Molecular Detection and Identification of Begomovirus Infecting Cucumber (Cucumis sativus) in Terengganu, Malaysia

https://doi.org/10.55230/mabjournal.v53i2.2798

Authors

  • Sakthivel Poraya Goundar School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin (UniSZA), Kampus Besut, 22000 Besut, Terengganu Malaysia; Green World Genetics Sdn. Bhd., No.40, Jalan KIP 10, Taman Perindustrian KIP, Kepong 52200, Kuala Lumpur, Malaysia
  • Sandhya Ramani School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin (UniSZA), Kampus Besut, 22000 Besut, Terengganu Malaysia
  • Nuramirashafikah Mohd Radzi School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin (UniSZA), Kampus Besut, 22000 Besut, Terengganu Malaysia
  • Mohd Fahmi Abu Bakar School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin (UniSZA), Kampus Besut, 22000 Besut, Terengganu Malaysia
  • Hasan Nudin Nur Fatihah School of Agriculture Science and Biotechnology, Faculty of Bioresources and Food Industry, Universiti Sultan Zainal Abidin (UniSZA), Kampus Besut, 22000 Besut, Terengganu Malaysia

Keywords:

Begomovirus, Cucumis sativus, DNA-A, Phylogenetics, Terengganu, ToLCNDV

Abstract

The genus Begomovirus from the family Geminiviridae is responsible for causing significant economic losses to many important horticultural crops, including cucumber (Cucumis sativus L.). Begomovirus infection during the early stages of plant growth can lead to complete yield loss. Hence, the identification of begomovirus species is important to design a precise resistant breeding strategy. This study aims to detect the presence of begomovirus in typical symptomatic cucumber leaves, identify the species of begomovirus present, and investigate the evolutionary relationships with other reported begomoviruses using phylogenetic analysis. Leaf samples from symptomatic cucumber plants were collected from the Green World Genetics (GWG) research station and a farm in Lembah Bidong, Rhu Tapai, Setiu, Terengganu. To detect the presence of begomovirus, PCR was carried out using universal primers targeting DNA-A, DNA-B, and betasatellite regions. DNA-A and betasatellite fragments were amplified, but not DNA-B. The amplified partial sequences of DNA-A were then analysed and compared with other begomovirus sequences in the GenBank database managed by the National Centre for Biotechnology Information (NCBI). The newly isolated DNA-A sequence from cucumber was 100% identical to the tomato leaf curl New Delhi virus (ToLCNDV). The phylogenetic tree was divided into two groups: group A, consisting of the newly isolated DNA-A sequence from cucumber, ToLCNDV, followed by squash leaf curl China virus (SLCCNV) and a monopartite begomovirus Ageratum yellow vein virus (AYVV); and group B, consisting of tomato yellow leaf curl Kanchanaburi virus (TYLCKaV), pepper yellow leaf curl Indonesia virus (PepYLCIV), and pepper yellow leaf curl Aceh virus (PepYLCAV). For the first time in cucumber, betasatellite is reported in association with ToLCNDV, a bipartite old-world begomovirus. This study provides a basis for the selection and breeding of begomovirus-resistant cucumber varieties in the future.

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References

Akhond, M.A.Y., Kabir, M.R., Muqit, A. & Mulholland, V. 2014. Survey and characterization of tomato infecting Geminiviruses in Bangladesh. (Unpublished).

Briddon, R.W. & Stanley, J. 2006. Subviral agents associated with plant single-stranded DNA viruses. Virology, 344(1): 198-210. DOI: https://doi.org/10.1016/j.virol.2005.09.042

Briddon, R.W., Bull, S.E., Amin, I., Idris, A.M., Mansoor, S., Bedford, I.D., Dhawan, P., Rishi, N., Siwatch, S.S., Abdel-Salam, A.M. & Brown, J.K. 2003. Diversity of DNA β, a satellite molecule associated with some monopartite begomoviruses. Virology, 312(1): 106-121. DOI: https://doi.org/10.1016/S0042-6822(03)00200-9

Briddon, R.W., Patil, B.L., Bagewadi, B., Nawaz-ul-Rehman, M.S. & Fauquet, C.M. 2010. Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evolutionary Biology, 10(1): 1-17. DOI: https://doi.org/10.1186/1471-2148-10-97

Briddon, R.W., Watts, J., Markham, P.G. & Stanley, J. 1989. The coat protein of beet curly top virus is essential for infectivity. Virology, 172(2): 628-633. DOI: https://doi.org/10.1016/0042-6822(89)90205-5

Chakraborty, S., Pandey, P.K., Banerjee, M.K., Kalloo, G. & Fauquet, C.M. 2003. Tomato leaf curl Gujarat virus, a new begomovirus species causing a severe leaf curl disease of tomato in Varanasi, India. Phytopathology, 93(12): 1485-1495. DOI: https://doi.org/10.1094/PHYTO.2003.93.12.1485

Chan, Y.L., Lee, L.M., Shih, S.L., Kuo, F.H. & Kenyon, L. 2019. Survey of virus diseases affecting squash (Cucurbita moschata) in Taiwan. Acta Horticulturae, 1257: 23-28. DOI: https://doi.org/10.17660/ActaHortic.2019.1257.4

Charoenvilaisiri, S., Seepiban, C., Phironrit, N., Phuangrat, B., Yoohat, K., Deeto, R., Chatchawankanphanich, O. & Gajanandana, O. 2020. Occurrence and distribution of begomoviruses infecting tomatoes, peppers and cucurbits in Thailand. Crop Protection 127: 104948. DOI: https://doi.org/10.1016/j.cropro.2019.104948

Chen, Y.J., Lai, H.C., Lin, C.C., Neoh, Z.Y. & Tsai, W.S. 2021. Genetic diversity, pathogenicity and pseudorecombination of cucurbit-infecting begomoviruses in Malaysia. Plants, 10(11): 2396. DOI: https://doi.org/10.3390/plants10112396

Dasgupta, I., Malathi, V.G. & Mukherjee, S.K. 2003. Genetic engineering for virus resistance. Current Science, 84(3): 341-354.

Department of Agriculture Malaysia. 2021. Vegetables and cash crops statistics, Malaysia 2021 [WWW Document]. URL http://www.doa.gov.my/index/resources/aktiviti_sumber/sumber_awam/maklumat_pertanian/perangkaan_tanaman/statistik_tanaman_sayur_tanaman_kontan_2021.pdf (accessed 8.13.23).

Fatihah, H.N.N., Fay, M.F. & Maxted, N. 2011. Molecular phylogenetics of Cypripedium L. (Cypripedioideae: Orchidaceae) based on plastid and nuclear DNA sequences. Journal of Agrobiotechnology, 2: 35-51.

Fondong, V.N. 2013. Geminivirus protein structure and function. Molecular Plant Pathology, 14(6): 635-649. DOI: https://doi.org/10.1111/mpp.12032

Food and Agriculture Organization of the United Nations. 2021. FAOSTAT 2021 [WWW Document]. URL https://www.fao.org/faostat/en/#home (accessed 5.25.23).

Frischmuth, T., Roberts, S. & von Arnim, A. & Stanley, J. 1993. Specificity of bipartite geminivirus movement proteins. Virology, 196(2): 666-673. https://doi.org/10.1006/viro.1993.1523 DOI: https://doi.org/10.1006/viro.1993.1523

Goundar, S.P., Ramani, S., Mohd, K.S., Aik, C.K. & Fatihah, H.N.N. 2022. Evaluation of new cucumber (Cucumis sativus L.) hybrids for agronomic characteristics and begomovirus resistance. Malaysian Journal of Biochemistry & Molecular Biology, Special Issue 2: 30-37.

Guerrero, J., Regedanz, E., Lu, L., Ruan, J., Bisaro, D.M. & Sunter, G. 2020. Manipulation of the plant host by the geminivirus AC2/C2 protein, a central player in the infection cycle. Frontiers in Plant Science, 11: 591. DOI: https://doi.org/10.3389/fpls.2020.00591

Harrison, B.D. & Robinson, D.J. 1999. Natural genomic and antigenic variation in whitefly transmitted geminivirus. Annual Review of Phytopathology, 37: 369-398.

Hein, J. 1990. Reconstructing evolution of sequences subject to recombination using parsimony. Mathematical Biosciences, 98(2): 185-200. DOI: https://doi.org/10.1016/0025-5564(90)90123-G

ICTV (International committee on Taxonomy of Virus). 2021. Virus taxonomy 2021 release [WWW Document]. URL https://ictv.global/ (accessed 5.25.23).

Inoue-Nagata, A.K., Albuquerque, L.C., Rocha, W.B. & Nagata, T. 2004. A simple method for cloning the complete begomovirus genome using the bacteriophage φ29 DNA polymerase. Journal of Virological Methods, 116(2): 209-211. DOI: https://doi.org/10.1016/j.jviromet.2003.11.015

Iqbal, Z., Shafiq, M., Ali, I., Mansoor, S. & Briddon, R.W. 2017. Maintenance of Cotton leaf curl Multan betasatellite by tomato leaf curl New Delhi virus-analysis by mutation. Frontiers in Plant Science, 8: 2208. DOI: https://doi.org/10.3389/fpls.2017.02208

Ito, T., Sharma, P., Kittipakorn, K. & Ikegami, M. 2008. Complete nucleotide sequence of a new isolate of tomato leaf curl New Delhi virus infecting cucumber, bottle gourd and muskmelon in Thailand. Archives of Virology, 153: 611-613. DOI: https://doi.org/10.1007/s00705-007-0029-y

Jia, H. & Wang, H. 2021. Introductory chapter: Studies on cucumber. In: Cucumber economic values and its cultivation and breeding. W. Haiping (Ed). Intechopen, London, UK. pp. 1-8. DOI: https://doi.org/10.5772/intechopen.97360

Kesumawati, E., Okabe, S., Homma, K., Fujiwara, I., Zakaria, S., Kanzaki, S. & Koeda, S. 2019. Pepper yellow leaf curl Aceh virus: a novel bipartite begomovirus isolated from chili pepper, tomato, and tobacco plants in Indonesia. Archives of Virology, 164(9): 2379-2383. DOI: https://doi.org/10.1007/s00705-019-04316-8

Kesumawati, E., Okabe, S., Khalil, M., Alfan, G., Bahagia, P., Pohan, N., Zakaria, S. & Koeda, S. 2020. Molecular characterization of begomoviruses associated with yellow leaf curl disease in Solanaceae and Cucurbitaceae crops from Northern Sumatra, Indonesia. Horticulture Journal, 89(4): 410-416. DOI: https://doi.org/10.2503/hortj.UTD-175

Kress, W.J., Prince, L.M. & Williams, K.J. 2002. The phylogeny and a new classification of the gingers (Zingiberaceae): Evidence from molecular data. American Journal of Botany, 89(10): 1682-1696. DOI: https://doi.org/10.3732/ajb.89.10.1682

Lazarowitz, S.G., Pinder, A.J., Damsteegt, V.D. & Rogers, S.G. 1989. Maize streak virus genes essential for systemic spread and symptom development. The EMBO Journal, 8(4): 1023-1032. DOI: https://doi.org/10.1002/j.1460-2075.1989.tb03469.x

Lee, C.H., Zheng, Y.X., Chan, C.H., Ku, H.M., Chang, C.J. & Jan, F.J. 2020. A single amino acid substitution in the movement protein enables the mechanical transmission of a geminivirus. Molecular Plant Pathology, 21(4): 571-588. DOI: https://doi.org/10.1111/mpp.12917

Liu, H., Boulton, M.I. & Davies, J.W. 1997. Maize streak virus coat protein binds single-and double-stranded DNA in vitro. Journal of General Virology, 78(6): 1265-1270. DOI: https://doi.org/10.1099/0022-1317-78-6-1265

Lozano, G., Trenado, H.P., Fiallo-Olivé, E., Chirinos, D., Geraud-Pouey, F., Briddon, R.W. & Navas-Castillo, J. 2016. Characterization of non-coding DNA satellites associated with sweepoviruses (genus Begomovirus, Geminiviridae)-definition of a distinct class of begomovirus-associated satellites. Frontiers in Microbiology, 7: 162. DOI: https://doi.org/10.3389/fmicb.2016.00162

Macedo, M.A., Albuquerque, L.C., Maliano, M.R., Souza, J.O., Rojas, M.R., Inoue-Nagata, A.K. & Gilbertson, R.L. 2018. Characterization of tomato leaf curl purple vein virus, a new monopartite New World begomovirus infecting tomato in Northeast Brazil. Archives of Virology, 163: 737-743. DOI: https://doi.org/10.1007/s00705-017-3662-0

Materatski, P., Jones, S., Patanita, M., Campos, M.D., Dias, A.B., Félix, M.D.R. & Varanda, C.M. 2021. A bipartite geminivirus with a highly divergent genomic organization identified in olive trees may represent a novel evolutionary direction in the family Geminiviridae. Viruses, 13(10): 2035. DOI: https://doi.org/10.3390/v13102035

Mondal, D., Mandal, S., Shil, S., Sahana, N., Pandit, G.K. & Choudhury, A. 2019. Genome wide molecular evolution analysis of begomoviruses reveals unique diversification pattern in coat protein gene of old world and new world viruses. VirusDisease, 30(1): 74-83. DOI: https://doi.org/10.1007/s13337-019-00524-7

Nawaz-ul-Rehman, M.S. & Fauquet, C.M. 2009. Evolution of geminiviruses and their satellites. FEBS Letters, 583(12): 1825-1832. DOI: https://doi.org/10.1016/j.febslet.2009.05.045

Patel, G., Patel, K., Barat, S. & Jarullah, B. 2020. Distribution of TLCNDV in Gujarat. (Unpublished).

Qazi, J., Ilyas, M., Mansoor, S. & Briddon, R.W. 2007. Legume yellow mosaic viruses: Genetically isolated begomoviruses. Molecular Plant Pathology, 8(4): 343-348. DOI: https://doi.org/10.1111/j.1364-3703.2007.00402.x

Retes-Manjarrez, J.E., Hernández-Verdugo, S., López-Orona, C.A., Medina-López, R., Garzón-Tiznado, J.A. & Retes-Cázarez, J.E. 2019. Inheritance of resistance to Pepper huasteco yellow vein virus in Capsicum annuum L.. HortScience, 54(5): 783-786. DOI: https://doi.org/10.21273/HORTSCI13745-18

Rojas, M.R., Hagen, C., Lucas, W.J. & Gilbertson, R.L. 2005. Exploiting chinks in the plant's armor: Evolution and emergence of geminiviruses. Annual Review of Phytopathology, 43: 361-394. DOI: https://doi.org/10.1146/annurev.phyto.43.040204.135939

Roshan, P., Kulshreshtha, A., Kumar, S., Purohit, R. & Hallan, V. 2018. AV2 protein of tomato leaf curl Palampur virus promotes systemic necrosis in Nicotiana benthamiana and interacts with host Catalase2. Scientific Reports, 8(1): 1273. DOI: https://doi.org/10.1038/s41598-018-19292-3

Rouhibakhsh, A. & Malathi, V.G. 2005. Severe leaf curl disease of cowpea-a new disease of cowpea in northern India caused by Mungbean yellow mosaic India virus and a satellite DNA β. Plant Pathology, 54(2): 259-259. DOI: https://doi.org/10.1111/j.1365-3059.2005.01139.x

Ruhel, R. & Chakraborty, S. 2019. Multifunctional roles of geminivirus encoded replication initiator protein. VirusDisease, 30: 66-73. DOI: https://doi.org/10.1007/s13337-018-0458-0

Saitou, N. & Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4(4): 406-425.

Sanchez-Chavez, S., Regla-Marquez, C.F., Cardenas-Conejo, Z.E., Garcia-Rodriguez, D.A., Centeno-Leija, S., Serrano-Posada, H., Liñan-Rico, A., Partida-Palacios, B.L. & Cardenas-Conejo, Y. 2020. First report of begomoviruses infecting Cucumis sativus L. in North America and identification of a proposed new begomovirus species. PeerJ, 2020(7): 1-18. DOI: https://doi.org/10.7717/peerj.9245

Sattar, M.N., Ligthart, M. & Kvarnheden, A. 2019. Compatibility and interaction of begomoviruses and DNA-satellites causing leaf curl disease in Asia, Africa and Mediterranean Region. European Journal of Plant Pathology, 155: 111-124. DOI: https://doi.org/10.1007/s10658-019-01753-8

Saunders, K. & Stanley, J. 1995. Complementation of African cassava mosaic virus AC2 gene function in a mixed bipartite geminivirus infection. Journal of General Virology, 76(9): 2287-2292. DOI: https://doi.org/10.1099/0022-1317-76-9-2287

Saunders, K., Bedford, I.D. & Stanley, J. 2001. Pathogenicity of a natural recombinant associated with ageratum yellow vein disease: Implications for geminivirus evolution and disease aetiology. Virology, 282(1): 38-47. DOI: https://doi.org/10.1006/viro.2000.0832

Saunders, K., Briddon, R.W. & Stanley, J. 2008. Replication promiscuity of DNA-β satellites associated with monopartite begomoviruses; deletion mutagenesis of the Ageratum yellow vein virus DNA-β satellite localizes sequences involved in replication. Journal of General Virology, 89(12): 3165-3172. DOI: https://doi.org/10.1099/vir.0.2008/003848-0

Saunders, K., Salim, N., Mali, V.R., Malathi, V.G., Briddon, R., Markham, P.G. & Stanley, J. 2002. Characterisation of Sri Lankan cassava mosaic virus and Indian cassava mosaic virus: evidence for acquisition of a DNA-B component by a monopartite begomovirus. Virology, 293(1): 63-74. DOI: https://doi.org/10.1006/viro.2001.1251

Seal, S.E., VandenBosch, F. & Jeger, M.J. 2006. Factors influencing Begomovirus evolution and their increasing global significance: Implications for sustainable control. Critical Reviews in Plant Sciences, 25(1): 23-46. DOI: https://doi.org/10.1080/07352680500365257

Sivalingam, P.N., Malathi, V.G. & Varma, A. 2010. Molecular diversity of the DNA-β satellites associated with tomato leaf curl disease in India. Archives of Virology, 155: 757-764. DOI: https://doi.org/10.1007/s00705-010-0634-z

Snehi, S.K., Purvia, A.S., Parihar, S.S., Gupta, G., Singh, V. & Raj, S.K. 2017. Overview of begomovirus genomic organization and its impact. International Journal of Current Research, 9(11): 61368-61380.

Sohrab, S.S., Yasir, M. & El-Kafrawy, S.A. 2017. Begomovirus Infection on cucumber in Saudi Arabia. Plant OMICS, 10(1): 7-14. DOI: https://doi.org/10.21475/poj.10.01.17.281

Sung, Y.K. & Coutts, R.H. 1995. Mutational analysis of potato yellow mosaic geminivirus. Journal of General Virology, 76(7): 1773-1780. DOI: https://doi.org/10.1099/0022-1317-76-7-1773

Sunter, G., Hartitz, M.D., Hormuzdi, S.G., Brough, C.L. & Bisaro, D.M. 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(1): 69-77. DOI: https://doi.org/10.1016/0042-6822(90)90275-V

Tamura, K., Stecher, G. & Kumar, S. 2021. MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38(7): 3022-3027. DOI: https://doi.org/10.1093/molbev/msab120

Tao, X., Qing, L. & Zhou, X. 2004. Function of A-Rich region in DNAβ associated with tomato yellow leaf curl China virus. Chinese Science Bulletin, 49: 1490-1493. DOI: https://doi.org/10.1360/04wc0132

Torres-Herrera, S.I., Romero-Osorio, A., Moreno-Valenzuela, O., Pastor-Palacios, G., Cardenas-Conejo, Y., Ramírez-Prado, J.H., Riego-Ruiz, L., Minero-García, Y., Ambriz-Granados, S. & Argüello-Astorga, G.R. 2019. A lineage of begomoviruses encode Rep and AC4 proteins of enigmatic ancestry: Hints on the evolution of geminiviruses in the New World. Viruses, 11(7): 644. DOI: https://doi.org/10.3390/v11070644

Venkataravanappa, V., Reddy, C.L., Shankarappa, K.S. & Reddy, M.K. 2019. Association of Tomato leaf curl New Delhi virus, betasatellite, and alphasatellite with mosaic disease of spine gourd (Momordica dioica Roxb. Willd) in India. Iranian Journal of Biotechnology, 17(1): e2134. DOI: https://doi.org/10.21859/ijb.2134

Wu, H., Liu, M., Kang, B., Liu, L., Hong, N., Peng, B. & Gu, Q. 2022. AC5 protein encoded by squash leaf curl China virus is an RNA silencing suppressor and a virulence determinant. Frontiers in Microbiology, 13: 980147. DOI: https://doi.org/10.3389/fmicb.2022.980147

Zaidi, S.S.E.A., Martin, D.P., Amin, I., Farooq, M. & Mansoor, S. 2017. Tomato leaf curl New Delhi virus: A widespread bipartite begomovirus in the territory of monopartite begomoviruses. Molecular Plant Pathology, 18(7): 901-911. DOI: https://doi.org/10.1111/mpp.12481

Zerbini, F.M., Briddon, R.W., Idris, A., Martin, D.P., Moriones, E., Navas-Castillo, J., Rivera-Bustamante, R., Roumagnac, P. & Varsani, A. 2017. ICTV virus taxonomy profile: Geminiviridae. Journal of General Virology, 98(2): 131-133. DOI: https://doi.org/10.1099/jgv.0.000738

Zhou, X. 2013. Advances in understanding begomovirus satellites. Annual Review of Phytopathology, 51: 357-381. DOI: https://doi.org/10.1146/annurev-phyto-082712-102234

Published

30-06-2024

How to Cite

Goundar, S. P. ., Ramani, S. ., Mohd Radzi, N. ., Abu Bakar, M. F. ., & Nur Fatihah, H. N. (2024). Molecular Detection and Identification of Begomovirus Infecting Cucumber (Cucumis sativus) in Terengganu, Malaysia. Malaysian Applied Biology, 53(2), 81–92. https://doi.org/10.55230/mabjournal.v53i2.2798

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