Identification of genes required for Cf-dependent hypersensitive cell death by combined proteomic and RNA interfering analyses

Journal of Experimental Botany

Volumn 63, Issue 7, 2012, Pages 2421-2435

  Xu, Qiu Fang ^a   Cheng, Wei Shun ^a   Li, Shuang Sheng ^a   Li, Wen ^a   Zhang, Zhi Xin ^a   Xu, You Ping ^a   Zhou, Xue Ping ^a,b   Cai, Xin Zhong ^a,b  

^a ZHEJIANG UNIVERSITY   (China)

^b BEIJING HOSPITAL   (China)

Author keywords

Cf; Cladosporium fulvum; defence; gene silencing; hypersensitive cell death; proteomics; regulation; resistance; RNAi

Indexed keywords

FUNGAL PROTEIN; VEGETABLE PROTEIN;

ARTICLE; CELL DEATH; CLADOSPORIUM; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PROTEOMICS; RNA INTERFERENCE; TOBACCO; TOMATO; TRANSGENIC PLANT;

CELL DEATH; CLADOSPORIUM; DISEASE RESISTANCE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEOMICS; RNA INTERFERENCE; TOBACCO;

BACTERIA (MICROORGANISMS); CLADOSPORIUM FULVUM; LYCOPERSICON ESCULENTUM; NICOTIANA BENTHAMIANA; TOBACCO RATTLE VIRUS; XANTHOMONAS ORYZAE PV. ORYZAE;

EID: 84861052812     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err397     Document Type: Article

References (59)

1. + channels of Cf-9 transgenic tobacco guard cells as targets for Cladosporium fulvum Avr9 elicitor-dependent signal transduction. The Plant Journal 19, 453-462.
2. Brenner ED, Lambert KN, Kaloshian I, Williamson VM. 1998. Characterization of LeMir, a root-knot nematode-induced gene in tomato with an encoded product secreted from the root. Plant Physiology 118, 237-247. (Pubitemid 128652986)
3. Burch-Smith TM, Anderson JC, Martin GB, Dinesh-Kumar SP. 2004. Applications and advantages of virus-induced gene silencing for gene function studies in plants. The Plant Journal 39, 734-746. (Pubitemid 39218781)
4. Cai X, Takken FLW, Joosten MHAJ, De Wit PJGM. 2001. Specific recognition of AVR4 and AVR9 results in distinct patterns of hypersensitive cell death in tomato, but similar patterns of defencerelated gene expression. Molecular Plant Pathology 2, 77-86. (Pubitemid 32532924)
5. Cai XZ, Wang CC, Xu YP, Xu QF, Zheng Z, Zhou XP. 2007. Efficient gene silencing induction in tomato by a viral satellite DNA vector. Virus Research 125, 169-175. (Pubitemid 46589678)
6. Damerval C, de Vienne D, Zivy M, Thiellement H. 1986. The technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7, 52-54.
7. De Jong CF, Honée G, Joosten MHAJ, De Wit PJGM. 2000. Early defence responses induced by AVR9 and mutant analogues in tobacco cell suspensions expressing the Cf-9 resistance gene. Physiological and Molecular Plant Pathology 56, 169-177.
8. De Jong CF, Takken FLW, Cai X, De Wit PJGM, Joosten MHAJ. 2002. Attenuation of Cf-mediated defence responses at elevated temperatures correlates with a decrease in elicitor-binding sites. Molecular Plant-Microbe Interactions 15, 1040-1049. (Pubitemid 35211758)
9. De Wit PJGM. 2007. How plants recognize pathogens and defend themselves. Cellular and Molecular Life Sciences 64, 2726-2732. (Pubitemid 351152262)
10. Dixon DP, Hawkins T, Hussey PJ, Edwards R. 2009. Enzyme activities and subcellular localization of members of the Arabidopsis glutathione transferase superfamily. Journal of Experimental Botany 60, 1207-1218.
11. Dixon MS, Jones DA, Keddie JS, Thomas CM, Harrison K, Jones JDG. 1996. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell 84, 451-459. (Pubitemid 26058570)
12. Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JDG. 2000. cDNA-AFLP reveals a striking overlap in race specific resistance and wound response gene expression profiles. The Plant Cell 12, 963-977. (Pubitemid 30458040)
13. Gabriëls SHEJ, Takken FLW, Vossen JH, et al. 2006. cDNA-AFLP combined with functional analysis reveals novel genes involved in the hypersensitive response. Molecular Plant-Microbe Interactions 19, 567-576. (Pubitemid 43787721)
14. Gabriëls SHEJ, Vossen JH, Ekengren SK, et al. 2007. An NB-LRR protein required for HR signalling mediated by both extra-and intracellular resistance proteins. The Plant Journal 50, 14-28. (Pubitemid 46493390)
15. Giannino D, Nicolodi C, Testone G, Frugis G, Pace E, Santamaria P, Guardasole M, Mariotti D. 2008. The overexpression of asparagine synthetase A from E. coli affects the nitrogen status in leaves of lettuce (Lactuca sativa L.) and enhances vegetative growth. Euphytica 162, 11-22. (Pubitemid 351792551)
16. Gonzalez-Lamothe R, Tsitsigiannis DI, Ludwig AA, Panicot M, Shirasu K, Jones JDG. 2006. The U-Box protein CMPG1 is required for efficient activation of defence mechanisms triggered by multiple resistance genes in tobacco and tomato. The Plant Cell 18, 1067-1083. (Pubitemid 43956154)
17. Hong W, Xu YP, Zheng Z, Cao JS, Cai XZ. 2007. Comparative transcript profiling by cDNA-AFLP reveals similar patterns of Avr4/Cf-4-and Avr9/Cf-9-dependent defence gene expression. Molecular Plant Pathology 8, 515-527. (Pubitemid 46985632)
18. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329. (Pubitemid 44764102)
19. Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG. 1994. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266, 789-793. (Pubitemid 24359284)
20. Joosten MHAJ, Cozijnsen TJ, De Wit PJGM. 1994. Host resistance to a fungal tomato pathogen lost by a single base-pair change in an avirulence gene. Nature 367, 384-386. (Pubitemid 24062348)
21. Joosten MHAJ, De Wit PJGM. 1999. The tomato-Cladosporium fulvum interaction: a versatile experimental system to study plant-pathogen interactions. Annual Review of Phytopathology 37, 335-367. (Pubitemid 29523939)
22. Karrer EE, Beachy RN, Holt CA. 1998. Cloning of tobacco genes that elicit the hypersensitive response. Plant Molecular Biology 36, 681-690. (Pubitemid 28153788)
23. Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, Gu C, Ilyas M, Win J, Kamoun S, van der Hoorn RAL. 2010. An effector-targeted protease contributes to defence against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiology 154, 1794-1804.
24. Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JDG. 2002. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 296, 744-747. (Pubitemid 34442004)
25. Luderer R, Takken FLW, De Wit PJGM, Joosten MHAJ. 2002. Cladosporium fulvum overcomes Cf-2-mediated resistance by producing truncated AVR2 elicitor proteins. Molecular Microbiology 45, 875-884. (Pubitemid 34989192)
26. Olea F, Perez-Garcia A, Canton FR, Rivera ME, Canas R, Avila C, Cazorla FM, Canovas FM, de Vicente A. 2004. Up-regulation and localization of asparagine synthetase in tomato leaves infected by the bacterial pathogen Pseudomonas syringae. Plant and Cell Physiology 45, 770-780. (Pubitemid 38893501)
27. Parisy V, Poinssot1 B, Owsianowski L, Buchala A, Glazebrook J, Mauch F. 2007. Identification of PAD2 as a c-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. The Plant Journal 49, 159-172. (Pubitemid 44952706)
28. Piedras P, Hammond-Kosack KE, Harrison K, Jones JDG. 1998. Rapid, Cf-9-and Avr9-dependent production of active oxygen species in tobacco suspension cultures. The Plant Cell 11, 1155-1166. (Pubitemid 28548143)
29. Rivas S, Rougon-Cardoso A, Smoker M, Schauser L, Yoshioka H, Jones JDG. 2004. CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence. The EMBO Journal 23, 2156-2165. (Pubitemid 38737742)
30. Rivas S, Thomas CM. 2005. Molecular interactions between tomato and the leaf mold pathogen Cladosporium fulvum. Annual Review of Phytopathology 43, 395-436. (Pubitemid 41318878)
31. Romeis T, Ludwig AA, Martin R, Jones JDG. 2001. Calciumdependent protein kinases play an essential role in a plant defence response. The EMBO Journal 20, 5556-5567. (Pubitemid 33010033)
32. Romeis T, Piedras P, Jones JDG. 2000. Resistance genedependent activation of a calcium-dependent protein kinase in the plant defence response. The Plant Cell 12, 803-815. (Pubitemid 30343589)
33. Romeis T, Piedras P, Zhang S, Klessig DF, Hirt H, Jones JDG. 1999. Rapid Avr9-and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. The Plant Cell 11, 273-287.
34. Rooney HCE, van 't Klooster JW, van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Wit PJGM. 2005. Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783-1786. (Pubitemid 40848005)
35. Rowland O, Ludwig AA, Merrick CJ, et al. 2005. Functional analysis of Avr9/Cf-9 rapidly elicited genes identifies a protein kinase, ACIK1, that is essential for full Cf-9-dependent disease resistance in tomato. The Plant Cell 17, 295-310. (Pubitemid 41673004)
36. Shabab M, Shindo T, Gu C, Kaschani F, Pansuriya T, Chintha R, Harzen A, Colby T, Kamoun S, van der Hoorn RAL. 2008. Fungal effector protein AVR2 targets diversifying defence-related Cys proteases of tomato. The Plant Cell 20, 1169-1183. (Pubitemid 352843986)
37. Song J, Win J, Tian M, Schornack S, Kaschani F, Ilyas M, van der Hoorn RA, Kamoun S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defence protease Rcr3. Proceedings of the National Academy of Sciences USA 106, 1654-1659.
38. Stergiopoulos I, de Wit PJGM. 2009. Fungal effector proteins. Annual Review of Phytopathology 47, 233-263.
39. Stulemeijer IJE, Joosten MHAJ, Jensen ON. 2009. Quantitative phosphoproteomics of tomato mounting a hypersensitive response reveals a swift suppression of photosynthetic activity and a differential role for Hsp90 isoforms. Journal of Proteome Research 8, 1168-1182.
40. Stulemeijer IJE, Stratmann JW, Joosten MHAJ. 2007. Tomato mitogen-activated protein kinases LeMPK1, LeMPK2, and LeMPK3 are activated during the Cf-4/Avr4-induced hypersensitive response and have distinct phosphorylation specificities. Plant Physiology 144, 1481-1494. (Pubitemid 47037466)
41. Suckau D, Resemann A, Schuerenberg M, Hufnagel P, Franzen J, Holle A. 2003. A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Analytical and Bioanalytical Chemistry 376, 952-965. (Pubitemid 40877913)
42. Takken FLW, Schipper D, Nijkamp HJJ, Hille J. 1998. Identification and Ds-tagged isolation of a new gene at the Cf-4 locus of tomato involved in disease resistance to Cladosporium fulvum race 5. The Plant Journal 14, 401-411. (Pubitemid 28295392)
43. Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JDG. 1997. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. The Plant Cell 9, 2209-2224. (Pubitemid 28174057)
44. Thomas CM, Tang S, Hammond-Kosack K, Jones JDG. 2000. Comparison of the hypersensitive response induced by the Cf-4 and Cf-9 genes in Nicotiana spp. Molecular Plant-Microbe Interactions 13, 465-469. (Pubitemid 30174530)
45. Tian M, Win J, Song J, van der Hoorn RAL, van der Knaap E, Kamoun S. 2007. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiology 143, 364-377. (Pubitemid 46133641)
46. Van den Ackerveken GFJM, Van Kan JAL, De Wit PJGM. 1992. Molecular analysis of the avirulence gene avr9 of the fungal tomato pathogen Cladosporium fulvum fully supports the gene-for-gene hypothesis. The Plant Journal 2, 359-366.
47. Van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, MacLean D, Takken FLW, Jones JDG. 2008. The F-box protein ACRE189/ACIF1 regulates cell death and defence responses activated during pathogen recognition in tobacco and tomato. The Plant Cell 20, 697-719. (Pubitemid 352844002)
48. van der Hoorn RA, Kamoun S. 2008. From guard to decoy: a new model for perception of plant pathogen effectors. The Plant Cell 20, 2009-2017. (Pubitemid 352844506)
49. Van der Hoorn RA, Laurent F, Roth R, De Wit PJGM. 2000. Agroinfiltration is a versatile tool that facilitates comparative analyses of Avr9/Cf-9-induced and Avr4/Cf-4-induced necrosis. Molecular Plant-Microbe Interactions 13, 439-446. (Pubitemid 30174527)
50. van Esse HP, van't Klooster JW, Bolton MD, Yadeta KA, Van Baarlen P, Boeren S, Vervoort J, de Wit PJGM, Thomma BPHJ. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defence. The Plant Cell 20, 1948-1963. (Pubitemid 352844543)
51. Wang C, Cai X, Wang X, Zheng Z. 2006a. Optimisation of tobacco rattle virus-induced gene silencing in Arabidopsis. Functional Plant Biology 33, 347-355.
52. Wang CC, Cai XZ, Xu YP. 2006b. Molecular mechanism of interaction between tomato and leaf mold pathogen Cladosporium fulvum. Acta Phytopathologica Sinica 36, 385-391.
53. Wang C, Cai X, Zheng Z. 2005. High humidity represses Cf-4/Avr4-and Cf-9/Avr9-dependent hypersensitive cell death and defence gene expression. Planta 222, 947-956. (Pubitemid 41706032)
54. Westerink N, Brandwagt BF, de Wit PJGM, Joosten MHAJ. 2004. Cladosporium fulvum circumvents the second functional resistance gene homologue at the Cf-4 locus (Hcr9-4E) by secretion of a stable avr4E isoform. Molecular Microbiology 54, 533-545. (Pubitemid 39388294)
55. Xu YP, Xu QF, Song XY, Zhang ZX, Cai XZ. 2008. Virus-induced gene silencing. Journal of Zhejiang University (Agric and Life Sci) 34, 119-131.
56. Xu YP, Zheng LP, Xu QF, Wang CC, Zhou XP, Wu ZJ, Cai XZ. 2007. Efficiency for gene silencing induction in Nicotiana species by a viral satellite DNA vector. Journal of Integrative Plant Biology 49, 1726-1733.
57. Yan JX, Wait R, Berkelman T, Harry RA. Westbrook JA, Wheeler CH, Dunn MJ. 2000. A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and elecctrospray ionizationmass spectrometry. Electrophoresis 21, 3666-3672.
58. Yang CW, Gonzalez-Lamothe R, Ewan RA, Rowland O, Yoshioka H, Shenton M, Ye H, O'Donnell E, Jones JDG, Sadanandom A. 2006. The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defence. The Plant Cell 18, 1084-1098. (Pubitemid 43956155)
59. Zhu JW, Xu YP, Zhang ZX, Cao WY, Cai XZ. 2008. Transcript profiling for Avr4/Cf-4-and Avr9/Cf-9-dependent defence gene expression. European Journal of Plant Pathology 122, 307-314.