Molecular and functional characterization of a Rho GDP dissociation inhibitor in the filamentous fungus Tuber borchii

BMC Microbiology

Volumn 8, Issue , 2008, Pages

  Menotta, Michele ^a   Amicucci, Antonella ^a   Basili, Giorgio ^a   Polidori, Emanuela ^a   Stocchi, Vilberto ^a   Rivero, Francisco ^b,c  

^a UNIVERSITY OF URBINO   (Italy)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF HULL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; RAC1 PROTEIN; RHO FACTOR; ACTIN; PROTEIN CDC42; SACCHAROMYCES CEREVISIAE PROTEIN;

ACTIN POLYMERIZATION; AMINO ACID SEQUENCE; ARTICLE; CORRELATION ANALYSIS; CYTOSKELETON; DICTYOSTELIUM DISCOIDEUM; ECTOMYCORRHIZA; FUNGUS; GENE; GENE EXPRESSION; GENOME; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION; ROOT EXUDATE; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STIMULATION; SYMBIOSIS; TUBER BORCHII; YEAST; ANIMAL; ASCOMYCETES; DICTYOSTELIUM; DRUG ANTAGONISM; ENZYMOLOGY; GENE DELETION; GENE DOSAGE; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PHYLOGENY; PROTEIN BINDING; SEQUENCE HOMOLOGY; SOUTHERN BLOTTING; TWO HYBRID SYSTEM;

DICTYOSTELIUM DISCOIDEUM; EUKARYOTA; FUNGI; MAMMALIA; TUBER BORCHII;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; ASCOMYCOTA; BASE SEQUENCE; BLOTTING, SOUTHERN; CDC42 GTP-BINDING PROTEIN; DICTYOSTELIUM; GENE DELETION; GENE DOSAGE; GENE EXPRESSION PROFILING; GENETIC COMPLEMENTATION TEST; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; PHYLOGENY; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 43149119292     PISSN: 14712180     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-8-57     Document Type: Article

References (61)

1. Menotta M, Amicucci A, Gioacchini AM, Sisti D, Stocchi V: Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad and Tilia americana L. Curr Genet 2004, 46:158-165.
2. Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G: The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 2000, 13:693-698.
3. Nehls U, Béguiristain T, Ditengou F, Lapeyrie F, Martin F: The expression of a symbiosis-regulated gene in eucalypt roots is regulated by auxins and hypaphorine, the tryptophan betaine of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Planta 1998, 207:296-302.
4. Podila GK, Zheng J, Balasubramanian S, Sundaram S, Hiremath S, Brand JH, Hymes MJ: Fungal gene expression in early symbiotic interaction between Laccaria bicolor and red pine. Plant Soil 2002, 244:117-128.
5. Lee N, Kronstad JW: ras2 controls morphogenesis, pheromone response, and pathogenicity in the fungal pathogen Ustilago maydis. Euk Cell 2002, 1:954-966.
6. Hazan I, Liu H: Hyphal tip-associated localization of Cdc42 is F-actin dependent in Candida albicans. Euk Cell 2002, 1:856-864.
7. Gorfer M, Tarkka MT, Hanif M, Pardo AG, Laitiainen E, Raudaskoski M: Characterization of small GTPases Cdc42 and Rac and the relationship between Cdc42 and actin cytoskeleton in vegetative and ectomycorrhizal hyphae of Suillus bovinus. Mol Plant Microbe Interact 2001, 14:135-144.
8. Uetake Y, Peterson RL: Changes in actin filament arrays in pro-tocorm cells of the orchid species, Spiranthes sinensis, induced by the symbiotic fungus Ceratobasidium corni-gerum. Can J Bot 1997, 75:1661-1669.
9. Ambra R, Macino G: Cloning and characterization of PKC-homologous genes in the truffle species Tuber borchii and Tuber magnatum. FEMS Microbiol Lett 2000, 189:45-53.
10. Lacourt I, Duplessis S, Abbà S, Bonfante P, Martin F: Isolation and characterization of differentially expressed genes in the mycelium and fruit body of Tuber borchii. Appl Environ Microbiol 2002, 68:4574-4582.
11. Soragni E, Bolchi A, Balestrini R, Gambaretto C, Percudani R, Bonfante P, Ottonello S: A nutrient-regulated, dual localization phospholipase A(2) in the symbiotic fungus Tuber borchii. EMBO J 2001, 20:5079-5090.
12. Balestrini R, Manieri D, Soragni E, Garnero L, Rollino S, Viotti A, Ottonello S, Bonfante P: Differential expression of chitin syn-thase III and IV mRNAs in ascomata of Tuber borchii Vittad. Fungal Genet Biol 2000, 31:219-232.
13. Menotta M, Amicucci A, Basili G, Rivero F, Polidori E, Sisti D, Stocchi V: Molecular characterisation of the small GTPase CDC42 in the ectomycorrhizal fungus Tuber borchii Vittad. Protoplasma 2007, 231:227-237.
14. Burridge K, Wennerberg K: Rho and Rac take center stage. Cell 2004, 116:167-179.
15. Jaffe AB, Hall A: Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 2005, 21:247-269.
16. Dransart E, Olofsson B, Cherfils J: RhoGDIs revisited: novel roles in Rho regulation. Traffic 2005, 6:957-966.
17. DerMardirossian C, Bokoch GM: GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 2005, 15:356-363.
18. Dovas A, Couchman JR: RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem J 2005, 390:1-9.
19. Togawa A, Miyoshi J, Ishizaki H, Tanaka M, Takakura A, Nishioka H, Yoshida H, Doi T, Mizoguchi A, Matsuura N, Niho Y, Nishimune Y, Nishikawa S, Takai Y: Progressive impairment of kidneys and reproductive organs in mice lacking Rho GDIa. Oncogene 1999, 18:5373-5380.
20. Yin L, Schwartzberg P, Scharton-Kersten TM, Staudt L, Lenardo M: Immune responses in mice defficient in Ly-GDI, a lymphoid-specific regulator of Rho GTPases. Mol Immunol 1997, 34:481-491.
21. Zalcman G, Closson V, Camonis J, Honore N, Rousseau-Merck MF, Tavitian A, Olofsson B: RhoGDI-3 is a new GDP dissociation inhibitor (GDI). J Biol Chem 1996, 271:30366-30374.
22. Imai K, Kijima T, Noda Y, Sutoh K, Yoda K, Adachi H: A Rho GDP-dissociation inhibitor is involved in cytokinesis in Dictyostelium. Biochem Biophys Res Commun 2002, 296:305-312.
23. Rivero F, Illenberger D, Somesh BP, Dislich H, Adam N, Meyer AK: Defects in cytokinesis, actin reorganization and the contractile vacuole in cells deficient in RhoGDI. EMBO J 2002, 21:4539-4549.
24. Masuda T, Tanaka K, Nonaka H, Yamochi W, Maeda A, Takai Y: Molecular cloning and characterization of yeast rho GDP dissociation inhibitor. J Biol Chem 1994, 269:19713-19718.
25. Koch G, Tanaka K, Masuda T, Yamochi W, Nonaka H, Takai Y: Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor in Saccharomyces cerevisiae. Oncogene 1997, 15:417-422.
26. Richman TJ, Toenjes KA, Morales SE, Cole KC, Wasserman BT, Taylor CM, Koster JA, Whelihan MF, Johnson DI: Analysis of cell-cycle specific localization of the Rdi1p RhoGDI and the structural determinants required for Cdc42p membrane localization and clustering at sites of polarized growth. Curr Genet 2004, 45:339-349.
27. Cole KC, McLaughlin HW, Johnson DI: Use of bimolecular fluorescence complementation to study in vivo interactions between Saccharomyces cerevisiae Cdc42p and Rdi1p. Euk Cell 2007, 6:378-387.
28. Rivero F, Somesh BP: Signal transduction pathways regulated by Rho GTPases in Dictyostelium. J Muscle Res Cell Motil 2002, 23:737-749.
29. Vlahou G, Rivero F: Rho GTPase signaling in Dictyostelium: insights from the genome. Eur J Cell Biol 2006, 85:947-959.
30. Gurr SJ, Unkles SE, Kinghorn JR: The structure and organisation of nuclear genes of filamentous fungi. In Gene structure in eukary-otic microbes (Soc Microbiol Spec Publ 23) Edited by: Kinghorn JR. Oxford, IRL Press; 1987:93-139.
31. Kozak M: An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res 1987, 15:8125-8148.
32. Hoffman GR, Nassar N, Cerione RA: Cell Structure of the Rho family GTP-binding protein Cdc42 in complex with the mul-tifunctional regulator RhoGDI. Cell 2000, 100:345-356.
33. Gosser YQ, Nomanbhoy TK, Aghazadeh B, Manor D, Combs C, Cerione RA, Rosen MK: C-terminal binding domain of Rho GDP-dissociation inhibitor directs N-terminal inhibitory peptide to GTPases. Nature 1997, 387:814-819.
34. Keep NH, Barnes M, Barsukov I, Badii R, Lian LY, Segal AW, Moody PC, Roberts GC: A modulator of rho family G proteins, rhoGDI, binds these G proteins via an immunoglobulin-like domain and a flexible N-terminal arm. Structure 1997, 15:623-633.
35. Hall AL, Schlein A, Condeelis J: Relationship of pseudopod extension to chemotactic hormone-induced actin polymerization in amoeboid cells. J Cell Biochem 1988, 37:285-299.
36. Menotta M, Gioacchini AM, Amicucci A, Buffalini M, D Sisti, Stocchi V: Headspace solid-phase microextraction with gas chroma-tography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system. Rapid Commun Mass Spectrom 2004, 18:206-210.
37. Cullen D: Recent advances on the molecular genetics of ligni-nolytic fungi. J Biotechnol 1997, 53:273-289.
38. Weig M, Haynes K, Rogers TR, Kurzai O, Frosch M, Muhlschlegel FA: A GAS-like gene family in the pathogenic fungus Candida glabrata. Microbiology 2001, 147:2007-2019.
39. De Bernardis F, Muhlschlegel FA, Cassone A, Fonzi WA: The pH of the host niche controls gene expression and virulence of Candida albicans. Infect Immunol 1998, 66:3317-3325.
40. Weber M, Salo V, Uuskallio M, Raudaskoski M: Ectopic expression of constitutively active Cdc42 small GTPase alters the morphology of haploid and dikaryotic hyphae in the filamentous homobasidiomycete Schizophyllum commune. Fungal Genet Biol 2005, 42:624-637.
41. Mahlert M, Leveleki L, Hlubek A, Sandrock B, Bölker M: Rac1 and Cdc42 regulate hyphal growth and cytokinesis in the dimor-phic fungus Ustilago maydis. Mol Microbiol 2006, 59:567-578.
42. Boyce KJ, Hynes MJ, Andrianopoulos A: The Ras and Rho GTPases genetically interact to co-ordinately regulate cell polarity during development in Penicillium marneffei. Mol Microbiol 2005, 55:1487-1501.
43. Harris SD, Momany M: Polarity in filamentous fungi: moving beyond the yeast paradigm. Fungal Genet Biol 2004, 41:391-400.
44. Hanif M, Pardo AG, Gorfer M, Raudaskoski M: T-DNA transfer and integration in the ectomycorrhizal fungus Suillus bovinus using hygromycin B as a selectable marker. Curr Genet 2002, 41:183-188.
45. Pardo AG, Hanif M, Raudaskoski M, Gorfer M: Genetic transformation of ectomycorrhizal fungi mediated by Agrobacte-rium tumefaciens. Mycol Res 2002, 106:132-137.
46. Combier JP, Melayah D, Raffier C, Gay G, Marmeisse R: Agrobacte-rium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum. FEMS Microbiol Lett 2003, 220:141-148.
47. Grimaldi B, de Raaf MA, Filetici P, Ottonello S, Ballario P: Agrobac-terium-mediated gene transfer and enhanced green fluorescent protein visualization in the mycorrhizal ascomycete Tuber borchii: a first step towards truffle genetics. Curr Genet 2005, 48:69-74.
48. Tanaka K, Takai Y: Control of reorganization of the actin cytoskeleton by Rho family small GTP-binding proteins in yeast. Curr Opin Cell Biol 1998, 10:112-116.
49. Charest PG, Firtel RA: Big roles for small GTPases in the control of directed cell movement. Biochem J 2007, 401:377-390.
50. Platko J, Leonard DA, Adra CN, Shaw RJ, Cerione RA: A single residue can modify target-binding affinity and activity of the functional domain of the Rho-subfamily GDP dissociation inhibitors. Proc Natl Acad Sci USA 1995, 92:2974-2978.
51. Park KC, Rivero F, Meili R, Lee S, Apone F, Firtel RA: Rac regulation of chemotaxis and morphogenesis. EMBO J 2004, 23:4177-4189.
52. Murashige T, Skoog F: A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 1962, 15:473-497.
53. Urushihara H: Cultivation, spore production and mating. Methods Mol Biol 2006, 346:113-124.
54. Erland S, Henrion B, Martin F, Glover LA, Alexander IJ: Identification of ectomycorrhizal basidiomycete Tylospora fibrillosa Donk by RFLPs analysis of the PCR-amplified ITS and IGS regions of ribosomal DNA. New Phytologist 1994, 126:525-532.
55. Polidori E, Agostini D, Zeppa S, Potenza L, Palma F, Sisti D, Stocchi V: Identification of differentially expressed cDNA clones in Tilia platyphyllos-Tuber borchii ectomycorrhizae using a differential screening approach. Mol Genet Genomics 2002, 266:858-864.
56. Sambrook J, Fritsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. 2nd edition. New York, Cold Spring Harbor Laboratory Press; 1989.
57. Winer J, Jung CKS, Shackel I, Williams PM: Development and validation of the real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Analyt Biochem 1999, 270:41-49.
58. Illenberger D, Schwald F, Pimmer D, Binder W, Maier G, Dietrich A, Gierschik P: Stimulation of phospholipase C-b2 by the Rho GTPases Cdc42 and Racl. EMBO J 1998, 17:6241-6249.
59. Westphal M, Jungbluth A, Heidecker M, Mühlbauer B, Heizer C, Schwartz JM, Marriott G, Gerisch G: Microfilament dynamics during cell movement and chemotaxis monitored using a GFP-actin fusion protein. Curr Biol 1997, 7:176-183.
60. Kimmel AR, Faix J: Generation of multiple knockout mutants using the Cre-loxP system. Methods Mol Biol 2006, 346:187-199.
61. Scheffzek K, Stephan I, Jensen ON, Illenberger D, Gierschik P: The Rac-RhoGDI complex and the structural basis for the regulation of Rho proteins by RhoGDI. Nature Struct Biol 2000, 7:122-126.