Production of an S RNase with Dual Specificity Suggests a Novel Hypothesis for the Generation of New S Alleles

Abstract

Gametophytic self-incompatibility in plants involves rejection of pollen when pistil and pollen share the same allele at the S locus. This locus is highly multiallelic, but the mechanism by which new functional S alleles are generated in nature has not been determined and remains one of the most intriguing conceptual barriers to a full understanding of self-incompatibility. The S(11) and S(13) RNases of Solanum chacoense differ by only 10 amino acids, but they are phenotypically distinct (i.e., they reject either S(11) or S(13) pollen, respectively). These RNases are thus ideally suited for a dissection of the elements involved in recognition specificity. We have previously found that the modification of four amino acid residues in the S(11) RNase to match those in the S(13) RNase was sufficient to completely replace the S(11) phenotype with the S(13) phenotype. We now show that an S(11) RNase in which only three amino acid residues were modified to match those in the S(13) RNase displays the unprecedented property of dual specificity (i.e., the simultaneous rejection of both S(11) and S(13) pollen). Thus, S(12)S(14) plants expressing this hybrid S RNase rejected S(11), S(12), S(13), and S(14) pollen yet allowed S(15) pollen to pass freely. Surprisingly, only a single base pair differs between the dual-specific S allele and a monospecific S(13) allele. Dual-specific S RNases represent a previously unsuspected category of S alleles. We propose that dual-specific alleles play a critical role in establishing novel S alleles, because the plants harboring them could maintain their old recognition phenotype while acquiring a new one.

Gametophytic self-incompatibility in Lycium parishii (Solanaceae): allelic diversity, genealogical structure, and patterns of molecular evolution at the S-RNase locus

“…There are four sites (in our alignment, sites 18, 20, 21, and 46) within the S-RNase hypervariable regions that Matton et al (1997) modified in the S. chacoense S11 allele to match the S13 allele, resulting in a change to the S13 specificity. When only three of these four sites were modified (sites 18, 21, and 46), the result was a dual-specificity allele that rejected both S11 and S13 pollen (Matton et al, 1999). In our analyses, these four sites were found to be under positive selection for both species (Figure 2) with the exception of site 46 in L. parishii and site 20 in L. andersonii.…”

Structural and Transcriptional Analysis of the Self-Incompatibility Locus of Almond: Identification of a Pollen-Expressed F-Box Gene with Haplotype-Specific Polymorphism

“…Amino acid sequence alignment showed that SFB contained two quite variable regions, as did S-RNase (Ioerger et al, 1991;Ushijima et al, 1998). The hypervariable region of S-RNase is exposed on the surface of the folded protein molecule and plays a pivotal role in the recognition of self-pollen (Matton et al, 1997(Matton et al, , 1999Ida et al, 2001;Matsuura et al, 2001). The two variable regions of SFB at the C terminus were found to be hydrophilic enough to be exposed on the surface (data not shown) and may have important recognition functions analogous to those of the S-RNase.…”

The population genetics of sporophytic self-incompatibility in Senecio squalidus L. (Asteraceae) I: S allele diversity in a natural population

“…New S alleles are thought to evolve only under a limited range of evolutionary scenarios, such as the temporary evolution of dual specificity S alleles (Matton et al, 1999), or temporary breakdown of SI (Uyenoyama et al, 2001). Ancient S polymorphisms, often predating speciation, are typical of SI systems and further emphasise the rarity with which new S alleles arise (Ioerger et al, 1990;Richman et al, 1996a).…”

“…New S alleles, complementary sets of male and female S genes, are believed to evolve very rarely and only under limited selective scenarios, including temporary breakdown of SI, or through dual-specificity alleles (Matton et al, 1999;Uyenoyama et al, 2001). A fundamental consequence of SI is that the selective advantage of an S allele is inversely proportional to its frequency (negative frequency dependent selection) such that rare or new S alleles are favoured and maintained in popu-431 lations for extended periods of evolutionary time (Ioerger et al, 1990;Richman et al, 1996a).…”