Genetic polymorphism of self-incompatibility in flowering plants

Ebert, Paul R.; Anderson, Marilyn A.; Bernatzky, Robert; Altschuler, Mitchell; Clarke, Adrienne E.

doi:10.1016/0092-8674(89)90899-4

Cited by 78 publications

(27 citation statements)

References 40 publications

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“…Comparable evidence for ancient polymorphism that predates speciation has previously been found in the mammalian major histocompatibility complex (MHC) class I locus (24)(25)(26)(27). Both the MHC locus and the S locus are highly polymorphic and have highly divergent alleles.…”

Section: Discussionmentioning

confidence: 99%

Polymorphism at the self-incompatibility locus in Solanaceae predates speciation.

Ioerger

Clark

Kao

1990

Proc. Natl. Acad. Sci. U.S.A.

243

169

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Sequences of 11 alleles of the gametophytic self-incompatibility locus (S locus) from three species of the Solanaceae family have recently been determined. Pairwise comparisons of these alleles reveal two unexpected observations: (i) amino acid sequence similarity can be as low as 40% within species and (ii) some interspecific similarities are higher than intraspecific similarities. The gene genealogy clearly illustrates this unusual pattern of relationships. The data suggest that some of the polymorphism at the S locus existed prior to the divergence of these species and has been maintained to the present. In support of this hypothesis, the number of shared polymorphic sites was found to exceed the number found in simulations with independent accumulation of mutations. Strictly neutral evolution is exceedingly unlikely to maintain the polymorphism for such a long time. The allele multiplicity and extreme age of the alleles is consistent with Wright's classic one-locus population genetic model of gametophytic self-incompatibility. Similarities between the plant S locus and the mammalian major histocompatibility complex are discussed.Self-incompatibility is a natural, genetically determined barrier to inbreeding. In many plant species, self-incompatibility is controlled by a single locus, the S locus, which elicits recognition and rejection of self-pollen (1). In gametophytic self-incompatibility, inhibition of pollen germination or pollen-tube growth results when the S allele expressed by the pollen matches one of the two S alleles expressed in the pistil. A highly expressed, pistil-specific protein, the S protein, has been identified as a product of the S locus. The cDNA sequences of several alleles of the S protein from three species in the Solanaceae family have been determined, and extraordinary divergence, even between alleles from the same species, is apparent (T.R.I. and T.-h.K., unpublished work).The self-incompatibility systems of many plant species have long been of interest to evolutionary biologists, and the extreme levels of polymorphism in S-protein sequences suggest that an unusual array of evolutionary forces operate at the S locus. Early appreciation of the allelic diversity of Oenothera organensis, with 37 alleles identified in a population of 1000 plants (2, 3), prompted Wright (4) to examine population genetic models of self-incompatibility loci. A consequence of gametophytic self-incompatibility is that all individuals in a population are heterozygotes. Wright noticed that rare alleles have a reproductive advantage because pollen bearing a rare allele is less likely to land on a stigma with the same allele, so that rare alleles suffer fewer aborted pollinations. This frequency dependence made it less likely for a new mutation to be rapidly lost compared with a neutral allele, and Wright's model produced a balance between mutation and random genetic drift that could maintain many alleles in the population. Additionally, this model predicts that the alleles could be far older than neut...

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Section: Discussionmentioning

confidence: 99%

Polymorphism at the self-incompatibility locus in Solanaceae predates speciation.

Ioerger

Clark

Kao

1990

Proc. Natl. Acad. Sci. U.S.A.

243

169

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“…In the sporophytic system, both point mutations and intragenic recombination appear to have contributed to S allele polymorphism (Kusaba et al, 1997;Nasrallah, 1997). In the gametophytic system, several studies (Clark and Kao, 1991;Coleman and Kao, 1992;Saba-El-Leil et al, 1994;Matton et al, 1995Matton et al, , 1997Ishimizu et al, 1998) have suggested that point mutations rather than intragenic recombination (Fisher, 1961;Pandey, 1970;Ebert et al, 1989) are the primary source of S allele polymorphism. Phenotypically distinct yet highly similar S RNase sequences have been described in Solanum chacoense (Saba-El-Leil et al, 1994) and Pyrus pyriflora (Ishimizu et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 1999

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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 selfincompatibility. 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 dualspecific 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. INTRODUCTIONAmong the cell-cell recognition phenomena present in living organisms, self-incompatibility (SI) plays a major evolutionary role because it constitutes an important mechanism for preventing inbreeding. SI is present in hermaphroditic animals such as tunicates (Grosberg, 1988), in fungi (Kronstad and Leong, 1990), and in many Angiosperm families (de Nettancourt, 1977). In the most widespread type of SI, gametophytic SI, the genotype of the haploid pollen determines its own incompatibility phenotype. For the Solanaceae, the gametophytic SI phenotype is specified by a highly multiallelic S locus (de Nettancourt, 1977(de Nettancourt, , 1997 whose only known product is a ribonuclease (S RNase; McClure et al., 1989) expressed in the transmitting tissue of the style (Anderson et al., 1986). Gain-of-function experiments have shown that expression of an S RNase transgene is sufficient to alter the SI phenotype of the pistil but not that of the pollen Murfett et al., 1994;Matton et al., 1997), and thus the identity of the pollen S gene (unknown to date) is likely to be different from that of the S RNase (Kao and McCubbin, 1997). RNase activity, although essential for expression of the SI phenotype , seems not to be involved in the specificity of the cell-cell recognition phenomenon. In closely related S RNases, such specificity has been shown to depend on the amino acid sequence at the two hypervariable ...

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“…In gametophytic systems, rejection generally occurs within the style by heavy callose deposition (Ebert et al, 1989), and the fate of the pollen is determined by its own haploid gametophytic genotype. As exhibited in most plant species, the control is exerted through the action of a single multiallelic locus (Richards, 1986).…”

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confidence: 99%

Self- and cross-pollination effects on pollen tube growth and seed set in holm oak Quercus ilex L (Fagaceae)

Yacine

Bouras

1997

Ann. For. Sci.

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Summary -Patterns of the self-incompatibility system have been more often described for hermaphroditic, entomophilous and short-lived plant species. Quercus ilex is a long-lived, monoecious, anemophilous and highly self-incompatible species. We used pollination experiments to investigate phenotypic responses of the self-incompatibility system. Flowers from 14 individuals of the same stand were hand-pollinated with self-pollen, cross-pollen from a single donor and a mixture of the two types. We observed a slower pollen tube growth and no or nearly no seed production after self-pollination. The more self-pollen tubes reach the style, the more flowers will stop their ovule development, resulting in a high flower abortion rate. In open pollination, pollen load is not a limiting factor, but incompatible pollen may reach stigma simultaneously or before compatible cross-pollen, which will induce an early abortion of flowers. When pollination is qualitatively and quantitatively effective, the regulation of seed production related to the resources availability acts by the late abortion of fruit.self-incompatibility / pollen tube growth / seed set / Quercus ilex L Résumé -Effets de l'auto-et de l'allopollen sur la croissances des tubes polliniques et la production de fruits chez le chêne vert (Quercus ilex L). Les

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Genetic polymorphism of self-incompatibility in flowering plants

Cited by 78 publications

References 40 publications

Polymorphism at the self-incompatibility locus in Solanaceae predates speciation.

Polymorphism at the self-incompatibility locus in Solanaceae predates speciation.

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

Self- and cross-pollination effects on pollen tube growth and seed set in holm oak Quercus ilex L (Fagaceae)

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