Glycine betaine improves oxidative stress tolerance and biocontrol efficacy of the antagonistic yeast Cystofilobasidium infirmominiatum

International Journal of Food Microbiology

Volumn 146, Issue 1, 2011, Pages 76-83

  Liu, Jia ^a,c   Wisniewski, Michael ^a   Droby, Samir ^b   Vero, Silvana ^d   Tian, Shiping ^c   Hershkovitz, Vera ^b  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b VOLCANI CENTER   (Israel)

^c INSTITUTE OF BOTANY   (China)

^d UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

Antioxidant enzymes; Biocontrol efficacy; Glycine betaine; Oxidative stress tolerance; ROS

Indexed keywords

BETAINE; CATALASE; GLUTATHIONE PEROXIDASE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

APPLE; ARTICLE; BIOLOGICAL PEST CONTROL; CYSTOFILOBASIDIUM INFIRMOMINIATUM; NONHUMAN; OXIDATION; OXIDATIVE STRESS; YEAST; YEAST CELL;

ANTIBIOSIS; ANTIOXIDANTS; BASIDIOMYCOTA; BETAINE; CATALASE; FRUIT; GLUTATHIONE PEROXIDASE; MALUS; MICROBIAL VIABILITY; OXIDATION-REDUCTION; OXIDATIVE STRESS; PENICILLIUM; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

CYSTOFILOBASIDIUM INFIRMOMINIATUM; MALUS X DOMESTICA; PENICILLIUM EXPANSUM;

EID: 79953066734     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.02.007     Document Type: Article

References (56)

1. Abegg M.A., Alabarse P.V.G., Casanova A., Hoscheid J., Salomon T.B., Hackenhaar F.S., Medeiros T.M., Benfato M.S. Response to oxidative stress in eight pathogenic yeast species of the genus Candida. Mycopathologia 2010, 170:11-20.
2. Alfieri R.R., Cavazzoni A., Petronini P.G., Bonelli M.A., Caccamo A.E., Borghetti A.F., Wheeler K.P. Compatible osmolytes modulate the response of porcine endothelial cells to hypertonicity and protect them from apoptosis. The Journal of Physiology 2002, 540:499-508.
3. Ashraf M., Foolad M.R. Roles of glycinebetaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany 2007, 59:206-216.
4. Boncompagni E., Østerås M., Poggi M.C., Rudulier D.L. Occurrence of choline and glycine betaine uptake and metabolism in the family Rhizobiaceae and their roles in osmoprotection. Applied and Environmental Microbiology 1999, 65:2072-2077.
5. Boniolo F.S., Rodrigues R.C., Delatorre E.O., da Silveira M.M., Flores V.M., Berbert-Molina M.A. Glycine betaine enhances growth of nitrogen-fixing bacteria Gluconacetobacter diazotrophicus PAL5 under saline stress conditions. Current Microbiology 2009, 59:593-595.
6. Bouvier J., Bordes P., Romeo Y., Fourcans A., Bouvier I., Gutierrez C. Characterization of opuA, a glycine-betaine uptake system of Lactococcus lactis. Journal of Molecular Microbiology and Biotechnology 2000, 2:199-205.
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
8. Branduardi P., Fossati T., Sauer M., Pagani R., Mattanovich D., Porro D. Biosynthesis of vitamin C by yeast leads to increased stress resistance. PLoS One 2007, 2:e1092.
9. Cañamás T.P., Viñas I., Usall J., Magan N., Morelló J.R., Teixidó N. Relative importance of amino acids, glycine-betaine and ectoine synthesis in the biocontrol agent Pantoea agglomerans CPA-2 in response to osmotic, acidic and heat stress. Letters in Applied Microbiology 2007, 45:6-12.
10. Cao S., Yuan Y., Hu Z., Zheng Y. Combination of Pichia membranifaciens and ammonium molybdate for controlling blue mould caused by Penicillium expansum in peach fruit. International Journal of Food Microbiology 2010, 141:173-176.
11. Castoria R., Caputo L., De Curtis F., De Cicco V. Resistance of postharvest biocontrol yeasts to oxidative stress: a possible new mechanism of action. Phytopathology 2003, 93:564-572.
12. Cayley S., Record M.T. Roles of cytoplasmic osmolytes, water, and crowding in response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine. Biochemistry 2003, 42:12596-12609.
13. Chand-Goyal T., Spotts R.A. Biological control of postharvest diseases of apple and pear under semi-commercial and commercial conditions using three saprophytic yeasts. Biological Control 1997, 10:199-206.
14. de Zwart F.J., Slow S., Payne R.J., Lever M., George P.M., Gerrard J.A., Chambers S.T. Glycine betaine and glycine betaine analogues in common foods. Food Chemistry 2003, 83:197-204.
15. Delamare A.P.L., Dalcin T., Müller G., Olavo S., da Costa P., Echeverrigaray S. The effect of organic osmoprotectors on Aeromonas trota and A. hydrophila grown under high sodium chloride concentrations. Brazilian Journal of Microbiology 2003, 34:128-130.
16. Deveau A., Piispanen A.E., Jackson A.A., Hogan D.A. Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the ras-cyclic AMP signaling pathway. Eukaryotic Cell 2010, 9:569-577.
17. Droby S., Chalutz E., Wilson C.L., Wisniewski M.E. Characterization of the biocontrol activity of Debaryomyces hansenii in the control of Penicillium digitatum on grapefruit. Canadian Journal of Microbiology 1989, 35:794-800.
18. Droby S., Wisniewski M., Macarisin D., Wilson C. Twenty years of postharvest biocontrol research: is it time for a new paradigm?. Postharvest Biology and Technology 2009, 52:137-145.
19. Einset J., Connolly E.L. Glycine betaine enhances extracellular processes blocking ROS signaling during stress. Plant Signaling & Behavior 2009, 4:197-199.
20. Fagan J.M., Sleczka B.G., Sohar I. Quantitation of oxidative damage to tissue proteins. The International Journal of Biochemistry & Cell Biology 1999, 31:751-757.
21. Farooq M., Basra S.M.A., Wahid A., Cheema1 Z.A., Cheema1 M.A., Khaliq A. Physiological role of exogenously applied glycinebetaine to improve drought tolerance in fine grain aromatic rice (Oryza sativa L.). Journal of Agronomy and Crop Science 2008, 194:325-333.
22. Hoque M.A., Banu M.N.A., Nakamura Y., Shimoishi Y., Murata Y. Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. Journal of Plant Physiology 2008, 165:813-824.
23. Hossain M.A., Fujita M. Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. Physiology and Molecular Biology of Plants 2010, 16:19-29.
24. Islam M.M., Hoque M.A., Okuma E., Banu M.N., Shimoishi Y., Nakamura Y., Murata Y. Exogenous proline and glycinebetaine increase antioxidant enzyme activities and confer tolerance to cadmium stress in cultured tobacco cells. Journal of Plant Physiology 2009, 166:1587-1597.
25. Janisiewicz W.J., Korsten L. Biological control of postharvest diseases of fruits. Annual Review of Phytopathology 2002, 40:411-441.
26. Kim J.H., Sedlak M., Gao Q., Riley C.P., Regnier F.E., Adamec J. Oxidative stress studies in yeast with a frataxin mutant: a proteomics perspective. Journal of Proteome Research 2010, 9:730-736.
27. Kumar V., Yadav S.K. Proline and betaine provide protection to antioxidant and methylglyoxal detoxification systems during cold stress in Camellia sinensis (L.) O. Kuntze. Acta Physiologiae Plantarum 2009, 31:261-269.
28. Li B.Q., Tian S.P. Effects of trehalose on stress tolerance and biocontrol efficacy of Cryptococcus laurentii. Journal of Applied Microbiology 2006, 100:854-861.
29. Li B.Q., Zhou Z.W., Tian S.P. Combined effects of endo- and exogenous trehalose on stress tolerance and biocontrol efficacy of two antagonistic yeasts. Biological Control 2008, 46:187-193.
30. Liu J., Zhang Y., Huang D., Song G. Cadmium induced MTs synthesis via oxidative stress in yeast Saccharomyces cerevisiae. Molecular and Cellular Biochemistry 2005, 280:139-145.
31. Liu J., Tian S.P., Li B.Q., Qin G.Z. Enhancing viability of two biocontrol yeasts in liquid formulation by applying sugar protectant combined with antioxidant. Biocontrol 2009, 54:817-824.
32. Lu H., Higgins V.J. The effect of hydrogen peroxide on the viability of tomato cells and of the fungal pathogen Cladosporium fulvum. Physiological and Molecular Plant Pathology 1999, 54:131-143.
33. Macarisin D., Cohen L., Eick A., Rafael G., Belausov E., Wisniewski M., Droby S. Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of citrus fruit. Phytopathology 2007, 97:1491-1500.
34. Macarisin D., Droby S., Bauchan G., Wisniewski M. Superoxide anion and hydrogen peroxide in the yeast antagonist-fruit interaction: a new role for reactive oxygen species in postharvest biocontrol?. Postharvest Biology and Technology 2010, 58:194-202.
35. Monobe M., Hamano N., Sumi M., Mukai K., Moritake T., Anzai K., Uzawa A., Ando K. Effects of glycine betaine on bone marrow death and intestinal damage by gamma rays and carbon ions. Radiation Protection Dosimetry 2006, 122:494-497.
36. Patiño-Vera M., Jiménez B., Balderas K., Ortiz M., Allende R., Carrillo A., Galindo E. Pilot-scale production and liquid formulation of Rhodotorula minuta, a potential biocontrol agent of mango anthracnose. Journal of Applied Microbiology 2005, 99:540-550.
37. Pinheiro R., Belo I., Mota M. Oxidative stress response of Kluyveromyces marxianus to hydrogen peroxide, paraquat and pressure. Applied Microbiology and Biotechnology 2002, 58:842-847.
38. Raza S.H., Athar H.R., Ashraf M., Hameed A. Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance. Environmental and Experimental Botany 2007, 60:368-376.
39. Reverberi M., Fabbri A.A., Zjalic S., Ricelli A., Punelli F., Fanelli C. Antioxidant enzymes stimulation in Aspergillus parasiticus by Lentinula edodes inhibits aflatoxin production. Applied Microbiology and Biotechnology 2005, 69:207-215.
40. Reverter-Branchat G., Cabiscol E., Tamarit J., Ros J. Oxidative damage to specific proteins in replicative and chronological-aged Saccharomyces cerevisiae: common targets and prevention by calorie restriction. The Journal of Biological Chemistry 2004, 279:31983-31989.
41. Rhodes D., Hanson A.D. Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 1993, 144:357-384.
42. Sharma R.R., Singh D., Singh R. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biological Control 2009, 50:205-221.
43. Spadaro D., Gullino M.L. State of the art and future prospects of the biological control of postharvest fruit diseases. International Journal of Food Microbiology 2004, 91:185-194.
44. Spotts R.A., Cervantes L.A., Facteau T.J. Integrated control of brown rot of sweet cherry fruit with a preharvest fungicide, a postharvest yeast, modified atmosphere packaging, and cold storage temperature. Postharvest Biology and Technology 2002, 24:251-257.
45. Spotts R.A., Wallis K.M., Serdani M., O'Gorman D.T., Sholberg P.L. Real time polymerase chain reaction for rapid and quantitative determination of Cystofilobasidium infirmominiatum on the surfaces of apple, pear, and sweet cherry fruit. Postharvest Biology and Technology 2009, 51:227-231.
46. Stadtman E.R., Levine R.L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 2003, 25:207-218.
47. Teixidó N., Cañamás T.P., Usall J., Torres R., Magan N., Viñas I. Accumulation of the compatible solutes, glycine-betaine and ectoine, in osmotic stress adaptation and heat shock cross-protection in the biocontrol agent Pantoea agglomerans CPA-2. Letters in Applied Microbiology 2005, 41:248-252.
48. Teixidó N., Cañamás T.P., Abadias M., Usall J., Solsona C., Casals C., Viñas I. Improving low water activity and desiccation tolerance of the biocontrol agent Pantoea agglomerans CPA-2 by osmotic treatments. Journal of Applied Microbiology 2006, 101:927-937.
49. Thomas K.C., Hynes S.H., Ingledew W.M. Effects of particulate materials and osmoprotectants on very-high-gravity ethanolic fermentation by Saccharomyces cerevisiae. Applied and Environmental Microbiology 1994, 60:1519-1524.
50. Tolaini V., Zjalic S., Reverberi M., Fanelli C., Fabbri A.A., Del Fiore A., De Rossi P., Ricelli A. Lentinula edodes enhances the biocontrol activity of Cryptococcus laurentii against Penicillium expansum contamination and patulin production in apple fruits. International Journal of Food Microbiology 2010, 138:243-249.
51. Torres R., Valentines M.C., Usall J., Viñas I., Larrigaudiere C. Possible involvement of hydrogen peroxide in the development of resistance mechanisms in 'Golden Delicious' apple fruit. Postharvest Biology and Technology 2003, 27:235-242.
52. Vero, S., Garmendia, G., de Aurrecoeches, I., Garat, F., Wisniewski, M., in press. Cystofilobasidium infirmominiatum as a biocontrol agent of postharvest diseases on apples and citrus. Acta Horticulturae.
53. Wang S., Yao Q., Tao J., Qiao Y., Zhang Z. Co-ordinate expression of glycine betaine synthesis genes linked by the FMDV 2A region in a single open reading frame in Pichia pastoris. Applied and Microbiology Biotechnology 2007, 77:891-899.
54. Wang Y., Wang P., Xia J., Yu T., Lou B., Wang J., Zheng X.D. Effect of water activity on stress tolerance and biocontrol activity in antagonistic yeast Rhodosporidium paludigenum. International Journal of Food Microbiology 2010, 143:103-108.
55. Wisniewski M., Wilson C., Droby S., Chalutz E., El Ghaouth A., Stevens C. Postharvest biocontrol: new concepts and applications. Biological Control: A Global Perspective 2007, 262-273. CABI, Cambridge, MA, USA. C. Vincent, M.S. Goettal, G. Lazarovits (Eds.).
56. Yao H.J., Tian S.P., Wang Y.S. Sodium bicarbonate enhances biocontrol efficacy of yeasts on fungal spoilage of pears. International Journal of Food Microbiology 2004, 93:297-304.