Abstract
The complete nucleotide sequences of a monopartite begomovirus and an associated alphasatellite and betasatellite isolated from naturally infected okra (Abelmoschus esculentus) plants originating from Jordan were determined. The sequences of the begomovirus, alphasatellite, and betasatellites were determined to be 2,764, 1,307, and 1,354 nucleotides in length, respectively. Sequence Demarcation Tool (SDT) and phylogenetic analysis revealed that the begomovirus isolate shared the highest (99.5-99.8%) nt sequence identity with isolates of cotton leaf curl Gezira virus (CLCuGeV), a begomovirus found to exclusively infect cotton in Africa, and recently, in Asia and the Middle East. The DNA sequences of the alphasatellite and betasatellite exhibited the highest nt sequence identity (98.7-98.9% and 92.2-95.3%, respectively) to cotton leaf curl Gezira alphasatellite and cotton leaf curl Gezira betasatellite, respectively. This is the first identification of an African begomovirus, associated with DNA satellites, infecting okra in Jordan.
Similar content being viewed by others
References
Abbas Q, Amin I, Mansoor S et al (2019) The Rep proteins encoded by alphasatellites restore expression of a transcriptionally silenced green fluorescent protein transgene in Nicotiana benthamiana. Virus Dis 30:101–105
Al-Musa A, Anfoka G, Misbeh S et al (2008) Detection and molecular characterization of squash leaf curl virus (SLCV) in Jordan. J Phytopathol 156:311–316
Al-Musa A, Anfoka G, Al-Abdulat A et al (2011) Watermelon chlorotic stunt virus (WmCSV): a serious disease threatening watermelon production in Jordan. Virus Genes 43:79–89
Anfoka G, Abhary M, Haj Ahmad F et al (2008) Survey of tomato yellow leaf curl disease-associated viruses in the Eastern Mediterranean Basin. J Plant Pathol 90:311–320
Anfoka G, Al-Talb M, Haj-Ahmad F (2016) A new isolate of tomato yellow leaf curl Axarquia virus associated with tomato yellow leaf curl disease in Jordan. J Plant Pathol 98:145–149
Briddon RW, Bull SE, Mansoor S et al (2002) Universal primers for the PCR-mediated amplification of DNA β. Mol Biotechnol 20:315–318
Briddon RW, Stanley J (2006) Sub-viral agents associated with plant-infecting single-stranded DNA viruses. Virology 344:198–210
Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olivé E, Moriones E, Lett J-M, Zerbini FM, Varsani A (2018) Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch Virol 163:2587–2600
Bull SE, Briddon RW, Markham PG (2003) Universal primers for the PCR-mediated amplification of DNA1: a satellite-like molecule associated with begomovirus-DNA b complexes. Mol Biotechnol 23:83–86
Claverie S, Varsani A, Hoareau M et al (2020) Sorghum mastrevirus-associated alphasatellites: new geminialphasatellites associated with an African streak mastrevirus infecting wild Poaceae plants on Reunion Island. Arch Virol 165:1925–1928
Cui X, Li G, Wang D et al (2005) A Begomovirus DNA β-encoded protein binds DNA, functions as a suppressor of RNA silencing, and targets the cell nucleus. J Virol 79:10764–10775
Haj-Ahmad F, Odeh W, Anfoka G (2013) First report on the association of squash leaf curl virus and watermelon chlorotic stunt virus with tomato yellow leaf curl disease. Plant Dis 97:428
Idris AM, Shahid MS, Briddon RW et al (2011) An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol 92:706–717
Inoune-Nagata AK, Albuquerque LC, Roche WB, Nagata T (2004) A simple method for cloning the complete begomovirus genome using the bacteriophage ɸ29 DNA polymerase. J Virol Methods 116:209–211
Lapidot M, Gelbart D, Gal-On A et al (2014) Frequent migration of introduced cucurbit-infecting begomoviruses among Middle Eastern countries. Virol J 11:181
Martin DP, Murrell B, Golden M et al (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003
Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9:e108277
Navas-Castillo J, Fiallo-Olivé E, Sánchez-Campos S (2011) Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol 49:219–248
Nawaz-ul-Rehman MS, Nahid N, Mansoor S et al (2010) Post-transcriptional gene silencing suppressor activity of two non-pathogenic alphasatellites associated with a begomovirus. Virology 405:300–308
Rojas MR, Macedo MA, Maliano MR et al (2018) World management of geminiviruses. Annu Rev Phytopathol 56:637–677
Rosario K, Marr C, Varsani A et al (2016) Begomovirus-associated satellite DNA diversity captured through vector-enabled metagenomic (VEM) surveys using whiteflies (Aleyrodidae). Viruses 8:36
Tahir MN, Amin I, Briddon RW, Mansoor S (2011) The merging of two dynasties—identification of an African cotton leaf curl disease-associated begomovirus with cotton in Pakistan. PLoS ONE 6:e20366
Villegas C, Ramos-Sobrinho R, Jifon JL et al (2019) First report of cotton leaf curl Gezira virus and its associated alphasatellite and betasatellite from disease affected okra plants in the United States. Plant Dis 103:3291
Wyatt SD, Brown JK (1996) Detection of subgroup III geminivirus isolates in leaf extracts by degenerate primers and polymerase chain reaction. Phytopathology 86:1288–1293
Zerbini FM, Briddon RW, Idris A et al (2017) ICTV virus taxonomy profile: Geminiviridae. J Gen Virol 98:131–133
Zhou XP (2013) Advances in understanding begomovirus satellites. Annu Rev Phytopathol 51:357–381
Acknowledgements
We are thankful to the research assistants and farmers for their support in field surveys and sample collection. We also thank Dr. Joanna Gress for critically reviewing the English language of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare there is no conflict of interest.
Ethical approval
This study does not include any experiments involving humans or animals by any of the authors.
Additional information
Handling Editor: Tim Skern.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Begomovirus sequences: GenBank Acc. No. MT316185-MT316187. Betasatellite sequences: GenBank Acc. No. MT316188-MT316190. Alphasatellite sequences: GenBank Acc. No. MT316191-MT316193.
Supplementary Information
Below is the link to the electronic supplementary material.
705_2021_5075_MOESM1_ESM.jpg
Supplementary Fig. S1 Genome-wide pairwise identity color matrix constructed with sequences of begomoviruses (or DNA A genomic components) (a), alphasatellites (b), and betasatellites (c) determined in this study and representatives of the different isolates of the virus and DNA satellites, calculated by SDT (v1.2) (DOC 35 KB)
705_2021_5075_MOESM2_ESM.doc
Supplementary Table S1 Features of monopartite begomoviruses, alphasatellites and betasatellites isolated from okra in Jordan (DOC 35 KB)
Rights and permissions
About this article
Cite this article
Salem, N.M., Shahid, M.S., Idris, A. et al. Complete nucleotide sequence of a begomovirus associated with an alphasatellite and a betasatellite naturally infecting okra in Jordan. Arch Virol 166, 2033–2036 (2021). https://doi.org/10.1007/s00705-021-05075-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-021-05075-1