Identification and molecular analysis of watermelon chlorotic stunt virus infecting snake gourd in Saudi Arabia
DOI:
https://doi.org/10.15835/nbha52313857Keywords:
agroinoculation, bipartite begomovirus, Nicotiana benthamiana, snake gourd, WmCSVAbstract
Snake gourd (Trichosanthes cucumerina) plants exhibiting typical begomovirus-like symptoms of stunted growth, leaf yellowing and mottling were observed at an open field in the Eastern region of Saudi Arabia. Sequencing analysis of the amplified complete DNA molecules revealed that the plants were infected with watermelon chlorotic stunt virus (WmCSV), which is a bipartite begomovirus prevalent mostly in the Old World and a serious threat to cucurbit production in the Arabian Peninsula, Middle East and Africa. The two WmCSV DNA-A isolates (SG31A and SG52A) were 98.9% identical and showed their highest nucleotide (nt) sequence identities (98.7%) with the isolates from Iran and Saudi Arabia. The DNA-B isolates (SG31B and SG52B), on the other hand, were 97.4% identical and exhibited their highest nt sequence identities (99.5 and 97%) with isolates reported from Iran and Oman. In the phylogenetic dendrograms the identified isolates clustered closely with previously reported WmCSV isolates from Iran and Saudi Arabia. Infectivity assays revealed that the DNA-A components alone could not induce infection in Nicotiana benthamiana plants however, together with DNA-B these isolates successfully caused typical begomovirus symptoms and both components were detected successfully using Southern blot hybridization. This study highlights the importance of conducting extensive future begomovirus surveillance to detect spillover events that could threaten native vegetable production in Saudi Arabia. This is crucial as begomoviruses pose a serious threat to vegetable cultivation throughout the Middle East.
References
Abudy A, Sufrin-Ringwald T, Dayan-Glick C, Guenoune-Gelbart D, Livneh O, Zaccai M, Lapidot M (2010). Watermelon chlorotic stunt and Squash leaf curl begomoviruses-New threats to cucurbit crops in the Middle East. Israel Journal of Plant Sciences 58(1):33-42. https://doi.org/10.1560/IJPS.58.1.33
Al-Musa A, Anfoka G, Al-Abdulat A, Misbeh S, Ahmed FH, Otri I (2011). Watermelon chlorotic stunt virus (WmCSV): a serious disease threatening watermelon production in Jordan. Virus Genes 43(1):79-89. https://doi.org/10.1007/s11262-011-0594-8.
Al-Saleh M, Ahmad M, Al-Shahwan I, Brown JK, Idris A (2014). First report of watermelon chlorotic stunt virus infecting watermelon in Saudi Arabia. Plant Disease 98(10):1451-1451. https://doi.org/10.1094/PDIS-06-14-0583-PDN
Alhubaishi A, Walkey D, Webb M, Bolland C, Cook A (1987). A survey of horticultural plant virus diseases in the Yemen Arab Republic. FAO Plant Protection Bulletin 35(4):135-143.
AlHudaib KA, Almaghasla MI, El-Ganainy SM, Arshad M, Drou N, Sattar MN (2022). High-throughput sequencing identified distinct bipartite and monopartite begomovirus variants associated with DNA-satellites from tomato and muskmelon plants in Saudi Arabia. Plants (Basel) 12(1):6. https://doi.org/10.3390/plants12010006
Alhudaib KA, Rezk AA, Soliman AM (2018). Current status of watermelon chlorotic stunt virus (WmCSV) on some cucurbit plants (Cucurbitaceae) in Alahsa region of Saudi Arabia. Scientific Journal of King Faisal University 19(2).
Ali-Shtayeh MS, Jamous RM, Mallah OB, Abu-Zeitoun SY (2014). Molecular characterization of watermelon chlorotic stunt virus (WmCSV) from Palestine. Viruses-Basel 6(6): 2444-2462. https://doi.org/10.3390/v6062444
Ashraf MA, Shahid AA, Rao AQ, Bajwa KS, Husnain T (2014). Functional characterization of a bidirectional plant promoter from cotton leaf curl burewala virus using an agrobacterium-mediated transient assay. Viruses 6(1): 223-242. https://doi.org/10.3390/v6010223
Briddon RW, Bull SE, Mansoor S, Amin I, Markham P (2002). Universal primers for the PCR-mediated amplification of DNA β. Molecular Biotechnology 20(3):315-318.
Briddon RW, Martin DP, Roumagnac P, Navas-Castillo J, Fiallo-Olive E, Moriones E, … Varsani A (2018). Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Archives of Virology 163(9):2587-2600. https://doi.org/10.1007/s00705-018-3854-2.
Briddon RW, Patil BL, Bagewadi B, Nawaz-ul-Rehman MS, Fauquet CM (2010). Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses. BMC Evolutionary Biology 10:97. https://doi.org/10.1186/1471-2148-10-97.
Brown JK, Zerbini FM, Navas-Castillo J, Moriones E, Ramos-Sobrinho R, Silva JC, . . . Idris A (2015). Revision of Begomovirus taxonomy based on pairwise sequence comparisons. Springer.
Bull S, Briddon R, Markham P (2003). Universal primers for the PCR-mediated amplification of DNA 1: a satellite-like molecule associated with begomovirus-DNA β complexes. Molecular Biotechnology 23(1):83-86.
Dominguez-Duran G, Rodriguez-Negrete EA, Morales-Aguilar JJ, Camacho-Beltran E, Romero-Romero JL, Rivera-Acosta MA, . . . Mendez-Lozano J (2018). Molecular and biological characterization of watermelon chlorotic stunt virus (WmCSV): An Eastern Hemisphere begomovirus introduced in the Western Hemisphere. Crop Protection 103:51-55. https://doi.org/10.1016/j.cropro.2017.09.006.
Doyle JJ, Doyle JL, Hortoriun LB (1990). Isolation of plant DNA from fresh tissue. Focus 12:13-15.
Esmaeili M, Heydarnejad J, Massumi H, Varsani A (2015). Analysis of watermelon chlorotic stunt virus and tomato leaf curl Palampur virus mixed and pseudo-recombination infections. Virus Genes 51(3):408-416. https://doi.org/10.1007/s11262-015-1250-5.
Fiallo-Olivé E, Navas-Castillo J (2020). Molecular and biological characterization of a New World monobipartite begomovirus/deltasatellite complex infecting Corchorus siliquosus. Frontiers in Microbiology 1755. https://doi.org/10.3389/fmicb.2020.01755
Fondong VN (2013). Geminivirus protein structure and function. Molecular Plant Pathology 14(6):635-649. https://doi.org/10.1111/mpp.12032.
Fontenele RS, Bhaskara A, Cobb IN, Majure LC, Salywon AM, Avalos-Calleros JA, . . . Ribeiro SG (2021). Identification of the begomoviruses squash leaf curl virus and watermelon chlorotic stunt virus in various plant samples in North America. Viruses 13(5):810. https://doi.org/10.3390/v13050810
Gong P, Tan H, Zhao S, Li H, Liu H, Ma Y, . . . Zhou X (2021). Geminiviruses encode additional small proteins with specific subcellular localizations and virulence function. Nature Communications 12(1):4278. https://doi.org/10.1038/s41467-021-24617-4.
Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013). Geminiviruses: masters at redirecting and reprogramming plant processes. Nature Reviews Microbiology 11(11):777-788. https://doi.org/10.1038/nrmicro3117
Iqbal Z, Sattar MN, Kvarnheden A, Mansoor S, Briddon RW (2012). Effects of the mutation of selected genes of cotton leaf curl Kokhran virus on infectivity, symptoms and the maintenance of cotton leaf curl Multan betasatellite. Virus Research 169(1): 107-116. https://doi.org/10.1016/j.virusres.2012.07.016.
Iqbal Z, Shafiq M, Ali I, Mansoor S, Briddon RW (2017). Maintenance of cotton leaf curl multan betasatellite by tomato leaf curl New Delhi virus-analysis by mutation. Frontiers in Plant Science 8:2208. https://doi.org/ARTN220810.3389/fpls.2017.02208.
Just K, Arif U, Luik A, Kvarnheden A (2017). Monitoring infection of tomato fruit by tomato yellow leaf curl virus. Plant Pathology 66(4):522-528. https://doi.org/10.1111/ppa.12596.
Khan AJ, Akhtar S, Briddon RW, Ammara U, Al-Matrooshi AM, Mansoor S (2012). Complete nucleotide sequence of watermelon chlorotic stunt virus originating from Oman. Viruses 4(7):1169-1181. https://doi.org/10.3390/v4071169.
Kheyr-Pour A, Bananej K, Dafalla GA, Caciagli P, Noris E, Ahoonmanesh A, . . . Gronenborn B (2000). Watermelon chlorotic stunt virus from the Sudan and Iran: Sequence comparisons and identification of a whitefly-transmission determinant. Phytopathology 90(6):629-635. https://doi.org/10.1094/Phyto.2000.90.6.629.
Leke WN, Sattar MN, Ngane EB, Ngeve JM, Kvarnheden A, Brown JK (2013). Molecular characterization of begomoviruses and DNA satellites associated with okra leaf curl disease in Cameroon. Virus Research 174(1-2):116-125. https://doi.org/10.1016/j.virusres.2013.03.010.
Liu H, Chang Z, Zhao S, Gong P, Zhang M, Lozano-Duran R, . . . Li F (2023). Functional identification of a novel C7 protein of tomato yellow leaf curl virus. Virology 585:117-126. https://doi.org/10.1016/j.virol.2023.05.011.
Muhire B, Martin DP, Brown JK, Navas-Castillo J, Moriones E, Zerbini FM, . . . Varsani A (2013). A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Archives of Virology 158(6):1411-1424. https://doi.org/10.1007/s00705-012-1601-7.
Qurashi F, Sattar M, Iqbal Z, Haider M (2017). First report of cherry tomato leaf curl virus and associated DNA satellites infesting an invasive weed in Pakistan. Journal of Plant Pathology 99(1):267-272. http://dx.doi.org/10.4454/jpp.v99i1.3818.s12
Ranjan P, Singh AK, Kumar RV, Basu S, Chakraborty S (2014). Host-specific adaptation of diverse betasatellites associated with distinct Indian tomato-infecting begomoviruses. Virus Genes 48(2):334-342. https://doi.org/10.1007/s11262-013-1031-y.
Rezk AA, Sattar MN, Alhudaib KA, Soliman AM (2019). Identification of watermelon chlorotic stunt virus from watermelon and zucchini in Saudi Arabia. Canadian Journal of Plant Pathology 41(2):285-290. https://doi.org/10.1080/07060661.2019.1567590
Rojas MR, Macedo MA, Maliano MR, Soto-Aguilar M, Souza JO, Briddon RW, . . . Adkins S (2018). World management of geminiviruses. Annual Review of Phytopathology 56:637-677. https://doi.org/10.1146/annurev-phyto-080615-100327
Romay G, Geraud-Pouey F, Chirinos DT, Mahillon M, Gillis A, Mahillon J, Bragard C (2019). Tomato twisted leaf virus: a novel indigenous new world monopartite begomovirus infecting tomato in Venezuela. Viruses 11(4):327. https://doi.org/10.3390/v11040327.
Saeed F, Sattar MN, Hameed U, Ilyas M, Haider MS, Hamza M, . . . Amin I (2018). Infectivity of okra enation leaf curl virus and the role of its V2 protein in pathogenicity. Virus Research 255:90-94. https://doi.org/10.1016/j.virusres.2018.07.007.
Samsatly J, Sobh H, Jawhari M, Najjar C, Haidar A, Abou-Jawdah Y (2012). First report of watermelon chlorotic stunt virus in cucurbits in Lebanon. Plant Disease 96(11):1703-1703. https://doi.org/10.1094/PDIS-04-12-0366-PDN.
Sattar MN (2018). Partial characterization of watermelon chlorotic stunt virus from Trichosanthes cucumerina in Al-Ahsa, Saudi Arabia. Journal of Environmental and Agricultural Sciences 17:1-11.
Sattar MN, Iqbal Z, El-Ganainy SM, Alamer AA, Alhudaib KA (2021). In planta interaction and transreplication of distinct begomoviruses and their associated components. International Journal of Agriculture & Biology 26:45-51. http://dx.doi.org/10.17957/IJAB/15.1807
Sattar MN, Iqbal Z, Tahir MN, Ullah S (2017). The prediction of a new CLCuD epidemic in the Old World. Frontiers in Microbiology 8:631. https://doi.org/10.3389/fmicb.2017.00631.
Sattar MN, Kvarnheden A, Saeed M, Briddon RW (2013). Cotton leaf curl disease - an emerging threat to cotton production worldwide. Journal of General Virology 94(Pt 4):695-710. https://doi.org/10.1099/vir.0.049627-0.
Sattar MN, 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(1):111-124. https://doi.org/10.1007/s10658-019-01753-8.
Shafiq M, Sattar MN, Shahid MS, Al-Sadi AM, Briddon RW (2021). Interaction of watermelon chlorotic stunt virus with satellites. Australasian Plant Pathology 50(1):117-128. https://doi.org/10.1007/s13313-020-00757-x
Shahid MS, Sattar MN, Iqbal Z, Raza A, Al-Sadi AM (2021). Next-generation sequencing and the CRISPR-Cas nexus: A molecular plant virology perspective. Frontiers in Microbiology 11:609376. https://doi.org/10.3389/fmicb.2020.609376
Tamura K, Stecher G, Kumar S (2021). MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38(7):3022-3027. https://doi.org/10.1093/molbev/msab120.
Verma N, Dhatt AS, Sharma A, Garcha KS, Sharma M, Bhatia D, . . . Kaur B (2023). Genetics of begomovirus resistance in Cucurbita moschata Duchesne: a novel resistant source PVR-1343. Scientia Horticulturae 322:112393. http://dx.doi.org/10.1016/j.scienta.2023.112393
Wyatt S, Brown JK (1996). Detection of subgroup III geminivirus isolates in leaf extracts by degenerate primers and polymerase chain reaction. Phytopathology 86(12):1288-1293. https://doi.org/10.1094/Phyto-86-1288.
Xiao Y-X, Li D, Wu Y-J, Liu S-S, Pan L-L (2023). Constant ratio between the genomic components of bipartite begomoviruses during infection and transmission. Virology Journal 20(1):186. https://doi.org/10.1186/s12985-023-02148-2
Yang X, Guo W, Li F, Sunter G, Zhou X (2019). Geminivirus-associated betasatellites: exploiting chinks in the antiviral arsenal of plants. Trends in Plant Science 24(6):519-529. https://doi.org/10.1016/j.tplants.2019.03.010.
Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, . . . Consortium IR (2017). ICTV virus taxonomy profile: Geminiviridae. Journal of General Virology 98(2):131. https://doi.org/10.1099/jgv.0.000738.
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