LETTERS TO THE EDITOR

How Can Two-Gene Models of Self-Incompatibility Generate New Specificities?

The unsolved problem of how the pollen and pistil components of angiosperm self-incompatibility (SI) are inherited has a long history (Lewis 1960 ). A recent paper provides evidence, based on transgenic experiments in Solanum chacoense, that a single amino acid difference between proteins encoded by two very similar SI-specifying (S) alleles can result in plants that reject the pollen of both alleles (Matton et al. 1999 ). The authors propose that this result may help solve the difficult problem of how new S allele specificities could arise over evolutionary time if there are separate (but linked) loci for pollen and pistil specificities. The purpose of the present Letter is to suggest, however, that this proposal is implausible.

The first step in the proposed pathway from one allele (S_x) to a new functional allele (S_y) could be a change in the pistil component of recognition, from an allele that recognizes its own corresponding pollen specificity (S_x), to a dual-function allele (designated S_xyF for specificities x and y in the female function) that recognizes both S_y and S_x pollen. The S_y component of such a dual-recognition allele should be effectively "neutral" to the extent that no corresponding S_yM (male) function would preexist in the population. As pointed out by Matton et al. 1999 , the S_xyF allele could therefore persist in the population, and would not suffer the evident disadvantage (in a two-gene system) that a changed pollen or pistil specificity, without a change in the other component, would simply cause self-compatibility (Charlesworth, 1995). Matton et al. 1999 propose that this first change, to dual specificity, might later be followed by changes in the male function, creating a new specificity haplotype with female and male alleles S_xyF and S_yM, respectively. Finally, loss of the dual specificity by replacement of S_xyF by S_yF could lead to a fully functional system of SI based on the novel S haplotype, S_yF;–S_yM. (The opposite order of the changes, i.e., pollen reaction changed first, followed by changed pistil reaction, would also be possible, and everything below can also be applied to this version.)

On closer examination, this attractive scenario appears less easy to accept. Consider a two-locus model, as hypothesized by Matton et al. 1999 . In a population in which the first change has occurred, so that the population contains both the initial S_xF;–S_xM haplotype and the new S_xyF;–S_xM one, the requisite change to generate S_yM must subsequently happen in the very same haplotype that carries the S_xyF allele at the female function gene. Otherwise, if the S_yM allele appeared in a different haplotype, say the S_a haplotype, the new "y-type" specificity would encounter two disadvantages. Table 1 shows how the model of Matton et al. 1999 would behave in this case and illustrates the difficulties. First, S_aF;–S_yM plants would have the disadvantage of being self-compatible; the disadvantage that new specificities cause loss of self-incompatibility thus appears at this stage of the evolutionary process, rather than at the first step, and is not eliminated by allowing dual-specificity alleles. Second, the new S_yM pollen would be incompatible with unrelated plants carrying S_xyF, leading to lower fertility for this pollen type than for other pollen types. (S_xM would also manifest this problem, but would confer self-incompatibility.) Thus, S_yM would be a cross-incompatibility allele, not a new SI allele, and would be more likely to be eliminated from the population than to be selectively advantageous. In view of the two disadvantages of the S_aF;–S_yM haplotype, it seems that S_yM could be an evolutionary successful mutation only if it were to occur in the haplotype that carries the S_xyF allele. It is therefore unnecessary to discuss mechanisms by which the two "y-type" components might subsequently be brought together into a single S_yF;–S_yM haplotype.

Can we then envisage the evolution of an S_yF;–S_yM haplotype by assuming that the S_yM mutation arises from the S_xyF;–S_xM haplotype? This would produce self-incompatibility and cross-compatibility, as required, but the difficulties are not eliminated. We still have a process requiring three successive mutations all within the same haplotype (loci affected shown in bold):

(1)

(2)

(3)

Note that the second of these mutations must create a male determinant that is rejected by the pistil y specificity of the haplotype (but not by its x specificity, because the new haplotype ultimately generated by these mutations should not be rejected by pistils with x specificity). The other two mutations (steps 1 and 3), moreover, must both occur in the same gene. This might be plausible, given the large amounts of time available for self-incompatibility to evolve, but it is difficult to accept that this process could occur for each new specificity, given the very high numbers of specificities in some species (sometimes as many as a hundred or more; e.g., Bernatzky et al. 1988 ; Okazaki et al. 1997 ).

Given the mounting evidence that separate pollen and pistil genes exist in a self-incompatible Brassica species (Schopfer et al. 1999 ), along with the clear implication of two-gene systems in fugal incompatibility (see Casselton 1997 , Casselton 1998 ), there is a pressing need to solve the puzzle of how new specificities arise. It seems, however, that the possibility of dual specificities does not provide an easy solution to this puzzle.

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Bernatzky, R., Anderson, M.A., and Clarke, A.E. (1988) Molecular genetics of self-incompatibility in flowering plants. Dev. Genet. 9:1-12.

Casselton, L.A. (1997) Molecular recognition in fungal mating. Endeavour 21:159-163[Medline].

Casselton, L.A. (1998) Molecular genetics of mating recognition in Basidiomycete fungi. Microbiol. Mol. Biol. Rev. 62:55-70[Abstract/Free Full Text].

Lewis, D. (1960) Genetic control of specificity and activity of the S antigen in plants. Proc. Roy. Soc. Lond. B 151:468-477[Medline].

Matton, D.P., Luu, D.T., Xike, Q., Laublin, G., O'Brien, M., Maes, O., Morse, D., and Cappadocia, M. (1999) Production of an S RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell 11:2087-2098[Abstract/Free Full Text].

Okazaki, K., Kusaba, M., Ockendon, D., and Nishio, T. (1997) Characterization of S-tester lines in Brassica oleracea: polymorphism of restriction fragment length of SLG homologues and isoelectric points of S-locus glycoproteins. Theor. Appl. Genet. 98:1329-1334[CrossRef].

Schopfer, C.R., Nasrallah, M.E., and Nasrallah, J.B. (1999) The male determinant of self-incompatibility in Brassica.. Science 286:1697-1700[Abstract/Free Full Text].

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