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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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Synteny in matA regions of F. velutipes, C. cinerea, L. bicolor and S. commune.Syntenic mapping of the matA regions from F. velutipes (Fv), C. cinerea (Cc) and S. commune (Sc) in Chromomapper [41] reveals significant differences in gene arrangement. Distances are shown in kilo base pair (Kb) and F. velutipes contigs are depicted above the F. velutipes gene bar. A comparison of C. cinerea and L. bicolor (Lb) is shown in ‘panel A’ demonstrating the high synteny between those species. The black line under the gene bar of C. cinerea and above L. bicolor marks the 350 Kb, high syntenic region of in the figure and in panel A. MatA loci of all species are indicated by green boxes. Rearranged regions in F. velutipes and S. commune are indicated by blue and purple lines respectively. Dashed light purple lines in S. commune indicate non syntenic regions. Borders of the highly syntenic region can be clearly recognized by yellow genes in C. cinerea and coincide both with borders of rearranged gene clusters in F. velutipes and S. commune and with individually rearranged genes in L. bicolor (panel A). MatA loci (green) and a second spot (red triangle, red bars in panel A) are conserved sites of recombination in all four species. The gene order in F. velutipes and S. commune is changed by different events. F velutipes shows many inversions of gene clusters when compared to C. cinerea. S. commune shows rearrangements of larger, different gene groups. The overall gene orders of F. velutipes and S. commune are very similar to that of C. cinerea and L. bicolor which strongly suggests that these latter models represents an ancestral organization.
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pone-0022249-g004: Synteny in matA regions of F. velutipes, C. cinerea, L. bicolor and S. commune.Syntenic mapping of the matA regions from F. velutipes (Fv), C. cinerea (Cc) and S. commune (Sc) in Chromomapper [41] reveals significant differences in gene arrangement. Distances are shown in kilo base pair (Kb) and F. velutipes contigs are depicted above the F. velutipes gene bar. A comparison of C. cinerea and L. bicolor (Lb) is shown in ‘panel A’ demonstrating the high synteny between those species. The black line under the gene bar of C. cinerea and above L. bicolor marks the 350 Kb, high syntenic region of in the figure and in panel A. MatA loci of all species are indicated by green boxes. Rearranged regions in F. velutipes and S. commune are indicated by blue and purple lines respectively. Dashed light purple lines in S. commune indicate non syntenic regions. Borders of the highly syntenic region can be clearly recognized by yellow genes in C. cinerea and coincide both with borders of rearranged gene clusters in F. velutipes and S. commune and with individually rearranged genes in L. bicolor (panel A). MatA loci (green) and a second spot (red triangle, red bars in panel A) are conserved sites of recombination in all four species. The gene order in F. velutipes and S. commune is changed by different events. F velutipes shows many inversions of gene clusters when compared to C. cinerea. S. commune shows rearrangements of larger, different gene groups. The overall gene orders of F. velutipes and S. commune are very similar to that of C. cinerea and L. bicolor which strongly suggests that these latter models represents an ancestral organization.

Mentions: One F. velutipes HD1 gene (FvHD1-1), two HD2 genes (FvHD2-1, FvHD2-2) and the Mitochondrial Intermediate Peptidase (MIP) gene were identified in the F. velutipes genome located on a single contig; Fv01174 (Figure 4, Table S1). MIP was included because this gene is closely linked to HD genes in all Agaricomycetes [11], [12]. Analysis of the FvHD2-1 and FvHD2-2 gene models (accession codes in materials and methods) showed intron-exon distributions and long C-terminal exons similar to that of homeodomain gene a2-1 and b2-1 of C. cinerea [14]. The first and the second intron interrupted the homeodomain at the exact same locations in F. velutipes and C. cinerea. The second introns have been reported to be conserved in several other basidiomycetes as well [7], [14], [48], [49]. FvHD1-1 (six predicted introns) showed no intron-exon resemblance to C. cinerea HD1 genes associated with a2-1 and b2-1. No reliable coiled coils (less than 20–30% drops in the probability between weighted/non-weighted analysis) that could indicate dimerization motifs were found in the F. velutipes HD genes but nine-amino acid transactivation domains were detected in the N-termini of FvHd1-1, FvHd2-1 and FvHd2-2 (Table S3). These domains are generally found in mammalian and yeast transcription factors [40]. FvHd1-1, FvHd2-1 and FvHd2-2 were further predicted to contain single and or bipartite nuclear localization signals (Table S3).


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 in matA regions of F. velutipes, C. cinerea, L. bicolor and S. commune.Syntenic mapping of the matA regions from F. velutipes (Fv), C. cinerea (Cc) and S. commune (Sc) in Chromomapper [41] reveals significant differences in gene arrangement. Distances are shown in kilo base pair (Kb) and F. velutipes contigs are depicted above the F. velutipes gene bar. A comparison of C. cinerea and L. bicolor (Lb) is shown in ‘panel A’ demonstrating the high synteny between those species. The black line under the gene bar of C. cinerea and above L. bicolor marks the 350 Kb, high syntenic region of in the figure and in panel A. MatA loci of all species are indicated by green boxes. Rearranged regions in F. velutipes and S. commune are indicated by blue and purple lines respectively. Dashed light purple lines in S. commune indicate non syntenic regions. Borders of the highly syntenic region can be clearly recognized by yellow genes in C. cinerea and coincide both with borders of rearranged gene clusters in F. velutipes and S. commune and with individually rearranged genes in L. bicolor (panel A). MatA loci (green) and a second spot (red triangle, red bars in panel A) are conserved sites of recombination in all four species. The gene order in F. velutipes and S. commune is changed by different events. F velutipes shows many inversions of gene clusters when compared to C. cinerea. S. commune shows rearrangements of larger, different gene groups. The overall gene orders of F. velutipes and S. commune are very similar to that of C. cinerea and L. bicolor which strongly suggests that these latter models represents an ancestral organization.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3140503&req=5

pone-0022249-g004: Synteny in matA regions of F. velutipes, C. cinerea, L. bicolor and S. commune.Syntenic mapping of the matA regions from F. velutipes (Fv), C. cinerea (Cc) and S. commune (Sc) in Chromomapper [41] reveals significant differences in gene arrangement. Distances are shown in kilo base pair (Kb) and F. velutipes contigs are depicted above the F. velutipes gene bar. A comparison of C. cinerea and L. bicolor (Lb) is shown in ‘panel A’ demonstrating the high synteny between those species. The black line under the gene bar of C. cinerea and above L. bicolor marks the 350 Kb, high syntenic region of in the figure and in panel A. MatA loci of all species are indicated by green boxes. Rearranged regions in F. velutipes and S. commune are indicated by blue and purple lines respectively. Dashed light purple lines in S. commune indicate non syntenic regions. Borders of the highly syntenic region can be clearly recognized by yellow genes in C. cinerea and coincide both with borders of rearranged gene clusters in F. velutipes and S. commune and with individually rearranged genes in L. bicolor (panel A). MatA loci (green) and a second spot (red triangle, red bars in panel A) are conserved sites of recombination in all four species. The gene order in F. velutipes and S. commune is changed by different events. F velutipes shows many inversions of gene clusters when compared to C. cinerea. S. commune shows rearrangements of larger, different gene groups. The overall gene orders of F. velutipes and S. commune are very similar to that of C. cinerea and L. bicolor which strongly suggests that these latter models represents an ancestral organization.
Mentions: One F. velutipes HD1 gene (FvHD1-1), two HD2 genes (FvHD2-1, FvHD2-2) and the Mitochondrial Intermediate Peptidase (MIP) gene were identified in the F. velutipes genome located on a single contig; Fv01174 (Figure 4, Table S1). MIP was included because this gene is closely linked to HD genes in all Agaricomycetes [11], [12]. Analysis of the FvHD2-1 and FvHD2-2 gene models (accession codes in materials and methods) showed intron-exon distributions and long C-terminal exons similar to that of homeodomain gene a2-1 and b2-1 of C. cinerea [14]. The first and the second intron interrupted the homeodomain at the exact same locations in F. velutipes and C. cinerea. The second introns have been reported to be conserved in several other basidiomycetes as well [7], [14], [48], [49]. FvHD1-1 (six predicted introns) showed no intron-exon resemblance to C. cinerea HD1 genes associated with a2-1 and b2-1. No reliable coiled coils (less than 20–30% drops in the probability between weighted/non-weighted analysis) that could indicate dimerization motifs were found in the F. velutipes HD genes but nine-amino acid transactivation domains were detected in the N-termini of FvHd1-1, FvHd2-1 and FvHd2-2 (Table S3). These domains are generally found in mammalian and yeast transcription factors [40]. FvHd1-1, FvHd2-1 and FvHd2-2 were further predicted to contain single and or bipartite nuclear localization signals (Table S3).

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