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Lateral Transfer of Mating System in Stemphylium Lateral transfer of mating system in Stemphylium Patrik Inderbitzin†‡§, Jennifer Harkness†, B. Gillian Turgeon¶, and Mary L. Berbee† †Department of Botany, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, Canada V6T 1Z4; and ¶Department of Plant Pathology, 334 Plant Science Building, Cornell University, Ithaca, NY 14853 Edited by Barbara A. Schaal, Washington University, St. Louis, MO, and approved June 16, 2005 (received for review March 8, 2005) The fungal genus Stemphylium (Ascomycota) contains selfing species physical linkage of the MAT alleles could be accounted for by a that evolved from outcrossing ancestors. To find out how selfing crossover event, for other arrangements the mechanism remained originated, we analyzed the Stemphylium MAT loci that regulate unknown (7). Phylogenies from housekeeping loci were congruent sexual reproduction in ascomycetes and compared MAT structures with one another, and they supported the MAT gene arrangements and phylogeny with a multigene Stemphylium species phylogeny. in showing that each self-fertile Cochliobolus species evolved inde- We found that some Stemphylium species’ MAT loci contained a pendently from a self-sterile ancestor. single gene, either MAT1-1 or MAT1-2, whereas others contained a To investigate the origin of self-fertility in Stemphylium,we unique fusion of the MAT1-1 and MAT1-2 regions. In all fused MAT compared the position of self-fertile species in an organismal regions, MAT1-1 was inverted and joined to a forward-oriented phylogeny and in a phylogeny of the mating-type genes. We MAT1-2 region. As in the closely related Cochliobolus, Stemphylium analyzed the mating-type loci to assess homology of the gene species with fused MAT regions were able to self. Structural and arrangements in selfing and outcrossing species. We had expected phylogenetic analyses of the MAT loci showed that the selfing- that, as in Cochliobolus, self-fertility would have originated in conferring fused MAT regions were monophyletic with strong sup- different species by independent mating-type gene fusions. Instead, port. However, in an organismal phylogeny of Stemphylium species we found evidence for a single fusion that was transferred across based on 106 isolates and four loci unrelated to mating, selfing arose lineages. in two clades, each time with strong support. Isolates with identical fused MAT regions were present in both clades. We showed that a Materials and Methods one-time origin of the fused MAT loci, followed by a horizontal Fungal Strains Used. The 106 isolates of Stemphylium used were from transfer across lineages, was compatible with the data. Another the collection of P.I. or from other culture collections. Isolates were group of selfers in Stemphylium only had forward-oriented MAT1-1 chosen to represent the genetic diversity of known Stemphylium at their MAT loci, constituting an additional and third origin of selfing strains, with an increased sampling around the type species S. her- in Stemphylium. barum. See Table 1, which is published as supporting information on the PNAS web site, for details. filamentous ascomycetes ͉ nonvertical inheritance ͉ evolution ͉ Pleospora ͉ horizontal transfer Assessment of Self-Fertility. Self-fertility of the fungal strains was evaluated in the laboratory. Single ascospores or conidia were mong bacteria, lateral gene flow has redistributed charac- germinated on water agar, transferred to V8 agar plates upon Aters of evolutionary importance (1). In eukaryotes including germination (8), stored at room temperature or at 4°C, and fungi, evolution through lateral gene transfer is often proposed, periodically examined for the formation of sexual spores (ascos- but alternative explanations for character distributions have pores) (9). been difficult to rule out (2). The mating type locus in the ascomycetous fungal genus Stemphylium has provided an op- Molecular Work. Mycelium was scraped off the surface of a Petri portunity to detect an ancient lateral transfer that changed a plate, and DNA was extracted by using a standard phenol- fungal breeding system. We used phylogenetic analyses based on chloroform extraction method (10). PCR reactions were performed five loci in conjunction with gene rearrangement data to show by using a variety of conditions (see Supporting Methods in Sup- that the distribution of mating strategies in Stemphylium is best porting Text, which is published as supporting information on the explained by a lateral transfer of the genes controlling mating. PNAS web site). In haploid filamentous ascomycetes, self-sterility and self-fertility Loci sequenced for species phylogenies were the ribosomal depend on the configuration of genes at MAT, the mating type internal transcribed spacer (ITS), glyceraldehyde-3-phosphate dehy- locus (3). Each self-sterile individual has only one of the two drogenase (GPD), elongation factor-1 ␣ (EF-1 ␣) and the noncoding alternative single-copy genes, MAT1-1 or MAT1-2,atitsMAT region between the vacuolar membrane ATPase catalytic subunit A locus. Like large portions of the human X and Y chromosomes, the gene (vmaA), and vpsA, a gene involved in vacuolar biogenesis (11). DNA and amino acid sequences of MAT1-1 and MAT1-2 are no Primers were from refs. 12–14 or designed for this study based on more similar than expected by chance. Outside of the Ϸ1,100- to DNA sequences available from GenBank (see Table 2, which is 4,200-bp MAT region, sequence similarity between homologous published as supporting information on the PNAS web site). chromosomes reappears and haploid individuals of opposite mating Primers for the intergenic spacer between vmaA and vpsA were 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), This paper was submitted directly (Track II) to the PNAS office. contain both MAT1-1 and MAT1-2 genes in the same genome. Abbreviation: ITS, internal transcribed spacers. Demonstrating that the presence of a MAT1-1͞MAT1-2 fusion was Data deposition: The DNA sequences reported in this paper have been deposited in the enough to confer self-fertility, transformation of a mating-type GenBank database (accession nos. AY316968–AY316973, AY316975–AY316978, AY316980, AY316982–AY316989, AY316991–AY317074, AY324671–AY324776, AY329168–AY329270, deletion strain of the self-sterile species Cochliobolus heterostrophus AY329271–AY329323, AY335164–AY335180, AY339853–AY339864, and AY340940– with the fused MAT genes produced self-fertile individuals (7). AY340945). Alignments have been submitted to TreeBASE (study accession no. S1313; Matrix Suggesting that self-fertility originated convergently, each of the accession nos. M2301–M2305). four selfing species of Cochliobolus had unique splice sites adjacent ‡Present address: Department of Plant Pathology, 334 Plant Science Building, Cornell to its MAT1-1 and͞or MAT1-2 genes, and the direction of tran- University, Ithaca, NY 14853. scription of the two genes along with the length of the intergenic §To whom correspondence should be addressed. E-mail: [email protected]. intervening sequences differed across species. In some cases, the © 2005 by The National Academy of Sciences of the USA 11390–11395 ͉ PNAS ͉ August 9, 2005 ͉ vol. 102 ͉ no. 32 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0501918102 Downloaded by guest on September 28, 2021 based on Cochliobolus heterostrophus sequences that G. Saenz and Generation of Mating-Type DNA Phylogenies. For MAT1-1 analyses, B. G. Turgeon obtained from the former Torrey Mesa Research the inverted parts of the fused MAT region from 11 selfing species Institute. were combined in an alignment with homologous regions from 11 Primers used for amplification of the MAT regions were de- species with separate MAT regions. Similarly, the MAT1-2 parts signed based on DNA sequences (15, 16), and later, on sequences from species with fused MAT regions were used for analyses from this study (see Tables 3–8, which are published as supporting together with homologous regions from five species with separate information on the PNAS web site). MAT regions. Settings for phylogenetic analyses were as for the To determine DNA sequences of the entire mating-type genes four loci species data set except that likelihood bootstrap support and flanking regions, the chromosome walking kit Vectorette was percentages were based on 500 replicates. used (Sigma-Genosys, The Woodlands, TX). Additional primers were designed from previously sequenced conserved DNA binding Generation of Mating-Type Protein Phylogenies. The MAT gene regions of the MAT genes and used together with the kit primers DNA sequences were translated into amino acids. To the MAT1-1 for PCR amplifications of MAT flanks (see Supporting Methods and protein alignment, five outgroup taxa from GenBank were added Tables 9–11, which are published as supporting information on the (Alternaria alternata, AB009451; Cochliobolus cymbopogonis, PNAS web site). AF129744; C. heterostrophus, AF029913; C. ellisii, AF129746; C. sa- PCR products were completely sequenced in both directions by tivus AF275373). The MAT1-2 alignment contained the same using a Big Dye Terminator Cycle Sequencing Kit v2.0 or 3.0 outgroup taxa as MAT1-1 (A. alternata, AB009452; C. cymbopogo- (Applied Biosystems, Foster City, CA) according to the manufac- nis, AF129745; C. heterostrophus, AF027687; C. ellisii, AF129747; C. turer’s instructions with a variety of sequencing primers (see sativus,
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