2,104
Views
22
CrossRef citations to date
0
Altmetric
Research Paper

Functional analysis of seven regulators of G protein signaling (RGSs) in the nematode-trapping fungus Arthrobotrys oligospora

, , , , , , , & show all
Pages 1825-1840 | Received 31 Dec 2020, Accepted 18 Jun 2021, Published online: 05 Jul 2021

References

  • Li LD, Wright SJ, Krystofova S, et al. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol. 2007;61:423–452.
  • Wang Y, Geng Z, Jiang D, et al. Characterizations and functions of regulator of G protein signaling (RGS) in fungi. Appl Microbiol Biotechnol. 2013;97(18):7977–7987.
  • Brown NA, Schrevens S, van Dijck P, et al. Fungal G-protein-coupled receptors: mediators of pathogenesis and targets for disease control. Nat Microbiol. 2018;3(4):402–414.
  • Tong Y, Wu H, Liu Z, et al. G-protein subunit Gαi in mitochondria, MrGPA1, affects conidiation, stress resistance, and virulence of entomopathogenic fungus Metarhizium robertsii. Front Microbiol. 2020;11:1251.
  • Liu S, Dean RA. G protein α subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant Microbe Interact. 1997;10(9):1075–1086.
  • Liebmann B, Müller M, Braun A, et al. The Cyclic AMP-dependent protein kinase a network regulates development and virulence in Aspergillus fumigatus. Infect Immun. 2004;72(9):5193–5203.
  • Shin KS, Kwon NJ, Yu JH. Gβγ-mediated growth and developmental control in Aspergillus fumigatus. Curr Genet. 2009;55(6):631–641.
  • Koelle MR. A new family of G-protein regulators–the RGS proteins. Curr Opin Cell Biol. 1997;9(2):143–147.
  • Berman DM, Gilman AG. Mammalian RGS proteins: barbarians at the gate. J Biol Chem. 1998;273(3):1269–1272.
  • Hepler JR. Emerging roles for RGS proteins in cell signalling. Trends Pharmacol Sci. 1999;20(9):376–382.
  • De Vries L, Zheng B, Fischer T, et al. The regulator of G protein signaling family. Annu Rev Pharmacol Toxicol. 2000;40:235–271.
  • Park HS, Kim MJ, Yu JH, et al. Heterotrimeric G-protein signalers and RGSs in Aspergillus fumigatus. Pathogens. 2020;9(11):902.
  • Dohlman HG, Song J, Ma D, et al. Sst2, a negative regulator of pheromone signaling in the yeast Saccharomyces cerevisiae: expression, localization, and genetic interaction and physical association with Gpa1 (the G-protein alpha subunit). Mol Cell Biol. 1996;16(9):194–5209.
  • Park AR, Cho AR, Seo JA, et al. Functional analyses of regulators of G protein signaling in Gibberella zeae. Fungal Genet Biol. 2012;49(7):511–520.
  • Han KH, Seo JA, Yu JH. Regulators of G-protein signalling in Aspergillus nidulans: rgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Gα) signalling. Mol Microbiol. 2004;53(2):529–540.
  • Heterotrimeric YJ. G protein signaling and RGSs in Aspergillus nidulans. J Microbiol. 2006;44(2):145–154.
  • Zhang H, Tang W, Liu K, et al. Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaporthe oryzae. PLoS Pathog. 2011;7(12):e1002450. .
  • Nordbring-Hertz B, Jansson HB, Tunlid A. Nematophagous fungi. In: Encyclopedia of Life Sciences. Chichester, OH: JohnWiley & Sons; 2011. p. 1–13.
  • Su H, Zhao Y, Zhou J, et al. Trapping devices of nematode-trapping fungi: formation, evolution, and genomic perspectives. Biol Rev. 2017;92(1):357–368.
  • Yang CT, Vidal-Diez de Ulzurrun G, Gonçalves AP, et al. Natural diversity in the predatory behavior facilitates the establishment of a robust model strain for nematode-trapping fungi. Proc Natl Acad Sci USA. 2020;117(12):6762–6770.
  • Ji X, Yu Z, Yang J, et al. Expansion of adhesion genes drives pathogenic adaptation of nematode-trapping fungi. iScience. 2020;23(5):101057.
  • Yang JK, Wang L, Ji X, et al. Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathog. 2011;7(9):e1002179. .
  • Zhen Z, Xing X, Xie M, et al. MAP kinase Slt2 orthologs play similar roles in conidiation, trap formation, and pathogenicity in two nematode-trapping fungi. Fungal Genet Biol. 2018;116:42–50.
  • Kuo CY, Chen SA, Hsueh YP. The high osmolarity glycerol (HOG) pathway functions in osmosensing, trap morphogenesis and conidiation of the nematode-trapping fungus Arthrobotrys oligospora. J Fungi. 2020;6(4):191.
  • Xie M, Bai N, Yang J, et al. Protein kinase Ime2 is required for mycelial growth, conidiation, osmoregulation, and pathogenicity in nematode-trapping fungus Arthrobotrys oligospora. Front Microbiol. 2020;10:3065.
  • Zhen Z, Zhang G, Yang L, et al. Characterization and functional analysis of calcium/calmodulin-dependent protein kinases (CaMKs) in the nematode-trapping fungus Arthrobotrys oligospora. Appl Microbiol Biotechnol. 2019;103(2):819–832.
  • Colot HV, Park G, Turner GE, et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA. 2006;103(27):10352–10357.
  • Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–1874.
  • Tunlid A, Åhman J, Oliver RP. Transformation of the nematode-trapping fungus Arthrobotrys oligospora. FEMS Microbiol Lett. 1999;173(1):111–116.
  • Yang X, Ma N, Yang L, et al. Two Rab GTPases play different roles in conidiation, trap formation, stress resistance, and virulence in the nematode-trapping fungus Arthrobotrys oligospora. Appl Microbiol Biotechnol. 2018;102(10):4601–4613.
  • Xie M, Wang Y, Tang L, et al. AoStuA, an APSES transcription factor, regulates the conidiation, trap formation, stress resistance and pathogenicity of the nematode-trapping fungus Arthrobotrys oligospora. Environ Microbiol. 2019;21(12):4648–4661. .
  • Ma Y, Yang X, Xie M, et al. The Arf-GAP AoGlo3 regulates conidiation, endocytosis, and pathogenicity in the nematode-trapping fungus Arthrobotrys oligospora. Fungal Genet Biol. 2020;138:103352.
  • Liu J, Wang ZK, Sun HH, et al. Characterization of the Hog1 MAPK pathway in the entomopathogenic fungus Beauveria bassiana. Environ Microbiol. 2017;19(5):808–1821.
  • Mitchison JM, Nurse P. Growth in cell length in the fission yeast Schizosaccharomyces pombe. J Cell Sci. 1985;75:357–376.
  • Li C, Melesse M, Zhang S, et al. FgCDC14 regulates cytokinesis, morphogenesis, and pathogenesis in Fusarium graminearum. Mol Microbiol. 2015;98(4):770–786.
  • Xie M, Yang J, Jiang K, et al. AoBck1 and AoMkk1 are necessary to maintain cell wall integrity, vegetative growth, conidiation, stress resistance, and pathogenicity in the nematode-trapping fungus Arthrobotrys oligospora. Front Microbiol. 2021. DOI:10.3389/fmicb.2021.649582.
  • Liu H, Suresh A, Willard FS, et al. Rgs1 regulates multiple G alpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. EMBO J. 2007;26(3):690–700.
  • Yang J, Yu Y, Li J, et al. Characterization and functional analyses of the chitinase-encoding genes in the nematode-trapping fungus Arthrobotrys oligospora. Arch Microbiol. 2013;195(7):453–462. .
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 2001;25:402–408.
  • Klopfenstein DV, Zhang L, Pedersen BS, et al. GOATOOLS: a Python library for Gene Ontology analyses. Sci Rep. 2018;8(1):10872.
  • Kanehisa M, Furumichi M, Tanabe M, et al. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–D361.
  • Gao BJ, Mou YN, Tong SM, et al. Subtilisin-like Pr1 proteases marking the evolution of pathogenicity in a wide-spectrum insect-pathogenic fungus. Virulence. 2020;11(1):365–380.
  • Cao Y, Zhu X, Jiao R, et al. The Magas1 gene is involved in pathogenesis by affecting penetration in Metarhizium acridum. J Microbiol Biotechnol. 2012;22(7):889–893.
  • Xue C, Park G, Choi W, et al. Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell. 2002;14(9):2107–2119.
  • Bölker M. Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol. 1998;25(3):143–156.
  • Mukherjee M, Kim JE, Park YS, et al. Regulators of G-protein signalling in Fusarium verticillioides mediate differential host-pathogen responses on nonviable versus viable maize kernels. Mol Plant Pathol. 2011;12(5):479–491.
  • Yu JH, Wieser J, Adams TH. The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development. EMBO J. 1996;15(19):5184–5190.
  • Lwin HP, Choi YH, Lee MW, et al. RgsA attenuates the PKA signaling, stress response, and virulence in the human opportunistic pathogen Aspergillus fumigatus. Int J Mol Sci. 2019;20(22):5628.
  • Ramanujam R, Naqvi NI. PdeH, a high-affinity cAMP phosphodiesterase, is a key regulator of asexual and pathogenic differentiation in Magnaporthe oryzae. PLoS Pathog. 2010;6(5):e1000897.
  • Xu JR, Hamer JE. MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev. 1996;10(21):2696–2706.
  • Ding JL, Hou J, Feng MG, et al. Transcriptomic analyses reveal comprehensive responses of insect hemocytes to mycopathogen Beauveria bassiana, and fungal virulence-related cell wall protein assists pathogen to evade host cellular defense. Virulence. 2020;11(1):1352–1365.
  • Zhang H, Ma H, Xie X, et al. Comparative proteomic analyses reveal that the regulators of G-protein signaling proteins regulate amino acid metabolism of the rice blast fungus Magnaporthe oryzae. Proteomics. 2014;14(21–22):2508–2522.
  • Chen XL, Wang Z, Liu C. Roles of peroxisomes in the rice blast fungus. Biomed Res Int. 2016;2016:9343417.
  • Wang ZY, Soanes DM, Kershaw MJ, et al. Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid beta-oxidation during appressorium-mediated plant infection. Mol Plant Microbe Interact. 2007;20(5):475–491.
  • Li L, Wang J, Zhang Z, et al. MoPex19, which is essential for maintenance of peroxisomal structure and woronin bodies, is required for metabolism and development in the rice blast fungus. PLoS One. 2014;9(1):e85252.
  • Min K, Son H, Lee J, et al. Peroxisome function is required for virulence and survival of Fusarium graminearum. Mol Plant Microbe Interact. 2012;25(12):1617–1627.
  • Ahrén D, Tholander M, Fekete C, et al. Comparison of gene expression in trap cells and vegetative hyphae of the nematophagous fungus Monacrosporium haptotylum. Microbiology. 2005;151(Pt 3):789–803.