihood and Bayesian tests did not reject transitions from SI to SC and from SC to SI across the Dendrobium phylogeny. In addition, postzygotic isolation (embryo mortality) was found to evolve gradually with genetic divergence, in agreement with previous results observed for other plant species, including orchids.ConclusionsTransitions between SC and SI and the gradual accumulation of genetic incompatibilities affecting postzygotic isolation are important mechanisms preventing gene flow among Dendrobium species, and may constitute important evolutionary processes contributing to the high levels of species diversity in this tropical orchid group.

Dataset Information

Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia.

Publications

Secondary evolution of a self-incompatibility locus in the Brassicaceae genus Leavenworthia.

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