Abstract
The genome sequence of a bipartite begomovirus was identified in an ornamental plant, Golden duranta (GD) (Duranta erecta) exhibiting crinkled leaves and apical leaf curling, collected from three districts Lucknow (Lko), Basti (Bas) and Deoria (Deo) of Eastern Uttar Pradesh, India. Three complete genome sequences of each DNA-A and DNA-B, were amplified by rolling circular amplification (RCA), cloned and sequenced. The analysis for both DNA-A and DNA-B revealed 91–99% nucleotide sequence identity to tomato leaf curl New Delhi virus (ToLCNDV). Phylogenetic studies revealed that all three ToLCNDV-A isolates form a separate clade, whereas, isolates of ToLCNDV-B clustered together with ToLCNDV-Chi- RKG2 (MT264782). Furthermore, when compared to other DNA-A and DNA-B, ToLCNDV-[GD-Deo-In] DNA-A showed the most recombination events. The nucleotide substitution rates of ToLCNDV-A and ToLCNDV-B were established to be 8.152 10− 4 substitutions site− 1 year− 1 and 6.684 10− 4 substitutions site− 1 year− 1 respectively. However, the transitional and transversal substitution rates were shown to be higher in DNA-B with a total number of mutations (η) 691 in comparison with DNA-A. The combined negative values of the neutrality tests, Tajima’s D and Fu and Li’s D*, indicate purified selection with low-frequency polymorphism. The dN/dS ratio for ToLCNDV-A and ToLCNDV-B revealed the selective control of evolutionary relationships. Our study supports the theory that begomoviruses have expanded their host range and that the fast evolutionary rates are mostly due to recurrent recombination and mutation. This is the first record of bipartite ToLCNDV infecting D. erecta in India.
Similar content being viewed by others
Data availability
All sequencing data of virus isolates are available in the NCBI database. Further data analysis will be available from the corresponding authors upon request.
References
Altschul SF, GishW, Miller W, Myers EW, David JLDJ (1990) Basic local alignment search tool. J Mol Biol 215(3):403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Bahjatnia S, Izadpanah K, Barry DI, Rezaian M (2004) Molecular characterization and taxonomic position of the Iranian isolate of Tomato leaf curl virus. Iran J Plant Pathol 40(1–2):77–94
Bottcher B, Unseld S, Ceulemans H, Russell RB, Jeske H (2004) Geminate structures of African cassava mosaic virus. J Virol 78(13):6758–6765. https://doi.org/10.1128/JVI.78.13.6758-6765.2004
Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG (2002) Universal primers for the PCR-mediated amplification of DNA β a molecule associated with some monopartite begomoviruses Mol. Biotechnol 20:315–318. https://doi.org/10.1385/mb:20:3:315
Brown J, Fauquet C, Briddon R, Zerbini M, Moriones E, Navas Castillo J (2012) Family Geminiviridae. In: King AMQ, Adams MJ, Carstens EB,and, Lefkowitz EJ (eds) Virus Taxonomy: classification and nomenclature of viruses—Ninth Report of the International Committee on Taxonomy of viruses. AM Elsevier Academic, London
Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Silva JC, Fiallo-Olivé E, Briddon RW, Hernández-Zepeda C, Idris A (2015) Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Arch Virol 160(6):1593–1619. https://doi.org/10.1007/s00705-015-2398-y
Bull SE, Briddon RW, Markham PG (2003) Universal primers for the PCR-mediated amplification of DNA 1: a satellite-like molecule associated with begomovirus-DNAβ complexes. Mol Biotechnol 23:83–86. https://doi.org/10.1385/MB:23:1:83
Crespo-Bellido A, Hoyer JS, Dubey D, Jeannot RB, Duffy S (2021) Interspecies recombination has driven the macroevolution of cassava mosaic begomoviruses. Journal of Virology 95(17):e0054121. http//:00541-00521.10.1128/JVI.00541– 21
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27(8):1164–1165 http//. https://doi.org/10.1093/bioinformatics/btr088
Duffy S, Holmes EC (2008) Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. J Virol 82:957–965. https://doi.org/10.1128/JVI.01929-07
Duffy S, Holmes EC (2009) Validation of high rates of nucleotide substitution in Geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol 90:1539–1547. https://doi.org/10.1099/vir.0.009266-0
Hill T, Unckless RL (2017) Baculovirus Molecular Evolution via Gene turnover and recurrent positive selection of key genes. J Virol 91. https://doi.org/10.1128/JVI.01319-17
Huson DH, Bryant D (2006) Application of phylogenetic networks in Evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Jenkins GM, Rambaut A, Pybus OG, Holmes EC (2002) Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165. https://doi.org/10.1007/s00239-001-0064-3
Kenyon L, Kumar S, Tsai WS, Hughes JA (2014) Virus diseases of Peppers (Capsicum spp.) and their control. Adv Virus Res 90:297–354. https://doi.org/10.1016/B978-0-12-801246-8.00006-8
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):1547–1549. https://doi.org/10.1093/molbev/msy096
Lefeuvre P, Harkins GW, Lett JM, Briddon RW, Chase MW, Moury B, Martin DP (2011) Evolutionary time-scale of the begomoviruses: evidence from Integrated sequences in the Nicotiana Genome. PLoS ONE 6(5):e19193. https://doi.org/10.1371/journal.pone.0019193
Lima A, Silva JC, Silva FN, Castillo-Urquiza GP, Silva F, Seah YM, Mizubuti ESG, Duffy S, Zerbini FM (2017) The diversification of begomovirus populations is predominantly driven by mutational dynamics. Virus Evol 3:1–14. vex005
Manen J-F, Sinitsyna O, Aeschbach L, Markov AV, Sinitsyn A (2005) A fully automatable enzymatic method for DNA extraction from plant tissues. BMC Plant Biol 5(1):1–9. https://doi.org/10.1186/1471-2229-5-23
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1(1):vev003. https://doi.org/10.1093/ve/vev003
Marwal A, Nehra C, Verma RK, Mishra M, Srivasatava D, Choudhary P, Gaur R (2021) First report of papaya leaf curl virus and its associated papaya leaf curl betasatellite infecting Catharanthus roseus plants in India. J Hortic Sci Biotechnol 1–6. https://doi.org/10.1080/14620316.2021.1912646
Melgarejo TA, Kon T, Rojas MR, Paz-Carrasco L, Zerbini FM, Gilbertson RL (2013) Characterization of a new world monopartite begomovirus causing leaf curl disease of tomato in Ecuador and Peru reveals a new direction in geminivirus evolution. J Virol 87(10):5397–5413. https://doi.org/10.1128/jvi.00234-13
Mishra M, Verma RK, Marwal A, Sharma P, Gaur R (2020) Biology and interaction of the natural occurrence of distinct monopartite begomoviruses associated with satellites in capsicum annum from India. Front Microbiol 11:2366. https://doi.org/10.3389/fmicb.2020.512957
Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9(9):e108277. https://doi.org/10.1371/journal.pone.0108277
Nawaz-ul-Rehman MS, Fauquet CM (2009) Evolution of geminiviruses and their satellites. FEBS Lett 583(12):1825–1832. https://doi.org/10.1016/j.febslet.2009.05.045
Pagan I, Garcia-Arenal F (2018) Population Genomics of Plant Viruses, in Population Genomics: Microorganisms, eds M. F. Polz and O. P. Rajora. Cham: Springer International Publishing 233–265. https://doi.org/10.1007/13836_2018_15
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394. https://www.annualreviews.org/doi/abs/10.1146/annurev.phyto.43.040204.135939
Roy A, Zhai Y, Ortiz J, Neff M, Mandal B, Mukherjee SK, Pappu HR (2019) Multiplexed editing of a begomovirus genome restricts escape mutant formation and disease development. PLoS ONE 14(10):e0223765. https://doi.org/10.1371/journal.pone.0223765
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio J C, Guirao-Rico S, Librado P, Ramos-Onsins S E, Sánchez-Gracia A (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302.Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-475 Onsins SE (2017) 476 Mol Biology Evol 34(12):3299–3302. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets https://doi.org/10.1093/molbev/msx248
Sahu AK, Verma RK, Gaur R, Sanan-Mishra N (2018) Complexity and recombination analysis of novel begomovirus associated with spinach yellow vein disease in India. Plant Gene 13:42–49. https://doi.org/10.1016/j.plgene.2018.01.001
Silva SJC, Castillo-Urquiza GP, Hora-Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM (2012) Species diversity, phylogeny and genetic variability of Begomovirus populations infecting leguminous weeds in Northeastern Brazil: degomovirus diversity in leguminous weeds in Brazil. Plant Pathol 61:457–467. https://doi.org/10.1111/j.1365-3059.2011.02543.x
Subsongsang R, Jiraungkoorskul W (2016) An updated review on phytochemical properties of golden dewdrop Duranta erecta. Pharmacogn Rev 10(20):115. https://doi.org/10.4103/0973-7847.194042
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4(1):vey016. https://doi.org/10.1093/ve/vey016
Varsani A, Roumagnac P, Marc Fuchs, Castillo JN, Moriones E, Idris A, Briddon RW, Bustamante RR, Zerbini FM, Darren P, Martin DP (2017) Capulavirus and Grablovirus: two new genera in the family Geminiviridae. Arch Virol 162:1819–1831. https://doi.org/10.1007/s00705-017-3268-6
Venkataravanappa V, Prasanna H, Reddy CL, Chauhan N, Shankarappa K, Reddy MK (2021) Molecular characterization of recombinant bipartite begomovirus associated with mosaic and leaf curl disease of cucumber and muskmelon. Indian Phytopathol 74:775-7851–11. https://doi.org/10.1007/s42360-020-00308-w
Vivek P, Jeyaraj G, Geetanjali AS (2021) A review on the occurrence of begomoviruses in ornamental plant families. J Plant Dis Prot:1–11. https://doi.org/10.1007/s41348-021-00467-6
Wyatt SD, Brown JK (1996) Detection of Subgroup III Geminivrirus isolates in leaf extracts by degenerate primers and polymerase chain reaction. Phytopathology 86:1288–1293. https://doi.org/10.1094/Phyto-86-1288
Acknowledgements
The authors are thankful to the Department of Biotechnology, D.D.U. Gorakhpur University, Gorakhpur Uttar Pradesh, India. A.A. is also grateful to the Office of Research and Sponsored Program, The University of Tulsa, Oklahoma. AKS and NSM thank International Centre for Genetic Engineering and Biotechnology (ICGEB), New Delhi for providing the laboratory space.
Funding
There is a no funding agency.
Author information
Authors and Affiliations
Contributions
AKS, VP and AS contributed equally to the experiments and computational work. RKV helped with computational analysis. NSM, AA and RKG. are the mentor and supervised the experiments, edited, proofread, and finalized the manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Ethical approval
The work did not contain studies with human participants or animals performed.
Consent for publication
All authors has given their consent to publish this work.
Consent to participate
Consents from all the authors have been taken.
Competing interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
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.
About this article
Cite this article
Sahu, A., Pandey, V., Srivastava, A. et al. Molecular characterization of a bipartite begomovirus associated with leaf crinkle and curling symptoms of Duranta erecta in India. Indian Phytopathology 77, 191–201 (2024). https://doi.org/10.1007/s42360-024-00718-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42360-024-00718-0