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Archives of Virology

, Volume 160, Issue 6, pp 1499–1509 | Cite as

Differential response of diverse solanaceous hosts to tomato leaf curl New Delhi virus infection indicates coordinated action of NBS-LRR and RNAi-mediated host defense

  • Nirbhay Kushwaha
  • Ashish Kumar Singh
  • Saumik Basu
  • Supriya ChakrabortyEmail author
Original Article

Abstract

Tomato leaf curl New Delhi virus (ToLCNDV) is a bipartite begomovirus (family Geminiviridae) that infects a wide range of plants. ToLCNDV has emerged as an important pathogen and a serious threat to tomato production in India. A comparative and molecular analysis of ToLCNDV pathogenesis was performed on diverse solanaceous hosts (Capsicum annuum, Nicotiana benthamiana, N. tabacum, and Solanum lycopersicum). N. benthamiana was found to be the most susceptible host, whereas C. annuum showed resistance against an isolate of ToLCNDV collected in New Delhi from tomato (GenBank accession no. U15015 and U15017). S. lycopersicum and N. tabacum developed conspicuous symptoms and allowed virus to accumulate to significantly high titers. The viral DNA level was concurrent with symptom severity. ToLCNDV-specific siRNA levels were directly proportional to the amount of viral DNA. To investigate the basis for the differences in response of these hosts to ToLCNDV, a comparative expression analysis of selected defense-related genes was carried out. The results indicated differences in expression levels of genes involved in the posttranscriptional gene silencing machinery (RDR6, AGO1 and SGS3) as well as basal host defense responses (nucleotide-binding site and leucine-rich repeat [NBS-LRR] proteins and lipid transfer protein [LTP]). Among these, expression of NBS-LRR genes was found to be significantly higher in C. annuum following ToLCNDV infection. Our analyses suggest that the expression of host defense responses determines the level of ToLCNDV accumulation and degree of symptom development.

Keywords

Cucumber Mosaic Virus Lipid Transfer Protein Tomato Leaf Viral Suppressor Tomato Golden Mosaic Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank Dr. Veerendra Kumar Sharma for his critical comments and discussion. This work was funded by the Department of Biotechnology, Govt. of India (Grant No. BT/PR6504/AGII/106/878/2012).

Conflict of interest

The authors do not have any conflict of interest.

References

  1. 1.
    Bendahmane A, Kanyuka K, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–792CrossRefPubMedCentralPubMedGoogle Scholar
  2. 2.
    Bisaro DM (2006) Silencing suppression by geminivirus proteins. Virology 344:158–168CrossRefPubMedGoogle Scholar
  3. 3.
    Buchmann RC, Asad S, Wolf JN, Mohannath G, Bisaro DM (2009) Geminivirus AL2 and L2 proteins suppress transcriptional gene silencing and cause genome-wide reductions in cytosine methylation. J Virol 83:5005–5013CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Chakraborty S, Vanitharani R, Chattopadhyay B, Fauquet CM (2008) Supervirulent pseudorecombination and asymmetric synergism between genomic components of two distinct species of begomovirus associated with severe tomato leaf curl disease in India. J Gen Virol 89:818–828CrossRefPubMedGoogle Scholar
  5. 5.
    Chattopadhyay B, Singh AK, Yadav T, Fauquet CM, Sarin NB, Chakraborty S (2008) Infectivity of the cloned components of a begomovirus: DNA beta complex causing chilli leaf curl disease in India. Arch Virol 153:533–539CrossRefPubMedGoogle Scholar
  6. 6.
    Chellappan P, Vanitharani R, Fauquet CM (2005) MicroRNA-binding viral protein interferes with Arabidopsis development. Proc Natl Acad Sci USA 102:10381–10386CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Chen T, Lv T, Zhao T, Li N, Yang Y, Yu W, He X, Liu T, Zhang B (2013) Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS ONE 8:e80816CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    Dawson WO, Hilf ME (1992) Host-range determinants of plant viruses. Annu Rev Plant Physiol Plant Mol Biol 43:527–555CrossRefGoogle Scholar
  9. 9.
    de Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci 5:1–17CrossRefGoogle Scholar
  10. 10.
    Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Biol Rep 1:19–21CrossRefGoogle Scholar
  11. 11.
    Fukunaga R, Doudna JA (2009) dsRNA with 5’ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J 28:545–555CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    García-Neria MA, Rivera-Bustamante RF (2011) Characterization of geminivirus resistance in an accession of capsicum Chinense Jacq. Mol Plant Microbe Interact 24:172–182CrossRefPubMedGoogle Scholar
  13. 13.
    Garcia-Olmedo F, Molina A, Segura A, Moreno M (1995) The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol 3:72–74CrossRefPubMedGoogle Scholar
  14. 14.
    Glick E, Zrachya A, Levy Y, Mett A, Gidoni D, Belausov E, Citovsky V, Gafni Y (2008) Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc Natl Acad Sci USA 105:157–161CrossRefPubMedCentralPubMedGoogle Scholar
  15. 15.
    Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant–pathogen interactions. Mol Plant Microbe Interact 21:1015–1026CrossRefPubMedGoogle Scholar
  16. 16.
    Gorovits R, Moshe A, Ghanim M, Czosnek H (2013) Recruitment of the host plant heat shock protein 70 by tomato yellow leaf curl virus coat protein is required for virus infection. PLoS ONE 8:e70280CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11:777–788CrossRefPubMedGoogle Scholar
  18. 18.
    Huang Z, Yeakley JM, Garcia EW, Holdridge JD, Fan JB, Whitham SA (2005) Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiol 137:1147–1159CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    Hussain M, Mansoor S, Iram S, Zafar Y, Briddon RW (2004) First report of tomato leaf curl New Delhi virus affecting chilli pepper in Pakistan. Plant Pathol 53:794CrossRefGoogle Scholar
  20. 20.
    Incarbone M, Dunoyer P (2013) RNA silencing and its suppression: novel insights from in planta analyses. Trends Plant Sci 18:382–392CrossRefPubMedGoogle Scholar
  21. 21.
    Juárez M, Tovar R, Fiallo-Olivé E, Aranda MA, Gosálvez B, Castillo P, Moriones E, Navas-Castillo J (2014) First detection of tomato leaf curl New Delhi virus infecting zucchini in Spain. Plant Dis 98:857CrossRefGoogle Scholar
  22. 22.
    Jyothsna P, Haq QMI, Singh P, Sumiya KV, Praveen S, Rawat R, Briddon RW, Malathi VG (2013) Infection of tomato leaf curl New Delhi virus (ToLCNDV), a bipartite begomovirus with betasatellites, results in enhanced level of helper virus components and antagonistic interaction between DNA B and betasatellites. Appl Microbiol Biotechnol 97:5457–5471CrossRefPubMedGoogle Scholar
  23. 23.
    Kumari P, Singh AK, Chattopadhyay B, Chakraborty S (2010) Molecular characterization of a new species of Begomovirus and betasatellite causing leaf curl disease of tomato in India. Virus Res 152:19–29CrossRefPubMedGoogle Scholar
  24. 24.
    Kushwaha N, Sahu PP, Prasad M, Chakraborty S (2015) Chilli leaf curl virus infection highlights the differential expression of genes involved in protein homeostasis and defense in resistant chilli plants. Appl Microbiol Biotechnol. doi: 10.1007/s00253-015-6415-6 PubMedGoogle Scholar
  25. 25.
    Lee S, Stenger DC, Bisaro DM, Davis KR (1994) Identification of loci in Arabidopsis that confer resistance to geminivirus infection. Plant J 6:525–535CrossRefPubMedGoogle Scholar
  26. 26.
    Llave C, Kasschau KD, Carrington JC (2000) Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc Natl Acad Sci USA 97:13401–13406CrossRefPubMedCentralPubMedGoogle Scholar
  27. 27.
    Lozano-Duran R, Rosas-Diaz T, Luna AP, Bejarano ER (2011) Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE 6:e22383CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Cheng Lu, Meyers BC, Green PJ (2007) Construction of small RNA cDNA libraries for deep sequencing. Methods 43:110–117CrossRefGoogle Scholar
  29. 29.
    Maiti S, Paul S, Pal A (2012) Isolation, characterization, and structure analysis of a non-TIR-NBS-LRR encoding candidate gene from MYMIV-resistant Vigna mungo. Mol Biotechnol 52:217–233CrossRefPubMedGoogle Scholar
  30. 30.
    Mandadi KK, Scholthof KBG (2013) Plant immune responses against viruses: how does a virus cause disease? Plant Cell 25:1489–1505CrossRefPubMedCentralPubMedGoogle Scholar
  31. 31.
    Maule A, Leh V, Lederer C (2002) The dialogue between viruses and hosts in compatible interactions. Curr Opin Plant Biol 5:279–284CrossRefPubMedGoogle Scholar
  32. 32.
    Moffett P (2009) Mechanisms of recognition in dominant R gene mediated resistance. Adv Virus Res 75:1–33CrossRefPubMedGoogle Scholar
  33. 33.
    Navas-Castillo J, Sanchez-Campos S, Noris E, Louro D, Accotto GP, Moriones E (2000) Natural recombination between tomato yellow leaf curl virus-is and tomato leaf curl virus. J Gen Virol 81:2797–2801PubMedGoogle Scholar
  34. 34.
    Padidam M, Beachy RN, Fauquet CM (1995) Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol 76:25–35CrossRefPubMedGoogle Scholar
  35. 35.
    Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760CrossRefPubMedGoogle Scholar
  36. 36.
    Qin C, Shi N, Gu M, Zhang H, Li B, Shen J, Mohammed A, Ryabov E, Li C, Wang H, Liu Y, Osman T, Vatish M, Hong Y (2012) Involvement of RDR6 in short-range intercellular RNA silencing in Nicotiana benthamiana. Nat Sci Rep 2:467. doi: 10.1038/srep00467 Google Scholar
  37. 37.
    Raja P, Wolf JN, Bisaro DM (2010) RNA silencing directed against geminiviruses: post-transcriptional and epigenetic components. Biochim Biophys Acta 1799:337–351CrossRefPubMedGoogle Scholar
  38. 38.
    Rodriguez-Negrete E, Lozano-Duran R, Piedra-Aguilera A, Cruzado L, Bejarano ER, Castillo AG (2013) Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol 199:464–475CrossRefPubMedGoogle Scholar
  39. 39.
    Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394CrossRefPubMedGoogle Scholar
  40. 40.
    Sahu PP, Rai NK, Chakraborty S, Singh M, Chandrappa PH, Ramesh B, Chattopadhyay D, Prasad M (2010) Tomato cultivar tolerant to tomato leaf curl New Delhi virus infection induces virus-specific short interfering RNA accumulation and defence-associated host gene expression. Mol Plant Pathol 11:531–544CrossRefPubMedGoogle Scholar
  41. 41.
    Sambrook J, Russell RD (2001) Molecular cloning, 3rd edn. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  42. 42.
    Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28:419–427CrossRefPubMedGoogle Scholar
  43. 43.
    Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y, Dinesh-Kumar SP (2002) RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J 32:655–667CrossRefPubMedGoogle Scholar
  44. 44.
    Trinks D, Rajeswaran R, Shivaprasad PV, Akbergenov R, Oakeley EJ, Veluthambi K, Hohn T, Pooggin MM (2005) Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J Virol 79:2517–2527CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Vanitharani R, Chellappan P, Pita JS, Fauquet CM (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. J Virol 78:9487–9498CrossRefPubMedCentralPubMedGoogle Scholar
  46. 46.
    Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RG, Scott JW, Edwards JD, Bai Y (2013) The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-class RNA-dependent RNA polymerases. PLoS Genetics 9:e1003399CrossRefPubMedCentralPubMedGoogle Scholar
  47. 47.
    Wang XB, Jovel J, Udomporn P, Wang Y, Wu Q, Li WX, Gasciolli V, Vaucheret H, Ding SW (2011) The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23:1625–1638CrossRefPubMedCentralPubMedGoogle Scholar
  48. 48.
    Xie Z, Fan B, Chen C, Chen Z (2001) An important role of an inducible RNA-dependent RNA polymerase in plant antiviral defense. Proc Natl Acad Sci USA 98:6516–6521CrossRefPubMedCentralPubMedGoogle Scholar
  49. 49.
    Yang SJ, Carter SA, Cole AB, Cheng NH, Nelson RS (2004) A natural variant of a host RNA-dependent RNA polymerase is associated with increased susceptibility to viruses by Nicotiana benthamiana. Proc Natl Acad Sci USA 101:6297–6302CrossRefPubMedCentralPubMedGoogle Scholar
  50. 50.
    Ying XB, Dong L, Zhu H, Duan CG, Du QS, Lv DQ, Fang YY, Garcia JA, Fang RX, Guo HS (2010) RNA-Dependent RNA polymerase 1 from Nicotiana tabacum uppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell 22:1358–1372CrossRefPubMedCentralPubMedGoogle Scholar
  51. 51.
    Ying-Li Zhang, Qing-Li Jia, Da-Wei Li, Jun-E Wang, Yan-Xu Yin, Zhen-Hui Gong (2013) Characteristic of the pepper CaRGA2Gene in defense responses against Phytophthora capsici Leonian. Int J Mol Sci 14:8985–9004CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Nirbhay Kushwaha
    • 1
  • Ashish Kumar Singh
    • 1
  • Saumik Basu
    • 1
  • Supriya Chakraborty
    • 1
    Email author
  1. 1.Molecular Virology Laboratory, School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia

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