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, 96 (10), 5592-7

Evolution of the Fungal Self-Fertile Reproductive Life Style From Self-Sterile Ancestors

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Evolution of the Fungal Self-Fertile Reproductive Life Style From Self-Sterile Ancestors

S H Yun et al. Proc Natl Acad Sci U S A.

Abstract

In most fungal ascomycetes, mating is controlled by a single locus (MAT). Fungi requiring a partner to mate are heterothallic (self-sterile); those not requiring a partner are homothallic (self-fertile). Structural analyses of MAT sequences from homothallic and heterothallic Cochliobolus species support the hypothesis that heterothallism is ancestral. Homothallic species carry both MAT genes in a single nucleus, usually closely linked or fused, in contrast to heterothallic species, which have alternate MAT genes in different nuclei. The structural organization of MAT from all heterothallic species examined is highly conserved; in contrast, the organization of MAT in each homothallic species is unique. The mechanism of conversion from heterothallism to homothallism is a recombination event between islands of identity in otherwise dissimilar MAT sequences. Expression of a fused MAT gene from a homothallic species confers self-fertility on a MAT-null strain of a heterothallic species, suggesting that MAT alone is sufficient to change reproductive life style.

Figures

Figure 1
Figure 1
Strategies to clone MAT genes from homothallic Cochliobolus species, as described in the text. Textures of boxes indicate MAT-1 (black), MAT-2 (hatches), ORF1 (dotted diagonal lines); lines extending from boxes represent sequences flanking idiomorphs. Arrowheads identify locations and 5′ → 3′ direction of PCR primers. Numbers with decimals are in kb, those without are in bp.
Figure 2
Figure 2
Organization of MAT in heterothallic and homothallic species. The arrangement is identical in all heterothallic species examined to date, including C. heterostrophus and C. ellisii (shown here), C. carbonum, C. victoriae, C. intermedius, and asexual B. sacchari and A. alternata (not shown, see Fig. 5). Organization of each homothallic locus is unique, as described in the text. Textures of boxes are as in Fig. 1 for MAT-1, MAT-2, and ORF1; gene encoding β-glucosidase (open boxes); all other textures represent noncoding sequences 5′ or 3′ of MAT that are either unique to a particular species or common to more than one. Arrows indicate direction of transcription. Tightly linked to MAT in all species (except C. kusanoi) is a highly conserved ORF (ORF1) that shows similarity to a Saccharomyces cerevisiae ORF (GenBank accession no. U22383) of unknown function. Note that all genes are linked or fused, except that linkage has not yet been detected between the C. cymbopogonis MAT genes (which reside in the same nucleus unlike the heterothallic ones which reside in separate nuclei) or between ORF1 and C. kusanoi MAT.
Figure 3
Figure 3
Models for evolution, by recombination events, of fused homothallic MAT genes in C. luttrellii and C. homomorphus from opposite heterothallic MAT genes in C. heterostrophus (the heterothallic progenitor of C. homomorphus is unknown). (A) Misalignment of homologous flanking sequences could bring into register short islands of identity between the largely dissimilar MAT idiomorphs. A homologous recombination event at the point of identity would result in two fused MAT genes, both incomplete with respect to their heterothallic counterparts. If the crossover point were on either side of the DNA binding region (14), one fusion product would have both DNA-binding motifs and one would have neither. The number of amino acids eliminated (C. luttrellii, 115 from the 3′ end of MAT-1, 49 from the 5′ end of MAT-2; C. homomorphus, 9 from the 3′ end of MAT-2, 7 from the 5′ end of MAT-1) depends on the position of the crossover point (compare A Left with A Right). Textures are described in Fig. 1; small boxes within idiomorphs represent DNA-binding motifs; gray, α-box in MAT-1, white, HMG box in MAT-2 (14). (B) Inspection of the actual nucleotide sequences of the C. heterostrophus MAT-1 and MAT-2 genes reveals an 8-bp region of complete identity (shaded box, B Left) and a 9-bp region, with one mismatch (shaded box, B Right), corresponding to the C. luttrellii and C. homomorphus fusion points, respectively. Recombination in the Upper Left box creates precisely the sequence found in the C. luttrellii MAT-1/MAT-2 fused gene (Lower Left box); the left side of the fused sequence is similar to C. heterostrophus MAT-1 and the right side to MAT-2. Recombination in the Upper Right box creates the C. homomorphus MAT-2/MAT-1 fused gene (Lower Right box). Single letters above or below codons are standard amino acid abbreviations.
Figure 4
Figure 4
The C. luttrellii homothallic MAT gene alone confers on heterothallic C. heterostrophus the ability to self and cross. (Top) Plate with a senescent corn leaf as substrate for mating (18) inoculated with C. heterostrophus carrying the fused C. luttrellii MAT gene. Black bodies (arrowhead) are pseudothecia, indicating selfing. (Middle) Part of a mating plate, inoculated first with an albino C. heterostrophus MAT-1 tester strain, followed by inoculum (black rectangle) of a pigmented C. heterostrophus MAT-deletion strain carrying the fused C. luttrellii MAT gene. White pseudothecia (arrowhead) indicate crossing with the albino parent as female, because pseudothecial walls are of maternal origin. (Bottom Left) Progeny of a selfed transformant (Top), demonstrating that pseudothecia from selfed strains yield viable ascospores and that all progeny of a selfed pigmented strain are pigmented. (Bottom Right) Progeny of a cross (Middle), demonstrating that ascospores are viable and that alleles at the color marker Alb1 segregate (1:1).
Figure 5
Figure 5
Maximum likelihood tree generated from combined ITS and GPD sequence data by using paup Version 4.0 d61a (35). Homothallic species (thick lines) are scattered among heterothallic species, indicating their polyphyletic origin. Numbers are percentages (only those over 50 are shown) of times a group was found in 500 parsimony bootstrap replicates. ∗ indicate species from which MAT loci were examined.

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