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Identification and characterization of Ageratum yellow vein Malaysia virus (AYVMV) and an associated betasatellite among begomoviruses infecting Solanum lycopersicum in Malaysia

  • Microbial Genetics • Original Paper
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Abstract

The study describes results of a survey of tomato fields for the presence of begomoviruses from different regions of Peninsular Malaysia. An ORF-based (C2 and C3) study was performed to determine the distribution of begomoviruses associated with a severe leaf curl disease in tomato-growing areas of Peninsular Malaysia. Viral DNA was isolated from symptomatic tomato plants, and begomovirus association was confirmed by PCR using DNA-A degenerate primers. The C2 and C3 sequences of the putative begomoviruses were similar to two corresponded ORFs of different geographically separated strains of begomoviruses: Pepper yellow leaf curl Indonesia virus and Tomato yellow leaf curl Kanchanaburi virus. The present study also identified a unique isolate, Ageratum yellow vein Malaysia virus (AYVMV) among above mentioned survey. It has a single-stranded DNA component and its associated betasatellite. The single-stranded DNA component is consisting of 2750 nt with six open reading frames and an organization resembling that of monopartite geminiviruses. The full length of viral single-stranded DNA component genome obtained using next generation sequencing (NGS) showed the highest sequence identity (99%) with Ageratum yellow vein virus (AYVV-BA). The betasatellite component genome obtained by NGS has 1342 nt and showed the highest sequence identity (91%) with the Pepper yellow leaf curl betasatellite. Following ICTV guidelines, Ageratum yellow vein Malaysia virus was assigned the abbreviation AYVMV with sequence and phylogenetic analysis indicating that it might have evolved by recombination of two or more viral ancestors.

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References

  • Alias EF, Baharom A, Ismail I, Radam A (2012) The impact of exchange rate on tomato trade: evidence from Malaysia. Asian Soc Sci 8:p20

    Google Scholar 

  • Anwar I, Bukhari HA, Nahid N, Rashid K, Amin I, Shaheen S, Hussain K, Mansoor S (2019) Association of cotton leaf curl Multan betasatellite and Ageratum conyzoides symptomless alphasatellite with tomato leaf curl New Delhi virus in Luffa cylindrica in Pakistan. Australas Plant Pathol 30:1–5

    Google Scholar 

  • Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Belabess Z, Urbino C, Granier M, Tahiri A, Blenzar A, Peterschmitt M (2018) The typical RB76 recombination breakpoint of the invasive recombinant tomato yellow leaf curl virus of Morocco can be generated experimentally but is not positively selected in tomato. Virus Res 243:44–51

    CAS  PubMed  Google Scholar 

  • Briddon R, Mansoor S, Bedford I, Pinner M, Saunders K, Stanley J, Zafar Y, Malik K, Markham P (2001) Identification of DNA components required for induction of cotton leaf curl disease. Virology 285:234–243

    CAS  PubMed  Google Scholar 

  • 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 160:1593–1619

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fauquet C, Briddon R, Brown J, Moriones E, Stanley J, Zerbini M, Zhou X (2008) Geminivirus strain demarcation and nomenclature. Arch Virol 153:783–821

    CAS  PubMed  Google Scholar 

  • Goodman R, Bird J (1978) Bean golden mosaic virus. CMI/AAB Descriptions of Plant Viruses:4

  • Green S, Tsai W, Shih S, Black L, Rezaian A, Rashid M, Roff M, Myint Y, Hong L (2001) Molecular characterization of begomoviruses associated with leafcurl diseases of tomato in Bangladesh, Laos, Malaysia, Myanmar, and Vietnam. Plant Dis 85:1286–1286

    CAS  PubMed  Google Scholar 

  • Guo F-B, Zhang C-T (2006) ZCURVE_V: a new self-training system for recognizing protein-coding genes in viral and phage genomes. BMC Bioinformatics 7:9

    PubMed  PubMed Central  Google Scholar 

  • Gutierrez C (2002) Strategies for geminivirus DNA replication and cell cycle interference. Physiol Mol Plant Pathol 60:219–230

    CAS  Google Scholar 

  • Harrison B, Zhou X, Otim-Nape G, Liu Y, Robinson D (1997) Role of a novel type of double infection in the geminivirus-induced epidemic of severe cassava mosaic in Uganda. Ann Appl Biol 131:437–448

    Google Scholar 

  • Huang X, Miller W (1991) Lalign-find the best local alignments between two sequences. Adv Appl Math 12:373–381

    Google Scholar 

  • Idris A, Al-Saleh M, Piatek MJ, Al-Shahwan I, Ali S, Brown JK (2014) Viral metagenomics: analysis of begomoviruses by illumina high-throughput sequencing. Viruses 6:1219–1236

    PubMed  PubMed Central  Google Scholar 

  • Koeda S, Kesumawati E, Tanaka Y, Hosokawa M, Kitajima A (2016) Mixed infection of begomoviruses on pepper plants at northern Sumatra, Indonesia. Trop Agr Develop 60:59–64

    Google Scholar 

  • Koravieh MM, Roff MM, Othman R (2008) First report of a whitefly-transmitted geminivirus infecting Mimosa invisa in Malaysia. Australas Plant Dis Notes 3:25–26

    Google Scholar 

  • Kozubek E, Irzykowski W, Lehmann P (2007) Genetic and molecular variability of a Turnip mosaic virus population from horseradish (Cochlearia armoracia L.). J Appl Genet 48:295–306

    PubMed  Google Scholar 

  • Kumar J, Gunapati S, Singh SP, Kumar A, Lalit A, Sharma NC, Puranik R, Tuli R (2013) A new betasatellite associated with cotton leaf curl Burewala virus infecting tomato in India: influence on symptoms and viral accumulation. Arch Virol 158:1349–1353

    CAS  PubMed  Google Scholar 

  • Liu S, Bedford ID, Briddon RW, Markham PG (1997) Efficient whitefly transmission of African cassava mosaic geminivirus requires sequences from both genomic components. J Gen Virol 78:1791–1794

    CAS  PubMed  Google Scholar 

  • Luisoni E, Milne R, Vecchiati M (1995) Purification of tomato yellow leaf curl geminivirus. New Microbiol 18:253–260

    CAS  PubMed  Google Scholar 

  • Mahmoudieh M, Noor MR, Harikrishna JA, Othman RY (2019) Tomato Solanum lycopersicum expressing the overlapping regions of three begomovirus genes exhibit resistance to Ageratum yellow vein Malaysia virus. Physiol Mol Plant Path 108:101425

    CAS  Google Scholar 

  • Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meliansyah R, Hidayat SH, Mutaqin KH (2012) Geminiviruses associated with the weed species Ageratum conyzoides, Centipeda minima, Porophyllum ruderale, and Spilanthes iabadicensis from Java, Indonesia. Microbiol Indones 5:4

    Google Scholar 

  • Monci F, Sánchez-Campos S, Navas-Castillo J, Moriones E (2002) A natural recombinant between the geminiviruses, Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303:317–326

    CAS  PubMed  Google Scholar 

  • Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation

  • Muniyappa V, Venkatesh H, Ramappa H, Kulkarni R, Zeidan M, Tarba C-Y, Ghanim M, Czosnek H (2000) Tomato leaf curl virus from Bangalore (ToLCV-Ban4): sequence comparison with Indian ToLCV isolates, detection in plants and insects, and vector relationships. Arch Virol 145:1583–1598

    CAS  PubMed  Google Scholar 

  • Omar M, Othman RY (2019) The infectious clone construction of ageratum yellow vein virus isolate and its associated betasatellite from Malaysia. Plant Cell Biotechnol Mol Biol 20(21-22):962–972

    Google Scholar 

  • Prasanna H, Rai M (2007) Detection and frequency of recombination in tomato-infecting begomoviruses of South and Southeast Asia. Virol J 4:111

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qadir R, Khan ZA, Monga D, Khan JA (2019) Diversity and recombination analysis of Cotton leaf curl Multan virus: a highly emerging begomovirus in northern India. BMC Genomics 20:274

    PubMed  PubMed Central  Google Scholar 

  • Rocha CS, Castillo-Urquiza GP, Lima AT, Silva FN, Xavier CA, Hora-Júnior BT, Beserra-Júnior JE, Malta AW, Martin DP, Varsani A (2013) Brazilian begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. J Virol 87:5784–5799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rojas M, Gilbertson R, Maxwell D (1993) Use of degenerate primers in the polymerase chain reaction to detect whitefly-transmitted geminiviruses. Plant Dis 77:340–347

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Scholthof KBG, Adkins S, Czosnek H, Palukaitis P, Jacquot E, Hohn T, Hohn B, Saunders K, Candresse T, Ahlquist P (2011) Top 10 plant viruses in molecular plant pathology. Mol Plant Pathol 12:938–954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shih S, Roff M, Nakhla M, Maxwell D, Green S (1998) A new geminivirus associated with a leaf curl disease of tomato in Malaysia. J Zhiwu Baohuxue Hui Huikan 40:435–435

    Google Scholar 

  • Shivaprasad P, Akbergenov R, Trinks D, Rajeswaran R, Veluthambi K, Hohn T, Pooggin MM (2005) Promoters, transcripts, and regulatory proteins of Mungbean yellow mosaic geminivirus. J Virol 79:8149–8163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sung Y, Coutts RH (1995) Pseudorecombination and complementation between potato yellow mosaic geminivirus and tomato golden mosaic geminivirus. J Gen Virol 76:2809–2815

    CAS  PubMed  Google Scholar 

  • Sunter G, Hartitz MD, Hormuzdi SG, Brough CL, Bisaro DM (1990) Genetic analysis of tomato golden mosaic virus: ORF AL2 is required for coat protein accumulation while ORF AL3 is necessary for efficient DNA replication. Virology 179:69–77

    CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan PH, Wong SM, Wu M, Bedford ID, Saunders K, Stanley J (1995) Genome organization of ageratum yellow vein virus, a monopartite whitefly-transmitted geminivirus isolated from a common weed. J Gen Virol 76:2915–2922

    CAS  PubMed  Google Scholar 

  • 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 Genet 9:e1003399

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiongbiao X, Qian Y, Wang Y, Li Z, Zhou X (2019) Iterons homologous to helper geminiviruses are essential for efficient replication of betasatellites. J Virol 93(5):e01532–e01518

  • Zhou X, Liu Y, Calvert L, Munoz C, Otim-Nape GW, Robinson DJ, Harrison BD (1997) Evidence that DNA-A of a geminivirus associated with severe cassava mosaic disease in Uganda has arisen by interspecific recombination. J Gen Virol 78:2101–2111

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We appreciate the assistance provided by Dr. Ching Ang Ong, Ranganath Gudimella and Mahendra A.L Saravanamuthu for this work.

Funding

The authors would like to thank the funding from the University of Malaya (RG070-12BIO) and UM-MOE High Impact Research grants (UM.C/625/1/HIR/MOHE/SCI/18) for this study.

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Authors and Affiliations

  1. Centre for Research in Biotechnology for Agriculture and Institute of Biological Science, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Mohtaram Mahmoudieh, Jennifer Ann Harikrishna & Rofina Yasmin Othman

  2. Horticulture Research Centre, MARDI Headquarters, P.O.Box 12301, GPO, 50774, Kuala Lumpur, Malaysia

    Mohamad Roff Mohd Noor

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  1. Mohtaram Mahmoudieh
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  2. Mohamad Roff Mohd Noor
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  3. Jennifer Ann Harikrishna
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  4. Rofina Yasmin Othman
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Correspondence to Mohtaram Mahmoudieh.

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Communicated by: Agnieszka Szalewska-Palasz

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Mahmoudieh, M., Noor, M.R.M., Harikrishna, J.A. et al. Identification and characterization of Ageratum yellow vein Malaysia virus (AYVMV) and an associated betasatellite among begomoviruses infecting Solanum lycopersicum in Malaysia. J Appl Genetics 61, 619–628 (2020). https://doi.org/10.1007/s13353-020-00574-4

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  • DOI: https://doi.org/10.1007/s13353-020-00574-4

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