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7 Heterotrimeric G Proteins

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Biochemistry and Molecular Biology

Part of the book series: The Mycota ((MYCOTA,volume III))

Abstract

A major system used by eukaryotic organisms to sense and respond to environmental stimuli involves heterotrimeric G-proteins and their cognate membrane-bound receptors, known as G protein-coupled receptors (GPCRs). This chapter introduces the components of heterotrimeric G-protein-mediated signaling and highlights the effector pathways downstream of the receptors. Also, the cellular functions that are regulated are presented, which include, but are not limited to, nutrient sensing, mating and pheromone response, and pathogenesis.

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References

  • Adachi K, Hamer JE (1998) Divergent cAMP signaling pathways regulate growth and pathogenesis in the rice blast fungus Magnaporthe grisea. Plant Cell 10(8):1361–1374

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Affeldt KJ, Brodhagen M, Keller NP (2012) Aspergillus oxylipin signaling and quorum sensing pathways depend on G protein-coupled receptors. Toxins 4(9):695–717

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Affeldt KJ, Carrig J, Amare M, Keller NP (2014) Global survey of canonical Aspergillus flavus G protein-coupled receptors. mBio 5(5):e01501–e01514

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Afshar K, Willard FS, Colombo K, Johnston CA, McCudden CR, Siderovski DP, Gonczy P (2004) RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos. Cell 119(2):219–230

    Article  PubMed  CAS  Google Scholar 

  • Albuquerque P, Casadevall A (2012) Quorum sensing in fungi–a review. Med Mycol 50(4):337–345. doi:10.3109/13693786.2011.652201

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Alkhayyat F, Yu JH (2014) Upstream regulation of mycotoxin biosynthesis. Adv Appl Microbiol 86:251–278

    Article  PubMed  CAS  Google Scholar 

  • Alspaugh JA, Perfect JR, Heitman J (1997) Cryptococcus neoformans mating and virulence are regulated by the G-protein alpha subunit GPA1 and cAMP. Genes Dev 11(23):3206–3217

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Alspaugh JA, Pukkila-Worley R, Harashima T, Cavallo LM, Funnell D, Cox GM, Perfect JR, Kronstad JW, Heitman J (2002) Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot Cell 1(1):75–84

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Anger T, Zhang W, Mende U (2004) Differential contribution of GTPase activation and effector antagonism to the inhibitory effect of RGS proteins on Gq-mediated signaling in vivo. J Biol Chem 279(6):3906–3915

    Article  PubMed  CAS  Google Scholar 

  • Apanovitch DM, Slep KC, Sigler PB, Dohlman HG (1998) Sst2 is a GTPase-activating protein for Gpa1: purification and characterization of a cognate RGS-Galpha protein pair in yeast. Biochemistry 37(14):4815–4822

    Article  PubMed  CAS  Google Scholar 

  • Bakkeren G, Kronstad JW (1996) The pheromone cell signaling components of the Ustilago a mating-type loci determine intercompatibility between species. Genetics 143(4):1601–1613

    PubMed Central  PubMed  CAS  Google Scholar 

  • Banuett F (1995) Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu Rev Genet 29:179–208

    Article  PubMed  CAS  Google Scholar 

  • Bardwell L (2006) Mechanisms of MAPK signalling specificity. Biochem Soc Trans 34(Pt 5):837–841

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barr MM, Tu H, Van Aelst L, Wigler M (1996) Identification of Ste4 as a potential regulator of Byr2 in the sexual response pathway of Schizosaccharomyces pombe. Mol Cell Biol 16(10):5597–5603

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Bayram O, Bayram OS, Ahmed YL, Maruyama J, Valerius O, Rizzoli SO, Ficner R, Irniger S, Braus GH (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8(7):e1002816

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Berman DM, Gilman AG (1998) Mammalian RGS proteins: barbarians at the gate. J Biol Chem 273(3):1269–1272

    Article  PubMed  CAS  Google Scholar 

  • Birnbaumer L (1992) Receptor-to-effector signaling through G proteins: roles for beta gamma dimers as well as alpha subunits. Cell 71(7):1069–1072

    Article  PubMed  CAS  Google Scholar 

  • Bistis GN (1981) Chemotropic interactions between trichogynes and conidia of opposite mating-type in Neurospora crassa. Mycologia 73(5):959–975

    Article  Google Scholar 

  • Bistis GN (1983) Evidence for diffusible, mating-type-specific trichogyne attractants in Neurospora crassa. Exp Mycol 7:292–295

    Article  CAS  Google Scholar 

  • Bobrowicz P, Pawlak R, Correa A, Bell-Pedersen D, Ebbole DJ (2002) The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Mol Microbiol 45(3):795–804

    Article  PubMed  CAS  Google Scholar 

  • Bock A, Kostenis E, Trankle C, Lohse MJ, Mohr K (2014) Pilot the pulse: controlling the multiplicity of receptor dynamics. Trends Pharm Sci 35(12):630–638

    Article  PubMed  CAS  Google Scholar 

  • Bohm A, Gaudet R, Sigler PB (1997) Structural aspects of heterotrimeric G-protein signaling. Curr Opin Biotechnol 8(4):480–487

    Article  PubMed  CAS  Google Scholar 

  • Bolker M (1998) Sex and crime: heterotrimeric G proteins in fungal mating and pathogenesis. Fungal Genet Biol 25(3):143–156

    Article  PubMed  CAS  Google Scholar 

  • Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, Seiler S, Bell-Pedersen D, Paietta J, Plesofsky N, Plamann M, Goodrich-Tanrikulu M, Schulte U, Mannhaupt G, Nargang FE, Radford A, Selitrennikoff C, Galagan JE, Dunlap JC, Loros JJ, Catcheside D, Inoue H, Aramayo R, Polymenis M, Selker EU, Sachs MS, Marzluf GA, Paulsen I, Davis R, Ebbole DJ, Zelter A, Kalkman ER, O’Rourke R, Bowring F, Yeadon J, Ishii C, Suzuki K, Sakai W, Pratt R (2004) Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68(1):1–108

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brefort T, Doehlemann G, Mendoza-Mendoza A, Reissmann S, Djamei A, Kahmann R (2009) Ustilago maydis as a pathogen. Annu Rev Phytopathol 47:423–445

    Article  PubMed  CAS  Google Scholar 

  • Brown SH, Scott JB, Bhaheetharan J, Sharpee WC, Milde L, Wilson RA, Keller NP (2009) Oxygenase coordination is required for morphological transition and the host-fungus interaction of Aspergillus flavus. Mol Plant Microbe Interact 22(7):882–894

    Article  PubMed  CAS  Google Scholar 

  • Bruno KS, Aramayo R, Minke PF, Metzenberg RL, Plamann M (1996) Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO J 15(21):5772–5782

    PubMed Central  PubMed  CAS  Google Scholar 

  • Burack WR, Shaw AS (2000) Signal transduction: hanging on a scaffold. Curr Opin Cell Biol 12(2):211–216

    Article  PubMed  CAS  Google Scholar 

  • Burbelo PD, Drechsel D, Hall A (1995) A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem 270(49):29071–29074

    Article  PubMed  CAS  Google Scholar 

  • Burkholder AC, Hartwell LH (1985) The yeast alpha-factor receptor: structural properties deduced from the sequence of the STE2 gene. Nucleic Acids Res 13(23):8463–8475

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Busti S, Coccetti P, Alberghina L, Vanoni M (2010) Glucose signaling-mediated coordination of cell growth and cell cycle in Saccharomyces cerevisiae. Sensors 10(6):6195–6240

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cabib E, Drgonova J, Drgon T (1998) Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem 67:307–333

    Article  PubMed  CAS  Google Scholar 

  • Cairns BR, Ramer SW, Kornberg RD (1992) Order of action of components in the yeast pheromone response pathway revealed with a dominant allele of the STE11 kinase and the multiple phosphorylation of the STE7 kinase. Genes Dev 6(7):1305–1318

    Article  PubMed  CAS  Google Scholar 

  • Chan RK, Otte CA (1982) Isolation and genetic analysis of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and alpha factor pheromones. Mol Cell Biol 2(1):11–20

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chan P, Thomas CJ, Sprang SR, Tall GG (2013) Molecular chaperoning function of Ric-8 is to fold nascent heterotrimeric G protein alpha subunits. Proc Natl Acad Sci USA 110(10):3794–3799

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chasse SA, Dohlman HG (2003) RGS proteins: G protein-coupled receptors meet their match. Assay Drug Dev Technol 1(2):357–364

    Article  PubMed  CAS  Google Scholar 

  • Chasse SA, Flanary P, Parnell SC, Hao N, Cha JY, Siderovski DP, Dohlman HG (2006) Genome-scale analysis reveals Sst2 as the principal regulator of mating pheromone signaling in the yeast Saccharomyces cerevisiae. Eukaryot Cell 5(2):330–346

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chen JG, Willard FS, Huang J, Liang J, Chasse SA, Jones AM, Siderovski DP (2003) A seven-transmembrane RGS protein that modulates plant cell proliferation. Science 301(5640):1728–1731

    Article  PubMed  CAS  Google Scholar 

  • Chini B, Parenti M, Poyner DR, Wheatley M (2013) G-protein-coupled receptors: from structural insights to functional mechanisms. Biochem Soc Trans 41(1):135–136

    Article  PubMed  CAS  Google Scholar 

  • Chishiki K, Kamakura S, Yuzawa S, Hayase J, Sumimoto H (2013) Ubiquitination of the heterotrimeric G protein alpha subunits Galphai2 and Galphaq is prevented by the guanine nucleotide exchange factor Ric-8A. Biochem Biophys Res Commun 435(3):414–419

    Article  PubMed  CAS  Google Scholar 

  • Choi W, Dean RA (1997) The adenylate cyclase gene MAC1 of Magnaporthe grisea controls appressorium formation and other aspects of growth and development. Plant Cell 9(11):1973–1983

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chou S, Lane S, Liu H (2006) Regulation of mating and filamentation genes by two distinct Ste12 complexes in Saccharomyces cerevisiae. Mol Cell Biol 26(13):4794–4805. doi:10.1128/MCB.02053-05

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Colman-Lerner A, Gordon A, Serra E, Chin T, Resnekov O, Endy D, Pesce CG, Brent R (2005) Regulated cell-to-cell variation in a cell-fate decision system. Nature 437(7059):699–706

    Article  PubMed  CAS  Google Scholar 

  • De Vries L, Zheng B, Fischer T, Elenko E, Farquhar MG (2000) The regulator of G protein signaling family. Annu Rev Pharmacol Toxicol 40:235–271

    Article  PubMed  Google Scholar 

  • Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Thon M, Kulkarni R, Xu JR, Pan H, Read ND, Lee YH, Carbone I, Brown D, Oh YY, Donofrio N, Jeong JS, Soanes DM, Djonovic S, Kolomiets E, Rehmeyer C, Li W, Harding M, Kim S, Lebrun MH, Bohnert H, Coughlan S, Butler J, Calvo S, Ma LJ, Nicol R, Purcell S, Nusbaum C, Galagan JE, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434(7036):980–986

    Article  PubMed  CAS  Google Scholar 

  • Denic V, Dotsch V, Sinning I (2013) Endoplasmic reticulum targeting and insertion of tail-anchored membrane proteins by the GET pathway. CSL Perspect Biol 5(8):a013334

    Google Scholar 

  • DeZwaan TM, Carroll AM, Valent B, Sweigard JA (1999) Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell 11(10):2013–2030

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dohlman HG, Slessareva JE (2006) Pheromone signaling pathways in yeast. Sci STKE 2006(364):cm6

    Article  PubMed  Google Scholar 

  • Dohlman HG, Song J, Ma D, Courchesne WE, Thorner J (1996) 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 16(9):5194–5209

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Downes GB, Gautam N (1999) The G protein subunit gene families. Genomics 62(3):544–552

    Article  PubMed  CAS  Google Scholar 

  • Dyer PS, Paoletti M, Archer DB (2003) Genomics reveals sexual secrets of Aspergillus. Microbiology 149(Pt 9):2301–2303

    Article  PubMed  CAS  Google Scholar 

  • Eaton CJ, Cabrera IE, Servin JA, Wright SJ, Cox MP, Borkovich KA (2012) The guanine nucleotide exchange factor RIC8 regulates conidial germination through Galpha proteins in Neurospora crassa. PLoS One 7(10), e48026

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Egel R (1971) Physiological aspects of conjugation in fission yeast. Planta 98(1):89–96

    Article  PubMed  CAS  Google Scholar 

  • Elion EA (2000) Pheromone response, mating and cell biology. Curr Opin Microbiol 3(6):573–581

    Article  PubMed  CAS  Google Scholar 

  • Elion EA (2001) The Ste5p scaffold. J Cell Sci 114(Pt 22):3967–3978

    PubMed  CAS  Google Scholar 

  • Elion EA, Satterberg B, Kranz JE (1993) FUS3 phosphorylates multiple components of the mating signal transduction cascade: evidence for STE12 and FAR1. Mol Biol Cell 4(5):495–510

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fang W, Scully LR, Zhang L, Pei Y, Bidochka MJ (2008) Implication of a regulator of G protein signalling (BbRGS1) in conidiation and conidial thermotolerance of the insect pathogenic fungus Beauveria bassiana. FEMS Microbiol Lett 279(2):146–156

    Article  PubMed  CAS  Google Scholar 

  • Fernandez J, Wilson RA (2014) Cells in cells: morphogenetic and metabolic strategies conditioning rice infection by the blast fungus Magnaporthe oryzae. Protoplasma 251(1):37–47

    Article  PubMed  CAS  Google Scholar 

  • Ferrell JE Jr, Bhatt RR (1997) Mechanistic studies of the dual phosphorylation of mitogen-activated protein kinase. J Biol Chem 272(30):19008–19016

    Article  PubMed  CAS  Google Scholar 

  • Fong HK, Hurley JB, Hopkins RS, Miake-Lye R, Johnson MS, Doolittle RF, Simon MI (1986) Repetitive segmental structure of the transducin beta subunit: homology with the CDC4 gene and identification of related mRNAs. Proc Natl Acad Sci USA 83(7):2162–2166

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Francis SH, Corbin JD (1999) Cyclic nucleotide-dependent protein kinases: intracellular receptors for cAMP and cGMP action. Crit Rev Clin Lab Sci 36(4):275–328

    Article  PubMed  CAS  Google Scholar 

  • Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharm 63(6):1256–1272

    Article  CAS  Google Scholar 

  • Freissmuth M, Gilman AG (1989) Mutations of GS alpha designed to alter the reactivity of the protein with bacterial toxins. Substitutions at ARG187 result in loss of GTPase activity. J Biol Chem 264(36):21907–21914

    PubMed  CAS  Google Scholar 

  • Fuchs BB, Mylonakis E (2009) Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot Cell 8(11):1616–1625

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gabay M, Pinter ME, Wright FA, Chan P, Murphy AJ, Valenzuela DM, Yancopoulos GD, Tall GG (2011) Ric-8 proteins are molecular chaperones that direct nascent G protein alpha subunit membrane association. Sci Signal 4(200):ra79

    Article  PubMed  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, Rehman B, Elkins T, Engels R, Wang S, Nielsen CB, Butler J, Endrizzi M, Qui D, Ianakiev P, Bell-Pedersen D, Nelson MA, Werner-Washburne M, Selitrennikoff CP, Kinsey JA, Braun EL, Zelter A, Schulte U, Kothe GO, Jedd G, Mewes W, Staben C, Marcotte E, Greenberg D, Roy A, Foley K, Naylor J, Stange-Thomann N, Barrett R, Gnerre S, Kamal M, Kamvysselis M, Mauceli E, Bielke C, Rudd S, Frishman D, Krystofova S, Rasmussen C, Metzenberg RL, Perkins DD, Kroken S, Cogoni C, Macino G, Catcheside D, Li W, Pratt RJ, Osmani SA, DeSouza CP, Glass L, Orbach MJ, Berglund JA, Voelker R, Yarden O, Plamann M, Seiler S, Dunlap J, Radford A, Aramayo R, Natvig DO, Alex LA, Mannhaupt G, Ebbole DJ, Freitag M, Paulsen I, Sachs MS, Lander ES, Nusbaum C, Birren B (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature 422(6934):859–868

    Article  PubMed  CAS  Google Scholar 

  • Garg N, Manchanda G, Kumar A (2014) Bacterial quorum sensing: circuits and applications. Antonie van Leeuwenhoek 105(2):289–305

    Article  PubMed  Google Scholar 

  • Garrington TP, Johnson GL (1999) Organization and regulation of mitogen-activated protein kinase signaling pathways. Curr Opin Cell Biol 11(2):211–218

    Article  PubMed  CAS  Google Scholar 

  • Gartner A, Nasmyth K, Ammerer G (1992) Signal transduction in Saccharomyces cerevisiae requires tyrosine and threonine phosphorylation of FUS3 and KSS1. Genes Dev 6(7):1280–1292

    Article  PubMed  CAS  Google Scholar 

  • Gautam N, Downes GB, Yan K, Kisselev O (1998) The G-protein betagamma complex. Cell Signal 10(7):447–455

    Article  PubMed  CAS  Google Scholar 

  • Gold S, Duncan G, Barrett K, Kronstad J (1994) cAMP regulates morphogenesis in the fungal pathogen Ustilago maydis. Genes Dev 8(23):2805–2816

    Article  PubMed  CAS  Google Scholar 

  • Gold SE, Brogdon SM, Mayorga ME, Kronstad JW (1997) The Ustilago maydis regulatory subunit of a cAMP-dependent protein kinase is required for gall formation in maize. Plant Cell 9(9):1585–1594

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gong J, Grodsky JD, Zhang Z, Wang P (2014) A Ric8/Synembryn homolog promotes Gpa1 and Gpa2 activation to respectively regulate cyclic AMP and pheromone signaling in Cryptococcus neoformans. Eukaryot Cell 13(10):1290–1299

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Good M, Tang G, Singleton J, Remenyi A, Lim WA (2009) The Ste5 scaffold directs mating signaling by catalytically unlocking the Fus3 MAP kinase for activation. Cell 136(6):1085–1097

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Graziano MP, Gilman AG (1989) Synthesis in Escherichia coli of GTPase-deficient mutants of Gs alpha. J Biol Chem 264(26):15475–15482

    PubMed  CAS  Google Scholar 

  • Gruber S, Omann M, Zeilinger S (2013) Comparative analysis of the repertoire of G protein-coupled receptors of three species of the fungal genus Trichoderma. BMC Microbiol 13:108

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gustin MC, Albertyn J, Alexander M, Davenport K (1998) MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev 62(4):1264–1300

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hagen DC, McCaffrey G, Sprague GF Jr (1986) Evidence the yeast STE3 gene encodes a receptor for the peptide pheromone a factor: gene sequence and implications for the structure of the presumed receptor. Proc Natl Acad Sci USA 83(5):1418–1422

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hamel LP, Nicole MC, Duplessis S, Ellis BE (2012) Mitogen-activated protein kinase signaling in plant-interacting fungi: distinct messages from conserved messengers. Plant Cell 24(4):1327–1351

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hamm HE (1998) The many faces of G protein signaling. J Biol Chem 273(2):669–672

    Article  PubMed  CAS  Google Scholar 

  • Hamm HE, Gilchrist A (1996) Heterotrimeric G proteins. Curr Opin Cell Biol 8(2):189–196

    Article  PubMed  CAS  Google Scholar 

  • Hampoelz B, Hoeller O, Bowman SK, Dunican D, Knoblich JA (2005) Drosophila Ric-8 is essential for plasma-membrane localization of heterotrimeric G proteins. Nat Cell Biol 7(11):1099–1105

    Article  PubMed  CAS  Google Scholar 

  • Han KH, Seo JA, Yu JH (2004) Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Galpha) signalling. Mol Microbiol 53(2):529–540

    Article  PubMed  CAS  Google Scholar 

  • Hartmann HA, Kahmann R, Bolker M (1996) The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO J 15(7):1632–1641

    PubMed Central  PubMed  CAS  Google Scholar 

  • Herrero-Garcia E, Garzia A, Cordobes S, Espeso EA, Ugalde U (2011) 8-Carbon oxylipins inhibit germination and growth, and stimulate aerial conidiation in Aspergillus nidulans. Fungal Biol 115(4-5):393–400

    Article  PubMed  CAS  Google Scholar 

  • Hill SJ (2006) G-protein-coupled receptors: past, present and future. Br J Pharm 147(Suppl 1):S27–S37

    CAS  Google Scholar 

  • Hoffman CS (2005a) Except in every detail: comparing and contrasting G-protein signaling in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Eukaryot Cell 4(3):495–503

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hoffman CS (2005b) Glucose sensing via the protein kinase A pathway in Schizosaccharomyces pombe. Biochem Soc Trans 33(Pt 1):257–260

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hoffman CS, Winston F (1990) Isolation and characterization of mutants constitutive for expression of the fbp1 gene of Schizosaccharomyces pombe. Genetics 124(4):807–816

    PubMed Central  PubMed  CAS  Google Scholar 

  • Hoffman CS, Winston F (1991) Glucose repression of transcription of the Schizosaccharomyces pombe fbp1 gene occurs by a cAMP signaling pathway. Genes Dev 5(4):561–571

    Article  PubMed  CAS  Google Scholar 

  • Hollinger S, Hepler JR (2002) Cellular regulation of RGS proteins: modulators and integrators of G protein signaling. Pharm Rev 54(3):527–559

    Article  PubMed  CAS  Google Scholar 

  • Holsbeeks I, Lagatie O, Van Nuland A, Van de Velde S, Thevelein JM (2004) The eukaryotic plasma membrane as a nutrient-sensing device. Trends Biochem Sci 29(10):556–564

    Article  PubMed  CAS  Google Scholar 

  • Horowitz Brown S, Zarnowski R, Sharpee WC, Keller NP (2008) Morphological transitions governed by density dependence and lipoxygenase activity in Aspergillus flavus. Appl Environ Microbiol 74(18):5674–5685

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hsueh YP, Xue C, Heitman J (2009) A constitutively active GPCR governs morphogenic transitions in Cryptococcus neoformans. EMBO J 28(9):1220–1233

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hughes DA, Yabana N, Yamamoto M (1994) Transcriptional regulation of a Ras nucleotide-exchange factor gene by extracellular signals in fission yeast. J Cell Sci 107(Pt 12):3635–3642

    PubMed  CAS  Google Scholar 

  • Iniguez-Lluhi JA, Simon MI, Robishaw JD, Gilman AG (1992) G protein beta gamma subunits synthesized in Sf9 cells. Functional characterization and the significance of prenylation of gamma. J Biol Chem 267(32):23409–23417

    PubMed  CAS  Google Scholar 

  • Isshiki T, Mochizuki N, Maeda T, Yamamoto M (1992) Characterization of a fission yeast gene, gpa2, that encodes a G alpha subunit involved in the monitoring of nutrition. Genes Dev 6(12B):2455–2462

    Article  PubMed  CAS  Google Scholar 

  • Ivey FD, Hoffman CS (2005) Direct activation of fission yeast adenylate cyclase by the Gpa2 Galpha of the glucose signaling pathway. Proc Natl Acad Sci USA 102(17):6108–6113

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ivey FD, Hodge PN, Turner GE, Borkovich KA (1996) The Galphai homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Mol Biol Cell 7(8):1283–1297

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ivey FD, Yang Q, Borkovich KA (1999) Positive regulation of adenylyl cyclase activity by a Galphai homolog in Neurospora crassa. Fungal Genet Biol 26(1):48–61

    Article  PubMed  CAS  Google Scholar 

  • Ivey FD, Kays AM, Borkovich KA (2002) Shared and independent roles for a Galpha(i) protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot Cell 1(4):634–642

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jastrzebska B (2013) GPCR: G protein complexes—the fundamental signaling assembly. Amino Acids 45(6):1303–1314

    Article  PubMed  CAS  Google Scholar 

  • Johnston GC, Ehrhardt CW, Lorincz A, Carter BL (1979) Regulation of cell size in the yeast Saccharomyces cerevisiae. J Bacteriol 137(1):1–5

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kaffarnik F, Muller P, Leibundgut M, Kahmann R, Feldbrugge M (2003) PKA and MAPK phosphorylation of Prf1 allows promoter discrimination in Ustilago maydis. EMBO J 22(21):5817–5826

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kahmann R, Bolker M (1996) Self/nonself recognition in fungi: old mysteries and simple solutions. Cell 85(2):145–148

    Article  PubMed  CAS  Google Scholar 

  • Kahmann R, Kamper J (2004) Ustilago maydis: how its biology relates to pathogenic development. New Phytol 164:31–42

    Article  CAS  Google Scholar 

  • Katritch V, Cherezov V, Stevens RC (2012) Diversity and modularity of G protein-coupled receptor structures. Trends Pharm Sci 33(1):17–27

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kays AM, Borkovich KA (2004) Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics 166(3):1229–1240

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kays AM, Rowley PS, Baasiri RA, Borkovich KA (2000) Regulation of conidiation and adenylyl cyclase levels by the Galpha protein GNA-3 in Neurospora crassa. Mol Cell Biol 20(20):7693–7705

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Keshet Y, Seger R (2010) The MAP kinase signaling cascades: a system of hundreds of components regulates a diverse array of physiological functions. Methods Mol Biol 661:3–38

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Borkovich KA (2004) A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol Microbiol 52(6):1781–1798

    Article  PubMed  CAS  Google Scholar 

  • Kim H, Borkovich KA (2006) Pheromones are essential for male fertility and sufficient to direct chemotropic polarized growth of trichogynes during mating in Neurospora crassa. Eukaryot Cell 5(3):544–554

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim H, Metzenberg RL, Nelson MA (2002) Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Eukaryot Cell 1(6):987–999

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim H, Wright SJ, Park G, Ouyang S, Krystofova S, Borkovich KA (2012) Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics 190(4):1389–1404

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kitamura K, Shimoda C (1991) The Schizosaccharomyces pombe mam2 gene encodes a putative pheromone receptor which has a significant homology with the Saccharomyces cerevisiae Ste2 protein. EMBO J 10(12):3743–3751

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kobilka BK (2007) G protein coupled receptor structure and activation. Biochim Biophys Acta 1768(4):794–807

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kozubowski L, Heitman J (2012) Profiling a killer, the development of Cryptococcus neoformans. FEMS Microbiol Rev 36(1):78–94

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kraakman L, Lemaire K, Ma P, Teunissen AW, Donaton MC, Van Dijck P, Winderickx J, de Winde JH, Thevelein JM (1999) A Saccharomyces cerevisiae G-protein coupled receptor, Gpr1, is specifically required for glucose activation of the cAMP pathway during the transition to growth on glucose. Mol Microbiol 32(5):1002–1012

    Article  PubMed  CAS  Google Scholar 

  • Krebs EG (1989) The Albert Lasker Medical Awards. Role of the cyclic AMP-dependent protein kinase in signal transduction. JAMA 262(13):1815–1818

    Article  PubMed  CAS  Google Scholar 

  • Krishnan A, Almen MS, Fredriksson R, Schioth HB (2012) The origin of GPCRs: identification of mammalian like rhodopsin, adhesion, glutamate and frizzled GPCRs in fungi. PLoS One 7(1):e29817

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kronstad J, De Maria AD, Funnell D, Laidlaw RD, Lee N, de Sa MM, Ramesh M (1998) Signaling via cAMP in fungi: interconnections with mitogen-activated protein kinase pathways. Arch Microbiol 170(6):395–404

    Article  PubMed  CAS  Google Scholar 

  • Kruger J, Loubradou G, Regenfelder E, Hartmann A, Kahmann R (1998) Crosstalk between cAMP and pheromone signalling pathways in Ustilago maydis. Mol Gen Genet 260(2-3):193–198

    Article  PubMed  CAS  Google Scholar 

  • Krystofova S, Borkovich KA (2005) The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gbetagamma dimer required for normal female fertility, asexual development, and Galpha protein levels in Neurospora crassa. Eukaryot Cell 4(2):365–378

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kulkarni RD, Thon MR, Pan H, Dean RA (2005) Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biol 6(3):R24

    Article  PubMed Central  PubMed  Google Scholar 

  • Kunitomo H, Higuchi T, Iino Y, Yamamoto M (2000) A zinc-finger protein, Rst2p, regulates transcription of the fission yeast ste11(+) gene, which encodes a pivotal transcription factor for sexual development. Mol Biol Cell 11(9):3205–3217

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kurjan J (1992) Pheromone response in yeast. Annu Rev Biochem 61:1097–1129

    Article  PubMed  CAS  Google Scholar 

  • Kwon NJ, Park HS, Jung S, Kim SC, Yu JH (2012) The putative guanine nucleotide exchange factor RicA mediates upstream signaling for growth and development in Aspergillus. Eukaryot Cell 11(11):1399–1412

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kwon-Chung KJ (1975) A new genus, Filobasidiella, the perfect state of Cryptococcus neoformans. Mycologia 67(6):1197–1200

    Article  PubMed  CAS  Google Scholar 

  • Kwon-Chung KJ (1976) Morphogenesis of Filobasidiella neoformans, the sexual state of Cryptococcus neoformans. Mycologia 68(4):821–833

    Article  PubMed  CAS  Google Scholar 

  • Lafon A, Seo JA, Han KH, Yu JH, d’Enfert C (2005) The heterotrimeric G-protein GanB(alpha)-SfaD(beta)-GpgA(gamma) is a carbon source sensor involved in early cAMP-dependent germination in Aspergillus nidulans. Genetics 171(1):71–80

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lafon A, Han KH, Seo JA, Yu JH, d’Enfert C (2006) G-protein and cAMP-mediated signaling in Aspergilli: a genomic perspective. Fungal Genet Biol 43(7):490–502

    Article  PubMed  CAS  Google Scholar 

  • Lai RK, Perez-Sala D, Canada FJ, Rando RR (1990) The gamma subunit of transducin is farnesylated. Proc Natl Acad Sci USA 87(19):7673–7677

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Landry S, Hoffman CS (2001) The git5 Gbeta and git11 Ggamma form an atypical Gbetagamma dimer acting in the fission yeast glucose/cAMP pathway. Genetics 157(3):1159–1168

    PubMed Central  PubMed  CAS  Google Scholar 

  • Landry S, Pettit MT, Apolinario E, Hoffman CS (2000) The fission yeast git5 gene encodes a Gbeta subunit required for glucose-triggered adenylate cyclase activation. Genetics 154(4):1463–1471

    PubMed Central  PubMed  CAS  Google Scholar 

  • Lee BN, Adams TH (1994) Overexpression of flbA, an early regulator of Aspergillus asexual sporulation, leads to activation of brlA and premature initiation of development. Mol Microbiol 14(2):323–334

    Article  PubMed  CAS  Google Scholar 

  • Lee MJ, Dohlman HG (2008) Coactivation of G protein signaling by cell-surface receptors and an intracellular exchange factor. Curr Biol 18(3):211–215

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lemaire K, Van de Velde S, Van Dijck P, Thevelein JM (2004) Glucose and sucrose act as agonist and mannose as antagonist ligands of the G protein-coupled receptor Gpr1 in the yeast Saccharomyces cerevisiae. Mol Cell 16(2):293–299

    Article  PubMed  CAS  Google Scholar 

  • Lengeler KB, Davidson RC, D’Souza C, Harashima T, Shen WC, Wang P, Pan X, Waugh M, Heitman J (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64(4):746–785

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lengeler KB, Fox DS, Fraser JA, Allen A, Forrester K, Dietrich FS, Heitman J (2002) Mating-type locus of Cryptococcus neoformans: a step in the evolution of sex chromosomes. Eukaryot Cell 1(5):704–718

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li L, Borkovich KA (2006) GPR-4 is a predicted G-protein-coupled receptor required for carbon source-dependent asexual growth and development in Neurospora crassa. Eukaryot Cell 5(8):1287–1300

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li L, Shen G, Zhang ZG, Wang YL, Thompson JK, Wang P (2007a) Canonical heterotrimeric G proteins regulating mating and virulence of Cryptococcus neoformans. Mol Biol Cell 18(11):4201–4209

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li L, Wright SJ, Krystofova S, Park G, Borkovich KA (2007b) Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Yan X, Wang H, Liang S, Ma WB, Fang MY, Talbot NJ, Wang ZY (2010) MoRic8 Is a novel component of G-protein signaling during plant infection by the rice blast fungus Magnaporthe oryzae. Mol Plant Microbe Interact 23(3):317–331

    Article  PubMed  CAS  Google Scholar 

  • Li G, Zhou X, Xu JR (2012) Genetic control of infection-related development in Magnaporthe oryzae. Curr Opin Microbiol 15(6):678–684

    Article  PubMed  CAS  Google Scholar 

  • Liang S, Wang ZY, Liu PJ, Li DB (2006) A Gγ subunit promoter T-DNA insertion mutant—A1-412 of Magnaporthe grisea is defective in appressorium formation, penetration and pathogenicity. Chin Sci Bull 51:2214–2218

    Article  CAS  Google Scholar 

  • Liu S, Dean RA (1997) G protein alpha subunit genes control growth, development, and pathogenicity of Magnaporthe grisea. Mol Plant Microbe Interact 10(9):1075–1086

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Suresh A, Willard FS, Siderovski DP, Lu S, Naqvi NI (2007) Rgs1 regulates multiple Galpha subunits in Magnaporthe pathogenesis, asexual growth and thigmotropism. EMBO J 26(3):690–700

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu J, Wang X, Mitchell T, Hu Y, Liu X, Dai L, Wang GL (2010) Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol Plant Pathol 11(3):419–427

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Ilasaca M (1998) Signaling from G-protein-coupled receptors to mitogen-activated protein (MAP)-kinase cascades. Biochem Pharm 56(3):269–277

    Article  PubMed  CAS  Google Scholar 

  • Lorenz MC, Heitman J (1997) Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J 16(23):7008–7018

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lorenz MC, Pan X, Harashima T, Cardenas ME, Xue Y, Hirsch JP, Heitman J (2000) The G protein-coupled receptor gpr1 is a nutrient sensor that regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Genetics 154(2):609–622

    PubMed Central  PubMed  CAS  Google Scholar 

  • Maeda T, Watanabe Y, Kunitomo H, Yamamoto M (1994) Cloning of the pka1 gene encoding the catalytic subunit of the cAMP-dependent protein kinase in Schizosaccharomyces pombe. J Biol Chem 269(13):9632–9637

    PubMed  CAS  Google Scholar 

  • Marcus S, Polverino A, Barr M, Wigler M (1994) Complexes between STE5 and components of the pheromone-responsive mitogen-activated protein kinase module. Proc Natl Acad Sci USA 91(16):7762–7766

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mata J, Bahler J (2006) Global roles of Ste11p, cell type, and pheromone in the control of gene expression during early sexual differentiation in fission yeast. Proc Natl Acad Sci USA 103(42):15517–15522

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Matsumoto K, Uno I, Ishikawa T (1984) Identification of the structural gene and nonsense alleles for adenylate cyclase in Saccharomyces cerevisiae. J Bacteriol 157(1):277–282

    PubMed Central  PubMed  CAS  Google Scholar 

  • McClelland CM, Fu J, Woodlee GL, Seymour TS, Wickes BL (2002) Isolation and characterization of the Cryptococcus neoformans MATa pheromone gene. Genetics 160(3):935–947

    PubMed Central  PubMed  CAS  Google Scholar 

  • Mehrabi R, M’Barek SB, Saidi A, Abrinbana M, de Wit PJ, Kema GH (2012) MAP kinase phosphorylation and cAMP assessment in fungi. Methods Mol Biol 835:571–583

    Article  PubMed  CAS  Google Scholar 

  • Mende U, Zagrovic B, Cohen A, Li Y, Valenzuela D, Fishman MC, Neer EJ (1998) Effect of deletion of the major brain G-protein alpha subunit (alpha(o)) on coordination of G-protein subunits and on adenylyl cyclase activity. J Neurosci Res 54(2):263–272

    Article  PubMed  CAS  Google Scholar 

  • Merlini L, Dudin O, Martin SG (2013) Mate and fuse: how yeast cells do it. Open Biol 3(3):130008

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Miller KG, Rand JB (2000) A role for RIC-8 (Synembryn) and GOA-1 (G(o)alpha) in regulating a subset of centrosome movements during early embryogenesis in Caenorhabditis elegans. Genetics 156(4):1649–1660

    PubMed Central  PubMed  CAS  Google Scholar 

  • Miller KG, Emerson MD, McManus JR, Rand JB (2000) RIC-8 (Synembryn): a novel conserved protein that is required for G(q)alpha signaling in the C. elegans nervous system. Neuron 27(2):289–299

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mitchell TK, Dean RA (1995) The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7(11):1869–1878

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Moore TD, Edman JC (1993) The alpha-mating type locus of Cryptococcus neoformans contains a peptide pheromone gene. Mol Cell Biol 13(3):1962–1970

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mukherjee M, Kim JE, Park YS, Kolomiets MV, Shim WB (2011) Regulators of G-protein signalling in Fusarium verticillioides mediate differential host-pathogen responses on nonviable versus viable maize kernels. Mol Plant Pathol 12(5):479–491

    Article  PubMed  CAS  Google Scholar 

  • Muller P, Leibbrandt A, Teunissen H, Cubasch S, Aichinger C, Kahmann R (2004) The Gbeta-subunit-encoding gene bpp1 controls cyclic-AMP signaling in Ustilago maydis. Eukaryot Cell 3(3):806–814

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nadin-Davis SA, Nasim A (1990) Schizosaccharomyces pombe ras1 and byr1 are functionally related genes of the ste family that affect starvation-induced transcription of mating-type genes. Mol Cell Biol 10(2):549–560

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nagai Y, Nishimura A, Tago K, Mizuno N, Itoh H (2010) Ric-8B stabilizes the alpha subunit of stimulatory G protein by inhibiting its ubiquitination. J Biol Chem 285(15):11114–11120

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nakayama N, Miyajima A, Arai K (1985) Nucleotide sequences of STE2 and STE3, cell type-specific sterile genes from Saccharomyces cerevisiae. EMBO J 4(10):2643–2648

    PubMed Central  PubMed  CAS  Google Scholar 

  • Neer EJ, Schmidt CJ, Nambudripad R, Smith TF (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371(6495):297–300

    Article  PubMed  CAS  Google Scholar 

  • Neiman AM, Herskowitz I (1994) Reconstitution of a yeast protein kinase cascade in vitro: activation of the yeast MEK homologue STE7 by STE11. Proc Natl Acad Sci USA 91(8):3398–3402

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Neves SR, Ram PT, Iyengar R (2002) G protein pathways. Science 296(5573):1636–1639

    Article  PubMed  CAS  Google Scholar 

  • Nguyen AN, Ikner AD, Shiozaki M, Warren SM, Shiozaki K (2002) Cytoplasmic localization of Wis1 MAPKK by nuclear export signal is important for nuclear targeting of Spc1/Sty1 MAPK in fission yeast. Mol Biol Cell 13(8):2651–2663

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nishimura M, Park G, Xu JR (2003) The G-beta subunit MGB1 is involved in regulating multiple steps of infection-related morphogenesis in Magnaporthe grisea. Mol Microbiol 50(1):231–243

    Article  PubMed  CAS  Google Scholar 

  • Obara T, Nakafuku M, Yamamoto M, Kaziro Y (1991) Isolation and characterization of a gene encoding a G-protein alpha subunit from Schizosaccharomyces pombe: involvement in mating and sporulation pathways. Proc Natl Acad Sci USA 88(13):5877–5881

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Okazaki N, Okazaki K, Tanaka K, Okayama H (1991) The ste4 + gene, essential for sexual differentiation of Schizosaccharomyces pombe, encodes a protein with a leucine zipper motif. Nucleic Acids Res 19(25):7043–7047

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Palmer DA, Thompson JK, Li L, Prat A, Wang P (2006) Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem 281(43):32596–32605

    Article  PubMed  CAS  Google Scholar 

  • Paoletti M, Rydholm C, Schwier EU, Anderson MJ, Szakacs G, Lutzoni F, Debeaupuis JP, Latge JP, Denning DW, Dyer PS (2005) Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr Biol 15(13):1242–1248

    Article  PubMed  CAS  Google Scholar 

  • Paoletti M, Seymour FA, Alcocer MJ, Kaur N, Calvo AM, Archer DB, Dyer PS (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 17(16):1384–1389

    Article  PubMed  CAS  Google Scholar 

  • Park G, Xue C, Zhao X, Kim Y, Orbach M, Xu JR (2006) Multiple upstream signals converge on the adaptor protein Mst50 in Magnaporthe grisea. Plant Cell 18(10):2822–2835

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Payne DM, Rossomando AJ, Martino P, Erickson AK, Her JH, Shabanowitz J, Hunt DF, Weber MJ, Sturgill TW (1991) Identification of the regulatory phosphorylation sites in pp 42/mitogen-activated protein kinase (MAP kinase). EMBO J 10(4):885–892

    PubMed Central  PubMed  CAS  Google Scholar 

  • Peeters T, Louwet W, Gelade R, Nauwelaers D, Thevelein JM, Versele M (2006) Kelch-repeat proteins interacting with the Galpha protein Gpa2 bypass adenylate cyclase for direct regulation of protein kinase A in yeast. Proc Natl Acad Sci USA 103(35):13034–13039

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pel HJ, de Winde JH, Archer DB, Dyer PS, Hofmann G, Schaap PJ, Turner G, de Vries RP, Albang R, Albermann K, Andersen MR, Bendtsen JD, Benen JA, van den Berg M, Breestraat S, Caddick MX, Contreras R, Cornell M, Coutinho PM, Danchin EG, Debets AJ, Dekker P, van Dijck PW, van Dijk A, Dijkhuizen L, Driessen AJ, d’Enfert C, Geysens S, Goosen C, Groot GS, de Groot PW, Guillemette T, Henrissat B, Herweijer M, van den Hombergh JP, van den Hondel CA, van der Heijden RT, van der Kaaij RM, Klis FM, Kools HJ, Kubicek CP, van Kuyk PA, Lauber J, Lu X, van der Maarel MJ, Meulenberg R, Menke H, Mortimer MA, Nielsen J, Oliver SG, Olsthoorn M, Pal K, van Peij NN, Ram AF, Rinas U, Roubos JA, Sagt CM, Schmoll M, Sun J, Ussery D, Varga J, Vervecken W, van de Vondervoort PJ, Wedler H, Wosten HA, Zeng AP, van Ooyen AJ, Visser J, Stam H (2007) Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25(2):221–231

    Article  PubMed  Google Scholar 

  • Pierce KL, Premont RT, Lefkowitz RJ (2002) Seven-transmembrane receptors. Nat Rev Mol Cell Biol 3(9):639–650

    Article  PubMed  CAS  Google Scholar 

  • Posas F, Takekawa M, Saito H (1998) Signal transduction by MAP kinase cascades in budding yeast. Curr Opin Microbiol 1(2):175–182

    Article  PubMed  CAS  Google Scholar 

  • Qi M, Elion EA (2005) MAP kinase pathways. J Cell Sci 118(Pt 16):3569–3572

    Article  PubMed  CAS  Google Scholar 

  • Raju NB (1992) Genetic control of the sexual cycle in Neurospora. Mycol Res 96:241–262

    Article  Google Scholar 

  • Ramachander R, Kim CA, Phillips ML, Mackereth CD, Thanos CD, McIntosh LP, Bowie JU (2002) Oligomerization-dependent association of the SAM domains from Schizosaccharomyces pombe Byr2 and Ste4. J Biol Chem 277(42):39585–39593

    Article  PubMed  CAS  Google Scholar 

  • Ramanujam R, Calvert ME, Selvaraj P, Naqvi NI (2013) The late endosomal HOPS complex anchors active G-protein signaling essential for pathogenesis in Magnaporthe oryzae. PLoS Pathog 9(8):e1003527

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ramezani-Rad M (2003) The role of adaptor protein Ste50-dependent regulation of the MAPKKK Ste11 in multiple signalling pathways of yeast. Curr Genet 43(3):161–170

    PubMed  CAS  Google Scholar 

  • Ramirez-Prado JH, Moore GG, Horn BW, Carbone I (2008) Characterization and population analysis of the mating-type genes in Aspergillus flavus and Aspergillus parasiticus. Fungal Genet Biol 45(9):1292–1299

    Article  PubMed  CAS  Google Scholar 

  • Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9(6):847–859

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bolker M, Kahmann R (1997) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 16(8):1934–1942

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Resh MD (1996) Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins. Cell Signal 8(6):403–412

    Article  PubMed  CAS  Google Scholar 

  • Robison GA, Butcher RW, Sutherland EW (1968) Cyclic AMP. Annu Rev Biochem 37:149–174

    Article  PubMed  CAS  Google Scholar 

  • Rosen S, Yu JH, Adams TH (1999) The Aspergillus nidulans sfaD gene encodes a G protein beta subunit that is required for normal growth and repression of sporulation. EMBO J 18(20):5592–5600

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ross EM, Wilkie TM (2000) GTPase-activating proteins for heterotrimeric G proteins: regulators of G protein signaling (RGS) and RGS-like proteins. Annu Rev Biochem 69:795–827

    Article  PubMed  CAS  Google Scholar 

  • Roux AE, Leroux A, Alaamery MA, Hoffman CS, Chartrand P, Ferbeyre G, Rokeach LA (2009) Pro-aging effects of glucose signaling through a G protein-coupled glucose receptor in fission yeast. PLoS Genet 5(3):e1000408

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rubio-Texeira M, Van Zeebroeck G, Voordeckers K, Thevelein JM (2010) Saccharomyces cerevisiae plasma membrane nutrient sensors and their role in PKA signaling. FEMS Yeast Res 10(2):134–149

    Article  PubMed  CAS  Google Scholar 

  • Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192(2):289–318

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Schade MA, Reynolds NK, Dollins CM, Miller KG (2005) Mutations that rescue the paralysis of Caenorhabditis elegans ric-8 (synembryn) mutants activate the G alpha(s) pathway and define a third major branch of the synaptic signaling network. Genetics 169(2):631–649

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Seo JA, Han KH, Yu JH (2004) The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol Microbiol 53(6):1611–1623

    Article  PubMed  CAS  Google Scholar 

  • Seo JA, Han KH, Yu JH (2005) Multiple roles of a heterotrimeric G-protein gamma-subunit in governing growth and development of Aspergillus nidulans. Genetics 171(1):81–89

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shen J, Hsu CM, Kang BK, Rosen BP, Bhattacharjee H (2003) The Saccharomyces cerevisiae Arr4p is involved in metal and heat tolerance. Biometals 16(3):369–378

    Article  PubMed  CAS  Google Scholar 

  • Shen G, Wang YL, Whittington A, Li L, Wang P (2008) The RGS protein Crg2 regulates pheromone and cyclic AMP signaling in Cryptococcus neoformans. Eukaryot Cell 7(9):1540–1548

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shukla AK, Singh G, Ghosh E (2014) Emerging structural insights into biased GPCR signaling. Trends Biochem Sci 39(12):594–602

    Article  PubMed  CAS  Google Scholar 

  • Siderovski DP, Willard FS (2005) The GAPs, GEFs, and GDIs of heterotrimeric G-protein alpha subunits. Int J Biol Sci 1(2):51–66

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Siderovski DP, Hessel A, Chung S, Mak TW, Tyers M (1996) A new family of regulators of G-protein-coupled receptors? Curr Biol 6(2):211–212

    Article  PubMed  CAS  Google Scholar 

  • Sondek J, Bohm A, Lambright DG, Hamm HE, Sigler PB (1996) Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379(6563):369–374

    Article  PubMed  CAS  Google Scholar 

  • Squire RA (1981) Ranking animal carcinogens: a proposed regulatory approach. Science 214(4523):877–880

    Article  PubMed  CAS  Google Scholar 

  • Stanton BC, Giles SS, Staudt MW, Kruzel EK, Hull CM (2010) Allelic exchange of pheromones and their receptors reprograms sexual identity in Cryptococcus neoformans. PLoS Genet 6(2):e1000860

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sugimoto A, Iino Y, Maeda T, Watanabe Y, Yamamoto M (1991) Schizosaccharomyces pombe ste11+ encodes a transcription factor with an HMG motif that is a critical regulator of sexual development. Genes Dev 5(11):1990–1999

    Article  PubMed  CAS  Google Scholar 

  • Tall GG (2013) Ric-8 regulation of heterotrimeric G proteins. J Recept Signal Transduct Res 33(3):139–143

    Article  PubMed  CAS  Google Scholar 

  • Tall GG, Krumins AM, Gilman AG (2003) Mammalian Ric-8A (Synembryn) is a heterotrimeric Galpha protein guanine nucleotide exchange factor. J Biol Chem 278(10):8356–8362

    Article  PubMed  CAS  Google Scholar 

  • Tamaki H (2007) Glucose-stimulated cAMP-protein kinase A pathway in yeast Saccharomyces cerevisiae. J Biosci Bioeng 104(4):245–250

    Article  PubMed  CAS  Google Scholar 

  • Tamaki H, Yun CW, Mizutani T, Tsuzuki T, Takagi Y, Shinozaki M, Kodama Y, Shirahige K, Kumagai H (2005) Glucose-dependent cell size is regulated by a G protein-coupled receptor system in yeast Saccharomyces cerevisiae. Genes Cells 10(3):193–206

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Davey J, Imai Y, Yamamoto M (1993) Schizosaccharomyces pombe map3 + encodes the putative M-factor receptor. Mol Cell Biol 13(1):80–88

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tanoue T, Nishida E (2003) Molecular recognitions in the MAP kinase cascades. Cell Signal 15(5):455–462

    Article  PubMed  CAS  Google Scholar 

  • Tedford K, Kim S, Sa D, Stevens K, Tyers M (1997) Regulation of the mating pheromone and invasive growth responses in yeast by two MAP kinase substrates. Curr Biol 7(4):228–238

    Article  PubMed  CAS  Google Scholar 

  • Tesmer JJ (2010) The quest to understand heterotrimeric G protein signaling. Nat Struct Mol Biol 17(6):650–652

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Thomas CJ, Briknarova K, Hilmer JK, Movahed N, Bothner B, Sumida JP, Tall GG, Sprang SR (2011) The nucleotide exchange factor Ric-8A is a chaperone for the conformationally dynamic nucleotide-free state of Galphai1. PLoS One 6(8):e23197

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Turner GE, Borkovich KA (1993) Identification of a G protein alpha subunit from Neurospora crassa that is a member of the Gi family. J Biol Chem 268(20):14805–14811

    PubMed  CAS  Google Scholar 

  • Vallim MA, Miller KY, Miller BL (2000) Aspergillus SteA (sterile12-like) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol Microbiol 36(2):290–301

    Article  PubMed  CAS  Google Scholar 

  • Venkatakrishnan AJ, Deupi X, Lebon G, Tate CG, Schertler GF, Babu MM (2013) Molecular signatures of G-protein-coupled receptors. Nature 494(7436):185–194

    Article  PubMed  CAS  Google Scholar 

  • Versele M, de Winde JH, Thevelein JM (1999) A novel regulator of G protein signalling in yeast, Rgs2, downregulates glucose-activation of the cAMP pathway through direct inhibition of Gpa2. EMBO J 18(20):5577–5591

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T, Stock J, Feldbrugge M (2012) Fungal development of the plant pathogen Ustilago maydis. FEMS Microbiol Rev 36(1):59–77

    Article  PubMed  CAS  Google Scholar 

  • Wang Y (2013) Fungal adenylyl cyclase acts as a signal sensor and integrator and plays a central role in interaction with bacteria. PLoS Pathog 9(10):e1003612

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang Y, Xu HP, Riggs M, Rodgers L, Wigler M (1991) byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the ras1 mutant phenotype. Mol Cell Biol 11(7):3554–3563

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang P, Perfect JR, Heitman J (2000) The G-protein beta subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol Cell Biol 20(1):352–362

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang X, Sheff MA, Simpson DM, Elion EA (2011) Ste11p MEKK signals through HOG, mating, calcineurin and PKC pathways to regulate the FKS2 gene. BMC Mol Biol 12:51

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang Y, Geng Z, Jiang D, Long F, Zhao Y, Su H, Zhang KQ, Yang J (2013) Characterizations and functions of regulator of G protein signaling (RGS) in fungi. Appl Microbiol Biotechnol 97(18):7977–7987

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Shen G, Gong J, Shen D, Whittington A, Qing J, Treloar J, Boisvert S, Zhang Z, Yang C, Wang P (2014) Noncanonical Gbeta Gib2 is a scaffolding protein promoting cAMP signaling through functions of Ras1 and Cac1 proteins in Cryptococcus neoformans. J Biol Chem 289(18):12202–12216

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wei H, Requena N, Fischer R (2003) The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol Microbiol 47(6):1577–1588

    Article  PubMed  CAS  Google Scholar 

  • Wei Y, Shen W, Dauk M, Wang F, Selvaraj G, Zou J (2004) Targeted gene disruption of glycerol-3-phosphate dehydrogenase in Colletotrichum gloeosporioides reveals evidence that glycerol is a significant transferred nutrient from host plant to fungal pathogen. J Biol Chem 279(1):429–435

    Article  PubMed  CAS  Google Scholar 

  • Welton RM, Hoffman CS (2000) Glucose monitoring in fission yeast via the Gpa2 Galpha, the Git5 Gbeta and the Git3 putative glucose receptor. Genetics 156(2):513–521

    PubMed Central  PubMed  CAS  Google Scholar 

  • Whiteway MS, Wu C, Leeuw T, Clark K, Fourest-Lieuvin A, Thomas DY, Leberer E (1995) Association of the yeast pheromone response G protein beta gamma subunits with the MAP kinase scaffold Ste5p. Science 269(5230):1572–1575

    Article  PubMed  CAS  Google Scholar 

  • Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79(1):143–180

    PubMed  CAS  Google Scholar 

  • Wilkie TM, Kinch L (2005) New roles for Galpha and RGS proteins: communication continues despite pulling sisters apart. Curr Biol 15(20):R843–R854

    Article  PubMed  CAS  Google Scholar 

  • Wright SJ, Inchausti R, Eaton CJ, Krystofova S, Borkovich KA (2011) RIC8 is a guanine-nucleotide exchange factor for Galpha subunits that regulates growth and development in Neurospora crassa. Genetics 189:1–12

    Article  CAS  Google Scholar 

  • Wu C, Leberer E, Thomas DY, Whiteway M (1999) Functional characterization of the interaction of Ste50p with Ste11p MAPKKK in Saccharomyces cerevisiae. Mol Biol Cell 10(7):2425–2440

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10(21):2696–2706

    Article  PubMed  CAS  Google Scholar 

  • Xu HP, White M, Marcus S, Wigler M (1994) Concerted action of RAS and G proteins in the sexual response pathways of Schizosaccharomyces pombe. Mol Cell Biol 14(1):50–58

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xu JR, Staiger CJ, Hamer JE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA 95(21):12713–12718

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xue C, Bahn YS, Cox GM, Heitman J (2006) G protein-coupled receptor Gpr4 senses amino acids and activates the cAMP-PKA pathway in Cryptococcus neoformans. Mol Biol Cell 17(2):667–679

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Xue C, Hsueh YP, Heitman J (2008) Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev 32(6):1010–1032

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yamane HK, Farnsworth CC, Xie HY, Howald W, Fung BK, Clarke S, Gelb MH, Glomset JA (1990) Brain G protein gamma subunits contain an all-trans-geranylgeranylcysteine methyl ester at their carboxyl termini. Proc Natl Acad Sci USA 87(15):5868–5872

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yan X, Li Y, Yue X, Wang C, Que Y, Kong D, Ma Z, Talbot NJ, Wang Z (2011) Two novel transcriptional regulators are essential for infection-related morphogenesis and pathogenicity of the rice blast fungus Magnaporthe oryzae. PLoS Pathog 7(12):e1002385

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang Q, Poole SI, Borkovich KA (2002) A G-protein beta subunit required for sexual and vegetative development and maintenance of normal G alpha protein levels in Neurospora crassa. Eukaryot Cell 1(3):378–390

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yu JH (2006) Heterotrimeric G protein signaling and RGSs in Aspergillus nidulans. J Microbiol 44(2):145–154

    PubMed  CAS  Google Scholar 

  • Yu JH, Wieser J, Adams TH (1996) The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development. EMBO J 15(19):5184–5190

    PubMed Central  PubMed  CAS  Google Scholar 

  • Yun CW, Tamaki H, Nakayama R, Yamamoto K, Kumagai H (1997) G-protein coupled receptor from yeast Saccharomyces cerevisiae. Biochem Biophys Res Commun 240(2):287–292

    Article  PubMed  CAS  Google Scholar 

  • Zeller CE, Parnell SC, Dohlman HG (2007) The RACK1 ortholog Asc1 functions as a G-protein beta subunit coupled to glucose responsiveness in yeast. J Biol Chem 282(34):25168–25176

    Article  PubMed  CAS  Google Scholar 

  • Zhang FL, Casey PJ (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu Rev Biochem 65:241–269

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Tang W, Liu K, Huang Q, Zhang X, Yan X, Chen Y, Wang J, Qi Z, Wang Z, Zheng X, Wang P, Zhang Z (2011) Eight RGS and RGS-like proteins orchestrate growth, differentiation, and pathogenicity of Magnaporthe oryzae. PLoS Pathog 7(12):e1002450

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhao X, Kim Y, Park G, Xu JR (2005) A mitogen-activated protein kinase cascade regulating infection-related morphogenesis in Magnaporthe grisea. Plant Cell 17(4):1317–1329

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zheng H, Zhou L, Dou T, Han X, Cai Y, Zhan X, Tang C, Huang J, Wu Q (2010) Genome-wide prediction of G protein-coupled receptors in Verticillium spp. Fungal Biol 114(4):359–368

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We acknowledge NIH grant GM086565 to K.A.B.. and an Indo-US Research Fellowship to R.T.

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Correspondence to Katherine A. Borkovich .

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Deka, R., Ghosh, A., Tamuli, R., Borkovich, K.A. (2016). 7 Heterotrimeric G Proteins. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_7

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