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Redefinition of straw mushroom Volvariella volvacea as a bipolar heterothallic fungus
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摘要
The straw mushroom Volvariella volvacea is an important crop in East and Southeast Asia.Determination of its mating system is particularly difficult because of multinucleate hyphae and lack of clamp connections.About forty years ago,the mating system of this mushroom has been defined as homothalism,yet this has been debated.In this studies,the basidiospore-forming patterns of 276 basidia were observed with a scanning electron microscope,showing that 193 basidia were tetrasporic,58 basidia were trisporic and 25 basidia were bisporic.If the four nuclei drived from meiosis were segregated randomly into basidiospore,a results could be ratiocinated that 7.23% of spores were heterokaryon,92.77% were homokaryon.The nuclei of 2859 basidiospores were examined by fluorescence microscopy,showing that 282 spores contained two nuclei and 2577 spores were mononuclear,it also be ratiocinated that 6.58% of spores could be heterokaryotic and 93.42% were monokaryotic.A single spore isolate(Pyd21) derived from Py1,a commercial strain,was sequenced(Solexa,de novo sequencing) and assembled as the reference genome sequence for V.volvacea.Another single spore isolate(Pyd15),also derived from Py1 and mating compatible with Pyd21,was re-sequenced.The genomes of these two strains,together with the available genome of strain V23-1(downloaded from NCBI) were used to analyze the MAT loci.Alignment of 50 Kb genomic regions that surrounded the MAT-A loci in PYd15,PYd21 and V23-1 revealed very high sequence conservation except MAT-A loci.High sequence polymorphism of HD1 and HD2 protein encoding genes and their mating type specific combinations indicated that MAT-A was involved in mating type discrimination.Synteny mapping showed that the high conservation of these regions over different strains with different mating types indicated that the presented organization is common for V.volvacea.MAT-B loci are typically composed of pheromone receptor and pheromone precursor genes.Homology searches using C.cinerea okayama7#130 pheromone receptors indicated four pheromone receptor genes(Vv STE3.1,Vv STE3.2,Vv STE3.3and Vv STE3.4) in V.volvacea PYd15 and PYd21 as well as in the genome of strain V23-1.In addition,a pheromone precursor gene(Vvphb1) was found 719 bp upstream in the flanking region of pheromone receptor Vv STE3.1 in strain PYd21.Identical sequences for Vvphb1 were detected in the genomes of PYd15 and V23-1 at the same relative position,demonstrating that V.volvacea in general has a complete MAT-B locus.Gene Vvphb1 was predicted to encode a 47 amino acid(AA) with a typical conserved Glutamic Acid(Glu,"E") positioned ~10 AA upstream of the C-terminal CAAX box,and can be expected to mature properly.Alignment of the Vv STE3.1(1424 bp,378 AA),Vv STE3.2(1567 bp,447AA),Vv STE3.3(1115 bp,333 AA) and Vv STE3.4(2155 bp,601 AA) pheromone receptor genes revealed 100% sequence identity between the respective homologues of PYd15,PYd21 and V23-1,except for one single nucleotide polymorphism(SNP) in Vv STE3.4.Thus,no allelic variation was found in the MAT-B loci of the three V.volvacea genomes.In addition,the A and B MAT loci of 14 more single spore isolates that were derived from 7 wild and commercial strains were amplified and sequenced.The sequences of all B mating-type genes showed very high identity that indicated they do not participate in mating-type discrimination.Meanwhile,a total of 8 different A mating-type loci,each consisting of a unique HD1-HD2 pair,were demonstrated to control mating as heterokaryotization only occurred between strains that contained different A loci.All our data together indicates that more than ninety percent of V.volvacea basidiospores were monokaryon,they needed mating with another compatible monokaryotic strain,and the compatibility was controlled by MAT-A only because of MAT-B were the same either wild strains or cultivation one.We can conclude that V.volvacea has a bipolar heterothallic mating system instead of homothalism.
The straw mushroom Volvariella volvacea is an important crop in East and Southeast Asia.Determination of its mating system is particularly difficult because of multinucleate hyphae and lack of clamp connections.About forty years ago,the mating system of this mushroom has been defined as homothalism,yet this has been debated.In this studies,the basidiospore-forming patterns of 276 basidia were observed with a scanning electron microscope,showing that 193 basidia were tetrasporic,58 basidia were trisporic and 25 basidia were bisporic.If the four nuclei drived from meiosis were segregated randomly into basidiospore,a results could be ratiocinated that 7.23% of spores were heterokaryon,92.77% were homokaryon.The nuclei of 2859 basidiospores were examined by fluorescence microscopy,showing that 282 spores contained two nuclei and 2577 spores were mononuclear,it also be ratiocinated that 6.58% of spores could be heterokaryotic and 93.42% were monokaryotic.A single spore isolate(Pyd21) derived from Py1,a commercial strain,was sequenced(Solexa,de novo sequencing) and assembled as the reference genome sequence for V.volvacea.Another single spore isolate(Pyd15),also derived from Py1 and mating compatible with Pyd21,was re-sequenced.The genomes of these two strains,together with the available genome of strain V23-1(downloaded from NCBI) were used to analyze the MAT loci.Alignment of 50 Kb genomic regions that surrounded the MAT-A loci in PYd15,PYd21 and V23-1 revealed very high sequence conservation except MAT-A loci.High sequence polymorphism of HD1 and HD2 protein encoding genes and their mating type specific combinations indicated that MAT-A was involved in mating type discrimination.Synteny mapping showed that the high conservation of these regions over different strains with different mating types indicated that the presented organization is common for V.volvacea.MAT-B loci are typically composed of pheromone receptor and pheromone precursor genes.Homology searches using C.cinerea okayama7#130 pheromone receptors indicated four pheromone receptor genes(Vv STE3.1,Vv STE3.2,Vv STE3.3and Vv STE3.4) in V.volvacea PYd15 and PYd21 as well as in the genome of strain V23-1.In addition,a pheromone precursor gene(Vvphb1) was found 719 bp upstream in the flanking region of pheromone receptor Vv STE3.1 in strain PYd21.Identical sequences for Vvphb1 were detected in the genomes of PYd15 and V23-1 at the same relative position,demonstrating that V.volvacea in general has a complete MAT-B locus.Gene Vvphb1 was predicted to encode a 47 amino acid(AA) with a typical conserved Glutamic Acid(Glu,"E") positioned ~10 AA upstream of the C-terminal CAAX box,and can be expected to mature properly.Alignment of the Vv STE3.1(1424 bp,378 AA),Vv STE3.2(1567 bp,447AA),Vv STE3.3(1115 bp,333 AA) and Vv STE3.4(2155 bp,601 AA) pheromone receptor genes revealed 100% sequence identity between the respective homologues of PYd15,PYd21 and V23-1,except for one single nucleotide polymorphism(SNP) in Vv STE3.4.Thus,no allelic variation was found in the MAT-B loci of the three V.volvacea genomes.In addition,the A and B MAT loci of 14 more single spore isolates that were derived from 7 wild and commercial strains were amplified and sequenced.The sequences of all B mating-type genes showed very high identity that indicated they do not participate in mating-type discrimination.Meanwhile,a total of 8 different A mating-type loci,each consisting of a unique HD1-HD2 pair,were demonstrated to control mating as heterokaryotization only occurred between strains that contained different A loci.All our data together indicates that more than ninety percent of V.volvacea basidiospores were monokaryon,they needed mating with another compatible monokaryotic strain,and the compatibility was controlled by MAT-A only because of MAT-B were the same either wild strains or cultivation one.We can conclude that V.volvacea has a bipolar heterothallic mating system instead of homothalism.
引文
[1]Bao,D.,M.Gong,H.Zheng,M.Chen,L.Zhang et al.,2013 Sequencing and comparative analysis of the straw mushroom(Volvariella volvacea)genome.PLo S One 8:e58294.
    [2]Chang,S.T.,and C.K.Yau,1971.Volvariella volvacea and its life history.Am.J.Bot.58:552-561.
    [3]Chang,S.T.,John A.Buswell and Siu-wai Chiu,1998.Mushroom biology and mushroom products.The Chinese University Press,Page 78.
    [4]Chen,B.,F.Gui,B.Xie,Y.Deng,X.Sun et al.,2013 Composition and expression of genes encoding carbohydrate-active enzymes in the straw-degrading mushroom Volvariella volvacea.PLo S One 8:e58780.
    [5]Chen B Z,Gui F,Xie B G,et al.Sequence and comparative analysis of the MIP gene in Chinese straw mushroom,Volvariella volvacea.Genome,2012,55(9):667-72.
    [6]Chen B.,van Peer A.F.,Yan J.,2016.Fruiting Body Formation in Volvariella volvacea Can Occur Independently of Its MAT-A-Controlled Bipolar Mating System,Enabling Homothallic and Heterothallic Life Cycles.G3,6(7):2135-2146.

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