Transcriptome Analysis Reveals the Function of a G-Protein α Subunit Gene in the Growth and Development of Pleurotus eryngii

Pleurotus eryngii is a commercially important edible fungus with high nutritional and economic value. However, few functional studies have examined key genes affecting the growth and development of P. eryngii. In this study, transformed strains, including over-expression (PeGNAI-OE) and RNA interference (PeGNAI-RNAi) lines, were constructed to elucidate the role of GNAI in P. eryngii growth. GNAI expression was found to affect the mycelial growth and the number of clamp connections. Moreover, the transformed strains were shown to have higher endogenous cAMP levels, thus affecting amylase and laccase activity. Fruiting experiments showed that GNAI expression revealed the formation of P. eryngii primordia and the number of buttons, while transcription analysis identified GNAI gene involvement in the growth and development of P. eryngii. Seven downstream genes regulated by GNAI were differentially expressed in PeGNAI-OE and PeGNAI-RNAi compared to wild type (WT). These genes may be related to mycelial growth and enzyme activity. They were involved in the MAPK signaling pathway, inositol phosphate metabolism, ascorbate, aldarate metabolism, and starch and sucrose metabolism. In summary, GNAI performs different physiological functions in regulating the growth and development of P. eryngii. Importantly, the molecular mechanisms of GNAI regulatory function are relatively complex and need further study.

[1]  Yang Yang,et al.  Insights into intracellular signaling network in Fusarium species. , 2022, International journal of biological macromolecules.

[2]  Yongxin Tao,et al.  Flammulina filiformis Pkac Gene Complementing in Neurospora crassa Mutant Reveals Its Function in Mycelial Growth and Abiotic Stress Response , 2022, Life.

[3]  G. Zervakis,et al.  Genoprotective activity of the Pleurotus eryngii mushrooms following their in vitro and in vivo fermentation by fecal microbiota , 2022, Frontiers in Nutrition.

[4]  Jianbo Xie,et al.  Bacterial Infection Induces Ultrastructural and Transcriptional Changes in the King Oyster Mushroom (Pleurotus eryngii) , 2022, Microbiology spectrum.

[5]  B. Adelodun,et al.  Kinetic Studies on Delignification and Heavy Metals Uptake by Shiitake (Lentinula edodes) Mushroom Cultivated on Agro-Industrial Wastes , 2022, Horticulturae.

[6]  Meng Wang,et al.  FFGA1 Protein Is Essential for Regulating Vegetative Growth, Cell Wall Integrity, and Protection against Stress in Flammunina filiformis , 2022, Journal of fungi.

[7]  Zhijie Bao,et al.  Nitric oxide enhances resistance of Pleurotus eryngii to cadmium stress by alleviating oxidative damage and regulating of short-chain dehydrogenase/reductase family , 2022, Environmental Science and Pollution Research.

[8]  Liding Chen,et al.  Bacterial Community Composition in the Growth Process of Pleurotus eryngii and Growth-Promoting Abilities of Isolated Bacteria , 2022, Frontiers in Microbiology.

[9]  Xiaozhao Wang,et al.  Antifungal activity of 1-octen-3-ol against Monilinia fructicola and its ability in enhancing disease resistance of peach fruit , 2022, Food Control.

[10]  T. Hu,et al.  Host-Induced Gene Silencing of a G Protein α Subunit Gene CsGpa1 Involved in Pathogen Appressoria Formation and Virulence Improves Tobacco Resistance to Ciboria shiraiana. , 2021, Journal of fungi.

[11]  C. Camacho,et al.  A specific inhibitor of ALDH1A3 regulates retinoic acid biosynthesis in glioma stem cells , 2021, Communications Biology.

[12]  Qingxiu Hu,et al.  Transcriptomics Analysis of Primordium Formation in Pleurotus eryngii , 2021, Genes.

[13]  Dongmei Liu,et al.  Characterization of a G protein α subunit encoded gene from the dimorphic fungus-Tremella fuciformis , 2021, Antonie van Leeuwenhoek.

[14]  E. Kothe,et al.  Inositol Signaling in the Basidiomycete Fungus Schizophyllum commune , 2021, Journal of fungi.

[15]  Jin-Rong Xu,et al.  Coregulation of dimorphism and symbiosis by cyclic AMP signaling in the lichenized fungus Umbilicaria muhlenbergii , 2020, Proceedings of the National Academy of Sciences.

[16]  A. Geng,et al.  CRISPR-Cas9-mediated seb1 disruption in Talaromyces pinophilus EMU for its enhanced cellulase production. , 2020, Enzyme and microbial technology.

[17]  K. Chung,et al.  Structural mechanism underlying primary and secondary coupling between GPCRs and the Gi/o family , 2020, Nature Communications.

[18]  Soo Chan Lee,et al.  The heterotrimeric G-protein beta subunit Gpb1 controls hyphal growth under low oxygen conditions through the protein kinase A pathway and is essential for virulence in the fungus Mucor circinelloides. , 2020, Cellular microbiology.

[19]  I. Ahmad,et al.  Structural characterization and bioactivities of a polysaccharide from the stalk residue of Pleurotus eryngii , 2020, Food Science and Technology.

[20]  Y. Choi,et al.  Comparative Characterization of G Protein α Subunits in Aspergillus fumigatus , 2020, Pathogens.

[21]  Hao Wu,et al.  G-Protein Subunit Gαi in Mitochondria, MrGPA1, Affects Conidiation, Stress Resistance, and Virulence of Entomopathogenic Fungus Metarhizium robertsii , 2020, Frontiers in Microbiology.

[22]  Shujing Sun,et al.  Cyclic Dipeptides Mediating Quorum Sensing and Their Biological Effects in Hypsizygus Marmoreus , 2020, Biomolecules.

[23]  F. Govers,et al.  G protein α subunit suppresses sporangium formation through a serine/threonine protein kinase in Phytophthora sojae , 2020, PLoS pathogens.

[24]  R. Linhardt,et al.  Extraction, structure and bioactivities of the polysaccharides from Pleurotus eryngii: A Review. , 2019, International journal of biological macromolecules.

[25]  T. Goswami,et al.  Exploring the lignolytic potential of a new laccase producing strain Kocuria sp. PBS-1 and its application in bamboo pulp bleaching , 2019, International Biodeterioration & Biodegradation.

[26]  Wei Gao,et al.  Expression patterns of two pal genes of Pleurotus ostreatus across developmental stages and under heat stress , 2019, BMC Microbiology.

[27]  Fusheng Chen,et al.  Effects of Different G-Protein α-Subunits on Growth, Development and Secondary Metabolism of Monascus ruber M7 , 2019, Front. Microbiol..

[28]  Ping Wang,et al.  The seven transmembrane domain protein MoRgs7 functions in surface perception and undergoes coronin MoCrn1-dependent endocytosis in complex with Gα subunit MoMagA to promote cAMP signaling and appressorium formation in Magnaporthe oryzae , 2018, bioRxiv.

[29]  E. Kothe,et al.  The regulator of G‐protein signalling Thn1 links pheromone response to volatile production in Schizophyllum commune , 2018, Environmental microbiology.

[30]  K. Furuya,et al.  The Ras1-Cdc42 pathway is involved in hyphal development of Schizosaccharomyces japonicus , 2018, FEMS yeast research.

[31]  Yanjie Liu,et al.  Regulation of the Gα-cAMP/PKA signaling pathway in cellulose utilization of Chaetomium globosum , 2018, Microbial Cell Factories.

[32]  Yanjie Liu,et al.  Gα-cAMP/PKA pathway positively regulates pigmentation, chaetoglobosin A biosynthesis and sexual development in Chaetomium globosum , 2018, PloS one.

[33]  Yuxian Xia,et al.  The Ste12-like transcription factor MaSte12 is involved in pathogenicity by regulating the appressorium formation in the entomopathogenic fungus, Metarhizium acridum , 2017, Applied Microbiology and Biotechnology.

[34]  D. Martínez-Soto,et al.  Functional analysis of the MAPK pathways in fungi. , 2017, Revista iberoamericana de micologia.

[35]  Yu Li,et al.  Comparative Transcriptome Analysis Identified Candidate Genes Related to Bailinggu Mushroom Formation and Genetic Markers for Genetic Analyses and Breeding , 2017, Scientific Reports.

[36]  P. Bommert,et al.  G protein signaling in plants: minus times minus equals plus. , 2016, Current opinion in plant biology.

[37]  R. Dey,et al.  Regulation, Signaling, and Physiological Functions of G-Proteins. , 2016, Journal of molecular biology.

[38]  J. Fontaine,et al.  Arbuscular mycorrhizal fungal responses to abiotic stresses: A review. , 2016, Phytochemistry.

[39]  Jarrod R. Fortwendel,et al.  Orchestration of Morphogenesis in Filamentous Fungi: Conserved Roles for Ras Signaling Networks. , 2015, Fungal biology reviews.

[40]  Z. Cao,et al.  StSTE12 is required for the pathogenicity of Setosphaeria turcica by regulating appressorium development and penetration. , 2014, Microbiological research.

[41]  Y. Honda,et al.  The White-Rot Fungus Pleurotus ostreatus Transformant Overproduced Intracellular cAMP and Laccase , 2013, Bioscience, biotechnology and biochemistry.

[42]  Y. Qu,et al.  G protein-cAMP signaling pathway mediated by PGA3 plays different roles in regulating the expressions of amylases and cellulases in Penicillium decumbens. , 2013, Fungal genetics and biology : FG & B.

[43]  A. Ram,et al.  Functional characterization of Rho GTPases in Aspergillus niger uncovers conserved and diverged roles of Rho proteins within filamentous fungi , 2011, Molecular microbiology.

[44]  Linghuo Jiang,et al.  FgTep1p is linked to the phosphatidylinositol-3 kinase signalling pathway and plays a role in the virulence of Fusarium graminearum on wheat. , 2010, Molecular plant pathology.

[45]  C. Nombela,et al.  The Sko1 protein represses the yeast-to-hypha transition and regulates the oxidative stress response in Candida albicans. , 2010, Fungal genetics and biology : FG & B.

[46]  Yaosong Wang,et al.  Effect of different packaging films on postharvest quality and selected enzyme activities of Hypsizygus marmoreus mushrooms. , 2008, Journal of agricultural and food chemistry.

[47]  Anne J. Ridley,et al.  Mammalian Rho GTPases: new insights into their functions from in vivo studies , 2008, Nature Reviews Molecular Cell Biology.

[48]  K. Borkovich,et al.  Heterotrimeric G protein signaling in filamentous fungi. , 2007, Annual review of microbiology.

[49]  K. Neve,et al.  Sensitization of adenylate cyclase by Gαi/o-coupled receptors , 2005 .

[50]  D. Siderovski,et al.  G-protein signaling: back to the future , 2005, Cellular and Molecular Life Sciences.

[51]  J. Perfect,et al.  Gpr1, a Putative G-Protein-Coupled Receptor, Regulates Morphogenesis and Hypha Formation in the Pathogenic Fungus Candida albicans , 2004, Eukaryotic Cell.

[52]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[53]  J. Heitman,et al.  Conserved cAMP signaling cascades regulate fungal development and virulence. , 2001, FEMS microbiology reviews.

[54]  G. C. Johnston,et al.  TEP1, the yeast homolog of the human tumor suppressor gene PTEN/MMAC1/TEP1, is linked to the phosphatidylinositol pathway and plays a role in the developmental process of sporulation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[55]  U. Kües,et al.  Fruiting body production in basidiomycetes , 2000, Applied Microbiology and Biotechnology.

[56]  S. Fields,et al.  The yeast STE12 protein binds to the DNA sequence mediating pheromone induction. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Mingwen Zhao,et al.  Development of a simple and efficient transformation system for the basidiomycetous medicinal fungus Ganoderma lucidum , 2012, World journal of microbiology & biotechnology.

[58]  Thomas D. Schmittgen,et al.  Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2 2 DD C T Method , 2022 .