Genetic transformation of cotton with a harpin-encoding gene hpaXoo confers an enhanced defense response against different pathogens through a priming mechanism

BMC Plant Biology

Volumn 10, Issue , 2010, Pages

  Miao, Weiguo ^a,b   Wang, Xiben ^c   Li, Ming ^a   Song, Congfeng ^a   Wang, Yu ^a   Hu, Dongwei ^d   Wang, Jinsheng ^a  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b HAINAN UNIVERSITY   (China)

^c Cereal Research Centre   (Canada)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIUM; GOSSYPIUM HIRSUTUM; RHIZOBIUM; VERTICILLIUM DAHLIAE; XANTHOMONAS; XANTHOMONAS ORYZAE PV. ORYZAE;

BACTERIAL PROTEIN; HARPIN; OUTER MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE;

ARTICLE; CELL SURVIVAL; COTTON; CYTOLOGY; FUNGUS SPORE; GENETIC TRANSFORMATION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; MERISTEM; METABOLISM; MICROBIOLOGY; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PLANT ROOT; PROTEIN TRANSPORT; RESPIRATORY BURST; TRANSGENIC PLANT; ULTRASTRUCTURE; VERTICILLIUM; XANTHOMONAS;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL SURVIVAL; GOSSYPIUM; IMMUNITY, INNATE; MERISTEM; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RESPIRATORY BURST; SPORES, FUNGAL; TRANSFORMATION, GENETIC; VERTICILLIUM; XANTHOMONAS;

EID: 77950803977     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-10-67     Document Type: Article

References (69)

1. Bell AA. Verticillium wilt. Cotton Diseases 1992, 87-126. C.A.B. International, Wallingford, U.K., Hillocks RJ.
2. Hampton RE, Wullschleger SD, Oosterhuis DM. Impact of Verticillium wilt on net photosynthesis, respiration and photorespiration in field-grown cotton (Gossypium hirsutum L.). Physiological and Molecular Plant Pathology 1990, 37:271-280.
3. Paplomatas EJ, Bassett DM, Broome JC, DeVay JE. Incidence of Verticillium wilt and yield losses of cotton cultivars (Gossypium hirsutum) based on soil inoculum density of Verticillium dahliae. Phytopathology 1992, 82:1417-1420.
4. Pegg GF. Pathogenesis in vascular disease of plants. Vascular wilt diseases of plants 1989, 51-94. Springer, Berlin, Germany, Tjamos EC, Beckman C.
5. Xiao CL, Subbarao KV, Schulbach KF, Koike ST. Effects of crop rotation and irrigation on Verticillium dahliae microsclerotia in soil and wilt in cauliflower. Phytopathology 1998, 88:1046-1055. 10.1094/PHYTO.1998.88.10.1046, 18944816.
6. Huang J, Li H, Yuan H. Effect of organic amendments on Verticillium wilt of cotton. Crop Protection 2006, 25:1167-1173.
7. Gray FA, Koch DW. Influence of late season harvesting, fall grazing, and fungicide treatment on Verticillium wilt incidence, plant density, and forage yield of alfalfa. Plant Disease 2004, 88:811-816.
8. Kurt S, Dervis S, Sahinler S. Sensitivity of Verticillium dahliae to prochloraz and prochloraz-manganese complex and control of Verticillium wilt of cotton in the field. Crop Protection 2003, 22:51-55.
9. Colson-Hanks ES, Deverall BJ. Effect of 2,6-dichloroisonicotinic acid, its formulation materials and benzothiadiazole on systemic resistance to alternaria leaf spot in cotton. Plant Pathology 2000, 49:171-178.
10. Punja ZK. Genetic engineering of plants to enhance resistance to fungal pathogens: a review of progress and future prospects. Canadian Journal of Plant Pathology 2001, 23:216-235.
11. Gentile A, Deng Z, La-Malfa S, Distefano G, Domina F, Vitale A, Polizzi G, Lorito M, Tribulato E. Enhanced resistance to Phoma tracheiphila and Botrytis cinerea in transgenic lemon plants expressing a Trichoderma harzianum chitinase gene. Plant Breeding 2007, 126:146-151.
12. Wrobel-Kwiatkowska, Lorenc-Kukula MK, Starzycki M, Oszmianski J, Kepczynska E, Szopa J. Expression of beta-1,3-glucanase in flax causes increased resistance to fungi. Physiological and Molecular Plant Pathology 2004, 65:245-256.
13. Lee YH, Yoon IS, Suh SC, Kim HI. Enhanced disease resistance in transgenic cabbage and tobacco expressing a glucose oxidase gene from Aspergillus niger. Plant Cell Reports 2002, 20:857-863.
14. Komatsu K, Okuda S, Takahashi M, Matsunaga R, Nakazawa Y. QTL mapping of pubescence density and flowering time of insect-resistant soybean. Genetics and Molecular Biology 2007, 30:635-639.
15. Yang KY, Kim YM, Lee SH, Song PS, Soh MS. Overexpression of a mutant basic helix-loop-helix protein HFR1, HFR1-deltaN105, activates a branch pathway of light signaling in Arabidopsis. Plant Physiology 2003, 133:1630-1642. 10.1104/pp.103.029751, 300719, 14645731.
16. Cao H, Li X, Dong X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:6531-6536. 10.1073/pnas.95.11.6531, 34547, 9601001.
17. Chern M, Fitzgerald HA, Canlas PE, Navarre DA, Ronald PC. Overexpression of a Rice NPR1 Homolog Leads to Constitutive Activation of Defense Response and Hypersensitivity to Light. Molecular Plant-Microbe Interactions 2005, 18:511-520. 10.1094/MPMI-18-0511, 15986920.
18. Tohidfar M, Mohammadi M, Ghareyazie B. Agrobacterium-mediated transformation of cotton (Gossypium hirsutum) using a heterologous bean chitinase gene. Plant Cell Tissue and Organ Culture 2005, 83:83-96.
19. Wang YQ, Chen DJ, Wang DM, Huang QS, Yao ZP, Liu FJ, Wei XW, Li RJ, Zhang ZN, Sun YR. Over-expression of Gastrodia anti-fungal protein enhances Verticillium wilt resistance in coloured cotton. Plant Breeding 2004, 123:454-459.
20. Alfano JR, Collmer A. The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. Journal of Bacteriology 1997, 179:5655-5662. 179450, 9294418.
21. Dong H, Delaney TP, Bauer DW, Beer SV. Harpin induces disease resistance in Arabidopsis through the systemic acquired resistance pathway mediated by salicylic acid and the NIM1 gene. Plant Journal 1999, 20:207-215. 10.1046/j.1365-313x.1999.00595.x, 10571880.
22. Dong HP, Peng J, Bao Z, Meng X, Bonasera JM, Chen G, Beer SV, Dong H. Downstream divergence of the ethylene signaling pathway for harpin-stimulated Arabidopsis growth and insect defense. Plant Physiology 2004, 136:3628-2638. 10.1104/pp.104.048900, 527161, 15516507.
23. Li P, Long JY, Huang YC, Zhang Y, Wang JS. A novel member of avrBs3 gene family from Xanthomonas oryzae pv. oryzae has a dual function. Process in Natural Sciences 2004, 14:767-773.
24. Zou LF, Wang XP, Xiang Y, Zhang B, Li YR, Xiao YL, Wang JS, Walmsley AR, Chen GY. Elucidation of the hrp Clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host Rice. Applied and Environment Microbiology 2006, 72:6212-6224.
25. Gough CL, Genin S, Lopes V, Boucher CA. Homology between the HrpO protein of Pseudomonas solanacearum and bacterial proteins implicated in a signal peptide-independent secretion mechanism. Molecular and General Genetics: MGG 1993, 239:378-392.
26. Huguet E, Hahn K, Wengelnik K, Bonas U. hpaA mutants of Xanthomonas campestris pv. vesicatoria are affected in pathogenicity but retain the ability to induce host-specific hypersensitive reaction. Molecular Microbiology 1998, 29:1379-1390. 10.1046/j.1365-2958.1998.01019.x, 9781876.
27. Zhu W, Magbanua MM, White FF. Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. Journal of bacteriology 2000, 182:1844-1853. 10.1128/JB.182.7.1844-1853.2000, 101866, 10714988.
28. He SY, Huang HC, Collmer A. Pseudomonas syringae pv. syringae harpinPss: A protein that is secreted via the hrp pathway and elicits the hypersensitive response in plants. Cell 1993, 73:1255-1266. 10.1016/0092-8674(93)90354-S, 8324821.
29. Gaudriault S, Brisset MN, Barny MA. HrpW of Erwinia amylovora, a new Hrp-secreted protein. FEBS letters 1998, 428:224-228. 10.1016/S0014-5793(98)00534-1, 9654138.
30. Arlat M, Gijsegem FV, Huet JC, Pernollet JC, Boucher CA. PopA1, a protein which induces a hypersensitivity-like response on specific Petunia genotypes, is secreted via the Hrp pathway of Pseudomonas solanacearum. EMBO Journal 1994, 13:543-553. 394843, 8313899.
31. Lorenz C, Kirchner O, Egler M, Stuttmann J, Bonas U, Büttner D. HpaA from Xanthomonas is a regulator of type III secretion. Molecular Microbiology 2008, 69:344-360. 10.1111/j.1365-2958.2008.06280.x, 18485076.
32. Peng JL, Bao ZL, Ren HY, Wang JS, Dong HS. Expression of HarpinXoo in transgenic tobacco induces pathogen defense in the absence of hypersensitive cell death. Phytopathology 2004, 94:1048-1055. 10.1094/PHYTO.2004.94.10.1048, 18943792.
33. Shao M, Wang JS, Dean RA, Lin YG, Gao XW, Hu SJ. Expression of a harpin-encoding gene in rice confers durable nonspecific resistance to Magnaporthe grisea. Plant Biotechnology Journal 2008, 6:73-81.
34. Sohn S, Kim Y, Kim B, Lee S, Lim CK, Hur JH, Lee J. Transgenic tobacco expressing the hrpNEP Gene from Erwinia pyrifoliae triggers defense responses against Botrytis cinerea. Molecular Cells 2007, 24:232-239.
35. Li R, Fan Y. Reduction of lesion growth rate of late blight plant disease in transgenic potato expressing harpin protein. Science in China (Ser. C) 1999, 42:96-101.
36. Malnoy M, Venisse JS, Chevreau E. Expression of a bacterial effector, harpin N, causes increased resistance to fire blight in Pyrus communis. Tree Genet Genomes 2005, 1:41-49.
37. Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley powdery mildew interaction. Plant Journal 1997, 11:1187-1194.
38. Jiang M, Zhang J. Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant and Cell Physiology 2001, 42:1265-1273. 10.1093/pcp/pce162, 11726712.
39. Wang X, Dou D, Wang Z, Jia S. Cloning full-length cDNA of GbNPR1 gene from Gossypium barbadense and its expression in transgenic tobacco. Scientia Agricultura Sinica 2006, 39:886-894.
40. Li F, Zhang Y, Wang M, Zhang Y, Wu X, Guo X. Molecular cloning and expression characteristics of alternative oxidase gene of cotton (Gossypium hirsutum). Molecular Biology Reports 2008, 35:97-105. 10.1007/s11033-007-9058-6, 17351819.
41. Maxwell DP, Wang Y, McIntosh L. The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:8271-8276. 10.1073/pnas.96.14.8271, 22224, 10393984.
42. Pontier D, Godiard L, Marco Y, Roby D. Hsr203J, a tobacco gene whose activation is rapid, highly localized and specific for incompatible plant. Plant Journal 1994, 5:507-521. 10.1046/j.1365-313X.1994.5040507.x, 8012404.
43. Pontier D, Balague C, Bezombes MI, Tronchet M, Deslandes L, Roby D. Identification of a novel pathogen-responsive element in the promoter of the tobacco gene HSR203J, a molecular marker of the hypersensitive response. Plant Journal 2001, 26:495-507. 10.1046/j.1365-313x.2001.01049.x, 11439136.
44. Liu J, Benedict CR, Stipanovic RD, Magill CW, Bell AA. Cloning and expression of desoxyhemigossypol-6-O-methyltransferase from cotton (Gossypium barbadense). Journal of Agricultural and Food Chemistry 2002, 50:3165-3172. 10.1021/jf011701y, 12009981.
45. Miao W, Wang L, Zhang S, Nurzya, Sheng M, Jin W, Tan Z. Adjustment and control of two biocontrol products with hrp gene against cotton Verticillium wilt. Xinjiang Agricultural Sciences 2004, 41:299-302.
46. Chen R, Wang K. The population genetics of cotton Verticillium Wilt in China. Cotton Science 2001, 13:209-212.
47. Hoyos AE, Stanley CM, He SY, Pike S, Pu XA, Novacky A. The interaction of harpinPss with plant cell walls. Molecular Plant-Microbe Interactions 1996, 9:608-616.
48. Tampakaki AP, Panopoulos NJ. Elicitation of hypersensitive cell death by extracellularly targeted HrpZPsph produced in planta. Molecular Plant-Microbe Interactions 2000, 13:1366-1374. 10.1094/MPMI.2000.13.12.1366, 11106029.
49. Racapé J, Belbahri L, Engelhardt S, Lacombe B, Lee J, Lochman J, Arai AS, Nicole M, Nürnberger T, Parlange F, Puverel S, Keller H. Ca2+ dependent lipid binding and membrane integration of PopA, a harpin-like elicitor of the hypersensitive response in tobacco. Molecular Microbiology 2005, 58:1406-1420.
50. Lee J, Klusener B, Tsiamis G, Stevens C, Neyt C, Tampakaki AP, Panopoulos NJ, Nöller J, Weiler EW, Cornelis GR, Mansfield JW, Nürnberger T. HrpZ (Psph) from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion conducting pore in vitro. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:294.
51. Chevalier J, Kazatchkine MD. Distribution in clusters of complement receptor type one (CR1) on human erythrocytes. The Journal of Immunology 1989, 142:2031-2036.
52. Colitti M, Musetti R, Stefanon B. Detection of apoptosis-inducing factor in involuting mammary tissue by immunoelectron microscopy. Micron 2004, 35:307-310. 10.1016/j.micron.2003.08.002, 15003619.
53. Evergren E, Tomilin N, Vasylieva E, Sergeeva V, Bloom O, Gad H, Capani F, Shupliakov O. A pre-embedding immunogold approach for detection of synaptic endocytic proteins in situ. Journal of Neuroscience Methods 2004, 135:169-174. 10.1016/j.jneumeth.2003.12.010, 15020101.
54. Fahimi HD, Reich D, Völkl A, Baumgart E. Contributions of the immunogold technique to investigation of the biology of peroxisomes. Histochemistry and Cell Biology 1996, 106:105-114. 10.1007/BF02473205, 8858370.
55. Fournier J, Françoise E, Villemeur T, Robain O, Corinne I, Deslys J, Dormont D, Brown P. Distribution and submicroscopic immunogold localization of cellular prion protein (PrPc) in extracerebral tissues. Cell and Tissue Research 1998, 292:77-84. 10.1007/s004410051036, 9506914.
56. Dayakar BV, Lin HJ, Chen CH, Ger MJ, Lee BH, Pai CH, Chow D, Huang HE, Hwang SY, Chung MC, Feng TY. Ferredoxin from sweet pepper (Capsicum annuum L.) intensifying harpinPss-mediated hypersensitive response shows an enhanced production of active oxygen species (AOS). Plant Molecular Biology 2003, 51:913-924. 10.1023/A:1023061303755, 12777051.
57. Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CM, Poinssot JB, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B. Priming: Getting ready for battle. Molecular Plant-Microbe Interactions 2006, 19:1062-1071. 10.1094/MPMI-19-1062, 17022170.
58. Durrant WE, Dong X. Systemic acquired resistance. Annual Review of Phytopathology 2004, 42:185-209. 10.1146/annurev.phyto.42.040803.140421, 15283665.
59. Goellner K, Conrath U. Priming: it's all the world to induced disease resistance. European Journal of Plant Pathology 2008, 121:233-242.
60. Trouvelot S, Varnier AL, Allegre M, Mercier L, Baillieul F, Arnould C, Gianinazzi Pearson V, Klarzynski O, Joubert JM, Pugin A. A o-1,3 glucan sulfate induces resistance in grapevine against Plasmopara viticola through priming of defense responses, including HR-like cell death. Molecular Plant-Microbe Interactions 2008, 21:232-243. 10.1094/MPMI-21-2-0232, 18184067.
61. An G, Ebert P, Mitra A, Ha S. Binary vectors. Plant Molecular Biology Manual 1988, 1-19. Dordrecht, Netherlands: Kluwer Academic Publishers, Gelvin SB, Schilperoort RA.
62. Sunilkumar G, Rathore KS. Transgenic cotton: factors influencing Agrobacterium-mediated transformation and regeneration. Molecular Breeding 2001, 8:37-52.
63. Joost O, Bianchini G, Bell AA, Benedict CR, Magill CW. Differential induction of 3-hydroxy-3-methylglutaryl CoA reductase in two cotton species following inoculation with Verticillium. Molecular Plant-Microbe Interactions 1995, 8:880-885.
64. Yang C, Guo WZ, Li GY, Gao F, Lin SS, Zhang TZ. QTLs mapping for Verticillium wilt resistance at seedling and maturity stages in Gossypium barbadense L. Plant Science 2008, 174:290-298.
65. Slot JW, Geuze HJ. A new method of preparing gold probes for multiple-labeling cytochemistry. European Journal of Cell Biology 1985, 38:87-93.
66. Wu J, Zhang X, Nie Y, Luo X. High-efficiency transformation of Gossypium hirsutum embryogenic calli mediated by Agrobacterium tumefaciens and regeneration of insect-resistant plants. Plant Breeding 2005, 124:142-146.
67. Amano T, Hirasawa K, O'Donohue MJ, Pernolle JC, Shioi Y. A versatile assay for the accurate, time-resolved determination of cellular viability. Analytical Biochemistry 2003, 1-7. 10.1016/S0003-2697(02)00653-X, 12633596.
68. Lipka V, Dittgen J, Bednarek P, Bhat R, Wiermer M, Stein M, Landtag J, Brandt W, Rosahl S, Scheel D, Francisco LF, Molina A, Parker J, Somerville S, Schulze-Lefert P. Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 2005, 310:1180-1183. 10.1126/science.1119409, 16293760.
69. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-CT method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.