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Abstract

Pepper mild mottle virus (PMMoV) causes serious economic losses in pepper production in China. In a survey for viral diseases on pepper, two PMMoV isolates (named PMMoV-ZJ1 and PMMoV-ZJ2) were identified with different symptoms in Zhejiang province. Sequence alignment analysis suggested there were only four amino acid differences between the isolates: Val262Gly, Ile629Met and Ala1164Thr in the replicase, and Asp20Asn in the coat protein. Infectious cDNA clones of both isolates were constructed and shown to cause distinctive symptoms. Chlorosis symptoms appeared only on PMMoV-ZJ2-infected plants and the Asp20Asn substitution in the CP was shown to be responsible. Confocal assays revealed that the subcellular localization pattern of the two CPs was different, CP was mainly located at the cell periphery, whereas most CP located in the chloroplast. Thus, a single amino acid in the CP determined the chlorosis symptom, accompanied by an altered subcellular localization.

Funding
This study was supported by the:
  • International Science and Technology Cooperation Programme (Award 2015DFA30700)
    • Principle Award Recipient: Fei Yan
  • Agriculture Research System of China (Award CARS-24-C-04)
    • Principle Award Recipient: JIANPING CHEN
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-03-09
2024-05-12
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References

  1. Martínez-Ochoa N, Langston DB, Mullis SW, Flanders JT. First report of pepper mild mottle virus in jalapeno pepper in Georgia. Plant Health Progress 2003; 4:26 [View Article]
    [Google Scholar]
  2. Nakazono-Nagaoka E, Omura T, Uehara-Ichiki T. A single amino acid substitution in the 126-kDa protein of pepper mild mottle virus controls replication and systemic movement into upper non-inoculated leaves of bell pepper plants. Arch Virol 2011; 156:897–901 [View Article][PubMed]
    [Google Scholar]
  3. Lima MF, Inoue-Nagata AK, Reifschneider FJB, Souza KRR, Ulhoa AB et al. Detection, occurrence and natural incidence of pepper mild mottle virus (PMMOV) in hot peppers in Brazil. Acta Hortic 2011; 917:269–273 [View Article]
    [Google Scholar]
  4. Wang X, Liu F, Zhou G, Li X-H, Li Z. Detection and molecular characterization of pepper mild mottle virus in China. J Phytopathol 2006; 154:755–757 [View Article]
    [Google Scholar]
  5. Xiang B, Xie H, Cui X, Li C, Liu S et al. Isolation and identification of pepper mild mottle tobamovirus in Xinjiang. Chinese J Virol 1994
    [Google Scholar]
  6. XD L, An M, YH W. First report of pepper mild mottle virus in northeast China. Plant Dis 2016; 100:541
    [Google Scholar]
  7. Adams MJ, Antoniw JF, Kreuze J. Virgaviridae: a new family of rod-shaped plant viruses. Arch Virol 2009; 154:1967–1972 [View Article][PubMed]
    [Google Scholar]
  8. Avila-Rincon MJ, Ferrero ML, Alonso E, García-Luque I, Díaz-Ruíz JR. Nucleotide sequences of 5' and 3' non-coding regions of pepper mild mottle virus strain S RNA. J Gen Virol 1989; 70 (Pt 11:3025–3031 [View Article][PubMed]
    [Google Scholar]
  9. Alonso E, García-Luque I, de la Cruz A, Wicke B, Avila-Rincón MJ et al. Nucleotide sequence of the genomic RNA of pepper mild mottle virus, a resistance-breaking tobamovirus in pepper. J Gen Virol 1991; 72 (Pt 12:2875–2884 [View Article][PubMed]
    [Google Scholar]
  10. Velasco L, Janssen D, Ruiz-Garcia L, Segundo E, Cuadrado IM. The complete nucleotide sequence and development of a differential detection assay for a pepper mild mottle virus (PMMoV) isolate that overcomes L3 resistance in pepper. J Virol Methods 2002; 106:135–140 [View Article][PubMed]
    [Google Scholar]
  11. Derrick PM, Carter SA, Nelson RS. Mutation of the tobacco mosaic Tobamovirus 126-and 183-kDa proteins: effects on Phloem-Dependent virus accumulation and synthesis of viral proteins. MPMI 1997; 10:589–596 [View Article]
    [Google Scholar]
  12. Csorba T, Bovi A, Dalmay T, Burgyán J. The p122 subunit of tobacco mosaic virus replicase is a potent silencing suppressor and compromises both small interfering RNA- and microRNA-mediated pathways. J Virol 2007; 81:11768–11780 [View Article][PubMed]
    [Google Scholar]
  13. Kubota K, Tsuda S, Tamai A, Meshi T. Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J Virol 2003; 77:11016–11026 [View Article][PubMed]
    [Google Scholar]
  14. Genda Y, Sato K, Nunomura O, Hirabayashi T, Tsuda S. Immunolocalization of pepper mild mottle virus in developing seeds and seedlings of Capsicum annuum. J Gen Plant Pathol 2011; 77:201–208 [View Article]
    [Google Scholar]
  15. Peng J, Shi B, Zheng H, Lu Y, Lin L et al. Detection of pepper mild mottle virus in pepper sauce in China. Arch Virol 2015; 160:2079–2082 [View Article][PubMed]
    [Google Scholar]
  16. Hamza IA, Jurzik L, Uberla K, Wilhelm M. Evaluation of pepper mild mottle virus, human picobirnavirus and torque teno virus as indicators of fecal contamination in river water. Water Res 2011; 45:1358–1368 [View Article][PubMed]
    [Google Scholar]
  17. Haramoto E, Kitajima M, Kishida N, Konno Y, Katayama H et al. Occurrence of pepper mild mottle virus in drinking water sources in Japan. Appl Environ Microbiol 2013; 79:7413–7418 [View Article][PubMed]
    [Google Scholar]
  18. Nagata T, Inoue-Nagata AK. Simplified methods for the construction of RNA and DNA virus infectious clones. Methods Mol Biol 2015; 1236:241–254 [View Article][PubMed]
    [Google Scholar]
  19. Zheng H, Xiao C, Han K, Peng J, Lin L et al. Development of an agroinoculation system for full-length and GFP-tagged cDNA clones of cucumber green mottle mosaic virus. Arch Virol 2015; 160:2867–2872 [View Article][PubMed]
    [Google Scholar]
  20. Xiang C, Han P, Lutziger I, Wang K, Oliver DJ. A mini binary vector series for plant transformation. Plant Mol Biol 1999; 40:711–717 [View Article][PubMed]
    [Google Scholar]
  21. Yu M, Liu H, Zheng H, Yan F, Zhao X et al. Viral sequences required for efficient viral infection differ between two Chinese pepper mild mottle virus isolates. Virus Res 2019; 267:9–15 [View Article][PubMed]
    [Google Scholar]
  22. Zhao J, Zhang X, Hong Y, Liu Y. Chloroplast in Plant-Virus interaction. Front Microbiol 2016; 7:1565 [View Article][PubMed]
    [Google Scholar]
  23. Peng Y, Lei J, Huang L, Yu J. Effects of potato virus Y infection on chloroplast ultrastructure, photosynthesis and chlorophyll fluorescence quenching in potato leaves. Acta Phytopathologica Sinica 2004; 34:32–36
    [Google Scholar]
  24. Pineda M, Sajnani C, Barón M. Changes induced by the pepper mild mottle tobamovirus on the chloroplast proteome of Nicotiana benthamiana. Photosynth Res 2010; 103:31–45 [View Article][PubMed]
    [Google Scholar]
  25. Lindbeck AGC, Lewandowski J, Culver JN, Thomson WW, Dawson WO. Mutant coat protein of tobacco mosaic virus induces acute chlorosis in expanded and developing tobacco leaves. MPMI 1992; 5:235–241 [View Article]
    [Google Scholar]
  26. Ohnishi J, Hirai K, Kanda A, Usugi T, Meshi T et al. The coat protein of tomato mosaic virus L11Y is associated with virus-induced chlorosis on infected tobacco plants. J Gen Plant Pathol 2009; 75:297–306 [View Article]
    [Google Scholar]
  27. Ju H-K, Kim I-H, Hu W-X, Kim B, Choi G-W et al. A single nucleotide change in the overlapping MP and CP reading frames results in differences in symptoms caused by two isolates of Youcai mosaic virus. Arch Virol 2019; 164:1553–1565 [View Article][PubMed]
    [Google Scholar]
  28. Han S-H, Park J-S, Han J-Y, Gong J-S, Park C-H et al. New Korean isolates of Pepper mild mottle virus (PMMoV) differ in symptom severity and subcellular localization of the 126 kDa protein. Virus Genes 2017; 53:434–445 [View Article][PubMed]
    [Google Scholar]
  29. Pagán I, Firth C, Holmes EC. Phylogenetic analysis reveals rapid evolutionary dynamics in the plant RNA virus genus tobamovirus. J Mol Evol 2010; 71:298–307 [View Article][PubMed]
    [Google Scholar]
  30. Bhattacharyya D, Chakraborty S. Chloroplast: the Trojan horse in plant-virus interaction. Mol Plant Pathol 2018; 19:504–518 [View Article][PubMed]
    [Google Scholar]
  31. Bi Ji'an, Yang Y, Chen B, Zhao J, Chen Z et al. Retardation of the Calvin Cycle Contributes to the Reduced CO2 Assimilation Ability of Rice Stripe Virus-Infected N. benthamiana and Suppresses Viral Infection. Front Microbiol 2019; 10:568 [View Article][PubMed]
    [Google Scholar]
  32. Bendahmane M, Szécsi J, Chen I, Berg RH, Beachy RN. Characterization of mutant tobacco mosaic virus coat protein that interferes with virus cell-to-cell movement. Proc Natl Acad Sci USA 2002; 99:3645–3650 [View Article][PubMed]
    [Google Scholar]
  33. Bhattacharyya D, Gnanasekaran P, Kumar RK, Kushwaha NK, Sharma VK et al. A geminivirus betasatellite damages the structural and functional integrity of chloroplasts leading to symptom formation and inhibition of photosynthesis. J Exp Bot 2015; 66:5881–5895 [View Article][PubMed]
    [Google Scholar]
  34. Mochizuki T, Ogata Y, Hirata Y, Ohki ST. Quantitative transcriptional changes associated with chlorosis severity in mosaic leaves of tobacco plants infected with cucumber mosaic virus. Mol Plant Pathol 2014; 15:242–254 [View Article][PubMed]
    [Google Scholar]
  35. Shintaku M. Coat protein gene sequences of two cucumber mosaic virus strains reveal a single amino acid change correlating with chlorosis induction. J Gen Virol 1991; 72 (Pt 10:2587–2589 [View Article][PubMed]
    [Google Scholar]
  36. Qiu Y, Zhang Y, Wang C, Lei R, Wu Y et al. Cucumber mosaic virus coat protein induces the development of chlorotic symptoms through interacting with the chloroplast ferredoxin I protein. Sci Rep 2018; 8:1205 [View Article][PubMed]
    [Google Scholar]
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