Advances in Understanding Mating Type Gene Organization in the Mushroom-Forming Fungus<i>Flammulina velutipes</i>

Wang, Wei; Lian, Li; Xu, Ping; Chou, Tiansheng; Mukhtar, Irum; Aron, Osakina; Waqas, Muhammad Mohsin; Chen, Bingzhi; Liu, Xinrui; Liu, Fang; Xie, Baogui; Peer, Arend F. van

doi:10.1534/g3.116.034637

Cited by 26 publications

(47 citation statements)

References 66 publications

(109 reference statements)

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“…Six genes, encoding putative pheromone receptors, were downregulated in the pdd1 knockdown strain based on the RNA-seq analysis. FvSTE3.1 and FvSTE3.2 were pheromone receptors; the others (FvSTE3.s3, FvSTE3.s4, FvSTE3.s5, and FvSTE3.s6) were pheromone-receptor-like proteins (38). Further qPCR analysis performed using ␤-actin and gpd as the reference genes also showed that the transcriptional levels of six genes were reduced in the pdd1 knockdown strain compared to the wild-type strain in mycelia after the induction of basidioma development ( Fig.…”

Section: Figmentioning

confidence: 89%

A Single Transcription Factor (PDD1) Determines Development and Yield of Winter Mushroom ( Flammulina velutipes )

Xie

et al. 2019

Appl Environ Microbiol

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Most of the edible mushrooms cannot be cultivated or have low yield under industrial conditions, partially due to the lack of knowledge on how basidioma (fruiting body) development is regulated. From winter mushroom (Flammulina velutipes), one of the most popular industrially cultivated mushrooms, a transcription factor, PDD1, with a high-mobility group (HMG)-box domain was identified based on its increased transcription during basidioma development. pdd1 knockdown by RNA interference affected vegetative growth and dramatically impaired basidioma development. A strain with an 89.9% reduction in the level of pdd1 transcription failed to produce primordia, while overexpression of pdd1 promoted basidioma development. When the transcriptional level of pdd1 was increased to 5 times the base level, the mushroom cultivation time was shortened by 9.8% and the yield was increased by at least 33%. RNA sequencing (RNA-seq) analysis revealed that pdd1 knockdown downregulated 331 genes and upregulated 463 genes. PDD1 positively regulated several genes related to fruiting, including 6 pheromone receptor-encoding genes, 3 jacalin-related lectin-encoding genes, FVFD16, and 2 FVFD16 homolog-encoding genes. PDD1 is a novel transcription factor with regulatory function in basidioma development found in industrially cultivated mushrooms. Since its orthologs are widely present in fungal species of the Basidiomycota phylum, PDD1 might have important application prospects in mushroom breeding. IMPORTANCE Mushrooms are sources of food and medicine and provide abundant nutrients and bioactive compounds. However, most of the edible mushrooms cannot be cultivated commercially due to the limited understanding of basidioma development. From winter mushroom (Flammulina velutipes; also known as Enokitake), one of the most commonly cultivated mushrooms, we identified a novel transcription factor, PDD1, positively regulating basidioma development. PDD1 increases expression during basidioma development. Artificially increasing its expression promoted basidioma formation and dramatically increased mushroom yield, while reducing its expression dramatically impaired its development. In its PDD1 overexpression mutants, mushroom number, height, yield, and biological efficiency were significantly increased. PDD1 regulates the expression of some genes that are important in or related to basidioma development. PDD1 is the first identified transcription factor with defined functions in mushroom development among commercially cultivated mushroom species, and it might be useful in mushroom breeding.

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Section: Figmentioning

confidence: 89%

A Single Transcription Factor (PDD1) Determines Development and Yield of Winter Mushroom ( Flammulina velutipes )

Xie

et al. 2019

Appl Environ Microbiol

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“…Previous studies revealed molecular details in fruiting body development in Flammulina species at the transcriptome, proteome, single gene or protein level [20,[35][36][37][38][39]. A series of genes associated with mushroom formation, including the mating type genes, hydrophobins, and fruiting body specific genes have been identified [20,31,40]. Researches also investigated at least two genes controlling fruiting at >15˚C based on hybridization analysis [34].…”

Section: Introductionmentioning

confidence: 99%

Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis

Liu

Xia

et al. 2020

PLoS ONE

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Mushroom-forming fungi are complex multicellular organisms that form the basis of a large industry, yet, our understanding of the mechanisms of mushroom development and its responses to various stresses remains limited. The winter mushroom (Flammulina filiformis) is cultivated at a large commercial scale in East Asia and is a species with a preference for low temperatures. This study investigated fruiting body development in F. filiformis by comparing transcriptomes of 4 developmental stages, and compared the developmental genes to a 200-genome dataset to identify conserved genes involved in fruiting body development, and examined the response of heat sensitive and-resistant strains to heat stress. Our data revealed widely conserved genes involved in primordium development of F. filiformis, many of which originated before the emergence of the Agaricomycetes, indicating co-option for complex multicellularity during evolution. We also revealed several notable fruiting-specific genes, including the genes with conserved stipe-specific expression patterns and the others which related to sexual development, water absorption, basidium formation and sporulation, among others. Comparative analysis revealed that heat stress induced more genes in the heat resistant strain (M1) than in the heat sensitive one (XR). Of particular importance are the hsp70, hsp90 and fes1 genes, which may facilitate the adjustment to heat stress in the early stages of fruiting body development. These data highlighted novel genes involved in complex multicellular development in fungi and aid further studies on gene function and efforts to improve the productivity and heat tolerance in mushroom-forming fungi.

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“…Mating in basidiomycetous fungi is controlled by sets of specialized genes that are located at mating type (MAT) loci called MAT-A and MAT-B (Raper, 1966; Brown & Casselton, 2001; Raudaskoski & Kothe, 2010; Kües, James & Heitman, 2011; Raudaskoski, 2015), more recently referred to as HD (homeodomain) and PR (pheromone receptor) loci, respectively (Maia et al, 2015; Wang et al, 2016). Genes at these loci control the HD or PR mating type pathways that regulate various steps in the formation of a dikaryon and in sexual reproduction (Kües, James & Heitman, 2011; Kües, 2015; Maia et al, 2015; Coelho et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…These subloci are commonly di-or multiallelic when active (Kües, James & Heitman, 2011; Kües, 2015; Coelho et al, 2017). Heterozygosity at one of the subloci within the HD and one of the subloci in the PR locus, is generally sufficient to activate the corresponding mating type pathways, and does so in Flammulina velutipes (Kües, 2015; Wang et al, 2016). The genetic structure and control of the PR mating type pathway of F. velutipes has been attributed to two PR subloci: PR-a and PR-b.…”

Section: Introductionmentioning

confidence: 99%

“…The genetic structure and control of the PR mating type pathway of F. velutipes has been attributed to two PR subloci: PR-a and PR-b. The PR-a and PR-b-subloci are located on chromosome 3 at a distance of about 180 kb (van Peer et al, 2011; Wang et al, 2016). Both PR subloci have been found to be multiallelic, and to contain varying combinations of pheromone receptor ( FvSTE3 ) and pheromone precursor ( FvPp ) genes.…”

Section: Introductionmentioning

confidence: 99%

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A second HD mating type sublocus of Flammulina velutipes is at least di-allelic and active: new primers for identification of HD-a and HD-b subloci

Wang

Mukhtar

Chou

et al. 2019

PeerJ

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Background Sexual development in Flammulina velutipes is controlled by two different mating type loci (HD and PR). The HD locus contains homeodomain (Hd) genes on two separate HD subloci: HD-a and HD-b. While the functionality of the HD-b sublocus has been largely confirmed, the status and content of the HD-a sublocus has remained unclear. Methods To examine the function of the HD-a sublocus, genome sequences of a series of F. velutipes strains were analyzed and tested through series of amplification by specific primer sets. Furthermore, activity of di-allelic HD-a locus was confirmed by crossing strains with different combinations of HD-a and HD-b subloci. Results Sublocus HD-b contained a large variety of fixed Hd1/Hd2 gene pairs, while the HD-a sublocus either contained a conserved Hd2 gene or, a newly discovered Hd1 gene that was also conserved. Identification of whole HD loci, that is, the contents of HD-a and HD-b subloci in a strain, revealed that strains with similar HD-b subloci could still form normal dikaryons if the two genes at the HD-a sublocus differed. At least di-allelic HD-a sublocus, is thus indicated to be actively involved in mating type compatibility. Conclusions HD-a sublocus is active and di-allelic. Using the new information on the HD subloci, primers sets were developed that specifically amplify HD-a or HD-b subloci in the majority of F. velutipes strains. In this way, unknown HD mating types of F. velutipes can now be quickly identified, and HD mating type compatibility conferred by HD-a or HD-b can be confirmed by PCR.

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Advances in Understanding Mating Type Gene Organization in the Mushroom-Forming FungusFlammulina velutipes

Cited by 26 publications

References 66 publications

A Single Transcription Factor (PDD1) Determines Development and Yield of Winter Mushroom ( Flammulina velutipes )

A Single Transcription Factor (PDD1) Determines Development and Yield of Winter Mushroom ( Flammulina velutipes )

Transcriptome data reveal conserved patterns of fruiting body development and response to heat stress in the mushroom-forming fungus Flammulina filiformis

A second HD mating type sublocus of Flammulina velutipes is at least di-allelic and active: new primers for identification of HD-a and HD-b subloci

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