Comparative proteomic analysis in pea treated with microbial consortia of beneficial microbes reveals changes in the protein network to enhance resistance against Sclerotinia sclerotiorum

Journal of Plant Physiology

Volumn 182, Issue , 2015, Pages 79-94

  Jain, Akansha ^a   Singh, Akanksha ^a   Singh, Surendra ^a   Singh, Vinay ^a   Singh, Harikesh Bahadur ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

Bacillus subtilis; Microbial consortium; Pseudomonas aeruginosa; Sclerotinia sclerotiorum; Trichoderma harzianum

Indexed keywords

BACILLUS SUBTILIS; HYPOCREA LIXII; PISUM SATIVUM; PSEUDOMONAS AERUGINOSA; SCLEROTINIA SCLEROTIORUM;

VEGETABLE PROTEIN;

ASCOMYCETES; CLASSIFICATION; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PEA; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DISEASE; PROTEOMICS; PSEUDOMONAS AERUGINOSA; RHIZOSPHERE; TRICHODERMA;

ASCOMYCOTA; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PEAS; PLANT DISEASES; PLANT PROTEINS; PROTEOMICS; PSEUDOMONAS AERUGINOSA; RHIZOSPHERE; STRESS, PHYSIOLOGICAL; TRICHODERMA;

EID: 84930614853     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2015.05.004     Document Type: Article

References (76)

1. Agrios G.N. Plant Pathology 1997, Academic Press, San Diego. 4th edition.
2. Agustí J., Merelo P., Cercós M., Tadeo F.R., Talón M. Ethylene-induced differential gene expression during abscission of citrus leaves. J Exp Bot 2008, 59(10):2717-2733.
3. Ahn I.P., Lee S.W., Suh S.C. Rhizobacteria-induced priming in Arabidopsis is dependent on ethylene, jasmonic acid, and NPR1. Mol Plant Microbe Interact 2007, 20:759-768.
4. Artymiuk P.J., Green J. The double life of acotinase. Structure 2006, 14:2-4. 10.1016/j. str.2005.12.001.
5. Atik A.E., Bozdağ G.O., Akinci E., Kaya A., Koc A., Yalcin T., et al. Proteomic changes during boron tolerance in barley (Hordeum vulgare) and the role of vacuolar proton-translocating ATPase subunit E. Turk J Bot 2011, 35:379-388.
6. Bechtold U., Murphy D.J., Mullineaux P.M. Arabidopsis peptide methionine sulfoxide reductase2 prevents cellular oxidative damage in long nights. Plant Cell 2004, 16:908-919.
7. Boddu J., Cho S., Kruger W.M., Muehlbauer G.J. Transcriptome analysis of the barley-Fusarium graminearum interaction. Mol Plant Microbe Interact 2006, 19:407-417.
8. Bradford M.M. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Ann Biochem 1976, 72:248-254.
9. Broshé M., Strid A. Cloning, expression, and molecular characterization of a small pea gene family regulated by low levels of ultraviolet B radiation and other stresses. Plant Physiol 1999, 121:479-487.
10. Caldas T., Laalami S., Richarme G. Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. J Biol Chem 2000, 275(2):855-860.
11. Campos A., da Costa G., Coelho A.V., Fevereiro P. Identification of bacterial protein markers and enolase as a plant response protein in the infection of Olea europaea subsp. europaea by Pseudomonas savastanoi pv. savastanoi. Eur J Plant Pathol 2009, 125:603-616.
12. Cartieaux F., Contesto C., Gallou A., Desbrosses G., Kopka J., Taconnat L., et al. Simultaneous interaction of Arabidopsis thaliana with Bradyrhizobium sp. strain ORS278 and Pseudomonas syringae pv. tomato DC3000 leads to complex transcriptome changes. Mol Plant Microbe Interact 2008, 21:244-259.
13. Castro A.J., Carapito C., Zorn N., Magné C., Leize E., van Dorsselaer A., et al. Proteomic analysis of grapevine (Vitis vinifera L.) tissues subjected to herbicide stress. J Exp Bot 2005, 56:2783-2795.
14. Chi F., Yang P., Han F., Jing Y., Shen S. Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti. Proteomics 2010, 10:1861-1874.
15. Cipriano D.J., Wang Y., Bond S., Hinton A., Jefferies K.C., Qi J., et al. Structure and regulation of the vacuolar ATPases. Biochim Biophys Acta Bioenergetics 2008, 1777(7-8):599-604.
16. Dahal D., Heintz D., Dorsselaer A.V., Braun H.P., Wydra K. Pathogenesis and stress related, as well as metabolic proteins are regulated in tomato stems infected with Ralstonia solanacearum. Plant Physiol Biochem 2009, 47:838-846.
17. Dahal D., Pich A., Braun H.P., Wydra K. Analysis of cell wall proteins regulated in stem of susceptible and resistant tomato species after inoculation with Ralstonia solanacearum: a proteomic approach. Plant Mol Biol 2010, 73:643-658.
18. Davies M.J. The oxidative environment and protein damage. Biochim Biophys Acta 2005, 1703:93-109.
19. Delauré S.L., Hemelrijck W.V., Bolle M.F.C.D., Cammue B.P.A., Coninck B.M.A.D. Building up plant defenses by breaking down proteins. Plant Sci 2008, 174:375-385.
20. Díaz M., Achkor H., Titarenko E., Martínez M.C. The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Lett 2003, 543:136-139.
21. Diez E.M., Rubio B., Domínguez S., Hermosa R., Monte E., Nicolás C. Transcriptomic response of Arabidopsis thaliana after 24h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 2012, 169:614-620.
22. Dóczi R., Brader G., Pettkó-Szandtner A., Rajh I., Djamei A., Pitzschke A. The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signalling. Plant Cell 2007, 19:3266-3279.
23. Freitas-Astúal R., Bastianel M., Locali-Fabris E.C., Novelli V.M., Silva-Pinhati A.C., Basílio-Palmieri A.C. Differentially expressed stress-related genes in the compatible citrus-Citrus leprosis virus interaction. Genet Mol Biol 2007, 30(Suppl 3):980-990.
24. Fu J., Momčilović I., Vara Prasad P.V. Roles of protein synthesis elongation factor ef-tu in heat tolerance in plants. J Bot 2012, 10.1155/2012/835836.
25. Fukao T., Kennedy R.A., Yamasue Y., Rumpho M.E. Genetic and biochemical analysis of anaerobically induced enzymes during seed germination of Echinochloa crus-galli varieties tolerance and intolerant of anoxia. J Exp Bot 2003, 54:1421-1429.
26. Gottesman S. Proteases and their targets in Escherichia coli. Annu Rev Genet 1996, 30:465-506.
27. Guo A., Reimers P.J., Leach J.E. Effect of light on incompatible interactions between Xanthomonas oryzae pv oryzae and rice. Physiol Mol Plant Pathol 1993, 42:413-425.
28. Hamilton C., Good A.G., Taylor G.J. Induction of vacuolar ATPase and mitochondrial ATP synthase by aluminum in an aluminum-resistant cultivar of wheat. Plant Physiol 2001, 125:2067-2077.
29. Henkes S., Sonnewald U., Badur R., Flachmann R., Stiff M.A. Small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell 2001, 13:535-551.
30. Hossain M.M., Sultana F., Kubota M., Hyakumachi M. Differential inducible defense mechanisms against bacterial speck pathogen in Arabidopsis thaliana by plant-growth-promoting-fungus Penicillium sp. GP 16-2 and its cell free filtrate. Plant Soil 2008, 304:227-239.
31. Ito K., Akiyama A. Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Phytopathol 2005, 59:211-231.
32. Jain A., Singh A., Singh B.N., Singh S., Upadhyay R.S., Sarma B.K., et al. Biotic stress management in agricultural crops using microbial consortium. Bacteria in Agrobiology: Disease Management 2013, 427-448. Springer, Berlin, Heidelberg. D.K. Maheshwari (Ed.).
33. Jain A., Singh A., Singh S., Singh H.B. Biocontrol agents-mediated suppression of oxalic acid induced cell death during Sclerotinia sclerotiorum-pea interaction. J Basic Microbiol 2014, 54:1-6. 10.1002/jobm.201400156.
34. Jain A., Singh A., Singh S., Singh H.B. Microbial consortium-induced changes in oxidative stress markers in pea plants challenged with Sclerotinia sclerotiorum. J Plant Growth Regul 2013, 32:388-398.
35. Jain A., Singh S., Sarma B.K., Singh H.B. Microbial consortium mediated reprogramming of defense network in pea to enhance tolerance against Sclerotinia sclerotiorum. J Appl Microbiol 2012, 112(3):537-550.
36. Jain A., Singh S., Chaudhary A., Singh S., Singh H.B. Modulation of nutritional and antioxidant potential of seeds and pericarp of pea pods treated with microbial consortium. Food Res Int 2014, 64:275-282. 10.1016/j.foodres.2014.06.033.
37. Jain A., Singh A., Singh S., Singh H.B. Biological management of Sclerotinia sclerotiorum in pea using plant growth promoting microbial consortium. J Basic Microbiol 2015, 10.1002/jobm.201400628.
38. Jedrzejas M.J., Chander M., Setlow P., Krishnasamy G. Structure and mechanism of action of a novel phosphoglycerate mutase from Bacillus stearothermophilus. EMBO J 2000, 19(7):1419-1431.
39. Jones A.M., Bennett M.H., Mansfield J.W., Grant M. Analysis of the defence phosphoproteome of Arabidopsis thaliana using differential mass tagging. Proteomics 2006, 6:4155-4165.
40. Koistinen K.M., Hassinen V.H., Gynther P.A.M., Lehesranta S.J., Keinänen S.I., et al. Birch PR-10c is induced by factors causing oxidative stress but appears not to confer tolerance to these agents. New Phytol 2002, 155:381-391.
41. Konishi H., Ishiguro K., Komatsu S. A proteomics approach towards understanding blast fungus infection of rice grown under different levels of nitrogen fertilization. Proteomics 2001, 1:162-171.
42. Kumar S., Tamura K., Nei M.M.E.G.A. Molecular Evolutionary Genetics Analysis software for microcomputers. Comput Appl Biosci 1994, 10(2):189-191.
43. Lee J., Bricker T.M., Lefevre M., Pinson S.M., Oard J.H. Proteomic and genetic approaches to identifying defence-related proteins in rice challenged with the fungal pathogen Rhizoctonia solani. Mol Plant Pathol 2006, 7(5):405-416.
44. Lindermayr C., Saalbach G., Durner J. Proteomic identification of S-nitrosylated proteins in Arabidopsis 1. Plant Physiol 2005, 137:921-930.
45. Mahmood T., Jan A., Kakishima M., Komatsu S. Proteomic analysis of bacterial-blight defense responsive proteins in rice leaf blades. Proteomics 2006, 6:6053-6065.
46. Mueller L.A., Zhang P., Rhee S.Y. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol 2003, 132(2):453-460.
47. Mushegian A.R., Koonin E.V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 1996, 93:10268-10273.
48. Orengo C.A., Michie A.D., Jones S., Jones D.T., Swindells M.B., Thornton J.M. CATH-a hierarchic classification of protein domain structures. Structure 1997, 5(8):1093-1108.
49. Pieterse C.M.J., Leon-Reyes A., van der Ent S., Wees S.C.M. Networking by small-molecules hormones in plant immunity. Nat Chem Biol 2009, 5:308-316.
50. Rakwal R., Komatsu S. A role for jasmonate in the rice (Oryza sativa L.) self defense mechanism using proteome analysis. Electrophoresis 2000, 21:2492-2500.
51. Sarma B.K., Ameer Basha S., Singh D.P., Singh U.P. Use of non-conventional chemicals as an alternative approach to protect chickpea (Cicer arietinum) from Sclerotinia stem rot. Crop Prot 2007, 26:1042-1048.
52. Sedigheh H.G., Mortazavian M., Norouzian D., Atyabi M., Akbarzadeh A., Hasanpoor K., et al. Oxidative stress and leaf senescence. BMC Res Notes 2011, 4:477.
53. Segarra G., Casanova E., Bellido D., Odena M.A., Oliveira E., Trillas I. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 2007, 7:3943-3952.
54. Segarra G., Ent S.D., Trillas I., Pieterse C.M.J. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol 2009, 11:90-96.
55. Seo S., Okamoto M., Iwai T., Iwano M., Fukui K., Isogai A., et al. Reduced levels of chloroplast FtsH protein in tobacco mosaic virus-infected tobacco leaves accelerate the hypersensitive reaction. Plant Cell 2000, 12:917-932.
56. Shen S., Jing Y., Kuang T. Proteomics approach to identify wound-response related proteins from rice leaf sheath. Proteomics 2003, 3:527-535.
57. Shoresh M., Harman G.E. The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 2008, 147:2147-2163.
58. Shoresh M., Yedidia I., Chet I. Involvement of jasmonic acid/ethylene signaling pathway in the systemic resistance induced in cucumber by Trichoderma asperellum T203. Phytopathology 2005, 95:76-84.
59. Singh B.N., Mishra R.N., Agarwal P.K., Goswami M., Nair S., Sopory S.K., et al. A pea chloroplast translation elongation factor that is regulated by abiotic factors. Biochem Biophys Res Commun 2004, 320(2):523-530.
60. Speicher D.W. Proteomics: an infinite problem with infinite potential. Scientist 2002, 16:12.
61. Sweetlove L.J., Heazlewood J.L., Herald V., Holtzapffel R., Day D.A., Leaver C.J., et al. The impact of oxidative stress on Arabidopsis mitochondria. Plant J 2002, 32:891-904.
62. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22(22):4673-4680.
63. Vanninia C., Iritib M., Bracalea M., Locatellic F., Faorod F., Crocea P., et al. The ectopic expression of the rice Osmyb4 gene in Arabidopsis increases tolerance to abiotic, environmental and biotic stresses. Physiol Mol Plant Pathol 2006, 69:26-42.
64. Vincent D., Ergu A., Bohlman M.C., Tattersal E.A.R., Tillett R.L., Wheatley M.D., et al. Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J Exp Bot 2007, 58(7):1873-1892.
65. von Zychlinski A., Kleffmann T., Krishnamurthy N., Sjolander K., Baginsky S., Gruissem W. Proteome analysis of the rice etioplast metabolic and regulatory networks and novel protein functions. Mol Cell Proteomics 2005, 4:1072-1084.
66. Wan X.Y., Liu J.Y. Comparative proteomics analysis reveals an intimate protein network provoked by hydrogen peroxide stress in rice seedling leaves. Mol Cell Proteomics 2008, 7:1469-1488.
67. Wang F.X., Mal Y.P., Yang C.L., Zhao P.M., Yao Y., Jian G.L., et al. Proteomic analysis of the sea-island cotton roots infected by wilt pathogen Verticillium dahlia. Proteomics 2011, 11:1-14.
68. Wang W., Vinocur B., Shoseyov O., Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004, 9:244-252.
69. Xiong Y., Contento A.L., Nguyen P.Q., Bassham D.C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 2007, 143:291-299.
70. Yadav S.K., Singla-Pareek S.L., Sopory S.K. An overview on the role of methylglyoxal and glyoxalases in plants. Drug Metabol Drug Interact 2008, 23:51-68.
71. Yan S.P., Zhang Q.Y., Tang Z.C., Su W.A., Sun W.N. Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics 2006, 5(3):484-496.
72. Yang F., Jensen J.D., Svensson B., Jørgensen H.J.L., Collinge D.B., Finnie C. Analysis of early events in the interaction between Fusarium graminearum and the susceptible barley (Hordeum vulgare) cultivar Scarlett. Proteomics 2010, 10:3748-3755.
73. Yang L., Lin H., Takahashi Y., Chen F., Walker M.A., Civerolo E.L. Proteomic analysis of grapevine stem in response to Xylella fastidiosa inoculation. Physiol Mol Plant Pathol 2011, 75:90-99.
74. Zhang J.H., Sun L.W., Liu L.L., Lian J., An S.L., Wang X., et al. Proteomic analysis of interactions between the generalist herbivore Spodoptera exigua (Lepidoptera: Noctuidae) and Arabidopsis thaliana. Plant Mol Biol Rep 2010, 28:324-333.
75. Zhao Z., Assmann S.M. The glycolytic enzyme, phosphoglycerate mutase, has critical roles in stomatal movement, vegetative growth, and pollen production in Arabidopsis thaliana. J Exp Bot 2011, 62:5179-5218.
76. Zrenner R., Riegler H., Marquard C.R., Lange P.R., Geserick C., Bartosz C.E., et al. A functional analysis of the pyrimidine catabolic pathway in Arabidopsis. New Phytol 2009, 183:117-132.