リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Single Amino Acid Substitutions in the Cucumber Mosaic Virus 1a Protein Induce Necrotic Cell Death in Virus-Inoculated Leaves without Affecting Virus Multiplication」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Single Amino Acid Substitutions in the Cucumber Mosaic Virus 1a Protein Induce Necrotic Cell Death in Virus-Inoculated Leaves without Affecting Virus Multiplication

Ainan Tian Shuhei Miyashita Sugihiro Ando Hideki Takahashi 東北大学 DOI:10.3390/v12010091

2020.01.13

概要

When Arabidopsis thaliana ecotype Col-0 was inoculated with a series of reassortant viruses created by exchanging viral genomic RNAs between two strains of cucumber mosaic virus (CMV), CMV(Y), and CMV(H), cell death developed in the leaves inoculated with reassortant CMV carrying CMV(H) RNA1 encoding 1a protein, but not in noninoculated upper leaves. In general, cell death in virus-infected plants is a critical event for virus survival because virus multiplication is completely dependent on host cell metabolism. However, interestingly, this observed cell death did not affect either virus multiplication in the inoculated leaves or systemic spread to noninoculated upper leaves. Furthermore, the global gene expression pattern of the reassortant CMV-inoculated leaves undergoing cell death was clearly different from that in hypersensitive response (HR) cell death, which is coupled with resistance to CMV. These results indicated that the observed cell death does not appear to be HR cell death but rather necrotic cell death unrelated to CMV resistance. Interestingly, induction of this necrotic cell death depended on single amino acid substitutions in the N-terminal region surrounding the methyltransferase domain of the 1a protein. Thus, development of necrotic cell death might not be induced by non-specific damage as a result of virus multiplication, but by a virus protein-associated mechanism. The finding of CMV 1a protein-mediated induction of necrotic cell death in A. thaliana, which is not associated with virus resistance and HR cell death, has the potential to provide a new pathosystem to study the role of cell death in virus–host plant interactions.

参考文献

1. Mur, L.A.; Kenton, P.; Lloyd, A.J.; Ougham, H.; Prats, E. The hypersensitive response; the centenary is upon us but how much do we know? J. Exp. Bot. 2007, 59, 501–520. [CrossRef]

2. Künstler, A.; Bacsó, R.; Gullner, G.; Hafez, Y.M.; Király, L. Staying alive—Is cell death dispensable for plant disease resistance during the hypersensitive response? Physiol. Mol. Plant Pathol. 2016, 93, 75–84. [CrossRef]

3. Hofius, D.; Schultz-Larsen, T.; Joensen, J.; Tsitsigiannis, D.I.; Petersen, N.H.; Mattsson, O.; Jørgensen, L.B.; Jones, J.D.; Mundy, J.; Petersen, M. Autophagic components contribute to hypersensitive cell death in Arabidopsis. Cell 2009, 137, 773–783. [CrossRef]

4. Hofius, D.; Tsitsigiannis, D.I.; Jones, J.D.; Mundy, J. Inducible cell death in plant immunity. Semin. Cancer Biol. 2007, 17, 166–187. [CrossRef] [PubMed]

5. Richael, C.; Gilchrist, D. The hypersensitive response: A case of hold or fold? Physiol. Mol. Plant Pathol. 1999, 55, 5–12.[CrossRef]

6. Hull, R. Plant Virology, 5th ed.; Academic Press: Salt Lake, UT, USA, 2013.

7. Goodman, R.N.; Novacky, A.J. The Hypersensitive Reaction in Plants to Pathogens: A Resistance Phenomenon; APS Press: St. Paul, MN, USA, 1994.

8. Pontier, D.; Balagué, C.; Roby, D. The hypersensitive response. A programmed cell death associated with plant resistance. Comptes Rendus Acad. Sci. Ser. III Sci. 1998, 321, 721–734. [CrossRef]

9. Jones, J.D.; Dangl, J.L. The plant immune system. Nature 2006, 444, 323. [CrossRef] [PubMed]

10. Lam, E.; Kato, N.; Lawton, M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature 2001, 411, 848. [CrossRef] [PubMed]

11. Fomicheva, A.S.; Tuzhikov, A.I.; Beloshistov, R.E.; Trusova, S.V.; Galiullina, R.A.; Mochalova, L.V.; Chichkova, N.V.; Vartapetian, A.B. Programmed cell death in plants. Biochemistry (Moscow) 2012, 77, 1452–1464. [CrossRef]

12. Morel, J.-B.; Dangl, J.L. The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 1997, 4, 671. [CrossRef]

13. Greenberg, J.T.; Yao, N. The role and regulation of programmed cell death in plant–pathogen interactions. Cell. Microbiol. 2004, 6, 201–211. [CrossRef] [PubMed]

14. Heath, M.C. Hypersensitive response-related death. In Programmed Cell Death in Higher Plants; Springer: New York, NY, USA, 2000; pp. 77–90.

15. Canto, T.; Palukaitis, P. The hypersensitive response to cucumber mosaic virus in Chenopodium amaranticolor requires virus movement outside the initially infected cell. Virology 1999, 265, 74–82. [CrossRef] [PubMed]

16. Wright, K.M.; Duncan, G.H.; Pradel, K.S.; Carr, F.; Wood, S.; Oparka, K.J.; Santa Cruz, S. Analysis of the N gene hypersensitive response induced by a fluorescently tagged tobacco mosaic virus. Plant Physiol. 2000, 123, 1375–1386. [CrossRef] [PubMed]

17. Murphy, A.M.; Carr, J.P. Salicylic acid has cell-specific effects on tobacco mosaic virus replication and cell-to-cell movement. Plant Physiol. 2002, 128, 552–563. [CrossRef]

18. Lukan, T.; Baebler, Š.; Pompe-Novak, M.; Gucˇek, K.; Zagoršcˇak, M.; Coll, A.; Gruden, K. Cell death is not sufficient for the restriction of potato virus Y spread in hypersensitive response-conferred resistance in potato. Front. Plant Sci. 2018, 9, 168. [CrossRef]

19. Inaba, J.; Kim, B.M.; Shimura, H.; Masuta, C. Virus-induced necrosis is a consequence of direct protein-protein interaction between a viral RNA-silencing suppressor and a host catalase. Plant Physiol. 2011, 156, 2026–2036. [CrossRef]

20. Palukaitis, P.; García-Arenal, F. Cucumber Mosaic Virus; APS Press: St. Paul, MN, USA, 2018.

21. Rozanov, M.N.; Koonin, E.V.; Gorbalenya, A.E. Conservation of the putative methyltransferase domain: A hallmark of the ‘Sindbis-like’ supergroup of positive-strand RNA viruses. J. Gen. Virol. 1992, 73, 2129–2134. [CrossRef]

22. Habili, N.; Symons, R.H. Evolutionary relationship between luteoviruses and other RNA plant viruses based on sequence motifs in their putative RNA polymerases and nucleic acid helicases. Nucleic Acids Res. 1989, 17, 9543–9555. [CrossRef]

23. O’Reilly, E.K.; Wang, Z.; French, R.; Kao, C.C. Interactions between the structural domains of the RNA replication proteins of plant-infecting RNA viruses. J. Virol. 1998, 72, 7160–7169. [CrossRef]

24. Hayes, R.J.; Buck, K.W. Complete replication of a eukaryotic virus RNA in vitro by a purified RNA-dependent RNA polymerase. Cell 1990, 63, 363–368. [CrossRef]

25. Guo, H.S.; Ding, S.W. A viral protein inhibits the long range signaling activity of the gene silencing signal. EMBO J. 2002, 21, 398–407. [CrossRef] [PubMed]

26. Mlotshwa, S.; Voinnet, O.; Mette, M.F.; Matzke, M.; Vaucheret, H.; Ding, S.W.; Pruss, G.; Vance, V.B. RNA silencing and the mobile silencing signal. Plant Cell 2002, 14, S289–S301. [CrossRef] [PubMed]

27. Zhang, X.; Yuan, Y.-R.; Pei, Y.; Lin, S.-S.; Tuschl, T.; Patel, D.J.; Chua, N.-H. Cucumber mosaic virus-encoded 2b suppressor inhibits Arabidopsis Argonaute1 cleavage activity to counter plant defense. Genes Dev. 2006, 20, 3255–3268. [CrossRef] [PubMed]

28. González, I.; Martínez, L.; Rakitina, D.V.; Lewsey, M.G.; Atencio, F.A.; Llave, C.; Kalinina, N.O.; Carr, J.P.; Palukaitis, P.; Canto, T. Cucumber mosaic virus 2b protein subcellular targets and interactions: Their significance to RNA silencing suppressor activity. Mol. Plant Microbe Interact. 2010, 23, 294–303. [CrossRef]

29. Schwinghamer, M.W.; Symons, R.H. Fractionation of cucumber mosaic virus RNA and its translation in a wheat embryo cell-free system. Virology 1975, 63, 252–262. [CrossRef]

30. Ding, B.; Li, Q.; Nguyen, L.; Palukaitis, P.; Lucas, W.J. Cucumber mosaic virus 3a protein potentiates cell-to-cell trafficking of CMV RNA in tobacco plants. Virology 1995, 207, 345–353. [CrossRef]

31. Ding, S.W.; Anderson, B.J.; Haase, H.R.; Symons, R.H. New overlapping gene encoded by the cucumber mosaic virus genome. Virology 1994, 198, 593–601. [CrossRef]

32. Ando, S.; Miyashita, S.; Takahashi, H. Plant defense systems against cucumber mosaic virus: Lessons learned from CMV–Arabidopsis interactions. J. Gen. Plant Pathol. 2019, 85, 174–181. [CrossRef]

33. Sekine, K.; Kawakami, S.; Hase, S.; Kubota, M.; Ichinose, Y.; Shah, J.; Kang, H.G.; Klessig, D.F.; Takahashi, H. High level expression of a virus resistance gene, RCY1, confers extreme resistance to cucumber mosaic virus in Arabidopsis thaliana. Mol. Plant Microbe Interact. 2008, 21, 1398–1407. [CrossRef]

34. Takahashi, H.; Goto, N.; Ehara, Y. Hypersensitive response in cucumber mosaic virus-inoculated Arabidopsis thaliana. Plant J. 1994, 6, 369–377. [CrossRef]

35. Tomaru, K.; Hidaka, Z. Strains of cucumber mosaic virus isolated from tobacco plants. II. A mild strain. Bull. Hatano Tob. Exp. Stn. 1960, 46, 143–149. [CrossRef]

36. Suzuki, M.; Kuwata, S.; Kataoka, J.; Masuta, C.; Nitta, N.; Takanami, Y. Functional analysis of deletion mutants of cucumber mosaic virus RNA3 using an in vitro transcription system. Virology 1991, 183, 106–113. [CrossRef]

37. Sambrook, J.; Russel, D. Molecular Cloning: A Laboratory Manual, 3rd ed.; Cold Spring Harbor Laboratory Press: New York, NY, USA, 2001.

38. Takahashi, H.; Ehara, Y. Severe chlorotic spot symptoms in cucumber mosaic virus strain Y-infected tobaccos are induced by a combination of the virus coat protein gene and two host recessive genes. Mol. Plant Microbe Interact. 1993, 6, 182–189. [CrossRef] [PubMed]

39. Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254. [CrossRef]

40. Koenig, R. Indirect ELISA methods for the broad specificity detection of plant viruses. J. Gen. Virol. 1981, 55, 53–62. [CrossRef]

41. Bowling, S.A.; Guo, A.; Cao, H.; Gordon, A.S.; Klessig, D.F.; Dong, X. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 1994, 6, 1845–1857.

42. Bolger, A.M.; Lohse, M.; Usadel, B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 2014, 30, 2114–2120. [CrossRef]

43. Dobin, A.; Davis, C.A.; Schlesinger, F.; Drenkow, J.; Zaleski, C.; Jha, S.; Batut, P.; Chaisson, M.; Gingeras, T.R. STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 2013, 29, 15–21. [CrossRef]

44. Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [CrossRef]

45. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B 1995, 57, 289–300. [CrossRef]

46. Chen, H.; Boutros, P.C. VennDiagram: A package for the generation of highly-customizable Venn and Euler diagrams in R. BMC Bioinform. 2011, 12, 35. [CrossRef] [PubMed]

47. Zhou, Y.; Zhou, B.; Pache, L.; Chang, M.; Khodabakhshi, A.H.; Tanaseichuk, O.; Benner, C.; Chanda, S.K. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat. Commun. 2019, 10, 1523. [CrossRef] [PubMed]

48. Yu, G.; Wang, L.-G.; Han, Y.; He, Q.-Y. clusterProfiler: An R Package for Comparing Biological Themes Among Gene Clusters. OMICS J. Integr. Biol. 2012, 16, 284–287. [CrossRef] [PubMed]

49. Diveki, Z.; Salanki, K.; Balazs, E. The necrotic pathotype of the cucumber mosaic virus (CMV) ns strain is solely determined by amino acid 461 of the 1a protein. Mol. Plant Microbe Interact. 2004, 17, 837–845. [CrossRef]

50. Salánki, K.; Gellért, Á.; Náray-Szabó, G.; Balázs, E. Modeling-based characterization of the elicitor function of amino acid 461 of cucumber mosaic virus 1a protein in the hypersensitive response. Virology 2007, 358, 109–118. [CrossRef] [PubMed]

51. Kang, W.H.; Seo, J.K.; Chung, B.N.; Kim, K.H.; Kang, B.C. Helicase domain encoded by cucumber mosaic virus RNA1 determines systemic infection of Cmr1 in pepper. PLoS ONE 2012, 7, e43136. [CrossRef] [PubMed]

52. Seo, J.K.; Kwon, S.J.; Choi, H.S.; Kim, K.H. Evidence for alternate states of cucumber mosaic virus replicase assembly in positive-and negative-strand RNA synthesis. Virology 2009, 383, 248–260. [CrossRef] [PubMed]

53. Fujisaki, K.; Hagihara, F.; Azukawa, Y.; Kaido, M.; Okuno, T.; Mise, K. Identification and characterization of the SSB1 locus involved in symptom development by spring beauty latent virus infection in Arabidopsis thaliana. Mol. Plant Microbe Interact. 2004, 17, 967–975. [CrossRef] [PubMed]

54. Chen, H.; Adam Arsovski, A.; Yu, K.; Wang, A. Deep sequencing leads to the identification of eukaryotic translation initiation factor 5A as a key element in Rsv1-mediated lethal systemic hypersensitive response to soybean mosaic virus infection in soybean. Mol. Plant Pathol. 2017, 18, 391–404. [CrossRef]

55. Kim, B.M.; Suehiro, N.; Natsuaki, T.; Inukai, T.; Masuta, C. The P3 protein of turnip mosaic virus can alone induce hypersensitive response-like cell death in Arabidopsis thaliana carrying TuNI. Mol. Plant Microbe Interact. 2010, 23, 144–152. [CrossRef]

56. Hajimorad, M.; Eggenberger, A.; Hill, J. Loss and gain of elicitor function of soybean mosaic virus G7 provoking Rsv1-mediated lethal systemic hypersensitive response maps to P3. J. Virol. 2005, 79, 1215–1222. [CrossRef] [PubMed]

57. Komatsu, K.; Hashimoto, M.; Ozeki, J.; Yamaji, Y.; Maejima, K.; Senshu, H.; Himeno, M.; Okano, Y.; Kagiwada, S.; Namba, S. Viral-induced systemic necrosis in plants involves both programmed cell death and the inhibition of viral multiplication, which are regulated by independent pathways. Mol. Plant Microbe Interact. 2010, 23, 283–293. [CrossRef]

58. Hashimoto, M.; Komatsu, K.; Iwai, R.; Keima, T.; Maejima, K.; Shiraishi, T.; Ishikawa, K.; Yoshida, T.; Kitazawa, Y.; Okano, Y. Cell death triggered by a putative amphipathic helix of radish mosaic virus helicase protein is tightly correlated with host membrane modification. Mol. Plant Microbe Interact. 2015, 28, 675–688. [CrossRef] [PubMed]

59. Chen, P.; Buss, G.; Roane, C.; Tolin, S. Inheritance in soybean of resistant and necrotic reactions to soybean mosaic virus strains. Crop Sci. 1994, 34, 414–422. [CrossRef]

参考文献をもっと見る

全国の大学の
卒論・修論・学位論文

一発検索!

この論文の関連論文を見る