Lateral transfer of mating system in <em>Stemphylium</em>

Abstract

Among bacteria, lateral gene flow has redistributed characters of evolutionary importance (1). In eukaryotes including fungi, evolution through lateral gene transfer is often proposed, but alternative explanations for character distributions have been difficult to rule out (2). The mating type locus in the ascomycetous fungal genus Stemphylium has provided an opportunity to detect an ancient lateral transfer that changed a fungal breeding system. We used phylogenetic analyses based on five loci in conjunction with gene rearrangement data to show that the distribution of mating strategies in Stemphylium is best explained by a lateral transfer of the genes controlling mating.

In haploid filamentous ascomycetes, self-sterility and self-fertility depend on the configuration of genes at MAT, the mating type locus (3). Each self-sterile individual has only one of the two alternative single-copy genes, MAT1-1 or MAT1-2, at its MAT locus. Like large portions of the human X and Y chromosomes, the DNA and amino acid sequences of MAT1-1 and MAT1-2 are no more similar than expected by chance. Outside of the ≈1,100- to 4,200-bp MAT region, sequence similarity between homologous chromosomes reappears and haploid individuals of opposite mating types have syntenous flanking genes (4, 5).

In contrast to self-sterile species, haploid self-fertile species in Stemphylium (this study), as in the closely related Cochliobolus (6), contain both MAT1-1 and MAT1-2 genes in the same genome. Demonstrating that the presence of a MAT1-1/MAT1-2 fusion was enough to confer self-fertility, transformation of a mating-type deletion strain of the self-sterile species Cochliobolus heterostrophus with the fused MAT genes produced self-fertile individuals (7). Suggesting that self-fertility originated convergently, each of the four selfing species of Cochliobolus had unique splice sites adjacent to its MAT1-1 and/or MAT1-2 genes, and the direction of transcription of the two genes along with the length of the intergenic intervening sequences differed across species. In some cases, the physical linkage of the MAT alleles could be accounted for by a crossover event, for other arrangements the mechanism remained unknown (7). Phylogenies from housekeeping loci were congruent with one another, and they supported the MAT gene arrangements in showing that each self-fertile Cochliobolus species evolved independently from a self-sterile ancestor.

To investigate the origin of self-fertility in Stemphylium, we compared the position of self-fertile species in an organismal phylogeny and in a phylogeny of the mating-type genes. We analyzed the mating-type loci to assess homology of the gene arrangements in selfing and outcrossing species. We had expected that, as in Cochliobolus, self-fertility would have originated in different species by independent mating-type gene fusions. Instead, we found evidence for a single fusion that was transferred across lineages.

Acknowledgments

Notes

Author contributions: P.I., B.G.T., and M.L.B. designed research; P.I. and J.H. performed research; P.I. analyzed data; and P.I. and M.L.B. wrote the paper.

This paper was submitted directly (Track II) to the PNAS office.

Abbreviation: ITS, internal transcribed spacers.

Data deposition: The DNA sequences reported in this paper have been deposited in the GenBank database (accession nos. AY316968–AY316973, AY316975–AY316978, AY316980, AY316982–AY316989, AY316991–AY317074, AY324671–AY324776, AY329168–AY329270, AY329271–AY329323, AY335164–AY335180, AY339853–AY339864, and AY340940–AY340945). Alignments have been submitted to TreeBASE (study accession no. S1313; Matrix accession nos. M2301–M2305).