Characterization of defense-related genes in the 'Qinguan' apple in response to Marssonina coronaria

South African Journal of Botany

Volumn 80, Issue , 2012, Pages 36-43

  Zhou, Q ^a   Gao, H ^a   Wang, M ^a   Xu, Y ^a   Guo, Y Z ^a   Wan, Y Z ^a   Zhao, Z Y ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

Apple; Expressed sequence tags; Marssonina coronaria; Quantitative Real Time PCR; Suppression subtractive hybridization

Indexed keywords

DEFENSE BEHAVIOR; ENZYME ACTIVITY; FRUIT; FUNGAL DISEASE; GENE EXPRESSION; HYBRIDIZATION; INOCULATION; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; POLYMERASE CHAIN REACTION; PROTEIN;

CHINA;

BACTERIA (MICROORGANISMS); MALUS X DOMESTICA; MARSSONINA; VENTURIA INAEQUALIS;

EID: 84860483233     PISSN: 02546299     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sajb.2012.01.005     Document Type: Article

References (69)

1. Aglika E. Pathogenesis-related proteins: research progress in the last 15years. General and Applied Plant Physiology 2005, 31:105-124.
2. Ali G.S., Reddy V.S., Lindgren P.B., Jakobek J.L., Reddy A.S.N. Differential expression of genes encoding calmodulin-binding proteins in response to bacterial pathogens and inducers of defense responses. Plant Molecular Biology 2003, 51:803-815.
3. Bachem C.W.B., Van Der Hoeven R.S., De Bruijn S.M., Vreugdenhil D., Zabeau M., Visser R.G.F. Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. The Plant Journal 1996, 9:745-753.
4. Bae E.-K., Lee H., Lee J.-S., Noh E.-W. Isolation and characterization of osmotic stress-induced genes in poplar cells by suppression subtractive hybridization and cDNA microarray analysis. Plant Physiology and Biochemistry 2010, 48:136-141.
5. Blackman L.M., Hardham A.R. Regulation of catalase activity and gene expression during Phytophthora nicotianae development and infection of tobacco. Molecular Plant Pathology 2008, 9:495-510.
6. Bolwell P.P., Page A., Piślewska M., Wojtaszek P. Pathogenic infection and the oxidative defences in plant apoplast. Protoplasma 2001, 217:20-32.
7. Borges J.P., Jauneau A., Brulé C., Culerrier R., Barre A., Didier A., Rougé P. The lipid transfer proteins (LTP) essentially concentrate in the skin of Rosaceae fruits as cell surface exposed allergens. Plant Physiology and Biochemistry 2006, 44:535-542.
8. Carvalho A.D., Gomes V.M. Plant defensins-prospects for the biological functions and biotechnological properties. Peptides 2009, 30:1007-1020.
9. Chiasson D., Ekengren S.K., Martin G.B., Dobney S.L., Snedden W.A. Calmodulin-like proteins from Arabidopsis and tomato are involved in host defense against Pseudomonas syringae pv. tomato. Plant Molecular Biology 2005, 58:887-897.
10. Choi H.W., Lee D.H., Hwang B.K. The pepper calmodulin gene CaCaM1 is involved in reactive oxygen species and nitric oxide generation required for cell death and the defense response. Molecular Plant-Microbe Interactions 2009, 22:1389-1400.
11. Degenhardt J., Al-Masri A.N., Kürkcüoglu S., Szankowski I., Gau A.E. Characterization by suppression subtractive hybridization of transcripts that are differentially expressed in leaves of apple scab-resistant and susceptible cultivars of Malus domestica. Molecular Genetics and Genomics 2005, 273:326-335.
12. Diatchenko L., Lau Y.F., Campbell A.P., Chenchik A., Moqadam F., Huang B., Lukyanov S., Lukyanov K., Gurskaya N., Sverdlov E.D., Siebert P.D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences 1996, 93:6025-6030.
13. Diatchenko L., Lukyanov S., Lau Y.-F.C., Siebert P.D. Suppression subtractive hybridization: a versatile method for identifying differentially expressed genes. Methods in Enzymology 1999, vol. 303:349-380. Academic Press. M.W. Sherman (Ed.).
14. Du L., Ali G.S., Simons K.A., Hou J., Yang T., Reddy A.S.N., Poovaiah B.W. Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 2009, 457:1154-1158.
15. Dunaevskii Y.E., Tsybina T.A., Belyakova G.A., Domash V.I., Sharpio T.P., Zabreiko S.A., Belozerskii M.A. Proteinase inhibitors as antistress proteins in higher plants. Applied Biochemistry and Microbiology 2005, 41:344-348.
16. Egusa M., Ochi H., Tsuge T., Otani H., Kodama M. Identification of putative defense-related genes in Japanese pear against Alternaria alternata infection using suppression subtractive hybridization and expression analysis. Journal of General Plant Pathology 2009, 75:119-124.
17. Fan H., Wang F., Gao H., Wang L., Jihua Xu., Zhao Z. Pathogen-induced MdWRKY1 in 'Qinguan' apple enhances disease resistance. Journal of Plant Biology 2011, 54:150-158.
18. Fernandez-Caballero C., Romero I., Goñi O., Escribano M.I., Merodio C., Sanchez-Ballesta M.T. Characterization of an antifungal and cryoprotective Class I chitinase from table grape berries (Vitis vinifera Cv. Cardinal). Journal of Agricultural and Food Chemistry 2009, 57:8893-8900.
19. Gasic K., Hernandez A., Korban S. RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Molecular Biology Reporter 2004, 22:437-438.
20. Gau A.E., Koutb M., Piotrowski M., Kloppstech K. Accumulation of pathogenesis-related proteins in the apoplast of a susceptible cultivar of apple (Malus domestica cv. Elstar) after infection by Venturia inaequalis and constitutive expression of PR genes in the resistant cultivar Remo. European Journal of Plant Pathology 2004, 110:703-711.
21. Greenberg J.T., Yao N. The role and regulation of programmed cell death in plant-pathogen interactions. Cellular Microbiology 2004, 6:201-211.
22. Heath M.C. Hypersensitive response-related death. Plant Molecular Biology 2000, 44:321-334.
23. Ho V.S.M., Wong J.H., Ng T.B. A thaumatin-like antifungal protein from the emperor banana. Peptides 2007, 28:760-766.
24. Huckelhoven R. Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proceedings of the National Academy of Sciences 2003, 100:5555-5560.
25. Isbat M., Zeba N., Kim S.R., Hong C.B. A BAX inhibitor-1 gene in Capsicum annuum is induced under various abiotic stresses and endows multi-tolerance in transgenic tobacco. Journal of Plant Physiology 2009, 166:1685-1693.
26. Ishigaki E., Sugiyama R., Kurosaki F. Multiple forms of calmodulin genes in carrot treated with fungal mycelial walls. Biological & Pharmaceutical Bulletin 2005, 28:1109-1112.
27. Jean-Marc N. Plant Chitinases (PR-3, PR-4, PR-8, PR-11). Pathogenesis-related Proteins in Plants 1999, CRC Press.
28. Jindřichová B., Fodor J., Šindelářová M., Burketová L., Valentová O. Role of hydrogen peroxide and antioxidant enzymes in the interaction between a hemibiotrophic fungal pathogen, Leptosphaeria maculans, and oilseed rape. Environmental and Experimental Botany 2011, 72:149-156.
29. Joshi B.N., Sainani M.N., Bastawade K.B., Gupta V.S., Ranjekar P.K. Cysteine protease inhibitor from pearl millet: a new class of antifungal protein. Biochemical and Biophysical Research Communications 1998, 246:382-387.
30. Kader J.-C. Lipid-transfer proteins: a puzzling family of plant proteins. Trends in Plant Science 1997, 2:66-70.
31. Kim B.-G., Fukumoto T., Tatano S., Gomi K., Ohtani K., Tada Y., Akimitsu K. Molecular cloning and characterization of a thaumatin-like protein-encoding cDNA from rough lemon. Physiological and Molecular Plant Pathology 2009, 74:3-10.
32. Klee C.B., Vanaman T.C. Calmodulin. Advances in Protein Chemistry 1982, vol. 35:213-321. Academic Press. J.T.E.C.B. Anfinsen, M.R. Frederic (Eds.).
33. Kombrink E., Schmelzer E. The hypersensitive response and its role in local and systemic disease resistance. European Journal of Plant Pathology 2001, 107:69-78.
34. Kopparapu N.K., Liu Z., Fei F., Yan Q., Jiang Z. Purification and characterization of a chitinase (sAMC) with antifungal activity from seeds of Astragalus membranaceus. Process Biochemistry 2011, 46:1370-1374.
35. Krebitz M., Wagner B., Ferreira F., Peterbauer C., Campillo N., Witty M., Kolarich D., Steinkellner H., Scheiner O., Breiteneder H. Plant-based heterologous expression of Mal d 2, a thaumatin-like protein and allergen of apple (Malus domestica), and its characterization as an antifungal protein. Journal of Molecular Biology 2003, 329:721-730.
36. Lecourieux D., Ranjeva R., Pugin A. Calcium in plant defence-signalling pathways. The New Phytologist 2006, 171:249-269.
37. Lee D.-H., Back C.-G., Win N.K.K., Choi K.-H. Biological characterization of Marssonina coronaria associated with apple blotch disease. Mycobiology 2011, 39:200-205.
38. Levee V., Major I., Levasseur C., Tremblay L., MacKay J., Seguin A. Expression profiling and functional analysis of populus WRKY23 reveals a regulatory role in defense. The New Phytologist 2009, 184:48-70.
39. Li H.-E., Wang X.-P., Wang Y.-J. Isolation and sequence analysis of calmodulin gene of Chinese wild Vitis quinquangularis. Acta Botanica Boreali-Occidentalia Sinica 2010, 30:1507-1513.
40. Ma W., Smigel A., Tsai Y.-C., Braam J., Berkowitz G.A. Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiology 2008, 148:818-828.
41. Matsumura H., Nirasawa S., Kiba A., Urasaki N., Saitoh H., Ito M., Kawai-Yamada M., Uchimiya H., Terauchi R. Overexpression of Bax inhibitor suppresses the fungal elicitor-induced cell death in rice (Oryza sativa L.) cells. The Plant Journal 2003, 33:425-434.
42. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. The Plant Journal 2002, 29:257-268.
43. Mzid R., Marchive C., Blancard D., Deluc L., Barrieu F., Corio-Costet M.-F., Drira N., Hamdi S., Lauvergeat V. Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiologia Plantarum 2007, 131:434-447.
44. Newcomb R.D. Analyses of expressed sequence tags from apple. Plant Physiology 2006, 141:147-166.
45. Norelli J.L., Farrell R.E., Bassett C.L., Baldo A.M., Lalli D.A., Aldwinckle H.S., Wisniewski M.E. Rapid transcriptional response of apple to fire blight disease revealed by cDNA suppression subtractive hybridization analysis. Tree Genetics & Genomes 2008, 5:27-40.
46. Paris R., Cova V., Pagliarani G., Tartarini S., Komjanc M., Sansavini S. Expression profiling in HcrVf2-transformed apple plants in response to Venturia inaequalis. Tree Genetics & Genomes 2008, 5:81-91.
47. Peng X.X., Tang X.K., Zhou P.L., Hu Y.J., Deng X.B., He Y., Wang H.H. Isolation and expression patterns of rice WRKY82 transcription factor gene responsive to both biotic and abiotic stresses. Agricultural Sciences in China 2011, 10:893-901.
48. Ramamoorthy V., Zhao X., Snyder A.K., Xu J.-R., Shah D.M. Two mitogen-activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum. Cellular Microbiology 2007, 9:1491-1506.
49. Roberts D.M., Harmon A.C. Calcium-modulated proteins: targets of intracellular calcium signals in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 1992, 43:375-414.
50. Rushton P.J., Somssich I.E., Ringler P., Shen Q.J. WRKY transcription factors. Trends in Plant Science 2010, 15:247-258.
51. Sagaram U.S., Pandurangi R., Kaur J., Smith T.J., Shah D.M. Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PloS One 2011, 6. (Article No.: e18550).
52. Sanzani S.M., Schena L., De Girolamo A., Ippolito A., González-Candelas L. Characterization of genes associated with induced resistance against Penicillium expansum in apple fruit treated with quercetin. Postharvest Biology and Technology 2010, 56:1-11.
53. Sarowar S., Zhao Y., Soria-Guerra R.E., Ali S., Zheng D., Wang D., Korban S.S. Expression profiles of differentially regulated genes during the early stages of apple flower infection with Erwinia amylovora. Journal of Experimental Botany 2011, 10.1093/jxb/err147.
54. Schena M., Shalon D., Davis R.W., Brown P.O. Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 1995, 270:467-470.
55. Sels J., Mathys J., De Coninck B.M.A., Cammue B.P.A., De Bolle M.F.C. Plant pathogenesis-related (PR) proteins: a focus on PR peptides. Plant Physiology and Biochemistry 2008, 46:941-950.
56. Shetty N.P., Mehrabi R., Lütken H., Haldrup A., Kema G.H.J., Collinge D.B., Jørgensen H.J.L. Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. The New Phytologist 2007, 174:637-647.
57. Shou Y.-Y., Li C.-M. In vitro evaluation of resistance to Marssonina mali in apple. Journal of Fruit Science 2009, 26:912-914.
58. Stotz H.U., Thomson J., Wang Y. Plant defensins: defense, development and application. Plant Signaling & Behavior 2009, 4:1010-1012.
59. 2 in rice cells inoculated with rice blast fungus, Magnaporthe oryzae. Physiologia Plantarum 2009, 137:148-154.
60. van Loon L.C., Rep M., Pieterse C.M.J. Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 2006, 44:135-162.
61. Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 2002, 3. research0034.1-research0034.11.
62. Veluthakkal R., Dasgupta M. Pathogenesis-related genes and proteins in forest tree species. Trees - Structure and Function 2010, 24:993-1006.
63. Vieira F.A., Carvalho A.O., Vitoria A.P., Retamal C.A., Gomes V.M. Differential expression of defence-related proteins in Vigna unguiculata (L. Walp.) seedlings after infection with Fusarium oxysporum. Crop Protection 2010, 29:440-447.
64. Watanabe N., Lam E. The hypersensitive response in plant disease resistance multigenic and induced systemic resistance in plants 2006, 83-111. Springer, US. S. Tuzun, E. Bent (Eds.).
65. Wong J.H., Ng T.B., Cheung R.C.F., Ye X.J., Wang H.X., Lam S.K., Lin P., Chan Y.S., Fang E.F., Ngai P.H.K., Xia L.X., Ye X.Y., Jiang Y., Liu F. Proteins with antifungal properties and other medicinal applications from plants and mushrooms. Applied Microbiology and Biotechnology 2010, 87:1221-1235.
66. Zhang J., Li Z., Yao J., Hu C. Identification of flowering-related genes between early flowering trifoliate orange mutant and wild-type trifoliate orange (Poncirus trifoliata L. Raf.) by suppression subtraction hybridization (SSH) and macroarray. Gene 2009, 430:95-104.
67. Zhang K., Dang Z., Zhao L. Study on inheritance tendency of the resistance to apple early defoliation disease using 'Qinguan' and 'Fuji'. Journal of Northwest Forestry University 2007, 22:128-130.
68. Zhao H., Huang L.-L., Xie F.-Q., Kang Z.-S. Culture study of Marssonina coronaria from diseased apple leaves. Mycosystema 2009, 28:490-495.
69. Zhu Y.J., Agbayani R., Moore P.H. Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor. Planta 2007, 226:87-97.