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WIREs Dev Biol
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Self‐incompatibility in Petunia: a self/nonself‐recognition mechanism employing S‐locus F‐box proteins and S‐RNase to prevent inbreeding

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Abstract Many flowering plants producing bisexual flowers have adopted self‐incompatibility (SI), a reproductive strategy which allows pistils to distinguish between self and nonself pollen, and to only permit nonself pollen to effect fertilization. To date, three different SI mechanisms have been identified, and this article focuses on the S‐RNase‐based mechanism using Petunia (Solanaceae) as a model. The genetic basis of this type of SI was established nearly a century ago; the polymorphic S‐locus specifies the genetic identity of pollen and the pistil. Molecular genetic studies carried out since the late 1980s have led to the identification of the polymorphic genes at the S‐locus that control self/nonself‐recognition between pollen and the pistil. The S‐RNase gene, which controls pistil specificity, was identified first, and subsequent sequencing of the S‐locus region containing S‐RNase led to the identification of the S‐locus F‐box (SLF) gene (now named SLF1). A transgenic approach was used to show that S2‐SLF1 (SLF1 of S2‐halotype) of Petunia inflata controls pollen specificity. The S‐locus contains additional pollen‐expressed F‐box genes that show sequence similarity with SLF1, and initially they were thought not to be involved in pollen specificity. However, further studies of SLF1 suggested that it is not the only pollen specificity gene. Indeed, it has recently been shown that two previously identified SLF‐like genes in P. inflata (now named SLF2 and SLF3) and a yet unknown number of additional SLF‐like genes (named SLF4, SLF5, etc.) collaboratively function to control pollen specificity. The significance and implications of this new finding are discussed. WIREs Dev Biol 2012, 1:267–275. doi: 10.1002/wdev.10 This article is categorized under: Plant Development > Fertilization, Embryogenesis, and Seed Development

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Genetic basis of gametophytic self‐incompatibility (GSI) and of its breakdown in tetraploids. (a) Self‐pollination and cross‐pollination of a diploid self‐incompatible S1S2 plant. Both S1 and S2 pollen produced by the S1S2 plant are rejected during their tube growth in the pistil due to matching of the S‐haplotypes, whereas pollen of any other S‐haplotype is accepted by the S1S2 pistil for fertilization. (b) Breakdown of self‐incompatibility (SI) in a tetraploid S1S1S2S2 plant due to presence of two different S‐alleles in diploid pollen. The tetraploid plant produces three different S‐genotypes of diploid pollen. Upon self‐pollination, S1S1 and S2S2 pollen are rejected, but S1S2 (heteroallelic) pollen is accepted. The tetraploid plant rejects S1 and S2 pollen, consistent with the notion that the breakdown of SI lies on the pollen side.

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Strategy for studying structure–function relationships of SLF proteins involved in pollen specificity. First, all types of SLF genes encoding pollen specificity will be identified from a particular S‐haplotype (S2 given as an example). Second, each type of SLF gene will be introduced into transgenic plants of various S‐genotypes to test whether it can cause breakdown of SI in pollen carrying one of the test S‐haplotypes. For example, S2‐SLF1 is introduced into plants of SxSy genotype, and if it causes breakdown of SI in pollen of Sx‐haplotype but not Sy‐haplotype, this would suggest that S2‐SLF1 interacts with Sx‐RNase. Third, the interaction between an SLF and any S‐RNase identified in Step 2 will be confirmed by protein–protein interaction assays and/or coimmunoprecipitation experiments. Having established a comprehensive relationship between each type of SLF and all nonself‐S‐RNases tested, the potential region(s) responsible for the differential interactions with S‐RNases will be identified from comparing the amino acid sequences of different types of SLFs that interact with different subsets of S‐RNases. Finally, the putative specificity region(s) will be examined by constructing chimeric genes between different types of SLF genes, with the coding sequences for the specificity region(s) swapped, and examining the SI behavior of the chimeric genes using the transgenic approach as shown in Step 2.

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Biochemical models for S‐RNase‐based self‐incompatibility. (a) Competitive interaction explained by a protein degradation model based on a single SLF gene controlling pollen specificity. For S1S2 heteroallelic pollen, its S1‐locus contains the S1‐RNase and S1‐SLF genes and its S2‐locus contains the S2‐RNase and S2‐SLF genes. S1‐SLF and S2‐SLF are produced in the cytoplasm of the S1S2 heteroallelic pollen, and upon self‐pollination, S1‐RNase and S2‐RNase are taken up during tube growth in the pistil. As indicated by the arrow connecting S1‐SLF and S2‐RNase, and by the arrow connecting S2‐SLF and S1‐RNase, S1‐SLF and S2‐SLF interact with S2‐RNase and S1‐RNase, respectively, to mediate their ubiquitination and degradation. S1‐SLF and S2‐SLF can also interact with all other nonself‐S‐RNases (S3‐RNase, S4‐RNase, etc.) during cross‐pollinations. As a result, the S1S2 heteroallelic pollen will be universally accepted by pistils of any S‐genotype. (b) Collaborative nonself‐recognition model. Pollen of each S‐haplotype has a single S‐RNase gene controlling pistil specificity, but an as yet unknown number of SLF genes controlling pollen specificity. Each type of SLF protein recognizes and interacts with a specific subset of nonself‐S‐RNases to mediate their ubiquitination and degradation. As indicated by the arrows connecting a particular type of SLF and S‐RNases, S7‐SLF1 of P. hybrida interacts with S9‐RNase and S17‐RNase, and causes breakdown of SI in S9 and S17 transgenic pollen due to competitive interaction; S7‐SLF2 interacts with S9‐RNase, S11‐RNase, and S19‐RNase, and causes breakdown of SI in S9, S11, and S19 transgenic pollen.40 However, none of the three types of SLF proteins examined interact with S5‐RNase, suggesting that additional yet unidentified type(s) of SLF genes are also involved in controlling pollen specificity.40

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