Disruption of a novel gene for a NAC-domain protein in rice confers resistance to Rice dwarf virus

Plant Journal

Volumn 57, Issue 4, 2009, Pages 615-625

  Yoshii, Motoyasu ^a,b   Shimizu, Takumi ^a   Yamazaki, Muneo ^b   Higashi, Takahiko ^a   Miyao, Akio ^b   Hirochika, Hirohiko ^b   Omura, Toshihiro ^a  

^a NATIONAL AGRICULTURAL RESEARCH CENTER   (Japan)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Host factor; NAC transcription factor; Resistance; Rice; Rice dwarf virus; Tos17

Indexed keywords

PLANT RNA; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; HEMIPTERA; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT DISEASE; PLANT GENE; REOVIRUS; RICE; SEQUENCE ALIGNMENT; TRANSCRIPTION INITIATION; TRANSGENIC PLANT; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; HEMIPTERA; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; MUTATION; ORYZA SATIVA; PHYLOGENY; PLANT DISEASES; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; REOVIRIDAE; RNA, PLANT; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

CICADELLIDAE; MIRIDAE; ORYZA SATIVA; RICE DWARF VIRUS;

EID: 59149100214     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2008.03712.x     Document Type: Article

References (70)

1. Abramoff, M.D., Magelhaes, P.J. Ram, S.J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36 42.
2. Agrawal, G.K., Yamazaki, M., Kobayashi, M., Hirochika, R., Miyao, A. Hirochika, H. (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol. 125, 1248 1257.
3. Ahlquist, P., Noueiry, A.O., Lee, W.M., Kushner, D.B. Dye, B.T. (2003) Host factors in positive-strand RNA virus genome replication. J. Virol. 77, 8181 8186.
4. Ahmadi, N., Albar, L., Pressoir, G., Pinel, A., Fargette, D. Ghesquière, A. (2001) Genetic basis and mapping of the resistance to Rice yellow mottle virus. III. Analysis of QTL efficiency in introgressed progenies confirmed the hypothesis of complementary epistasis between two resistance QTLs. Theor. Appl. Genet. 103, 1084 1092.
5. Albar, L., Bangratz-Reyser, M., Hebrard, E., Ndjiondjop, M.N., Jones, M. Ghesquiere, A. (2006) Mutations in the eIF(iso)4G translation initiation factor confer high resistance of rice to Rice yellow mottle virus. Plant J. 47, 417 426.
6. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A. Struhl, K. (1998) Current Protocols in Molecular Biology. New York : Greene and Wiley Interscience.
7. Boccardo, G. Milne, R.G. (1984) Plant reovirus group. In CMI/AAB Descriptions of Plant Viruses (Morant, A.F. Harrison, B.D., eds). Kew, UK : Commonwealth Microbiology Institute/Association of Applied Biology, pp. 1 7.
8. Cao, X., Zhou, P., Zhang, X., Zhu, S., Zhong, X., Xiao, Q., Ding, B. Li, Y. (2005) Identification of an RNA silencing suppressor from a plant double-stranded RNA virus. J. Virol. 79, 13018 13027.
9. Carrington, J.C. Whitham, S.A. (1998) Viral invasion and host defense: strategies and counter-strategies. Curr. Opin. Plant Biol. 1, 336 341.
10. Chisholm, S.T., Mahajan, S.K., Whitham, S.A., Yamamoto, M.L. Carrington, J.C. (2000) Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc. Natl Acad. Sci. USA, 97, 489 494.
11. Chisholm, S.T., Parra, M.A., Anderberg, R.J. Carrington, J.C. (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol. 127, 1667 1675.
12. Chisholm, S.T., Coaker, G., Day, B. Staskawicz, B.J. (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell, 124, 803 814.
13. Choi, C.W., Qu, F., Ren, T., Ye, X. Morris, T.J. (2004) RNA silencing-suppressor function of Turnip crinkle virus coat protein cannot be attributed to its interaction with the Arabidopsis protein TIP. J. Gen. Virol. 85, 3415 3420.
14. Collinge, M. Boller, T. (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol. Biol. 46, 521 529.
15. Delessert, C., Kazan, K., Wilson, I.W., Van Der Straeten, D., Manners, J., Dennis, E.S. Dolferus, R. (2005) The transcription factor ATAF2 represses the expression of pathogenesis-related genes in Arabidopsis. Plant J. 43, 745 757.
16. Ding, X.L., Jiang, L., Liu, S.J., Wang, C.M., Chen, L.M., Cheng, Z.B., Fan, Y.J., Zhou, Y.J. Wan, J.M. (2004) QTL analysis for rice stripe disease resistance gene using recombinant inbred lines (RILs) derived from crossing of Kinmaze and DV85. Yi Chuan Xue Bao (Chinese), 31, 287 292.
17. Duprat, A., Caranta, C., Revers, F., Menand, B., Browning, K.S. Robaglia, C. (2002) The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J. 32, 927 934.
18. Duval, M., Hsieh, T.F., Kim, S.Y. Thomas, T.L. (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol. Biol. 50, 237 248.
19. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., Tran, L.S., Yamaguchi-Shinozaki, K. Shinozaki, K. (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J. 39, 863 876.
20. Fuse, T., Sasaki, T. Yano, M. (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol. 18, 219 222.
21. Hagiwara, Y., Komoda, K., Yamanaka, T., Tamai, A., Meshi, T., Funada, R., Tsuchiya, T., Naito, S. Ishikawa, M. (2003) Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J. 22, 344 353.
22. Hagiwara, K., Higashi, T., Miyazaki, N., Naitow, H., Cheng, R.H., Nakagawa, A., Mizuno, H., Tsukihara, T. Omura, T. (2004) The amino-terminal region of major capsid protein P3 is essential for self-assembly of single-shelled core-like particles of Rice dwarf virus. J. Virol. 78, 3145 3148.
23. Hegedus, D., Yu, M., Baldwin, D., Gruber, M., Sharpe, A., Parkin, I., Whitwill, S. Lydiate, D. (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol. Biol. 53, 383 397.
24. Hibino, H. (1996) Biology and epidemiology of rice viruses. Annu. Rev. Phytopathol. 34, 249 274.
25. Hiei, Y., Ohta, S., Komari, T. Kumashiro, T. (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271 282.
26. Hirochika, H. (2001) Contribution of the Tos17 retrotransposon to rice functional genomics. Curr. Opin. Plant Biol. 4, 118 122.
27. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature, 436, 793 800.
28. Janda, M. Ahlquist, P. (1993) RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell, 72, 961 970.
29. Lartey, R.T., Ghoshroy, S. Citovsky, V. (1998) Identification of an Arabidopsis thaliana mutation (vsm1) that restricts systemic movement of tobamoviruses. Mol. Plant Microbe Interact. 11, 706 709.
30. Lellis, A.D., Kasschau, K.D., Whitham, S.A. Carrington, J.C. (2002) Loss-of-susceptibility mutants of Arabidopsis thaliana reveal an essential role for eIF(iso)4E during potyvirus infection. Curr. Biol. 12, 1046 1051.
31. Leonard, S., Plante, D., Wittmann, S., Daigneault, N., Fortin, M.G. Laliberte, J.F. (2000) Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol. 74, 7730 7737.
32. Li, Y., Bao, Y.M., Wei, C.H., Kang, Z.S., Zhong, Y.W., Mao, P., Wu, G., Chen, Z.L., Schiemann, J. Nelson, R.S. (2004) Rice dwarf phytoreovirus segment S6-encoded nonstructural protein has a cell-to-cell movement function. J. Virol. 78, 5382 5389.
33. Liu, Y.G., Mitsukawa, N., Oosumi, T. Whittier, R.F. (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8, 457 463.
34. Maeda, H., Sugisawa, T., Nemoto, H. Sunohara, Y. (2004) QTL analysis for rice stripe resistance in the Japanese upland rice Kanto72. Breed. Sci. 54, 19 26.
35. Mahajan, S.K., Chisholm, S.T., Whitham, S.A. Carrington, J.C. (1998) Identification and characterization of a locus (RTM1) that restricts long-distance movement of tobacco etch virus in Arabidopsis thaliana. Plant J. 14, 177 186.
36. Mitsuhara, I., Ugaki, M., Hirochika, H. et al. (1996) Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 37, 49 59.
37. Miyao, A., Tanaka, K., Murata, K., Sawaki, H., Takeda, S., Abe, K., Shinozuka, Y., Onosato, K. Hirochika, H. (2003) Target site specificity of the Tos17 retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell, 15, 1771 1780.
38. Miyazaki, N., Hagiwara, K., Naitow, H., Higashi, T., Cheng, R.H., Tsukihara, T., Nakagawa, A. Omura, T. (2005) Transcapsidation and the conserved interactions of two major structural proteins of a pair of phytoreoviruses confirm the mechanism of assembly of the outer capsid layer. J. Mol. Biol. 345, 229 237.
39. Nakagawa, A., Miyazaki, N., Taka, J. et al. (2003) The atomic structure of rice dwarf virus reveals the self-assembly mechanism of component proteins. Structure, 11, 1227 1238.
40. Oh, S.K., Lee, S., Yu, S.H. Choi, D. (2005) Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta, 222, 876 887.
41. Ohnishi, T., Sugahara, S., Yamada, T., Kikuchi, K., Yoshiba, Y., Hirano, H.Y. Tsutsumi, N. (2005) OsNAC6, a member of the NAC gene family, is induced by various stresses in rice. Genes Genet. Syst. 80, 135 139.
42. Olsen, A.N., Ernst, H.A., Leggio, L.L. Skriver, K. (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci. 10, 79 87.
43. Ooka, H., Satoh, K., Doi, K. et al. (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res., 10, 239 247.
44. Osman, T.A. Buck, K.W. (1997) The tobacco mosaic virus RNA polymerase complex contains a plant protein related to the RNA-binding subunit of yeast eIF-3. J. Virol. 71, 6075 6082.
45. Quadt, R., Kao, C.C., Browning, K.S., Hershberger, R.P. Ahlquist, P. (1993) Characterization of a host protein associated with brome mosaic virus RNA-dependent RNA polymerase. Proc. Natl Acad. Sci. USA 90, 1498 1502.
46. Ren, T., Qu, F. Morris, T.J. (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell, 12, 1917 1926.
47. Ren, T., Qu, F. Morris, T.J. (2005) The nuclear localization of the Arabidopsis transcription factor TIP is blocked by its interaction with the coat protein of Turnip crinkle virus. Virology, 331, 316 324.
48. Sato, M., Nakahara, K., Yoshii, M., Ishikawa, M. Uyeda, I. (2005) Selective involvement of members of the eukaryotic initiation factor 4E family in the infection of Arabidopsis thaliana by potyviruses. FEBS Lett. 579, 1167 1171.
49. Selth, L.A., Dogra, S.C., Rasheed, M.S., Healy, H., Randles, J.W. Rezaian, M.A. (2005) A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell, 17, 311 325.
50. Shikata, E. (1972) Rice transitory yellowing virus. In CMI/AAB Descriptions of Plant Viruses (Morant, A.F. Harrison, B.D., eds). Kew, UK : Commonwealth Microbiology Institute/Association of Applied Biology, pp. 1 3.
51. 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.
52. Stein, N., Perovic, D., Kumlehn, J., Pellio, B., Stracke, S., Streng, S., Ordon, F. Graner, A. (2005) The eukaryotic translation initiation factor 4E confers multiallelic recessive Bymovirus resistance in Hordeum vulgare (L.). Plant J. 42, 912 922.
53. Takahashi, T., 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.
54. Takahashi, A., Agrawal, G.K., Yamazaki, M., Onosato, K., Miyao, A., Kawasaki, T., Shimamoto, K. Hirochika, H. (2007) Rice Pti1a negatively regulates RAR1-dependent defense responses. Plant Cell, 19, 2940 2951.
55. Toriyama, S. (1983) Rice stripe virus. In CMI/AAB Descriptions of Plant Viruses (Morant, A.F. Harrison, B.D., eds). Kew, UK : Commonwealth Microbiology Institute/Association of Applied Biology, pp. 1 5.
56. Tsujimoto, Y., Numaga, T., Ohshima, K., Yano, M.A., Ohsawa, R., Goto, D.B., Naito, S. Ishikawa, M. (2003) Arabidopsis TOBAMOVIRUS MULTIPLICATION (TOM) 2 locus encodes a transmembrane protein that interacts with TOM1. EMBO J. 22, 335 343.
57. Wei, T., Kikuchi, A., Moriyasu, Y., Suzuki, N., Shimizu, T., Hagiwara, K., Chen, H., Takahashi, M., Ichiki-Uehara, T. Omura, T. (2006a) The spread of Rice dwarf virus among cells of its insect vector exploits virus-induced tubular structures. J. Virol. 80, 8593 8602.
58. Wei, T., Kikuchi, A., Suzuki, N., Shimizu, T., Hagiwara, K., Chen, H. Omura, T. (2006b) Pns4 of rice dwarf virus is a phosphoprotein, is localized around the viroplasm matrix, and forms minitubules. Arch. Virol. 151, 1701 1712.
59. Wei, T., Shimizu, T., Hagiwara, K., Kikuchi, A., Moriyasu, Y., Suzuki, N., Chen, H. Omura, T. (2006c) Pns12 protein of Rice dwarf virus is essential for formation of viroplasms and nucleation of viral-assembly complexes. J. Gen. Virol. 87, 429 438.
60. Whitham, S.A. Wang, Y. (2004) Roles for host factors in plant viral pathogenicity. Curr. Opin. Plant Biol. 7, 365 371.
61. Wittmann, S., Chatel, H., Fortin, M.G. Laliberte, J.F. (1997) Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234, 84 92.
62. Xie, Q., Sanz-Burgos, A.P., Guo, H., Garcia, J.A. Gutierrez, C. (1999) GRAB proteins, novel members of the NAC domain family, isolated by their interaction with a geminivirus protein. Plant Mol. Biol. 39, 647 656.
63. Xie, Q., Frugis, G., Colgan, D. Chua, N.H. (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev. 14, 3024 3036.
64. Xu, H., Li, Y., Mao, Z. et al. (1998) Rice dwarf phytoreovirus segment S11 encodes a nucleic acid binding protein. Virology, 240, 267 272.
65. Yamanaka, T., Ohta, T., Takahashi, M., Meshi, T., Schmidt, R., Dean, C., Naito, S. Ishikawa, M. (2000) TOM1, an Arabidopsis gene required for efficient multiplication of a tobamovirus, encodes a putative transmembrane protein. Proc. Natl Acad. Sci. USA, 97, 10107 10112.
66. Yamanaka, T., Imai, T., Satoh, R., Kawashima, A., Takahashi, M., Tomita, K., Kubota, K., Meshi, T., Naito, S. Ishikawa, M. (2002) Complete inhibition of tobamovirus multiplication by simultaneous mutations in two homologous host genes. J. Virol. 76, 2491 2497.
67. Yamazaki, M., Tsugawa, H., Miyao, A., Yano, M., Wu, J., Yamamoto, S., Matsumoto, T., Sasaki, T. Hirochika, H. (2001) The rice retrotransposon Tos17 prefers low-copy-number sequences as integration targets. Mol. Genet. Genomics 265, 336 344.
68. Yoshii, M., Yoshioka, N., Ishikawa, M. Naito, S. (1998a) Isolation of an Arabidopsis thaliana mutant in which accumulation of cucumber mosaic virus coat protein is delayed. Plant J. 13, 211 219.
69. Yoshii, M., Yoshioka, N., Ishikawa, M. Naito, S. (1998b) Isolation of an Arabidopsis thaliana mutant in which the multiplication of both cucumber mosaic virus and turnip crinkle virus is affected. J. Virol. 72, 8731 8737.
70. Yoshii, M., Nishikiori, M., Tomita, K., Yoshioka, N., Kozuka, R., Naito, S. Ishikawa, M. (2004) The Arabidopsis cucumovirus multiplication 1 and 2 loci encode translation initiation factors 4E and 4G. J. Virol. 78, 6102 6111.