Genome-wide inventory of metal homeostasis-related gene products including a functional phytochelatin synthase in the hypogeous mycorrhizal fungus Tuber melanosporum

Fungal Genetics and Biology

Volumn 48, Issue 6, 2011, Pages 573-584

  Bolchi, Angelo ^a   Ruotolo, Roberta ^a   Marchini, Gessica ^a   Vurro, Emanuela ^a   di Toppi, Luigi Sanità ^a   Kohler, Annegret ^b   Tisserant, Emilie ^b   Martin, Francis ^b   Ottonello, Simone ^a  

^a UNIVERSITY OF PARMA   (Italy)

^b UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Black truffle genome; Metal homeostasis; Metal transportome; Metallothionein; Mycorrhizae; Phytochelatin synthase

Indexed keywords

CADMIUM; COPPER; GLUTATHIONE; METALLOTHIONEIN; PHYTOCHELATIN SYNTHASE; ZINC;

ANTIOXIDANT ACTIVITY; ARTICLE; ASPERGILLUS NIDULANS; BOTRYTIS CINEREA; CONTROLLED STUDY; DETOXIFICATION; ENZYME ACTIVITY; FUNGAL STRAIN; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; MAGNAPORTHE GRISEA; METAL METABOLISM; MYCORRHIZA; NEUROSPORA CRASSA; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHYLOGENY; PLANT ROOT; PRIORITY JOURNAL; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; SYMBIONT; TUBER (GENUS); TUBER MELANOSPORUM; UPREGULATION;

AMINOACYLTRANSFERASES; ASCOMYCOTA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; GENOME, FUNGAL; METALS; MOLECULAR SEQUENCE DATA; MYCORRHIZAE; PHYLOGENY;

ASCOMYCOTA; FUNGI; TUBER MELANOSPORUM;

EID: 78651306290     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.11.003     Document Type: Article

References (84)

1. Adriaensen K., Van Der Lelie D., Van Laere A., Vangronsveld J., Colpaert J.V. A zinc-adapted fungus protects pines from zinc stress. New Phytol. 2004, 161:549-555.
2. Allen J.W., Shachar-Hill Y. Sulfur transfer through an Arbuscular Mycorrhiza. Plant Physiol. 2009, 149:549-560.
3. Amaro F., Ruotolo R., Martin-Gonzalez A., Faccini A., Ottonello S., Gutierrez J.C. A pseudo-phytochelatin synthase in the ciliated protozoan Tetrahymena thermophila. Comp. Biochem. Physiol. - Part C: Toxicol. Pharmacol. 2009, 149:598-604.
4. Andreini C., Banci L., Bertini I., Rosato A. Counting the zinc-proteins encoded in the human genome. J. Proteome Res. 2006, 5:196-201.
5. Averbeck N.B., Borghouts C., Hamann A., Specke V., Osiewacz H.D. Molecular control of copper homeostasis in filamentous fungi: increased expression of a metallothionein gene during aging of Podospora anserina. Mol. Genet. Genomics 2001, 264:604-612.
6. Avery S.V. Metal toxicity in yeasts and the role of oxidative stress. Adv. Appl. Microbiol. 2001, 49:111-142.
7. Babcock M., de Silva D., Oaks R., Davis-Kaplan S., Jiralerspong S., Montermini L., Pandolfo M., Kaplan J. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 1997, 276:1709-1712.
8. Bellion M., Courbot M., Jacob C., Blaudez D., Chalot M. Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol. Lett. 2006, 254:173-181.
9. Berthelsen B.O., Olsenb R.A., Steinnes E. Ectomycorrhizal heavy metal accumulation as a contributing factor to heavy metal levels in organic surface soils Sci. Total Environ. 1995, 170:141-149.
10. Binz P.-A., Kägi J.H.R. Metallothionein: Molecular Evolution and Classification 1999, Birkhäuser Verlag, Basel.
11. Bobrowicz P., Wysocki R., Owsianik G., Goffeau A., Ulaszewski S. Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast 1997, 13:819-828.
12. Branco R., Chung A.P., Morais P.V. Sequencing and expression of two arsenic resistance operons with different functions in the highly arsenic-resistant strain Ochrobactrum tritici SCII24T. BMC Microbiol. 2008, 8:95.
13. Brown M.T., Wilkins D.A. Zinc tolerance of mycorrhizal Betula. New Phytol. 1985, 99:101-106.
14. Burgess T.I., Maljczuk N., Grove T.S. The ability of 16 ectomycorrhizal fungi to increase growth and phosphorus uptake of Eucalyptus globulus Labill. and E. diversicolor F. Muell. Plant Soil 1993, 153:155-164.
15. Butt T.R., Sternberg E.J., Gorman J.A., Clark P., Hamer D., Rosenberg M., Crooke S.T. Copper metallothionein of yeast, structure of the gene, and regulation of expression. Proc. Natl. Acad. Sci. USA 1984, 81:3332-3336.
16. Byrne A.R., Ravnik V., Kosta L. Trace element concentrations in higher fungi. Sci. Total Environ. 1976, 6:65-78.
17. Cellier M., Prive G., Belouchi A., Kwan T., Rodrigues V., Chia W., Gros P. Nramp defines a family of membrane proteins. Proc. Natl. Acad. Sci. USA 1995, 92:10089-10093.
18. Chaurasia N., Mishra Y., Rai L.C. Cloning expression and analysis of phytochelatin synthase (pcs) gene from Anabaena sp. PCC 7120 offering multiple stress tolerance in Escherichia coli. Biochem. Biophys. Res. Commun. 2008, 376:225-230.
19. Clarkson D.T. Factors affecting mineral nutrient acquisition by plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1985, 36:77-115.
20. Clemens S. Evolution and function of phytochelatin synthases. J. Plant Physiol. 2006, 163:319-332.
21. Clemens S., Peršoh D. Multi-tasking phytochelatin synthases. Plant Sci. 2009, 177:266-271.
22. Clemens S., Simm C. Schizosaccharomyces pombe as a model for metal homeostasis in plant cells: the phytochelatin-dependent pathway is the main cadmium detoxification mechanism. New Phytol. 2003, 159:323-330.
23. Clemens S., Kim E.J., Neumann D., Schroeder J.I. Tolerance to toxic metals by a gene family of phytochelatin synthases from plants and yeast. Embo J. 1999, 18:3325-3333.
24. Clemens S., Schroeder J.I., Degenkolb T. Caenorhabditis elegans expresses a functional phytochelatin synthase. Eur. J. Biochem. 2001, 268:3640-3643.
25. Cobbett C., Goldsbrough P. Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu. Rev. Plant Biol. 2002, 53:159-182.
26. Diffels J.F., Seret M.L., Goffeau A., Baret P.V. Heavy metal transporters in Hemiascomycete yeasts. Biochimie 2006, 88:1639-1649.
27. Dix D.R., Bridgham J.T., Broderius M.A., Byersdorfer C.A., Eide D.J. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J. Biol. Chem. 1994, 269:26092-26099.
28. Eide D.J. Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 2006, 1763:711-722.
29. Eitinger T., Suhr J., Moore L., Smith J.A. Secondary transporters for nickel and cobalt ions: theme and variations. Biometals 2005, 18:399-405.
30. Gaither L.A., Eide D.J. Eukaryotic zinc transporters and their regulation. Biometals 2001, 14:251-270.
31. Glerum D.M., Shtanko A., Tzagoloff A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J. Biol. Chem. 1996, 271:14504-14509.
32. Guerinot M.L. The ZIP family of metal transporters. Biochim. Biophys. Acta 2000, 1465:190-198.
33. Ha S.B., Smith A.P., Howden R., Dietrich W.M., Bugg S., O'Connell M.J., Goldsbrough P.B., Cobbett C.S. Phytochelatin synthase genes from Arabidopsis and the yeast Schizosaccharomyces pombe. Plant Cell 1999, 11:1153-1164.
34. Hall J.L. Cellular mechanisms for heavy metal detoxification and tolerance. J. Exp. Bot. 2002, 53:1-11.
35. Haselwandter K., Winkelmann G. Ferricrocin - an ectomycorrhizal siderophore of Cenococcum geophilum. Biometals 2002, 15:73-77.
36. Hérouarta D., Baudouina E., Frendoa P., Harrisona J., Santosb R., Jameta A., Van de Sypea G., Touatib D., Puppo A. Reactive oxygen species, nitric oxide and glutathione: a key role in the establishment of the legume - Rhizobium symbiosis?. Plant Physiol. Biochem. 2002, 40:619-624.
37. Horng Y.C., Cobine P.A., Maxfield A.B., Carr H.S., Winge D.R. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome C oxidase. J. Biol. Chem. 2004, 279:35334-35340.
38. Hwang C.S., Kolattukudy P.E. Isolation and characterization of genes expressed uniquely during appressorium formation by Colletotrichum gloeosporioides conidia induced by the host surface wax. Mol. Genet. Genomics 1995, 247:282-294.
39. Imlay J.A. Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 2008, 77:755-776.
40. Imlay K.R., Imlay J.A. Cloning and analysis of sodC, encoding the copper-zinc superoxide dismutase of Escherichia coli. J. Bacteriol. 1996, 178:2564-2571.
41. Ishikawa T., Li Z.S., Lu Y.P., Rea P.A. The GS-X pump in plant, yeast, and animal cells: structure, function, and gene expression. Biosci. Rep. 1997, 17:189-207.
42. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 1983, 153:163-168.
43. Kiranmayi P., Mohan P.M. Metal transportome of Neurospora crassa. In Silico Biol. 2006, 6:169-180.
44. Klug K. Systemic Effects of Mycorrhization on Root and Shoot Physiology of Lycopersicon esculentum 2006, Forschungszentrum Jülich, Zentralbibliothek, Verlag.
45. Le Quere A., Wright D.P., Soderstrom B., Tunlid A., Johansson T. Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol. Plant-Microbe Interact. 2005, 18:659-673.
46. Lepp N.W., Harrison S.C.S., Morrell B.G. A role for Amanita muscaria L. in the circulation of cadmium and vanadium in a non-polluted woodland. Environ. Geoch. Health 1987, 9:61-64.
47. Lerch K. Copper metallothionein, a copper-binding protein from Neurospora crassa. Nature 1980, 284:368-370.
48. Lin S.J., Pufahl R.A., Dancis A., O'Halloran T.V., Culotta V.C. A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. Chem. 1997, 272:9215-9220.
49. Martin F., Aerts A., Ahren D., Brun A., Danchin E.G., Duchaussoy F., Gibon J., Kohler A., Lindquist E., Pereda V., Salamov A., Shapiro H.J., Wuyts J., Blaudez D., Buee M., Brokstein P., Canback B., Cohen D., Courty P.E., Coutinho P.M., Delaruelle C., Detter J.C., Deveau A., DiFazio S., Duplessis S., Fraissinet-Tachet L., Lucic E., Frey-Klett P., Fourrey C., Feussner I., Gay G., Grimwood J., Hoegger P.J., Jain P., Kilaru S., Labbe J., Lin Y.C., Legue V., Le Tacon F., Marmeisse R., Melayah D., Montanini B., Muratet M., Nehls U., Niculita-Hirzel H., Oudot-Le Secq M.P., Peter M., Quesneville H., Rajashekar B., Reich M., Rouhier N., Schmutz J., Yin T., Chalot M., Henrissat B., Kues U., Lucas S., Van de Peer Y., Podila G.K., Polle A., Pukkila P.J., Richardson P.M., Rouze P., Sanders I.R., Stajich J.E., Tunlid A., Tuskan G., Grigoriev I.V. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
50. Martin F., Kohler A., Murat C., Balestrini R., Coutinho P.M., Jaillon O., Montanini B., Morin E., Noel B., Percudani R., Porcel B., Rubini A., Amicucci A., Amselem J., Anthouard V., Arcioni S., Artiguenave F., Aury J.M., Ballario P., Bolchi A., Brenna A., Brun A., Buee M., Cantarel B., Chevalier G., Couloux A., Da Silva C., Denoeud F., Duplessis S., Ghignone S., Hilselberger B., Iotti M., Marcais B., Mello A., Miranda M., Pacioni G., Quesneville H., Riccioni C., Ruotolo R., Splivallo R., Stocchi V., Tisserant E., Viscomi A.R., Zambonelli A., Zampieri E., Henrissat B., Lebrun M.H., Paolocci F., Bonfante P., Ottonello S., Wincker P. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 2010, 464:1033-1038.
51. Minet M., Dufour M.E., Lacroute F. Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 1992, 2:417-422.
52. Miyabe S., Izawa S., Inoue Y. Expression of ZRC1 coding for suppressor of zinc toxicity is induced by zinc-starvation stress in Zap1-dependent fashion in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 2000, 276:879-884.
53. Montanini B., Moretto N., Soragni E., Percudani R., Ottonello S. A high-affinity ammonium transporter from the mycorrhizal ascomycete Tuber borchii. Fungal Genet. Biol. 2002, 36:22-34.
54. Morel M., Kohler A., Martin F., Gelhaye E., Rouhier N. Comparison of the thiol-dependent antioxidant systems in the ectomycorrhizal Laccaria bicolor and the saprotrophic Phanerochaete chrysosporium. New Phytol. 2008, 180:391-407.
55. Moretto N., Bolchi A., Rivetti C., Imbimbo B.P., Villetti G., Pietrini V., Polonelli L., Del Signore S., Smith K.M., Ferrante R.J., Ottonello S. Conformation-sensitive antibodies against alzheimer amyloid-beta by immunization with a thioredoxin-constrained B-cell epitope peptide. J. Biol. Chem. 2007, 282:11436-11445.
56. Murasugi A., Wada C., Hayashi Y. Cadmium-binding peptide induced in fission yeast, Schizosaccharomyces pombe. J. Biochem. 1981, 90:1561-1564.
57. Nies D.H., Koch S., Wachi S., Peitzsch N., Saier M.H. CHR, a novel family of prokaryotic proton motive force-driven transporters probably containing chromate/sulfate antiporters. J. Bacteriol. 1998, 180:5799-5802.
58. Nilsson J., Persson B., von Heijne G. Consensus predictions of membrane protein topology. FEBS Lett. 2000, 486:267-269.
59. Nordberg, G., Fowler, B., Nordberg, M., Friberg, L., 2007. Handbook on the Toxicology of Metals, third ed.
60. Ortiz D.F., Kreppel L., Speiser D.M., Scheel G., McDonald G., Ow D.W. Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. Embo J. 1992, 11:3491-3499.
61. Palmer C.M., Guerinot M.L. Facing the challenges of Cu, Fe and Zn homeostasis in plants. Nat. Chem. Biol. 2009, 5:333-340.
62. Pocsi I., Prade R.A., Penninckx M.J. Glutathione, altruistic metabolite in fungi. Adv. Microb. Physiol. 2004, 49:1-76.
63. Rea P.A., Vatamaniuk O.K., Rigden D.J. Weeds, worms, and more. Papain's long-lost cousin, phytochelatin synthase. Plant Physiol. 2004, 136:2463-2474.
64. Romanyuk N.D., Rigden D.J., Vatamaniuk O.K., Lang A., Cahoon R.E., Jez J.M., Rea P.A. Mutagenic definition of a papain-like catalytic triad, sufficiency of the N-terminal domain for single-site core catalytic enzyme acylation, and C-terminal domain for augmentative metal activation of a eukaryotic phytochelatin synthase. Plant Physiol. 2006, 141:858-869.
65. Ruotolo R., Peracchi A., Bolchi A., Infusini G., Amoresano A., Ottonello S. Domain organization of phytochelatin synthase: functional properties of truncated enzyme species identified by limited proteolysis. J. Biol. Chem. 2004, 279:14686-14693.
66. Ruotolo R., Marchini G., Ottonello S. Membrane transporters and protein traffic networks differentially affecting metal tolerance. A genomic phenotyping study in yeast. Genome Biol. 2008, 9:R67.
67. Sahay R., Yadav R.S., Yadav K.D. Purification and characterization of laccase secreted by L. lividus. Appl. Biochem. Biotechnol. 2009, 157:311-320.
68. Saitoh Y., Izumitsu K., Tanaka C. Phylogenetic analysis of heavy-metal ATPases in fungi and characterization of the copper-transporting ATPase of Cochliobolus heterostrophus. Mycol. Res. 2009, 113:737-745.
69. Schützendübel A., Polle A. Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J. Exp. Bot. 2002, 53:1351-1365.
70. Shen J., Hsu C.M., Kang B.K., Rosen B.P., Bhattacharjee H. The Saccharomyces cerevisiae Arr4p is involved in metal and heat tolerance. Biometals 2003, 16:369-378.
71. Szaniszlo P.J., Powell P.E., Reid C.P.P., Cline G.R. Production of hydroxamate siderophore iron chelators by ectomycorrhizal fungi. Mycologia 1981, 73:1158-1174.
72. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
73. Tatry M.V., El Kassis E., Lambilliotte R., Corratge C., van Aarle I., Amenc L.K., Alary R., Zimmermann S., Sentenac H., Plassard C. Two differentially regulated phosphate transporters from the symbiotic fungus Hebeloma cylindrosporum and phosphorus acquisition by ectomycorrhizal Pinus pinaster. Plant J. 2009, 57:1092-1102.
74. Trampczynska A., Böttcher C., Clemens S. The transition metal chelator nicotianamine is synthesized by filamentous fungi. FEBS Lett. 2006, 580:3173-3178.
75. Tsuji N., Nishikori S., Iwabe O., Shiraki K., Miyasaka H., Takagi M., Hirata K., Miyamoto K. Characterization of phytochelatin synthase-like protein encoded by alr0975 from a prokaryote, Nostoc sp. PCC 7120. Biophys. Res. Commun. 2004, 315:751-755.
76. Tucker S.L., Thornton C.R., Tasker K., Jacob C., Giles G., Egan M., Talbot N.J. A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 2004, 16:1575-1588.
77. Vallino M., Martino E., Boella F., Murat C., Chiapello M., Perotto S. Cu, Zn superoxide dismutase and zinc stress in the metal-tolerant ericoid mycorrhizal fungus Oidiodendron maius Zn. FEMS Microbiol. Lett. 2009, 293:48-57.
78. Vatamaniuk O.K., Bucher E.A., Ward J.T., Rea P.A. A new pathway for heavy metal detoxification in animals. Phytochelatin synthase is required for cadmium tolerance in Caenorhabditis elegans. J. Biol. Chem. 2001, 276:20817-20820.
79. Vurro, E., Ruotolo, R., Ottonello, S., Elviri, L., Maffini, M., Falasca, G., Zanella, L., Altamura, M.M., Sanità di Toppi, L., in press. Phytochelatins govern zinc/copper homeostasis and cadmium detoxification in Cuscuta campestris parasitizing Daucus carota. Environ. Exp. Bot.
80. Williams R.J.P. The symbiosis of metal ion and protein chemistry. Pure Appl. Chem. 1983, 55:35-46.
81. Williams L.E., Mills R.F. P(1B)-ATPases - an ancient family of transition metal pumps with diverse functions in plants. Trends Plant Sci. 2005, 10:491-502.
82. Williams L.E., Pittman J.K., Hall J.L. Emerging mechanisms for heavy metal transport in plants. Biochim. Biophys. Acta 2000, 1465:104-126.
83. Wong P.C., Waggoner D., Subramaniam J.R., Tessarollo L., Bartnikas T.B., Culotta V.C., Price D.L., Rothstein J., Gitlin J.D. Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA 2000, 97:2886-2891.
84. Yun C.W., Bauler M., Moore R.E., Klebba P.E., Philpott C.C. The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J. Biol. Chem. 2001, 276:10218-10223.