Trehalose turnover during abiotic stress in arbuscular mycorrhizal fungi

New Phytologist

Volumn 174, Issue 4, 2007, Pages 879-891

  Ocón, Aurora ^a   Hampp, Rüdiger ^a   Requena, Natalia ^a,b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

Author keywords

Abiotic stress; Glomus intraradices; Glomus mosseae; Mycorrhizal fungi; Neutral trehalase; Trehalose; Trehalose 6 P phosphatase

Indexed keywords

ALPHA, ALPHA PHOSPHOTREHALASE; ALPHA, ALPHA-PHOSPHOTREHALASE; DISACCHARIDASE; FUNGAL PROTEIN; TREHALASE; TREHALOSE; UNCLASSIFIED DRUG;

ARBUSCULAR MYCORRHIZA; DISACCHARIDE; ENZYME ACTIVITY; OSMOSIS; RNA; SPORULATION; YEAST;

ARTICLE; ENZYMOLOGY; FUNGUS; GROWTH, DEVELOPMENT AND AGING; KINETICS; METABOLISM; MICROBIOLOGY; MYCORRHIZA; TREE;

DISACCHARIDASES; FUNGAL PROTEINS; FUNGI; KINETICS; MYCORRHIZAE; TREES; TREHALASE; TREHALOSE;

ARBUSCULAR; FUNGI; GLOMUS INTRARADICES; GLOMUS MOSSEAE;

EID: 34248345021     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2007.02048.x     Document Type: Article

References (76)

1. Amaral FC, Van Dijck P, Nicoli JR. 1997. Molecular cloning of the neutral trehalase gene from Kluveromyces lactis and the distinction between neutral and acids trehalases. Archives of Microbiology 167 : 202 208.
2. Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y. 2003. Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiology 131 : 1496 1507.
3. Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y. 2002. Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiology 128 : 108 124.
4. Bécard G, Doner LW, Rolin DB, Douds DD, Pfeffer PE. 1991. Identification and quantification of trehalose in vesicular-arbuscular mycorrhizal fungi by in vivo 13C NMR and HPLC analyses. New Phytology 108 : 547 552.
5. Bécard G, Fortin JA. 1988. Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytology 108 : 211 218.
6. Bell W, Klaassen P, Ohnacker M, Boller T, Herweijer M, Schoppink P, Van der Zee P, Wiemken A. 1992. Characterization of the 56-kDa subunit of yeast trehalose-6-phosphate synthase and cloning of its gene reveal its identity with the product of CIF1, a regulator of carbon catabolite inactivation. European Journal of Biochemistry 209 : 951 959.
7. Benaroudj N, Lee DH, Goldberg AL. 2001. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. Journal of Biological Chemistry 276 : 24261 24267.
8. Borgia PT, Miao Y, Dodge CL. 1996. The orlA gene from Aspergillus nidulans encodes a trehalose-6-phosphate phosphatase necessary for normal growth and chitin synthesis at elevated temperatures. Molecular Microbiology 20 : 1287 1296.
9. Breuninger M, Requena N. 2004. Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genetics and Biology 41 : 794 804.
10. Breuninger M, Trujillo CG, Serrano E, Fischer R, Requena N. 2004. Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genetics and Biology 41 : 542 552.
11. Budi SW, Blal B, Gianinazzi S. 1999. Surface-sterilization of Glomus mosseae sporocarps for studying endomycorrhization in vitro. Mycorrhiza 9 : 65 68.
12. Cansado J, Soto T, Fernandez J, Vicente-Soler J, Gacto M. 1998a. Characterization of mutants devoid of neutral trehalase activity in the fission yeast Schizosaccharomyces pombe: partial protection from heat shock and high salt stress. Journal of Bacteriology 180 : 1342 1345.
13. Cansado J, Vicente-Soler J, Soto T, Fernandez J, Gacto M. 1998b. Trehalose-6P synthase is essential for trehalase activation triggered by glucose, nitrogen source or heat-shock, but not by osmostress. Schizosaccharomyces pombe. Biochimica et Biophysica Acta 1381 : 271 278.
14. Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA. 2001. Remodeling of yeast genome expression in response to environmental changes. Molecular Biology of the Cell 12 : 323 337.
15. Chang EC, Kosman DJ, Willsky GR. 1989. Arsenic oxide-induced thermotolerance in Saccharomyces cerevisiae. Journal of Bacteriology 171 : 6349 6352.
16. Crowe JH, Hoekstra FA, Crowe LM. 1992. Anhydrobiosis. Annual Review of Physiology 54 : 579 599.
17. Döhlemann G, Berndt P, Hahn M. 2006. Trehalose metabolism is important for heat stress tolerance and spore germination of Botrytis cinerea. Microbiology 152 : 2625 2634.
18. Einig W, Hampp R. 1990. Carbon partitioning in Norway spruce: Amounts of fructose 1,6-bisphosphate and of intermediates of starch/sucrose synthesis in relation to needle age and degree of needle loss. Trees 4 : 9 15.
19. Elliot B, Haltiwanger RS, Fuchter B. 1996. Synergy between trehalose and hsp104 for thermotolerance in Saccharomyces cerevisiae. Genetics 144 : 923 933.
20. d'Enfert C, Bonini BM, Zapella PD, Fontaine T, da Silva AM, Terenzi HF. 1999. Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa. Molecular Microbiology 32 : 471 483.
21. Enjalbert B, Nantel A, Whiteway M. 2003. Stress-induced gene expression in Candida albicans: absence of a general stress response. Molecular Biology of the Cell 14 : 1460 1467.
22. Eroglu A, Russo MJ, Bieganski R, Fowler A, Cheley S, Bayley H, Torner M. 2000. Intracellular trehalose improves the survival of criopreserved mammalian cells. Nature Biotechnology 18 : 163 167.
23. Fillinger S, Chaveroche MK, Van Dijck P, de Vries R, Ruijter G, Thevelein J, d'Enfert C. 2001. Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147 : 1851 1862.
24. Franco A, Soto T, Vicente-Soler J, Paredes V, Madrid M, Gacto M, Cansado J. 2003. A role for calcium in the regulation of neutral trehalase activity in the fission yeast Schizosaccharomyces pombe. Biochemical Journal 376 : 209 217.
25. Franco A, Soto T, Vicente-Soler J, Valero Guillen P, Cansado J, Gacto M. 2000. Characterization of tpp1+ as encoding a main trehalose-6P phosphatase in the fission yeast Schizosaccharomyces pombe. Journal of Bacteriology 182 : 588 5884.
26. Gancedo C, Flores CL. 2004. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Research 4 : 351 359.
27. Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias A. 2000. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. Journal of Biological Chemistry 275 : 5668 5674.
28. Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Molecular Biology of the Cell 11 : 4241 4257.
29. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods in Enzymology 350 : 87 96.
30. Harrison MJ, van Buuren ML. 1995. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378 : 626 629.
31. Hohmann S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiology and Molecular Biology Reviews 66 : 300 372.
32. Hottiger T, Boller T, Wiemken A. 1987. Rapid changes of heat and desiccation tolerance correlated with changes of trehalose content in Saccharomyces cerevisiaie cells subjected to temperature shifts. FEBS Letters 220 : 113 115.
33. Iwahashi H, Nwaka S, Obuchi K. 2000. Evidence for contribution of neutral trehalase in barotolerance of Saccharomyces cerevisiae. Applied and Environmental Microbiology 66 : 5182 5185.
34. Jorge JA, Polizeli ML, Thevelein JM, Terenzi HF. 1997. Trehalases and trehalose hydrolysis in fungi. FEMS Microbiology Letters 154 : 165 171.
35. Jun J, Abubaker J, Rehrer C, Pfeffer PE, Shachar-Hill Y, Lammers PJ. 2002. Expression in an arbuscular mycorrhizal fungus of genes putatively involved in metabolism, transport, the cytoskeleton and the cell cycle. Plant and Soil 244 : 141 148.
36. Knop M, Siegers K, Pereira G, Zachariae W, Winsor B, Nasmyth K, Schiebel E. 1999. Epitope tagging of yeast genes using a PCR-based strategy, more tags and improved practical routines. Yeast 15 : 963 972.
37. van Laere A. 1989. Trehalose, reserve and/or stress metabolite? FEMS Microbiology Review 63 : 201 210.
38. Lanfranco L, Novero M, Bonfante P. 2005. The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiology 137 : 1319 1330.
39. Liu Y, Zhu YG, Chen BD, Christie P, Li XL. 2004. Influence of the arbuscular mycorrhizal fungus Glomus mosseae on uptake of arsenate by the As hyperaccumulator fern Pteris vittata L. Mycorrhiza 15 : 187 192.
40. Londesborough J, Varimo K. 1984. Characterization of two trehalases in baker's yeast. Biochemical Journal 219 : 511 518.
41. Nicolaus B, Gambacorta A, Basso AL, Riccio R, De Rosa M, Grant WD. 1988. Trehalose in archaebacteria. Systematic and Applied Microbiology 10 : 215 217.
42. Nwaka S, Mechler B, Destruelle M, Holzer H. 1995. Phenotypic features of trehalase mutants in Saccharomyces cerevisiae. FEBS Letters 360 : 286 290.
43. Ocón A. 2004. Characterization of the role of trehalose in arbuscular mycorrhizal fungi. PhD thesis. Tübingen, Germany : University of Tübingen.
44. Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y. 1999. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiology 120 : 587 598.
45. Piotrowski M, Morsomme P, Boutry M, Oecking C. 1998. Complementation of the Saccharomyces cerevisiae plasma membrane H+-ATPase by a plant H+-ATPase generates a highly abundant fusicoccin binding site. Journal of Biological Chemistry 273 : 30018 30023.
46. Piper P, Lockheart A. 1988. A temperature-sensitive mutant of Saccharomyces cerevisiae defective in the specific phosphatase of trehalose biosynthesis. FEMS Microbiological Letters 49 : 245 250.
47. Reinders A, Burckert N, Hohmann S, Thevelein JM, Boller T, Wiemken A, de Virgilio C. 1997. Structural analysis of the subunits of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae and their function during heat shock. Molecular Microbiology 24 : 687 695.
48. Requena N, Fuller P, Franken P. 1999. Molecular characterisation of GmFOX2, an evolutionarily highly conserved gene from the mycorrhizal fungus Glomus mosseae, down-regulated during interaction with rhizobacteria. Molecular Plant-Microbe Interactions 12 : 934 942.
49. Ribeiro MJ, Reinders A, Boller T, Wiemken A, de Virgilio C. 1997. Trehalose synthesis is important for the acquisition of thermotolerance in Schizosaccharomyces pombe. Molecular Microbiology 25 : 571 581.
50. Schellenbaum L, Müller J, Boller Th, Wiemken A, Schüepp H. 1998. Effects of drought on non-mycorrhizal and mycorrhizal maize: changes in the pools of non-structural carbohydrates, in the activities of invertase and trehalase, and in the pools of amino acids and imino acids. New Phytologist 138 : 59 66.
51. Schellenbaum L, Sprenger N, Schüepp H, Wiemken A, Boller T. 1999. Effect of drought, transgenic expression of a fructan synthesizing enzyme and of mycorrhizal symbiosis on growth and soluble carbohydrate pools in tobacco plants. New Phytology 142 : 67 77.
52. Schubert A, Wyss P. 1995. Trehalase activity in mycorrhizal and nonmycorrhizal roots of leek and soybean. Mycorrhiza 5 : 401 404.
53. Schubert A, Wyss P, Wiemken A. 1992. Occurrence of trehalose in vesicular-arbuscular mycorrhizal fungi and in mycorrhizal roots. Journal of Plant Physiology 140 : 41 45.
54. Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG. 1995. Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiology 108 : 7 15.
55. Shima J, Hino A, Yamada-Iyo C, Suzuki Y, Nakajima R, Watanabe H, Mori K, Takano H. 1999. Stress tolerance in doughs of Saccharomyces cerevisiae trehalase mutants derived from commercial baker's yeast. Applied Environmental Microbiology 65 : 2841 2846.
56. Singer MA, Lindquist S. 1998. Multiple effects of trehalose on protein folding in vitro and in vivo. Molecular Cell 1 : 639 648.
57. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA. 1996. Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycological Research 100 : 328 332.
58. Thevelein JM. 1984. Regulation of trehalose mobilization in fungi. Microbiological Review 48 : 42 59.
59. Thevelein JM, Hohmann S. 1995. Trehalose synthase: guard to the gate of glycolysis in yeast? Trends in Biochemistry and Science 20 : 3 10.
60. Van Dijck P, De Rop L, Szlufcik K, Van Ael E, Thevelein JM. 2002. Disruption of the Candida albicans TPS2 gene encoding trehalose-6-phosphate phosphatase decreases infectivity without affecting hypha formation. Infection and Immunity 70 : 1772 1782.
61. de Virgilio C, Burckert N, Barth G, Neuhaus JM, Boller T, Wiemken A. 1992. Cloning and disruption of a gene required for growth on acetate but not on ethanol: the acetyl-coenzyme A synthetase gene of Saccharomyces cerevisiae. Yeast 8 : 1043 1051.
62. de Virgilio C, Burckert N, Bell W, Jena P, Boller T, Wiemken A. 1993. Disruption of the TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. European Journal of Biochemistry 212 : 315 323.
63. de Virgilio C, Burckert N, Boller T, Wiemken A. 1991. A method to study the rapid phosphorylation-related modulation of neutral trehalase activity by temperature shifts in yeast. FEBS Letters 291 : 355 358.
64. Voit EO. 2003. Biochemical and genomic regulation of the trehalose cycle in yeast: review of observations and canonical model analysis. Journal of Theoretical Biology 223 : 55 78.
65. Vuorio OE, Kalkkinen N, Londesborough J. 1993. Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae. European Journal of Biochemistry 216 : 849 861.
66. Wera S, De Schrijver E, Geyskens I, Nwaka S, Thevelein JM. 1999. Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae. Biochemical Journal 343 : 621 626.
67. Wiemken A, Schellenberg M. 1982. Does a cyclic AMP-dependent phosphorylation initiate the transfer of trehalase from the cytosol into the vacuoles in Saccharomyces cerevisiae? FEBS Letters 27 : 329 331.
68. Winderickx J, de Winde JH, Crauwels M, Hino A, Hohmann P, VanDijck P, Thevelein JM. 1996. Regulation of genes encoding subunits of the trehalose synthase complex in Saccharomyces cerevisiae: novel variations of STRE-mediated transcription control? Molecular Genetics and Genomics 252 : 470 482.
69. Winkler K, Kienle I, Burgert M, Wagner JC, Holzer H. 1991. Metabolic regulation of the trehalose content of vegetative yeast. FEBS Letters 291 : 269 272.
70. Wolschek MF, Kubicek CP. 1997. The filamentous fungus Aspergillus niger contains two 'differentially regulated' trehalose-6-phosphate synthase-encoding genes, tpsA and tpsB. Journal of Biological Chemistry 272 : 2729 2735.
71. Xia Y, Gao M, Clarkson JM, Charnley AK. 2002. Molecular cloning, characterisation, and expression of a neutral trehalase from the insect pathogenic fungus Metarhizium anisopliae. Journal of Invertebrate Pathology 80 : 127 137.
72. Zähringer H, Burgert M, Holzer H, Nwaka S. 1997. Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by NTH1 gene is a multiple stress responsive protein. FEBS Letters 412 : 615 620.
73. Zähringer H, Holzer H, Nwaka S. 1998. Stability of neutral trehalase during heat stress in Saccharomyces cerevisiae is dependent on the activity of the catalytic subunits of cAMP-dependent protein kinase, Tpk1 and Tpk2. European Journal of Biochemistry 255 : 544 551.
74. Zähringer H, Thevelein JM, Nwaka S. 2000. Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth. Molecular Microbiology 35 : 397 406.
75. Zaragoza O, Blazquez MA, Gancedo C. 1998. Disruption of the Candida albicans TPS1 gene encoding trehalose-6-phosphate synthase impairs formation of hyphae and decreases infectivity. Journal of Bacteriology 180 : 3809 3815.
76. Zaragoza O, de Virgilio C, Ponton J, Gancedo C. 2002. Disruption in Candida albicans of the TPS2 gene encoding trehalose-6-phosphate phosphatase affects cell integrity and decreases infectivity. Microbiology 148 : 1281 1290.