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Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae).

ABSTRACT: The transition from self-incompatibility to self-compatibility is a common transition in angiosperms often reported in populations at the edge of species range limits. Geographically distinct populations of wild tomato species (Solanum section Lycopersicon (Solanaceae)) have been described as polymorphic for mating system with both self-incompatible and self-compatible populations. Using controlled pollinations and sequencing of the S-RNase mating system gene, we test the compatibility status of a population of S. peruvianum located near its southern range limit. Pollinations among plants of known genotypes revealed strong self-incompatibility; fruit set following compatible pollinations was significantly higher than following incompatible pollinations for all tested individuals. Sequencing of the S-RNase gene in parents and progeny arrays was also as predicted under self-incompatibility. Molecular variation at the S-RNase locus revealed a diverse set of alleles, and heterozygosity in over 500 genotyped individuals. We used controlled crosses to test the specificity of sequences recovered in this study; in all cases, results were consistent with a unique allelic specificity for each tested sequence, including two alleles sharing 92% amino-acid similarity. Site-specific patterns of selection at the S-RNase gene indicate positive selection in regions of the gene associated with allelic specificity determination and purifying selection in previously characterized conserved regions. Further, there is broad convergence between the present and previous studies in specific amino-acid positions inferred to be evolving under positive selection.

SUBMITTER: Miller JS

PROVIDER: S-EPMC3186115 | biostudies-literature | 2011 Jul

REPOSITORIES: biostudies-literature

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Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae).

Miller J S JS Kostyun J L JL

Heredity 20101201 1

The transition from self-incompatibility to self-compatibility is a common transition in angiosperms often reported in populations at the edge of species range limits. Geographically distinct populations of wild tomato species (Solanum section Lycopersicon (Solanaceae)) have been described as polymorphic for mating system with both self-incompatible and self-compatible populations. Using controlled pollinations and sequencing of the S-RNase mating system gene, we test the compatibility status of ...[more]

PMID: 21119705

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Project description:BACKGROUND:Fabaceae species are important in agronomy and livestock nourishment. They have a long breeding history, and most cultivars have lost self-incompatibility (SI), a genetic barrier to self-fertilization. Nevertheless, to improve legume crop breeding, crosses with wild SI relatives of the cultivated varieties are often performed. Therefore, it is fundamental to characterize Fabaceae SI system(s). We address the hypothesis of Fabaceae gametophytic (G)SI being RNase based, by recruiting the same S-RNase lineage gene of Rosaceae, Solanaceae or Plantaginaceae SI species. RESULTS:We first identify SSK1 like genes (described only in species having RNase based GSI), in the Trifolium pratense, Medicago truncatula, Cicer arietinum, Glycine max, and Lupinus angustifolius genomes. Then, we characterize the S-lineage T2-RNase genes in these genomes. In T. pratense, M. truncatula, and C. arietinum we identify S-RNase lineage genes that in phylogenetic analyses cluster with Pyrinae S-RNases. In M. truncatula and C. arietinum genomes, where large scaffolds are available, these sequences are surrounded by F-box genes that in phylogenetic analyses also cluster with S-pollen genes. In T. pratense the S-RNase lineage genes show, however, expression in tissues not involved in GSI. Moreover, levels of diversity are lower than those observed for other S-RNase genes. The M. truncatula and C. arietinum S-RNase and S-pollen like genes phylogenetically related to Pyrinae S-genes, are also expressed in tissues other than those involved in GSI. To address if other T2-RNases could be determining Fabaceae GSI, here we obtained a style with stigma transcriptome of Cytisus striatus, a species that shows significant difference on the percentage of pollen growth in self and cross-pollinations. Expression and polymorphism analyses of the C. striatus S-RNase like genes revealed that none of these genes, is the S-pistil gene. CONCLUSION:We find no evidence for Fabaceae GSI being determined by Rosaceae, Solanaceae, and Plantaginaceae S-RNase lineage genes. There is no evidence that T2-RNase lineage genes could be determining GSI in C. striatus. Therefore, to characterize the Fabaceae S-pistil gene(s), expression analyses, levels of diversity, and segregation analyses in controlled crosses are needed for those genes showing high expression levels in the tissues where GSI occurs.

Project description:Non-self gametophytic self-incompatibility (GSI) recognition system is characterized by the presence of multiple F-box genes tandemly located in the S-locus, that regulate pollen specificity. This reproductive barrier is present in Solanaceae, Plantaginacea and Maleae (Rosaceae), but only in Petunia functional assays have been performed to get insight on how this recognition mechanism works. In this system, each of the encoded S-pollen proteins (called SLFs in Solanaceae and Plantaginaceae /SFBBs in Maleae) recognizes and interacts with a sub-set of non-self S-pistil proteins, called S-RNases, mediating their ubiquitination and degradation. In Petunia there are 17 SLF genes per S-haplotype, making impossible to determine experimentally each SLF specificity. Moreover, domain -swapping experiments are unlikely to be performed in large scale to determine S-pollen and S-pistil specificities. Phylogenetic analyses of the Petunia SLFs and those from two Solanum genomes, suggest that diversification of SLFs predate the two genera separation. Here we first identify putative SLF genes from nine Solanum and 10 Nicotiana genomes to determine how many gene lineages are present in the three genera, and the rate of origin of new SLF gene lineages. The use of multiple genomes per genera precludes the effect of incompleteness of the genome at the S-locus. The similar number of gene lineages in the three genera implies a comparable effective population size for these species, and number of specificities. The rate of origin of new specificities is one per 10 million years. Moreover, here we determine the amino acids positions under positive selection, those involved in SLF specificity recognition, using 10 Petunia S-haplotypes with more than 11 SLF genes. These 16 amino acid positions account for the differences of self-incompatible (SI) behavior described in the literature. When SLF and S-RNase proteins are divided according to the SI behavior, and the positively selected amino acids classified according to hydrophobicity, charge, polarity and size, we identified fixed differences between SI groups. According to the in silico 3D structure of the two proteins these amino acid positions interact. Therefore, this methodology can be used to infer SLF/S-RNase specificity recognition.

Dataset Information

Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae).

Publications

Functional gametophytic self-incompatibility in a peripheral population of Solanum peruvianum (Solanaceae).

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