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Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions.

van Peer AF, Park SY, Shin PG, Jang KY, Yoo YB, Park YJ, Lee BM, Sung GH, James TY, Kong WS - PLoS ONE (2011)

Bottom Line: Regions near mating-type loci in fungi often show adapted recombination, facilitating the generation of novel mating types and reducing the production of self-compatible mating types.Next to this, it was revealed that large distance subloci can exist in matB as well.Finally, the genes that were linked to specific mating types will serve as molecular markers in breeding.

View Article: PubMed Central - PubMed

Affiliation: Mushroom Research Division, National Institute of Horticultural and Herbal Science, Rural Development Administration, Suwon, Republic of Korea.

ABSTRACT

Background: Mating-type loci of mushroom fungi contain master regulatory genes that control recognition between compatible nuclei, maintenance of compatible nuclei as heterokaryons, and fruiting body development. Regions near mating-type loci in fungi often show adapted recombination, facilitating the generation of novel mating types and reducing the production of self-compatible mating types. Compared to other fungi, mushroom fungi have complex mating-type systems, showing both loci with redundant function (subloci) and subloci with many alleles. The genomic organization of mating-type loci has been solved in very few mushroom species, which complicates proper interpretation of mating-type evolution and use of those genes in breeding programs.

Methodology/principal findings: We report a complete genetic structure of the mating-type loci from the tetrapolar, edible mushroom Flammulina velutipes mating type A3B3. Two matB3 subloci, matB3a that contains a unique pheromone and matB3b, were mapped 177 Kb apart on scaffold 1. The matA locus of F. velutipes contains three homeodomain genes distributed over 73 Kb distant matA3a and matA3b subloci. The conserved matA region in Agaricales approaches 350 Kb and contains conserved recombination hotspots showing major rearrangements in F. velutipes and Schizophyllum commune. Important evolutionary differences were indicated; separation of the matA subloci in F. velutipes was diverged from the Coprinopsis cinerea arrangement via two large inversions whereas separation in S. commune emerged through transposition of gene clusters.

Conclusions/significance: In our study we determined that the Agaricales have very large scale synteny at matA (∼350 Kb) and that this synteny is maintained even when parts of this region are separated through chromosomal rearrangements. Four conserved recombination hotspots allow reshuffling of large fragments of this region. Next to this, it was revealed that large distance subloci can exist in matB as well. Finally, the genes that were linked to specific mating types will serve as molecular markers in breeding.

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Related in: MedlinePlus

Synteny modeling of the events that separated the matA subloci of S. commune.Panel A and B show synteny maps of C. cinerea and S. commune, with the latter in opposite orientations. Map A shows high gene order similarity whereas B suggests inversion of nearly all major S. commune segments. In map A, two large segments (blue lines) that correspond to the highly conserved 350 Kb matA region (Figure 4) are displaced from the region flanked by the black lines. Repositioning of those fragments (in reversed order) reconstitutes the genomic organization also found in C. cinerea (C) with a single matA locus (green) and a continuous high syntenic 350 Kb matA region. Map B clearly shows two inversed gene clusters (purple lines) that have separated the S. commune matA locus. Repositioning of those clusters (map D) reunites the matA locus, but does not reunite the 350 Kb region. About one third (purple line most right, map D) of the genes corresponding to this region remains separated by a large non syntenic segment (∼250 Kb, red dotted line) and most other S. commune gene clusters still display inversed orientation in comparison to the gene order in C. cinerea.
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pone-0022249-g006: Synteny modeling of the events that separated the matA subloci of S. commune.Panel A and B show synteny maps of C. cinerea and S. commune, with the latter in opposite orientations. Map A shows high gene order similarity whereas B suggests inversion of nearly all major S. commune segments. In map A, two large segments (blue lines) that correspond to the highly conserved 350 Kb matA region (Figure 4) are displaced from the region flanked by the black lines. Repositioning of those fragments (in reversed order) reconstitutes the genomic organization also found in C. cinerea (C) with a single matA locus (green) and a continuous high syntenic 350 Kb matA region. Map B clearly shows two inversed gene clusters (purple lines) that have separated the S. commune matA locus. Repositioning of those clusters (map D) reunites the matA locus, but does not reunite the 350 Kb region. About one third (purple line most right, map D) of the genes corresponding to this region remains separated by a large non syntenic segment (∼250 Kb, red dotted line) and most other S. commune gene clusters still display inversed orientation in comparison to the gene order in C. cinerea.

Mentions: To unravel the events that altered the organization of the matA region of F. velutipes we mapped synteny of 200 successive genes surrounding the matA locus of C. cinerea (chromosome 1, bp2471986-2934538) with that of L. bicolor, F. velutipes and S. commune. The latter was included because this fungus also has separated matA subloci and is taxonomically closer to F. velutipes than C. cinerea and L. bicolor [50]. Since there had been no annotation of the F. velutipes genome, C. cinerea genes were acknowledged as “syntenic” in F. velutipes when similar protein sequences with expect values equal to or smaller than 10−9 were obtained by tblastn. Loss of syntenic genes in the matA region from C. cinerea was indicated by 11 unique genes, and 21 (L. bicolor), 17 (F. velutipes) and 21 (S. commune) genes from C. cinerea that were not detected in one or two of these species. The selected C. cinerea region covered the matA containing F. velutipes contig Fv01174 (304 Kb) as well as parts of contig Fv02632 and Fv03236, the last which was found to contain the missing Beta flanking gene. The three contigs were linked to scaffold 3 (3.8 Mb) of the F. velutipes draft genome where Fv01174 was flanked upstream at 2.1 Kb by Fv03236 and downstream by Fv02632 at 28 Kb (Figure 4). Our analysis identified synteny between C. cinerea and L. bicolor over a remarkably large segment of 350 Kb (Figure 4, panel A), much larger than previously demonstrated [31]. In addition, we identified the boundaries of this syntenic segment, which are clearly denoted by genes from C. cinerea that have no local homologue in L. bicolor, were differently distributed in L. bicolor, or were inverted (Figure 4, panel A). Those boundaries coincide with the ends of the syntenic part of the matA region from F. velutipes (Figure 4). The matA region in F. velutipes showed highest synteny over the first 250 Kb of the 350 Kb segment and somewhat lower in the last 100 Kb (Figure 4, black line, 250 Kb; start to red mark, 100 Kb; red mark to end). Though the specific gene order of F. velutipes in comparison to C. cinerea was changed by inversions, the overall gene order as found in C. cinerea was shown to be strongly preserved. None of the inverted gene groups was translocated (Figure 4). In S. commune the syntenic 350 Kb matA region was also recovered, albeit in three different sections with 140 Kb and 200 Kb interval distances (Figure 4, purple and dashed light purple lines). Synteny was highest in the two segments corresponding to the first 250 Kb of the 350 Kb matA region and lower for the third fragment, resembling F. velutipes. Moreover, synteny of the fragments in S. commune ended at the same relative locations that represented the synteny boundaries in C. cinerea, L. bicolor and F. velutipes. Finally, the gene order within the three segments was strongly conserved, indicating a high level of gene conservation in this entire region for all Agaricomycetes. Inside the 350 Kb segment, two spots showed high recombination in all four species. The first spot was the matA locus itself, the second spot formed a small gap in synteny located between C. cinerea genes CC1G_01875.3 and CC1G_01877.3 (both hypothetical genes) and their respective orthologues. Exemplary, one of the few genes that was repositioned in L. bicolor in comparison to C. cinerea was inserted in this gap. In F. velutipes and S. commune gene clusters were separated by inversion or translocation at both of these locations (Figure 4, 5, 6). Detailed comparison of the F. velutipes gene order to that of C. cinerea showed that the matA locus of F. velutipes was separated by inversion of two 70 Kb fragments directly left and right of FvHD1-1 and FvHD2-2 (Figure 4, 5). Modeling a reversion of those clusters reunited the Beta-flanking gene, FvHD2-1, MIP, FvHD1-1 and FvHD2-2 in a similar distribution as found in C. cinerea and L. bicolor. Notably, FvHD2-2 and FvHD1-1 were never moved during the rearrangements (Figure 5). Synteny mapping also revealed important differences between the matA regions of F. velutipes and S. commune. First, all S. commune homeodomain genes were repositioned, whereas FvHD2-2 and FvHD1-1 retained their position during rearrangements. This shows that the respective matA loci were split between different genes. Second, the S. commune fragments representing the first part of the high syntenic 350 Kb region, and whose rearangement caused separation of the matA subloci, constituted 140 Kb and 260 Kb (Figure 4, purple lines). This was significantly larger than the 70 Kb in F. velutipes (Figure 4, blue lines) and shows that different fragments were rearranged. Third, the S. commune fragments were wedged by sections not syntenic to the 350 Kb C. cinerea matA region (Figure 4, dotted light purple lines), which was not observed in F. velutipes.


Comparative genomics of the mating-type loci of the mushroom Flammulina velutipes reveals widespread synteny and recent inversions.

van Peer AF, Park SY, Shin PG, Jang KY, Yoo YB, Park YJ, Lee BM, Sung GH, James TY, Kong WS - PLoS ONE (2011)

Synteny modeling of the events that separated the matA subloci of S. commune.Panel A and B show synteny maps of C. cinerea and S. commune, with the latter in opposite orientations. Map A shows high gene order similarity whereas B suggests inversion of nearly all major S. commune segments. In map A, two large segments (blue lines) that correspond to the highly conserved 350 Kb matA region (Figure 4) are displaced from the region flanked by the black lines. Repositioning of those fragments (in reversed order) reconstitutes the genomic organization also found in C. cinerea (C) with a single matA locus (green) and a continuous high syntenic 350 Kb matA region. Map B clearly shows two inversed gene clusters (purple lines) that have separated the S. commune matA locus. Repositioning of those clusters (map D) reunites the matA locus, but does not reunite the 350 Kb region. About one third (purple line most right, map D) of the genes corresponding to this region remains separated by a large non syntenic segment (∼250 Kb, red dotted line) and most other S. commune gene clusters still display inversed orientation in comparison to the gene order in C. cinerea.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3140503&req=5

pone-0022249-g006: Synteny modeling of the events that separated the matA subloci of S. commune.Panel A and B show synteny maps of C. cinerea and S. commune, with the latter in opposite orientations. Map A shows high gene order similarity whereas B suggests inversion of nearly all major S. commune segments. In map A, two large segments (blue lines) that correspond to the highly conserved 350 Kb matA region (Figure 4) are displaced from the region flanked by the black lines. Repositioning of those fragments (in reversed order) reconstitutes the genomic organization also found in C. cinerea (C) with a single matA locus (green) and a continuous high syntenic 350 Kb matA region. Map B clearly shows two inversed gene clusters (purple lines) that have separated the S. commune matA locus. Repositioning of those clusters (map D) reunites the matA locus, but does not reunite the 350 Kb region. About one third (purple line most right, map D) of the genes corresponding to this region remains separated by a large non syntenic segment (∼250 Kb, red dotted line) and most other S. commune gene clusters still display inversed orientation in comparison to the gene order in C. cinerea.
Mentions: To unravel the events that altered the organization of the matA region of F. velutipes we mapped synteny of 200 successive genes surrounding the matA locus of C. cinerea (chromosome 1, bp2471986-2934538) with that of L. bicolor, F. velutipes and S. commune. The latter was included because this fungus also has separated matA subloci and is taxonomically closer to F. velutipes than C. cinerea and L. bicolor [50]. Since there had been no annotation of the F. velutipes genome, C. cinerea genes were acknowledged as “syntenic” in F. velutipes when similar protein sequences with expect values equal to or smaller than 10−9 were obtained by tblastn. Loss of syntenic genes in the matA region from C. cinerea was indicated by 11 unique genes, and 21 (L. bicolor), 17 (F. velutipes) and 21 (S. commune) genes from C. cinerea that were not detected in one or two of these species. The selected C. cinerea region covered the matA containing F. velutipes contig Fv01174 (304 Kb) as well as parts of contig Fv02632 and Fv03236, the last which was found to contain the missing Beta flanking gene. The three contigs were linked to scaffold 3 (3.8 Mb) of the F. velutipes draft genome where Fv01174 was flanked upstream at 2.1 Kb by Fv03236 and downstream by Fv02632 at 28 Kb (Figure 4). Our analysis identified synteny between C. cinerea and L. bicolor over a remarkably large segment of 350 Kb (Figure 4, panel A), much larger than previously demonstrated [31]. In addition, we identified the boundaries of this syntenic segment, which are clearly denoted by genes from C. cinerea that have no local homologue in L. bicolor, were differently distributed in L. bicolor, or were inverted (Figure 4, panel A). Those boundaries coincide with the ends of the syntenic part of the matA region from F. velutipes (Figure 4). The matA region in F. velutipes showed highest synteny over the first 250 Kb of the 350 Kb segment and somewhat lower in the last 100 Kb (Figure 4, black line, 250 Kb; start to red mark, 100 Kb; red mark to end). Though the specific gene order of F. velutipes in comparison to C. cinerea was changed by inversions, the overall gene order as found in C. cinerea was shown to be strongly preserved. None of the inverted gene groups was translocated (Figure 4). In S. commune the syntenic 350 Kb matA region was also recovered, albeit in three different sections with 140 Kb and 200 Kb interval distances (Figure 4, purple and dashed light purple lines). Synteny was highest in the two segments corresponding to the first 250 Kb of the 350 Kb matA region and lower for the third fragment, resembling F. velutipes. Moreover, synteny of the fragments in S. commune ended at the same relative locations that represented the synteny boundaries in C. cinerea, L. bicolor and F. velutipes. Finally, the gene order within the three segments was strongly conserved, indicating a high level of gene conservation in this entire region for all Agaricomycetes. Inside the 350 Kb segment, two spots showed high recombination in all four species. The first spot was the matA locus itself, the second spot formed a small gap in synteny located between C. cinerea genes CC1G_01875.3 and CC1G_01877.3 (both hypothetical genes) and their respective orthologues. Exemplary, one of the few genes that was repositioned in L. bicolor in comparison to C. cinerea was inserted in this gap. In F. velutipes and S. commune gene clusters were separated by inversion or translocation at both of these locations (Figure 4, 5, 6). Detailed comparison of the F. velutipes gene order to that of C. cinerea showed that the matA locus of F. velutipes was separated by inversion of two 70 Kb fragments directly left and right of FvHD1-1 and FvHD2-2 (Figure 4, 5). Modeling a reversion of those clusters reunited the Beta-flanking gene, FvHD2-1, MIP, FvHD1-1 and FvHD2-2 in a similar distribution as found in C. cinerea and L. bicolor. Notably, FvHD2-2 and FvHD1-1 were never moved during the rearrangements (Figure 5). Synteny mapping also revealed important differences between the matA regions of F. velutipes and S. commune. First, all S. commune homeodomain genes were repositioned, whereas FvHD2-2 and FvHD1-1 retained their position during rearrangements. This shows that the respective matA loci were split between different genes. Second, the S. commune fragments representing the first part of the high syntenic 350 Kb region, and whose rearangement caused separation of the matA subloci, constituted 140 Kb and 260 Kb (Figure 4, purple lines). This was significantly larger than the 70 Kb in F. velutipes (Figure 4, blue lines) and shows that different fragments were rearranged. Third, the S. commune fragments were wedged by sections not syntenic to the 350 Kb C. cinerea matA region (Figure 4, dotted light purple lines), which was not observed in F. velutipes.

Bottom Line: Regions near mating-type loci in fungi often show adapted recombination, facilitating the generation of novel mating types and reducing the production of self-compatible mating types.Next to this, it was revealed that large distance subloci can exist in matB as well.Finally, the genes that were linked to specific mating types will serve as molecular markers in breeding.

View Article: PubMed Central - PubMed

Affiliation: Mushroom Research Division, National Institute of Horticultural and Herbal Science, Rural Development Administration, Suwon, Republic of Korea.

ABSTRACT

Background: Mating-type loci of mushroom fungi contain master regulatory genes that control recognition between compatible nuclei, maintenance of compatible nuclei as heterokaryons, and fruiting body development. Regions near mating-type loci in fungi often show adapted recombination, facilitating the generation of novel mating types and reducing the production of self-compatible mating types. Compared to other fungi, mushroom fungi have complex mating-type systems, showing both loci with redundant function (subloci) and subloci with many alleles. The genomic organization of mating-type loci has been solved in very few mushroom species, which complicates proper interpretation of mating-type evolution and use of those genes in breeding programs.

Methodology/principal findings: We report a complete genetic structure of the mating-type loci from the tetrapolar, edible mushroom Flammulina velutipes mating type A3B3. Two matB3 subloci, matB3a that contains a unique pheromone and matB3b, were mapped 177 Kb apart on scaffold 1. The matA locus of F. velutipes contains three homeodomain genes distributed over 73 Kb distant matA3a and matA3b subloci. The conserved matA region in Agaricales approaches 350 Kb and contains conserved recombination hotspots showing major rearrangements in F. velutipes and Schizophyllum commune. Important evolutionary differences were indicated; separation of the matA subloci in F. velutipes was diverged from the Coprinopsis cinerea arrangement via two large inversions whereas separation in S. commune emerged through transposition of gene clusters.

Conclusions/significance: In our study we determined that the Agaricales have very large scale synteny at matA (∼350 Kb) and that this synteny is maintained even when parts of this region are separated through chromosomal rearrangements. Four conserved recombination hotspots allow reshuffling of large fragments of this region. Next to this, it was revealed that large distance subloci can exist in matB as well. Finally, the genes that were linked to specific mating types will serve as molecular markers in breeding.

Show MeSH
Related in: MedlinePlus