Ambient pH stress inhibits spore germination of Penicillium expansum by impairing protein synthesis and folding: A proteomic-based study

Journal of Proteome Research

Volumn 9, Issue 1, 2010, Pages 298-307

  Li, Boqiang ^a   Lai, Tongfei ^a   Qin, Guozheng ^a   Tian, Shiping ^a  

^a INSTITUTE OF BOTANY   (China)

Author keywords

Ambient pH; Penicillium expansum; Protein folding; Protein synthesis; Spore germination

Indexed keywords

ADENOSINE TRIPHOSPHATE; ADENYLYLSULFATE KINASE; ALCOHOL DEHYDROGENASE; ASPARTATE TRANSFER RNA LIGASE; CATALASE; CYCLINE; ELONGATION FACTOR 2; GLUCOSE REGULATED PROTEIN 78; GLUTAMATE DEHYDROGENASE; GLYCINE TRANSFER RNA LIGASE; GUANINE NUCLEOTIDE BINDING PROTEIN; HEAT SHOCK PROTEIN 70; MALATE DEHYDROGENASE; PROTEIN DISULFIDE ISOMERASE; RAN PROTEIN; TRANSCRIPTION FACTOR IID;

ARTICLE; CELL PH; MYCOSIS; NONHUMAN; PENICILLIUM EXPANSUM; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEOMICS; SPORE GERMINATION; STRESS; TIME OF FLIGHT MASS SPECTROMETRY;

ADENOSINE TRIPHOSPHATE; CULTURE MEDIA; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUNGAL PROTEINS; GERMINATION; HYDROGEN-ION CONCENTRATION; PENICILLIUM; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEOME; PROTEOMICS; SOLUBILITY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPORES, FUNGAL; STRESS, PHYSIOLOGICAL;

PENICILLIUM EXPANSUM;

EID: 73649147742     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr900622j     Document Type: Article

References (52)

1. Schmit, J. C.; Brody, S. Biochemical genetics of Neurospora crassa conidial germination. Bacteriol. Rev. 1976, 40, 1-41.
2. Osherov, N.; May, G. Conidial germination in Aspergillus nidulans requires RAS signaling and protein synthesis. Genetics 2000, 155, 647-656.
3. Bertolini, P.; Tian, S. P. Low temperature biology and pathogenicity of Penicillium hirsutum on garlic in storage. Postharvest Biol. Technol. 1996, 7, 83-89.
4. Qin, G. Z.; Tian, S. P.; Chan, Z. L.; Li, B. Q. Crucial role of antioxidant proteins and hydrolytic enzymes in pathogenicity of Penicillium expansum: Analysis based on proteomic approach. Mol. Cell. Proteomics 2007, 6, 425-438.
5. Stange, R.; Midland, S.; Sims, J.; McCollum, T. Differential effects of citrus peel extracts on growth of Penicillium digitatum, P. italicum, and P. expansum. Physiol. Mol. Plant Pathol. 2002, 61, 303-311.
6. Andersen, B.; Smedsgaard, J.; Frisvad, J. C. Penicillium expansum: consistent production of patulin, chaetoglobosins, and other secondary metabolites in culture and their natural occurrence in fruit products. J. Agric. Food Chem. 2004, 52, 2421-2428.
7. Mcquilken, M. P.; Budge, S. P.; Whipps, J. M. Effects of culture media and environmental factors on conidial germination, pycnidial production and hyphal extension of Coniothyrium minitans. Mycol. Res. 1997, 101, 11-17.
8. Estrada, A. B.; Dodd, J. C.; Jeffries, P. Effect of humidity and temperature on conidial germination and appressorium development of two Philippine isolates of the mango anthracnose pathogen Colletotrichum gloeosporioides. Plant Pathol. 2000, 49, 608-618.
9. Sautour, M.; Rouget, A.; Dantigny, P.; Divies, C.; Bensoussan, M. Application of Doehlert design to determine the combined effects of temperature, water activity and pH on conidial germination of Penicillium chrysogenum. J. Appl. Microbiol. 2001, 91, 900-906.
10. Pardo, E.; Lagunas, U.; Sanchis, V.; Ramos, A. J.; Marín, S. Influence of water activity and temperature on conidial germination and mycelial growth of ochratoxigenic isolates of Aspergillus ochraceus on grape juice synthetic medium. Predictive models. J. Sci. Food Agric. 2005, 85, 1681-1686.
11. Kope, H. H.; Alfaro, R. I.; Lavallée, R. Effects of temperature and water activity on Lecanicillium spp. conidia germination and growth, and mycosis of Pissodes strobe. Biocontrol 2008, 53, 489-500.
12. Manteau, S.; Abouna, S.; Lambert, B.; Legendre, L. Differential regulation by ambient pH of putative virulence factors secretion by the phytopathogenic fungus Botrytis cinerea. FEMS Microbiol. Ecol. 2003, 43, 359-366.
13. Peñalva, M. A.; Arst, H. J. Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol. Mol. Biol. Rev. 2002, 66, 426-446.
14. Peñalva, M. A.; Tilburn, J.; Bignell, E.; Arst, H. J. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 2008, 16, 291-300.
15. Bilgrami, K. S.; Verma, R. N. Growth. In Physiology of Fungi (2nd edition)Vikas, : New Delhi. 1981, 299-320.
16. Schmidt, P.; Walker, J.; Selway, L.; Stead, D.; Yin, Z.; Enjalbert, B.; Weig, M.; Brown, A. J. Proteomic analysis of the pH response in the fungal pathogen Candida glabrata. Proteomics 2008, 8, 534-544.
17. Thomas, J. D.; VanBogelen, R. A. Experimentalism in proteomics. Trends Biotechnol. 2000, 18 (Suppl. 1), 7-11.
18. Slonczewski, J. L.; Kirkpatrick, C. Proteomic analysis of pH-dependent stress responses in Escherichia coli and Helicobacter pylori using two-dimensional gel electrophoresis. Methods Enzymol. 2002, 358, 228-242.
19. Phan-Thanh, L.; Mahouin, F. A proteomic approach to study the acid response in Listeria monocytogenes. Electrophoresis 1999, 20, 2214-2224.
20. Zilm, P. S.; Bagley, C. J.; Rogers, A. H.; Milne, I. R.; Gully, N. J. The proteomic profile of Fusobacterium nucleatum is regulated by growth pH. Microbiology 2007, 153, 148-159.
21. Gabier, A. C.; Gourdon, P.; Reitz, J.; Leveau, J. Y.; Bouix, M. Intracellular physiological events of yeast Rhodotorula glutinis during storage at +4 °C. Int. J. Food Microbiol. 2005, 105, 97-109.
22. Vindeløv, J.; Arneborg, N. Saccharomyces cerevisiae and Zygosaccharomyces mellis exhibit different hyperosmotic shock responses. Yeast 2002, 19, 429-439.
23. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
24. Jang, H. H.; Lee, K. O.; Chi, Y. H.; Jung, B. G.; Park, S. K.; Park, J. H.; Lee, J. R.; Lee, S. S.; Moon, J. C.; Yun, J. W.; Choi, Y. O.; Kim, W. Y.; Kang, J. S.; Cheong, G. W.; Yun, D. J.; Rhee, S. G.; Cho, M. J.; Lee, S. Y. Two enzymes in one: two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function. Cell 2004, 117, 625-635.
25. Prusky, D.; McEvoy, J. L.; Saftner, R.; Conway, W. S.; Jones, R. Relationship between host acidification and virulence of Penicillium spp. on apple and citrus fruit. Phytopathology 2004, 94, 44-51.
26. van den Berg, M. A.; Albang, R.; Albermann, K.; Badger, J. H.; Daran, J. M.; Driessen, A. J.; Garcia-Estrada, C.; Fedorova, N. D.; Harris, D. M.; Heijne, W. H.; Joardar, V.; Kiel, J. A.; Kovalchuk, A.; Martín, J. F.; Nierman, W. C.; Nijland, J. G.; Pronk, J. T.; Roubos, J. A.; van der Klei, I. J.; van Peij, N. N.; Veenhuis, M.; von Döhren, H.; Wagner, C.; Wortman, J.; Bovenberg, R. A. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat. Biotechnol. 2008, 26, 1161-1168.
27. Jaenicke, R.; Seckler, R. Spontaneous versus assisted protein folding. In Molecular Chaperones and Folding Catalysts. Regulation, Cellular Function and Mechanism; Bukau, B., Ed.; Harwood Academic Publisher; Amsterdam, 1999; pp 407-436.
28. Madshus, I. H. Regulation of intracellular pH in eukaryotic cells. Biochem. J. 1988, 250, 1-8.
29. Lagadic-Gossmann, D.; Huc, L.; Lecureur, V. Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ. 2004, 11, 953-961.
30. Hesse, S. J. A.; Ruijter, G. J. G.; Dijkema, C.; Visser, J. Intracellular pH homeostasis in the filamentous fungus Aspergillus niger. Eur. J. Biochem. 2002, 269, 3485-3494.
31. Setlow, B.; Setlow, P. Measurements of the pH within dormant and germinated bacterial spores. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 2474-2476.
32. Basu, U.; Si, K.; Warner, J. R.; Maitra, U. The Saccharomyces cerevisiae TIF6 gene encoding translation initiation factor 6 is required for 60S ribosomal subunit biogenesis. Mol. Cell. Biol. 2001, 21, 1453-1462.
33. Hausmann, C. D.; Ibba, M.; Giraldo, R. Aminoacyl-tRNA synthetase complexes: molecular multitasking revealed. FEMS Microbiol. Rev. 2008, 32, 705-721.
34. Spahn, C. M. T.; Gomez-Lorenzo, M. G.; Grassucci, R. A.; Joergensen, R.; Andersen, G. R.; Beckmann, R.; Penczek, P. A.; Ballesta, J. P. G.; Frank, J. Domain movements of elongation factor eEF2 and the eukaryotic 80S ribosome facilitate tRNA translocation. EMBO J. 2004, 23, 1008-1019.
35. Shor, B.; Calaycay, J.; Rushbrook, J.; McLeod, M. Cpc2/RACK1 is a ribosome-associated protein that promotes efficient translation in Schizosaccharomyces pombe. J. Biol. Chem. 2003, 278, 49119-49128.
36. Coyle, S. M.; Gilbert, W. V.; Doudna, J. A. Direct link between RACK1 function and localization at the ribosome in vivo. Mol. Cell. Biol. 2009, 29, 1626-1634.
37. Cochrane, V. W.; Cochrane, J. C. Chlamydospore development in the absence of protein synthesis in Fusarium solani. Dev. Biol. 1970, 23, 345-354.
38. Loo, M. Some required events in conidial germination of Neurospora crassa. Dev. Biol. 1976, 54, 201-213.
39. Agashe, V. R.; Hartl, F. U. Roles of molecular chaperones in cytoplasmic protein folding. Semin. Cell Dev. Biol. 2000, 11, 15-25.
40. Hartl, F. U.; Hayer-Hartl, M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002, 295, 1852-1858.
41. Beatrix, B.; Sakai, H.; Wiedmann, M. The alpha and beta subunit of the nascent polypeptide-associated complex have distinct functions. J. Biol. Chem. 2000, 275, 37838-37845.
42. Albanèse, V.; Yam, A. Y.; Baughman, J.; Parnot, C.; Frydman, J. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 2006, 124, 75-88.
43. Flom, G.; Weekes, J.; Williams, J. J.; Johnson, J. L. Effect of mutation of the tetratricopeptide repeat and asparatate-proline 2 domains of Sti1 on Hsp90 signaling and interaction in Saccharomyces cerevisiae. Genetics 2006, 172, 41-51.
44. Kleizen, B.; Braakman, I. Protein folding and quality control in the endoplasmic reticulum. Curr. Opin. Cell Biol. 2004, 16, 343-349.
45. Gillece, P.; Luz, J. M.; Lennarz, W. J.; de La Cruz, F. J.; Römisch, K. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J. Cell Biol. 1999, 147, 1443-1456.
46. Fink, A. L. Chaperone-mediated protein folding. Physiol. Rev. 1999, 79, 425-449.
47. Voos, W.; Röttgers, K. Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochim. Biophys. Acta 2002, 1592, 51-62.
48. Naryzhny, S. N. Proliferating cell nuclear antigen: a proteomics view. Cell. Mol. Life Sci. 2008, 65, 3789-3808.
49. Sanders, S. L.; Garbett, K. A.; Weil, P. A. Molecular characterization of Saccharomyces cerevisiae TFIID. Mol. Cell. Biol. 2002, 22, 6000-6013.
50. Sanders, S. L.; Weil, P. A. Identification of two novel TAF subunits of the yeast Saccharomyces cerevisiae TFIID complex. J. Biol. Chem. 2000, 275, 13895-13900.
51. Mirkes, P. E. Polysomes, ribonucleic acid, and protein synthesis during germination of. Neurospora crassa conidia. J. Bacteriol. 1974, 117, 196-202.
52. Sazer, S. The search for the primary function of the Ran GTPase continues. Trends Cell Biol. 1996, 6, 81-85.