Skip to main content

Advertisement

Log in

Genome sequencing of cucumber mosaic virus (CMV) isolates infecting chilli and its interaction with host ferredoxin protein of different host for causing mosaic symptoms

  • Original Article
  • Published:
3 Biotech Aims and scope Submit manuscript

Abstract

Chilli (Capsicum annuum L.) is an important vegetable crop grown in the Indian sub-continent and is prone to viral infections under field conditions. During the field survey, leaf samples from chilli plants showing typical symptoms of disease caused by cucumber mosaic virus (CMV) such as mild mosaic, mottling and leaf distortion were collected. DAC-ELISA analysis confirmed the presence of CMV in 71 out of 100 samples, indicating its widespread prevalence in the region. Five CMV isolates, named Gu1, Gu2, BA, Ho, and Sal were mechanically inoculated onto cucumber and Nicotiana glutinosa plants to study their virulence. Inoculated plants expressed the characteristic symptoms of CMV such as chlorotic spots followed by mild mosaic and leaf distortion. Complete genomes of the five CMV isolates were amplified, cloned, and sequenced, revealing RNA1, RNA2, and RNA3 sequences with 3358, 3045, and 2220 nucleotides, respectively. Phylogenetic analysis classified the isolates as belonging to the CMV-IB subgroup, distinguishing them from subgroup IA and II CMV isolates. Recombination analysis showed intra and interspecific recombination in all the three RNA segments of these isolates. In silico protein–protein docking approach was used to decipher the mechanism behind the production of mosaic symptoms during the CMV-host interaction in 13 host plants. Analysis revealed that the production of mosaic symptoms could be due to the interaction between the coat protein (CP) of CMV and chloroplast ferredoxin proteins. Further, in silico prediction was validated in 13 host plants of CMV by mechanical sap inoculation. Twelve host plants produced systemic symptoms viz., chlorotic spot, chlorotic ringspot, chlorotic local lesion, mosaic and mild mosaic and one host plant, Solanum lycopersicum produced mosaic followed by shoestring symptoms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The nucleotide accession IDs (GenBank IDs) of all the five isolates under study are available publicly in NCBI with following accession IDs: RNA1: Gu1 (MN340987), Gu2 (MN340993), BA (MN340990), Sal (MN340998), Ho (MN340996) RNA2: Gu1 (MN340988), Gu2 (MN340994), BA (MN340991), Sal (MN3410000), Ho (MN340997) RNA3: Gu1 (MN340989), Gu2 (MN340995), BA (MN340992), Sal (MN3410001), Ho (MN340998)

References

  • Baspinar A, Cukuroglu E, Nussinov R, Keskin O, Gursoy A (2014) PRISM: a web server and repository for prediction of protein–protein interactions and modeling their 3D complexes. Nucleic Acids Res 42(W1):W285–W289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonnet J, Fraile A, Sacristán S, Malpica JM, García-Arenal F (2005) Role of recombination in the evolution of natural populations of cucumber mosaic virus, a tripartite RNA plant virus. Virology 332(1):359–368

    Article  CAS  PubMed  Google Scholar 

  • Biovia (2017) Biovia Workbook, Release 2017; BIOVIA Pipeline Pilot, Release 2017

  • Comeau SR, Gatchell DW, Vajda S, Camacho CJ (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20(1):45–50

    Article  CAS  PubMed  Google Scholar 

  • Daróczi G (2013) Saves: Fast load variables. R package version 0.5. http://cran.r-project.org/package=saves

  • DeLano (2009) The PyMOL Molecular Graphics System. https://pymol.org/2/

  • Doolittle SP (1916) A new infectious mosaic disease of cucumber. Phytopathology 6(2):145–147

    Google Scholar 

  • FAO (2022) World food and agriculture-statistical yearbook (https://www.fao.org/documents/card/en/c/cc2211en)

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Bioinformatics 12(6):543–548

    Article  CAS  Google Scholar 

  • García-Arenal PFP (2003) Cucumoviruses. Adv Virus Res 62:241–323

    Article  PubMed  Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31(13):3784–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guruprasad K, Reddy BVB, Pandit MW (1990) Correlation between stability of a protein and its dipeptide composition: a novel approach for predicting in vivo stability of a protein from its primary sequence. Protein Eng Des Sel 4(2):155–161

    Article  CAS  Google Scholar 

  • Hall T, Biosciences I, Carlsbad CJGBB (2011) BioEdit: an important software for molecular biology. GERF Bull Biosci 2(1):60–61

    Google Scholar 

  • Hareesh PS, Madhubala R, Bhat AI (2006) Characterization of cucumber mosaic virus infecting Indian long pepper (Piper longum L.) and betel vine (Piper betle L.) in India. Indian J Biotechnol 5:89–93

    CAS  Google Scholar 

  • Hobbs HA, Reddy DVR, Rajeshwari R, Reddy AS (1987) Use of direct antigen coating and protein a coating ELISA procedures. Plant Dis 71(8):747–749

    Article  Google Scholar 

  • Jacquemond M (2012) Cucumber mosaic virus. Adv Virus Res 84:439–504

    Article  PubMed  Google Scholar 

  • Kaur S, Kang SS, Sharma A, Sharma S (2014) First report of pepper mottle virus infecting chilli pepper in India. New Dis Rep 30(14):2044–0588

    Google Scholar 

  • Khan SM, Raj SK, Bano T, Garg VK (2006) Incidence and management of mosaic and leaf curl diseases in cultivars of chilli (Capsicum annuum). J Food Agric Environ 4(1):171

    Google Scholar 

  • Kim M-K, Jeong R-D, Kwak H-R, Lee S-H, Kim J-S, Kim K-H, Cha B, Choi H-S (2014) First report of cucumber mosaic virus isolated from Wild Vigna angularis var. nipponensis in Korea. Plant Pathol J 30(2):200

    Article  PubMed  PubMed Central  Google Scholar 

  • Krishnareddy M, Rani RU, Kumar KSA, Reddy KM, Pappu HR (2008) Capsicum chlorosis virus (Genus Tospovirus) infecting chili pepper (Capsicum annuum) in India. Plant Dis 92(10):1469–1469

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Gautam KK, Raj SK (2015) Sequence analysis and genetic diversity of five new Indian isolates of cucumber mosaic virus. Acta Virol 59(4):398–404

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari R, Bhardwaj P, Singh L, Zaidi AA, Hallan V (2013) Biological and molecular characterization of cucumber mosaic virus subgroup II isolate causing severe mosaic in cucumber. Indian J Virol 24(1):27–34

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee GR, Won J, Heo L, Seok C (2019) GalaxyRefine2: simultaneous refinement of inaccurate local regions and overall protein structure. Nucleic Acids Res 47(W1):W451–W455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. https://doi.org/10.1093/ve/vev003

    Article  PubMed  PubMed Central  Google Scholar 

  • Nagendran K, Priyanka R, Aravintharaj R, Balaji CG, Prashant S, Basavaraj B, Mohankumar S, Karthikeyan G (2018) Characterization of cucumber mosaic virus infecting snake gourd and bottle gourd in India. Physiolo Mol Plant Pathol 103:102–106

    Article  Google Scholar 

  • Nouri S, Arevalo R, Falk BW, Groves RL (2014) Genetic structure and molecular variability of cucumber mosaic virus isolates in the United States. PLoS ONE 9(5):e96582

    Article  PubMed  PubMed Central  Google Scholar 

  • Owen J, Palukaitis P (1988) Characterization of cucumber mosaic virus I. Molecular heterogeneity mapping of RNA 3 in eight CMV strains. Virology 166(2):495–502

    Article  CAS  PubMed  Google Scholar 

  • Palukaitis P, Roossinck MJ, Dietzgen RG, Francki RIB (1992) Cucumber mosaic virus. Adv Virus Res 41:281–348

    Article  CAS  PubMed  Google Scholar 

  • Pavithra BS, Govin K, Renuka HM, Krishnareddy M, Jalali S, Samuel DK, Himabindu K (2019) Characterization of cucumber mosaic virus infecting coleus (Plectranthus barbatus) in Karnataka. Virus Dis 30(3):403–412

    Article  CAS  Google Scholar 

  • Qiu Y, Zhang Y, Wang C, Lei R, Wu Y, Li X, Zhu S (2018) cucumber mosaic virus coat protein induces the development of chlorotic symptoms through interacting with the chloroplast ferredoxin I protein. Sci Rep 8(1):1–11

    Article  Google Scholar 

  • Raj SK, Chandra G, Singh BP (1997) Some Indian strains of cucumber mosaic virus (CMV) lacking satellite RNA. Indian J Exp Biol 35(10):1128–1131

    CAS  PubMed  Google Scholar 

  • Raj SK, Kumar S, Pratap D, Vishnoi R, Snehi SK (2007) Natural Occurrence of cucumber mosaic virus on Rauvolfia serpentina, a new record. Plant Dis 91(3):322–322

    Article  CAS  PubMed  Google Scholar 

  • Raj SK, Kumar S, Snehi SK, Pathre U (2008) First report of cucumber mosaic virus on Jatropha curcas in India. Plant Dis 92(1):171–171

    Article  CAS  PubMed  Google Scholar 

  • Roossinck MJ (2002) Evolutionary history of cucumber mosaic virus deduced by phylogenetic analyses. J Virol 76(7):3382–3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roossinck MJ, Zhang L, Hellwald K-H (1999) Rearrangements in the 5′ nontranslated region and phylogenetic analyses of cucumber mosaic virus RNA 3 indicate radial evolution of three subgroups. J Virol 73(8):6752–6758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samad A, Raj SK, Srivastava A, Chandra G, Ajayakumar PV, Zaim M, Singh BP (2000) Characterization of an Indian isolate of cucumber mosaic virus infecting Egyptian henbane (Hyoscyamus muticus L.). Acta Virol 44(3):131–136

    CAS  PubMed  Google Scholar 

  • Samad A, Ajayakumar PV, Gupta MK, Shukla AK, Darokar MP, Somkuwar B, Alam M (2008) Natural infection of periwinkle (Catharanthus roseus) with cucumber mosaic virus, subgroup IB. Austral Plant Dis Notes 3(1):30–34

    Google Scholar 

  • Sanabam R, Chanu N, Sharma SK, Roy SS, Ansari MA, Prakash N (2018) Genetic diversity of chilli veinal mottle virus infecting different chilli landraces in North East India indicates the possibility of transboundary movement of virus. 3 Biotech 8(8):1–7

    Article  Google Scholar 

  • Senanayake D, Mandal B, Lodha S, Varma A (2007) First report of chilli leaf curl virus affecting chilli in India. Plant Pathol 56(2):343

    Article  Google Scholar 

  • Srivastava A, Raj SK (2004) High molecular similarity among Indian isolates of cucumber mosaic virus suggests a common origin. Curr Sci 87:1126–1131

    CAS  Google Scholar 

  • Srivastava KM, Raj SK, Singh BP (1992) Properties of a cucumber mosaic virus strain naturally infecting chrysanthemum in India. Plant Dis 76:474

    Article  Google Scholar 

  • Swapna Geetanjali A, Kumar R, Srivastava PS, Mandal B (2011) Biological and molecular characterization of two distinct tomato strains of cucumber mosaic virus based on complete RNA-3 genome and subgroup specific diagnosis. Indian J Virol 22(2):117–126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma N, Singh AK, Singh L, Kulshreshtha S, Raikhy G, Hallan V, Ram R, Zaidi AA (2004) Occurrence of cucumber mosaic virus in Gerbera jamesonii in India. Plant Dis 88(10):1161–1161

    Article  CAS  PubMed  Google Scholar 

  • Verma N, Mahinghara BK, Ram R, Zaidi AA (2006) Coat protein sequence shows that cucumber mosaic virus isolate from geraniums (Pelargonium spp.) belongs to subgroup II. J Biosci 31(1):47–54

    Article  CAS  PubMed  Google Scholar 

  • Vinodhini J, Rajendran L, Abirami R, Karthikeyan G (2021) Co-existence of chlorosis inducing strain of cucumber mosaic virus with tospoviruses on hot pepper (Capsicum annuum) in India. Sci Rep 11(1):1–9

    Article  Google Scholar 

  • Vishnoi R, Kumar S, Raj SK (2013) Molecular characterization of a cucumber mosaic virus isolate associated with mosaic disease of banana in India. Phytoparasitica 41(5):545–555

    Article  CAS  Google Scholar 

  • Wahyuni WS, Dietzgen RG, Hanada K, Francki RIB (1992) Serological and biological variation between and within subgroup I and II strains of cucumber mosaic virus. Plant Pathol 41(3):282–297

    Article  CAS  Google Scholar 

  • Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46(W1):W296–W303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang J, Zhang Y (2015) Protein structure and function prediction using I-TASSER. Curr Protoc Bioinform 52(1):5–8

    Article  Google Scholar 

  • Yugandhar K, Gromiha MM (2014) Protein–protein binding affinity prediction from amino acid sequence. Bioinformatics 30(24):3583–3589

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was carried out with financial support from Department of Science Technology-Science and Engineering Research Board (DST-SERB, Grant no. YSS/2015/001449), Government of India through funding the project entitled “Understanding molecular mechanisms of Capsicum annuum L. and cucumber mosaic virus interaction through transcriptomics” University of Agricultural Sciences, GKVK, Bangalore.

Author information

Authors and Affiliations

Authors

Contributions

HDV carried out the overall work, SH, MN, MM helped in conducting the experiments. SH, VV, JCR, PSK and KSS helped in bioinformatics analysis, MR provided the materials for conducting an experiment. CNLR and MKR conceptualized the work, provided the overall guidance and funding.

Corresponding authors

Correspondence to M. Krishna Reddy or C. N. Lakshminarayana Reddy.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2056 KB)

Supplementary file2 (DOCX 19 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vinaykumar, H.D., Hiremath, S., Nandan, M. et al. Genome sequencing of cucumber mosaic virus (CMV) isolates infecting chilli and its interaction with host ferredoxin protein of different host for causing mosaic symptoms. 3 Biotech 13, 361 (2023). https://doi.org/10.1007/s13205-023-03777-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s13205-023-03777-8

Keywords

Navigation