Microarray analysis shows that recessive resistance to Watermelon mosaic virus in melon is associated with the induction of defense response genes

Molecular Plant-Microbe Interactions

Volumn 25, Issue 1, 2012, Pages 107-118

  Gonzalez Ibeas, Daniel ^a   Cañizares, Joaquin ^b   Aranda, Miguel A ^a  

^a RESEARCH GROUP ON QUALITY   (Spain)

^b UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT RNA; TRANSCRIPTOME;

ARTICLE; CITRULLUS; CLUSTER ANALYSIS; COTYLEDON; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETICS; GENOTYPE; IMMUNOLOGY; MELON; MOLECULAR GENETICS; PHYSIOLOGY; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; POTYVIRUS; SEEDLING; TIME; TRANSCRIPTION INITIATION; VIROLOGY; VIRUS LOAD;

CITRULLUS; CLUSTER ANALYSIS; COTYLEDON; CUCUMIS MELO; GENE EXPRESSION PROFILING; GENES, PLANT; GENOTYPE; MOLECULAR SEQUENCE ANNOTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT DISEASES; PLANT IMMUNITY; POTYVIRUS; RNA, PLANT; SEEDLING; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME; VIRAL LOAD;

EID: 84055190760     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-07-11-0193     Document Type: Article

References (65)

1. Abdel-Ghany, S. E., and Pilon, M. 2008. MicroRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J. Biol. Chem. 283:15932-15945.
2. Agudelo-Romero, P., Carbonell, P., Perez-Amador, M. A., and Elena, S. F. 2008. Virus adaptation by manipulation of host's gene expression. PLoS ONE 3:e2397. Published online.
3. Al-Shahrour, F., Minguez, P., Tárraga, J., Medina, I., Alloza, E., Montaner, D., and Dopazo, J. 2007. FatiGO+: A functional profiling tool for genomic data. Integration of functional annotation, regulatory motifs and interaction data with microarray experiments. Nucleic Acids Res. 35:W91-W96.
4. Al-Shahrour, F., Carbonell, J., Minguez, P., Goetz, S., Conesa, A., Tarraga, J., Medina, I., Alloza, E., Montaner, D., and Dopazo, J. 2008. Babelomics: Advanced functional profiling of transcriptomics, proteomics and genomics experiments. Nucleic Acids Res. 36:W341-W346.
5. Aranda, M. A., Escaler, M., Wang, D., and Maule, A. J. 1996. Induction of HSP70 and polyubiquitin expression associated with plant virus replication. Proc. Natl. Acad. Sci. U.S.A. 93:15289-15293. (Pubitemid 27009593)
6. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock G. 2000. Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25:25-29. (Pubitemid 30257031)
7. Babu, M., Gagarinova, A. G., Brandle, J. E., and Wang, A. 2008. Association of the transcriptional response of soybean plants with Soybean mosaic virus systemic infection. J. Gen. Mol. Virol. 89:1069-1080.
8. Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall K. A., Phillippy, K. H., Sherman, P. M., Muertter, R. N., Holko, M., Ayanbule, O., Yefanov, A., and Soboleva, A. 2011. NCBI GEO: Archive for functional genomics data sets-10 years on. Nucleic Acids Res. 39:D1005-D1010.
9. Benschop, J. J., Mohammed, S., O'Flaherty, M., Heck, A. J. R., Slijper, M., and Menke, F. L. H. 2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 6:1198-1214. (Pubitemid 47099230)
10. Büschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., van Daelen, R., van der Lee, T., Diergaarde, P., Groenendijk, J., Töpsch, S., Vos, P., Salamini, F., and Schulze-Lefert, P. 1997. The barley Mlo gene: A novel control element of plant pathogen resistance. Cell 88:695-705. (Pubitemid 27152412)
11. Carroll, A. J., Heazlewood, J. L., Ito, J., and Millar, A. H. 2008. Analysis of the Arabidopsis cytosolic ribosome proteome provides detailed insights into its components and their post-translational modification. Mol. Cell. Proteomics 7:347-369. (Pubitemid 351298448)
12. Carvalho, B., Bengtsson, H., Speed, T. P., and Irizarry, R. A. 2007. Exploration, normalization, and genotype calls of high-density oligonucleotide SNP array data. Biostatistics 8:485-499. (Pubitemid 46569607)
13. Catoni, M., Miozzi, L., Fiorilli, V., Lanfranco, L., and Accotto, G. P. 2009. Comparative analysis of expression profiles in shoots and roots of tomato systemically infected by Tomato spotted wilt virus reveals organspecific transcriptional responses. Mol. Plant-Microbe Interact. 22:1504-1513.
14. Chandra-Shekara, A. C., Venugopal, S. C., Barman, S. R., Kachroo, A., and Kachroo, P. 2007. Plastidial fatty acid levels regulate resistance gene-dependent defense signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104:7277-7282. (Pubitemid 47186045)
15. Clepet, C., Joobeur, T., Zheng, Y., Jublot, D., Huang, M., Truniger, V., Boualem, A., Hernandez-Gonzalez, M. E., Dolcet-Sanjuan, R., Portnoy, V., Mascarell-Creus, A., Cano-Delgado, A. I., Katzir, N., Bendahmane, A., Giovannoni, J. J., Aranda, M. A., Garcia-Mas, J., and Fei, Z. 2011. Analysis of expressed sequence tags generated from full-length enriched cDNA libraries of melon. BMC Genomics 12:252.
16. Conesa, A., Nueda, M. J., Ferrer, A., and Talon, M. 2006. maSigPro: A method to identify significantly differential expression profiles in time-course microarray experiments. Bioinformatics 22:1096-1102.
17. Dardick, C. 2007. Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses. Mol. Plant-Microbe Interact. 20:1004-1017. (Pubitemid 47105733)
18. Diaz-Pendon, J. A., Fernandez-Munoz, R., Gomez-Guillamon, M. L., and Moriones, E. 2005. Inheritance of resistance to Watermelon mosaic virus in Cucumis melo that impairs virus accumulation, symptom expression, and aphid transmission. Phytopathology 95:840-846. (Pubitemid 40856539)
19. Doudna, J. A., and Rath, V. L. 2002. Structure and function of the eukaryotic ribosome: The next frontier. Cell 109:153-156. (Pubitemid 34518254)
20. Dudoit, S., Gentleman, R. C., and Quackenbush, J. 2003. Open source software for the analysis of microarray data. BioTechniques Suppl.:45-51.
21. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95:14863-14868. (Pubitemid 29003722)
22. Espinoza, C., Vega, A., Medina, C., Schlauch, K., Cramer, G., and Arce-Johnson, P. 2007. Gene expression associated with compatible viral diseases in grapevine cultivars. Funct. Integr. Genomics 7:95-110. (Pubitemid 46336166)
23. Fraser, R. S. S. 1992. The genetics of plant-virus interactions: Implications for plant breeding. Euphytica 63:175-185.
24. Gammelgård, E. 2007. Interactions of Potato virus A with host plants. Thesis. Swedish University of Agricultural Sciences, Uppsala, Sweden.
25. Gandía, M., Conesa, A., Ancillo, G., Gadea, J., Forment, J., Pallás, V., Flores, R., Duran-Vila, N., Moreno, P., and Guerri, J. 2007. Transcriptional response of Citrus aurantifolia to infection by Citrus tristeza virus. Virology 367:298-306. (Pubitemid 47494526)
26. García-Marcos, A., Pacheco, R., Martiáñez, J., González-Jara, P., Díaz-Ruíz, J. R., and Tenllado, F. 2009. Transcriptional changes and oxidative stress associated with the synergistic interaction between Potato virus X and Potato virus Y and their relationship with symptom expression. Mol. Plant-Microbe Interact. 22:1431-1444.
27. Golem, S., and Culver, J. N. 2003. Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Mol. Plant-Microbe Interact. 16:681-688. (Pubitemid 36914670)
28. Gonzalez-Ibeas, D., Blanca, J., Roig, C., Gonzalez-To, M., Pico, B., Truniger, V., Gomez, P., Deleu, W., Cano-Delgado, A., Arus, P., Nuez, F., Garcia-Mas, J., Puigdomenech, P., and Aranda, M. 2007. MELOGEN: An EST database for melon functional genomics. BMC Genomics 8:306.
29. Gonzalez-Ibeas, D., Blanca, J., Donaire, L., Saladié, M., Mascarell-Creus, A., Cano-Delgado, A., Garcia-Mas, J., Llave, C., and Aranda, M. A. 2011. Analysis of the melon (Cucumis melo) small RNAome by highthroughput pyrosequencing. BMC Genomics 12:393.
30. Ishibashi, K., Masuda, K., Naito, S., Meshi, T., and Ishikawa, M. 2007. An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proc. Natl. Acad. Sci. U.S.A. 104:13833-13838. (Pubitemid 350003406)
31. Kang, B.-C., Yeam, I., and Jahn, M. M. 2005. Genetics of plant virus resistance. Annu. Rev. Phytopathol. 43:581-621. (Pubitemid 41318884)
32. Kassem, M. A., Sempere, R. N., Juarez, M., Aranda, M. A., and Truniger, V. 2007. Cucurbit aphid-borne yellows virus is prevalent in fieldgrown cucurbit crops of southeastern Spain. Plant Dis. 91:232-238.
33. Lee, M.-L. T. 2004. Analysis of Microarray Gene Expression Data. Kluwer Academic Publishers, Boston.
34. Madlung, A., and Comai, L. 2004. The effect of stress on genome regulation and structure. Ann. Bot. 94:481-495. (Pubitemid 41295552)
35. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H., and Dinesh-Kumar, S. P. 2004. Study of Arabidopsis thaliana resistome in response to Cucumber mosaic virus infection using whole genome microarray. Plant Mol. Biol. 55:501-520. (Pubitemid 40653980)
36. Mascarell-Creus, A., Cañizares, J., Vilarrasa-Blasi, J., Mora-García, S., Blanca, J., Gonzalez-Ibeas, D., Saladié, M., Roig, C., Deleu, W., Picó-Silvent, B., López-Bigas, N., Aranda, M. A., Garcia-Mas, J., Nuez, F., Puigdomènech, P., and Cano-Delgado, A. I. 2009. An oligo-based microarray offers novel transcriptomic approaches for the analysis of pathogen resistance and fruit quality traits in melon (Cucumis melo L.). BMC Genomics 10:467-467.
37. Maule, A., Leh, V., and Lederer, C. 2002. The dialogue between viruses and hosts in compatible interactions. Curr. Opin. Plant Biol. 5:279-284. (Pubitemid 34695963)
38. Nicaise, V., German-Retana, S., Sanjuan, R., Dubrana, M.-P., Mazier, M., Maisonneuve, B., Candresse, T., Caranta, C., and LeGall, O. 2003. The eukaryotic translation initiation factor 4E controls lettuce Susceptibility to the potyvirus Lettuce mosaic virus. Plant Physiol. 132:1272-1282. (Pubitemid 36872877)
39. Nieto, C., Morales, M., Orjeda, G., Clepet, C., Monfort, A., Sturbois, B., Puigdomènech, P., Pitrat, M., Caboche, M., Dogimont, C., Garcia-Mas, J., Aranda, M. A., and Bendahmane, A. 2006. An eIF4E allele confers resistance to an uncapped and non-polyadenylated RNA virus in melon. Plant J. 48:452-462. (Pubitemid 44571150)
40. Nieto, C., Piron, F., Dalmais, M., Marco, C. F., Moriones, E., Gómez-Guillamón, M. L., Truniger, V., Gómez, P., Garcia-Mas, J., Aranda, M. A., and Bendahmane, A. 2007. EcoTILLING for the identification of allelic variants of melon eIF4E, a factor that controls virus susceptibility. BMC Plant Biol. 7:34-34.
41. Page, G. P., and Coulibaly, I. 2008. Bioinformatic tools for inferring functional information from plant microarray data: Tools for the first steps. Int. J. Plant Genomics 2008:147563-147563.
42. Palukaitis, P., and Carr, J. P. 2008. Plant resistance responses to viruses. J. Plant Pathol. 90:153-171.
43. Park, T., Yi, S.-G., Lee, S., Lee, S. Y., Yoo, D.-H., Ahn, J.-I., and Lee, Y.-S. 2003. Statistical tests for identifying differentially expressed genes in time-course microarray experiments. Bioinformatics 19:694-703. (Pubitemid 36511894)
44. Pompe-Novak, M., Gruden, K., Baebler, S., Krecic-Stres, H., Kovac, M., Jongsma, M., and Ravnikar, M. 2005. Potato virus Y induced changes in the gene expression of potato (Solanum tuberosum L.). Physiol. Mol. Plant Pathol. 67:237-247. (Pubitemid 43795431)
45. Raffaele, S., Vailleau, F., Leger, A., Joubes, J., Miersch, O., Huard, C., Blee, E., Mongrand, S., Domergue, F., and Roby, D. 2008. A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20:752-767. (Pubitemid 352844005)
46. Raychaudhuri, S., Stuart, J. M., and Altman, R. B. 2000. Principal components analysis to summarize microarray experiments: Application to sporulation time series. Pac. Symp. Biocomput. 2000:455-466.
47. Revers, F., Lot, H., Souche, S., Le Gall, O., Candresse, T., and Dunez, J. 1997. Biological and molecular variability of Lettuce mosaic virus isolates. Phytopathology 87:397-403. (Pubitemid 27165275)
48. Robaglia, C., and Caranta, C. 2006. Translation initiation factors: A weak link in plant RNA virus infection. Trends Plant Sci. 11:40-45. (Pubitemid 43053977)
49. Rozen, S., and Skaletsky, H. J. 2000. Primer3 on the WWW for general users and for biologist programmers. Pages 365-386 in: Bioinformatics Methods and Protocols, Methods in Molecular Biology. S. Krawetz and S. Misener, eds. Humana Press, Totowa, NJ, U.S.A.
50. Saeed, A. I., Bhagabati, N. K., Braisted, J. C., Liang, W., Sharov, V., Howe, E. A., Li, J., Thiagarajan, M., White, J. A., and Quackenbush, J. 2006. TM4 microarray software suite. Methods Enzymol. 411:134-193.
51. Satoh, K., Kondoh, H., Sasaya, T., Shimizu, T., Choi, I.-R., Omura, T., and Kikuchi, S. 2010. Selective modification of rice (Oryza sativa) gene expression by Rice stripe virus infection. J. Gen. Virol. 91:294-305.
52. Sekine, K.-T., Nandi, A., Ishihara, T., Hase, S., Ikegami, M., Shah, J., and Takahashi, H. 2004. Enhanced resistance to Cucumber mosaic virus in the Arabidopsis thaliana ssi2 mutant is mediated via an SA-independent mechanism. Mol. Plant-Microbe Interact. 17:623-632. (Pubitemid 38642206)
53. Senthil, G., Liu, H., Puram, V. G., Clark, A., Stromberg, A., and Goodin, M. M. 2005. Specific and common changes in Nicotiana benthamiana gene expression in response to infection by enveloped viruses. J. Gen. Virol. 86:2615-2625. (Pubitemid 41167610)
54. Shi, C., Ingvardsen, C., Thümmler, F., Melchinger, A. E., Wenzel, G., and Lübberstedt, T. 2005. Identification by suppression subtractive hybridization of genes that are differentially expressed between nearisogenic maize lines in association with Sugarcane mosaic virus resistance. Mol. Genet. Genomics 273:450-461. (Pubitemid 41073965)
55. Smith, C. M., Rodriguez-Buey, M., Karlsson, J., and Campbell, M. M. 2004. The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen. New Phytol. 164:123-136. (Pubitemid 39260335)
56. Soria, C., Moriones, E., Fereres, A., Garzo, E., and Gómez- Guillamón, M.L. 2003. New source of resistance to mosaic virus transmission by Aphis gossypii in melon. Euphytica 133:313-318. (Pubitemid 37261649)
57. Truniger, V., and Aranda, M. A. 2009. Recessive resistance to plant viruses. Adv. Virus Res. 75:119-159.
58. Truniger, V., Nieto, C., González-Ibeas, D., and Aranda, M. 2008. Mechanism of plant eIF4E-mediated resistance against a Carmovirus (Tombusviridae): Cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J. 56:716-727.
59. Tusher, V. G., Tibshirani, R., and Chu, G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U.S.A. 98:5116-5121. (Pubitemid 32397092)
60. Vaucheret, H., Mallory, A. C., and Bartel, D. P. 2006. AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol. Cell 22:129-136.
61. Wang, D., and Maule, A. J. 1995. Inhibition of host gene expression associated with plant virus replication. Science 267:229-231.
62. Whitham, S. A., Quan, S., Chang, H.-S., Cooper, B., Estes, B., Zhu, T., Wang, X., and Hou, Y.-M. 2003. Diverse RNA viruses elicit the expression of common sets of genes in susceptible Arabidopsis thaliana plants. Plant J. 33:271-283. (Pubitemid 36178006)
63. Whitham, S. A., Yang, C., and Goodin, M. M. 2006. Global impact: Elucidating plant responses to viral infection. Mol. Plant-Microbe Interact. 19:1207-1215. (Pubitemid 44607332)
64. Yang, C., Guo, R., Jie, F., Nettleton, D., Peng, J., Carr, T., Yeakley, J. M., Fan, J.-B., and Whitham, S. A. 2007. Spatial analysis of Arabidopsis thaliana gene expression in response to Turnip mosaic virus infection. Mol. Plant-Microbe Interact. 20:358-370. (Pubitemid 46449394)
65. Yang, C., Zhang, C., Dittman, J. D., and Whitham, S. A. 2009. Differential requirement of ribosomal protein S6 by plant RNA viruses with different translation initiation strategies. Virology 390:163-173.