Rice stripe disease, caused by rice stripe virus (RSV), is one of the major virus diseases in east Asia. Rice plants infected with RSV usually show symptoms such as chlorosis, weakness, necrosis in newly emerged leaves and stunting. To reveal rice cellular systems influenced by RSV infection, temporal changes in the transcriptome of RSV-infected plants were monitored by a customized rice oligoarray system. The transcriptome changes in RSV-infected plants indicated that protein-synthesis machineries and energy production in the mitochondrion were activated by RSV infection, whereas energy production in the chloroplast and synthesis of cell-structure components were suppressed. The transcription of genes related to host-defence systems under hormone signals and those for gene silencing were not activated at the early infection phase. Together with concurrent observation of virus concentration and symptom development, such transcriptome changes in RSV-infected plants suggest that different sets of various host genes are regulated depending on the development of disease symptoms and the accumulation of RSV.


Article metrics loading...

Loading full text...

Full text loading...



  1. Amari, K., Díaz-Vivancos, P., Pallás, V., Sánchez-Pina, M. A. & Hernández, J. A.(2007). Oxidative stress induction by Prunus necrotic ringspot virus infection in apricot seeds. Physiol Plant 131, 302–310. [Google Scholar]
  2. Bannai, H., Tamada, Y., Maruyama, O., Nakai, K. & Miyano, S.(2002). Extensive feature detection of N-terminal protein sorting signals. Bioinformatics 18, 298–305.[CrossRef] [Google Scholar]
  3. Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Rudnev, D., Evangelista, C., Kim, I. F., Soboleva, A., Tomashevsky, M. & Edgar, R.(2007). NCBI GEO: mining tens of millions of expression profiles – database and tools update. Nucleic Acids Res 35, D760–D765.[CrossRef] [Google Scholar]
  4. Burn, J. E., Hurley, U. A., Birch, R. J., Arioli, T., Cork, A. & Williamson, R. E.(2002). The cellulose-deficient Arabidopsis mutant rsw3 is defective in a gene encoding a putative glucosidase II, an enzyme processing N-glycans during ER quality control. Plant J 32, 949–960.[CrossRef] [Google Scholar]
  5. Cabauatan, P. Q., Kobayashi, N., Ikeda, R. & Koganezawa, H.(1993).Oryza glaberrima: an indicator plant for rice tungro spherical virus. Int J Pest Manage 39, 273–276.[CrossRef] [Google Scholar]
  6. Chen, X. & Guo, Z.(2008). Tobacco OPBP1 enhances salt tolerance and disease resistance of transgenic rice. Int J Mol Sci 9, 2601–2613.[CrossRef] [Google Scholar]
  7. Cheng, Y. Q., Liu, Z. M., Xu, J., Zhou, T., Wang, M., Chen, Y. T., Li, H. F. & Fan, Z. F.(2008). HC-Pro protein of sugar cane mosaic virus interacts specifically with maize ferredoxin-5 in vitro and in planta. J Gen Virol 89, 2046–2054.[CrossRef] [Google Scholar]
  8. Coruzzi, G. M. & Zhou, L.(2001). Carbon and nitrogen sensing and signaling in plants: emerging 'matrix effects'. Curr Opin Plant Biol 4, 247–253.[CrossRef] [Google Scholar]
  9. Dardick, C.(2007). Comparative expression profiling of Nicotiana benthamiana leaves systemically infected with three fruit tree viruses. Mol Plant Microbe Interact 20, 1004–1017.[CrossRef] [Google Scholar]
  10. Díaz-Vivancos, P., Clemente-Moreno, M. J., Rubio, M., Olmos, E., García, J. A., Martínez-Gómez, P. & Hernández, J. A.(2008). Alteration in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to plum pox virus. J Exp Bot 59, 2147–2160.[CrossRef] [Google Scholar]
  11. Emanuelsson, O., Brunak, S., von Heijne, G. & Nielsen, H.(2007). Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2, 953–971.[CrossRef] [Google Scholar]
  12. Espinoza, C., Medina, C., Somerville, S. & Arce-Johnson, P.(2007). Senescence-associated genes induced during compatible viral interactions with grapevine and Arabidopsis. J Exp Bot 58, 3197–3212.[CrossRef] [Google Scholar]
  13. Fafournoux, P., Bruhat, A. & Jousse, C.(2000). Amino acid regulation of gene expression. Biochem J 351, 1–12.[CrossRef] [Google Scholar]
  14. Falk, B. W. & Tsai, J. H.(1998). Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol 36, 139–163.[CrossRef] [Google Scholar]
  15. Fang, Y., You, J., Xie, K., Xie, W. & Xiong, L.(2008). Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280, 547–563.[CrossRef] [Google Scholar]
  16. Finn, R. D., Tate, J., Mistry, J., Coggill, P. C., Sammut, S. J., Hotz, H. R., Ceric, G., Forslund, K., Eddy, S. R. & other authors(2008). The Pfam protein families database. Nucleic Acids Res 36, D281–D288.[CrossRef] [Google Scholar]
  17. Gendler, K., Paulsen, T. & Napoli, C.(2008). ChromDB: the chromatin database. Nucleic Acids Res 36, D298–D302. [Google Scholar]
  18. Golem, S. & Culver, J. N.(2003). Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Mol Plant Microbe Interact 16, 681–688.[CrossRef] [Google Scholar]
  19. Gutterson, N. & Reuber, T. L.(2004). Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7, 465–471.[CrossRef] [Google Scholar]
  20. Hedden, P. & Phillips, A. L.(2000). Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5, 523–530.[CrossRef] [Google Scholar]
  21. Ishiga, Y., Uppalapati, S. R., Ishiga, T., Elavarthi, S., Martin, B. & Bender, C. L.(2009). The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol 181, 147–160.[CrossRef] [Google Scholar]
  22. Jiménez, I., López, L., Alamillo, J. M., Valli, A. & García, J. A.(2006). Identification of a plum pox virus CI-interacting protein from chloroplast that has a negative effect in virus infection. Mol Plant Microbe Interact 19, 350–358.[CrossRef] [Google Scholar]
  23. Kandoth, P. K., Ranf, S., Pancholi, S. S., Jayanty, S., Walla, M. D., Miller, W., Howe, G. A., Lincoln, D. E. & Stratmann, J. W.(2007). Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc Natl Acad Sci U S A 104, 12205–12210.[CrossRef] [Google Scholar]
  24. Kanehisa, M., Araki, M., Goto, S., Hattori, M., Hirakawa, M., Itoh, M., Katayama, T., Kawashima, S., Okuda, S. & other authors(2008).kegg for linking genomes to life and the environment. Nucleic Acids Res 36, D480–D484. [Google Scholar]
  25. Kitanaga, Y., Jian, C., Hasegawa, M., Yazaki, J., Kishimoto, N., Kikuchi, S., Nakamura, H., Ichikawa, H., Asami, T. & other authors(2006). Sequential regulation of gibberellin, brassinosteroid, and jasmonic acid biosynthesis occurs in rice coleoptiles to control the transcript levels of anti-microbial thionin genes. Biosci Biotechnol Biochem 70, 2410–2419.[CrossRef] [Google Scholar]
  26. Lee, J. & Rudd, J. J.(2002). Calcium-dependent protein kinases: versatile plant signalling components necessary for pathogen defence. Trends Plant Sci 7, 97–98. [Google Scholar]
  27. Lehto, K., Tikkanen, M., Hiriart, J. B., Paakkarinen, V. & Aro, E. M.(2003). Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Mol Plant Microbe Interact 16, 1135–1144.[CrossRef] [Google Scholar]
  28. Levy, A., Dafny-Yelin, M. & Tzfira, T.(2008). Attacking the defenders: plant viruses fight back. Trends Microbiol 16, 194–197.[CrossRef] [Google Scholar]
  29. Li, H., Zhou, S. Y., Zhao, W. S., Su, S. C. & Peng, Y. L.(2009). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Mol Biol 69, 337–346.[CrossRef] [Google Scholar]
  30. Liang, D., Qu, Z., Ma, X. & Hull, R.(2005). Detection and localization of rice stripe virus gene products in vivo. Virus Genes 31, 211–221.[CrossRef] [Google Scholar]
  31. Liang, C., Jaiswal, P., Hebbard, C., Avraham, S., Buckler, E. S., Casstevens, T., Hurwitz, B., McCouch, S., Ni, J. & other authors(2008). Gramene: a growing plant comparative genomics resource. Nucleic Acids Res 36, D947–D953. [Google Scholar]
  32. Loake, G. & Grant, M.(2007). Salicylic acid in plant defence – the players and protagonists. Curr Opin Plant Biol 10, 466–472.[CrossRef] [Google Scholar]
  33. Love, A. J., Laval, V., Geri, C., Laird, J., Tomos, A. D., Hooks, M. A. & Milner, J. J.(2007). Components of Arabidopsis defense- and ethylene-signaling pathways regulate susceptibility to cauliflower mosaic virus by restricting long-distance movement. Mol Plant Microbe Interact 20, 659–670.[CrossRef] [Google Scholar]
  34. Lu, L., Du, Z., Qin, M., Wang, P., Lan, H., Niu, X., Jia, D., Xie, L., Lin, Q. & other authors(2009). Pc4, a putative movement protein of rice stripe virus, interacts with a type I DnaJ protein and a small Hsp of rice. Virus Genes 38, 320–327.[CrossRef] [Google Scholar]
  35. Marathe, R., Guan, Z., Anandalakshmi, R., Zhao, H. & 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.[CrossRef] [Google Scholar]
  36. Mitsuhara, I., Iwai, T., Seo, S., Yanagawa, Y., Kawahigasi, H., Hirose, S., Ohkawa, Y. & Ohashi, Y.(2008). Characteristic expression of twelve rice PR1 family genes in response to pathogen infection, wounding, and defense-related signal compounds (121/180). Mol Genet Genomics 279, 415–427.[CrossRef] [Google Scholar]
  37. Nakashima, K., Tran, L. S., Van Nguyen, D., Fujita, M., Maruyama, K., Todaka, D., Ito, Y., Hayashi, N., Shinozaki, K. & Yamaguchi-Shinozaki, K.(2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51, 617–630.[CrossRef] [Google Scholar]
  38. Ou, S. H.(1972). Virus diseases. In Rice Diseases, pp. 14–22. Surrey, UK: Commonwealth Mycological Institute.
  39. Ouyang, S., Zhu, W., Hamilton, J., Lin, H., Campbell, M., Childs, K., Thibaud-Nissen, F., Malek, R. L., Lee, Y. & other authors(2007). The TIGR Rice Genome Annotation Resource: improvements and new features. Nucleic Acids Res 35, D883–D887.[CrossRef] [Google Scholar]
  40. Radwan, D. E., Lu, G., Fayez, K. A. & Mahmoud, S. Y.(2008). Protective action of salicylic acid against bean yellow mosaic virus infection in Vicia faba leaves. J Plant Physiol 165, 845–857.[CrossRef] [Google Scholar]
  41. Raychaudhuri, S., Fontanes, V., Barat, B. & Dasgupta, A.(2009). Activation of ribosomal RNA transcription by hepatitis C virus involves upstream binding factor phosphorylation via induction of cyclin D1. Cancer Res 69, 2057–2064. [Google Scholar]
  42. Riano-Pachon, D. M., Ruzicic, S., Dreyer, I. & Mueller-Roeber, B.(2007). PlnTFDB: an integrative plant transcription factor database. BMC Bioinformatics 8, 42[CrossRef] [Google Scholar]
  43. Rice Annotation Project(2008). The Rice Annotation Project Database (rap-db): 2008 update. Nucleic Acids Res 36, D1028–D1033. [Google Scholar]
  44. Rice Full-length cDNA Consortium(2003). Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301, 376–379.[CrossRef] [Google Scholar]
  45. Ryu, C. M., Murphy, J. F., Mysore, K. S. & Kloepper, J. W.(2004). Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against cucumber mosaic virus by a salicylic acid and NPR1-independent and jasmonic acid-dependent signaling pathway. Plant J 39, 381–392.[CrossRef] [Google Scholar]
  46. Ryu, H. S., Han, M., Lee, S. K., Cho, J. I., Ryoo, N., Heu, S., Lee, Y. H., Bhoo, S. H., Wang, G. L. & other authors(2006). A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Rep 25, 836–847.[CrossRef] [Google Scholar]
  47. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T. & other authors(2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374–378. [Google Scholar]
  48. Satoh, K., Doi, K., Nagata, T., Kishimoto, N., Suzuki, K., Otomo, Y., Kawai, J., Nakamura, M., Hirozane-Kishikawa, T. & other authors(2007). Gene organization in rice revealed by full-length cDNA mapping and gene expression analysis through microarray. PLoS One 2, e1235[CrossRef] [Google Scholar]
  49. Senthil, G., Liu, H., Puram, V. G., Clark, A., Stromberg, A. & 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.[CrossRef] [Google Scholar]
  50. Shamir, R., Maron-Katz, A., Tanay, A., Linhart, C., Steinfeld, I., Sharan, R., Shiloh, Y. & Elkon, R.(2005).expander – an integrative program suite for microarray data analysis. BMC Bioinformatics 6, 232[CrossRef] [Google Scholar]
  51. Shimizu, T., Toriyama, S., Takahashi, M., Akutsu, K. & Yoneyama, K.(1996). Non-viral sequences at the 5′ termini of mRNAs derived from virus-sense and virus-complementary sequences of the ambisense RNA segments of rice stripe tenuivirus. J Gen Virol 77, 541–546.[CrossRef] [Google Scholar]
  52. Shimizu, T., Satoh, K., Kikuchi, S. & Omura, T.(2007). The repression of cell wall- and plastid-related genes and the induction of defense-related genes in rice plants infected with rice dwarf virus. Mol Plant Microbe Interact 20, 247–254.[CrossRef] [Google Scholar]
  53. Shimono, M., Sugano, S., Nakayama, A., Jiang, C. J., Ono, K., Toki, S. & Takatsuji, H.(2007). Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19, 2064–2076.[CrossRef] [Google Scholar]
  54. Shinkai, A.(1977). Rice waika, a new virus disease, and problems related to its occurrence and control. Jpn Agric Res Q 11, 151–155 (in Japanese). [Google Scholar]
  55. Silverstein, K. A., Moskal, W. A., Jr, Wu, H. C., Underwood, B. A., Graham, M. A., Town, C. D. & VandenBosch, K. A.(2007). Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51, 262–280.[CrossRef] [Google Scholar]
  56. Somerville, C.(2006). Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22, 53–78.[CrossRef] [Google Scholar]
  57. Syam Prakash, S. R. & Jayabaskaran, C.(2006). Expression and localization of calcium-dependent protein kinase isoforms in chickpea. J Plant Physiol 163, 1135–1149.[CrossRef] [Google Scholar]
  58. Takahashi, Y., Omura, T., Shohara, K. & Tsuchizaki, T.(1991). Comparison of four serological methods for practical detection of ten viruses of rice in plants and insects. Plant Dis 75, 458–461.[CrossRef] [Google Scholar]
  59. Tameling, W. I. & Baulcombe, D. C.(2007). Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19, 1682–1694.[CrossRef] [Google Scholar]
  60. Todeschini, A. L., Morillon, A., Springer, M. & Lesage, P.(2005). Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 25, 7459–7472.[CrossRef] [Google Scholar]
  61. Uzarowska, A., Dionisio, G., Sarholz, B., Piepho, H. P., Xu, M., Ingvardsen, C. R., Wenzel, G. & Lübberstedt, T.(2009). Validation of candidate genes putatively associated with resistance to SCMV and MDMV in maize (Zea mays L.) by expression profiling. BMC Plant Biol 9, 15[CrossRef] [Google Scholar]
  62. van Loon, L. C., Rep, M. & Pieterse, C. M.(2006). Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44, 135–162.[CrossRef] [Google Scholar]
  63. Wasternack, C.(2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot (Lond) 100, 681–697.[CrossRef] [Google Scholar]
  64. Whitham, S. A., Quan, S., Chang, H. S., Cooper, B., Estes, B., Zhu, T., Wang, X. & 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.[CrossRef] [Google Scholar]
  65. Wise, R. P., Moscou, M. J., Bogdanove, A. J. & Whitham, S. A.(2007). Transcript profiling in host–pathogen interactions. Annu Rev Phytopathol 45, 329–369.[CrossRef] [Google Scholar]
  66. Xiong, R., Wu, J., Zhou, Y. & Zhou, X.(2008). Identification of a movement protein of the tenuivirus rice stripe virus. J Virol 82, 12304–12311.[CrossRef] [Google Scholar]
  67. Xiong, R., Wu, J., Zhou, Y. & Zhou, X.(2009). Characterization and subcellular localization of an RNA silencing suppressor encoded by rice stripe tenuivirus. Virology 387, 29–40.[CrossRef] [Google Scholar]
  68. Yang, C., Guo, R., Jie, F., Nettleton, D., Peng, J., Carr, T., Yeakley, J. M., Fan, J. B. & 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.[CrossRef] [Google Scholar]
  69. Yu, F., Fu, A., Aluru, M., Park, S., Xu, Y., Liu, H., Liu, X., Foudree, A., Nambogga, M. & Rodermel, S.(2007). Variegation mutants and mechanisms of chloroplast biogenesis. Plant Cell Environ 30, 350–365.[CrossRef] [Google Scholar]
  70. Zhang, F., Kirouac, M., Zhu, N., Hinnebusch, A. G. & Rolfes, R. J.(1997). Evidence that complex formation by Bas1p and Bas2p (Pho2p) unmasks the activation function of Bas1p in an adenine-repressible step of ADE gene transcription. Mol Cell Biol 17, 3272–3283. [Google Scholar]
  71. Zhang, C., Liu, Y., Sun, X., Qian, W., Zhang, D. & Qiu, B.(2008a). Characterization of a specific interaction between IP-L, a tobacco protein localized in the thylakoid membranes, and tomato mosaic virus coat protein. Biochem Biophys Res Commun 374, 253–257.[CrossRef] [Google Scholar]
  72. Zhang, X., Wang, X. & Zhou, G.(2008b). A one-step real time RT-PCR assay for quantifying rice stripe virus in rice and in the small brown planthopper (Laodelphax striatellus Fallen). J Virol Methods 151, 181–187.[CrossRef] [Google Scholar]

Data & Media loading...


Summary of the microarray results in this study [ Excel file] (10.5 MB)


List of RSV-responsive genes categorized by protein domains encoded. The data are the source data for Fig. 2 in the paper [ Excel file] (7 MB)


List of RSV-responsive genes in each category. The data are the source data for Fig. 2 and Table 1 in the paper [ Excel file] (3 MB)


Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error