Molecular Characterization of a Bipartite Begomovirus and an Alphasatellite Associated with Leaf Curl and Mosaic Disease of Bitter Gourd in Punjab
PLANT CELL BIOTECHNOLOGY AND MOLECULAR BIOLOGY, Volume 24, Issue 1-2,
Page 52-63
DOI:
10.56557/pcbmb/2023/v24i1-28188
Abstract
Bitter gourd (Momordica charantia) is an economically important vegetable and medicinal plant that gets infected by a number of viruses. A survey was conducted in and around Jalandhar region of Punjab, India to study viral symptoms in the bitter gourd fields. The plants showed reduced fruit size, upward leaf curling and mosaic symptoms, indicating begomovirus infection. DNA was isolated from the symptomatic leaves and tested for begomovirus infection using group-specific PCR primers. Amplified products were cloned into pMD20-T vector and sequenced. Based on the obtained sequence, new sets of primers were designed and used for amplification of complete DNA-A and DNA-B. Complete DNA-A and DNA-B were cloned in pMD20-T and sequenced. Sequence analysis of the present DNA-A and DNA-B showed their highest identity with Tomato leaf curl New Delhi virus (ToLCNDV). The associated Tomato leaf curl New Delhi alphasatellite was amplified using universal primers, cloned and sequenced. In phylogenetic analysis, the present DNA-A and DNA-B grouped with ToLCNDV isolates and other begomoviruses reported from bitter gourd. Phylogenetic analysis of the present alphasatellite showed its closet identity with Tomato leaf curl New Delhi alphasatellite. Recombination analysis of the DNA-A sequence showed that the present bitter gourd isolate might be a recombinant of Squash leaf curl China virus (SLCChV) as a major parent and Chilli leaf curl virus as a minor parent. Analysis of the DNA-B suggested it to be a recombinant of SLCChV as a major parent and Chyaote enation yellow mosaic virus as a minor parent. The present alphasatellite might be a recombinant of Tomato yellow spot alphasatellite as a major parent and Croton yellow mosaic alphasatellite as a minor parent. The percent identities of the nucleotide and amino acid sequences validate and support the results of the phylogenetic and recombination analyses.
Keywords:
- Bitter gourd
- begomovirus
- tomato leaf curl new delhi virus
- bemisia tabaci
- phylogeny
- recombination
How to Cite
Lager, P., Sharma, J., & Kumar, Y. (2023). Molecular Characterization of a Bipartite Begomovirus and an Alphasatellite Associated with Leaf Curl and Mosaic Disease of Bitter Gourd in Punjab. PLANT CELL BIOTECHNOLOGY AND MOLECULAR BIOLOGY, 24(1-2), 52–63. https://doi.org/10.56557/pcbmb/2023/v24i1-28188
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Kubola J, Siriamornpun S. Phenolic contents and antioxidant activities of bitter gourd (Momordica charantia L.) leaf, stem and fruit fraction extracts In vitro. Food Chem. 2008;110(4):881-90.
Efrid JT, Choi YM, Davies SW, Mehra S, Anderson EJ, Katunga LA. Potential for improved glycemic control with dietary Momordica charantia in patients with insulin resistance and pre-diabetes. Int J Environ Res Public Health. 2014;11(2): 2328-2345.
Mahwish, Saeed F, Arshad MS, Nisa MU, Nadeem MT, Arshad MU. Hypoglycemic and hypolipidemic effects of different parts and formulations of bitter gourd (Momordica charantia). Lipids Health Dis. 2017;16(1):211.
Moffat AS. Geminiviruses emerge as serious crop threat. Science. 1999; 286(5446):1835.
Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Roumagnac P, Varsani A. ICTV Virus Taxonomy Profile: Geminiviridae. J Gen Virol. 2017; 98(2):131-133.
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Fiallo-Olivé E, Navas-Castillo J. Begomoviruses: what is the secret(s) of their success? Trends Plant Sci. 2023;S1360-1385(23):00032-8.
Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, Dhawan P, Rishi N, Siwatch SS, Abdel-Salam AM, Brown JK, Zafar Y, Markham PG. Diversity of DNA beta, a satellite molecule associated with some monopartite begomoviruses. Virology.2003;312(1):106-21.
Kikuno R, Toh H, Hayashida H, Miyata T. Sequence similarity between putative gene productsof geminiviral DNAs. Nature. 1984;308(5959):562.
Padidam M, Beachy RN, Fauquet CM. Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol. 1995;76(1):25-35.
Gomathi Devi R, Jothika C, Sankari A, Lakshmi S, Malathi VG, Renukadevi P. Seed Transmission of Begomoviruses: A Potential Threat for Bitter Gourd Cultivation. Plants (Basel). 2023;12(6): 1396.
Kiran GVNSM, Nagaraju N, Girish TR, Ashwini BN. Molecular investigations reveal bitter gourd crop is more susceptible to Tomato leaf curl New Delhi virus infection in diverse crop cultivation practices. 3 Biotech. 2021;11(12):500.
Qureshi MA, Lal A, Nawaz-Ul-Rehman MS, Vo TTB, Sanjaya GNPW, Ho PT, Nattanong B, Kil EJ, Jahan SMH, Lee KY, Tsai CW, Dao HT, Hoat TX, Aye TT, Win NK, Lee J, Kim SM, Lee S. Emergence of Asian endemic begomoviruses as a pandemic threat. with some monopartite begomoviruses. Virology. 2003;312(1): 106-21.
Varma A, Malathi VG. Emerging geminivirus problems. A serious threat to crop production. Ann Appl Biol. 2005; 142(2):145-164.
Janssen D, Simón A, Boulares M, Ruiz L. Host Species-Dependent Transmission of Tomato Leaf Curl New Delhi Virus-ES by Bemisia tabaci. Plants (Basel). 2022; 11(3):390.
Kil EJ, Vo TTB, Fadhila C, Ho PH, Lal A, Troiano E, Parrella G, Lee S. Seed Transmission of Tomato Leaf Curl New Delhi Virus from Zucchini Squash in Italy. Plants. 2020;9(5):563.
Nagendran K, Kumar SM, Manoranjitham SK, Karthikeyan G. Molecular detection and characterization of Tomato Leaf Curl New Delhi Virus causing mosaic disease on Bitter Gourd in Tamil Nadu, India. Trends in Biosciences. 2014;7(23):3925-3931.
Tahir M, Haider MS. First report of Tomato leaf curl New Delhi virus infecting bitter gourd in Pakistan. Plant Pathology. 2005;54(6):807.
Rojas MR, Gilbertson RL, Russell DR, Maxwell DP. Use of degenerate primers in the Polymerase Chain Reaction to detect whitefly-transmitted Geminiviruses. Plant Dis. 1993;77:340-347.
Bull SE, Briddon RW, Markham PG. Universal primers for the PCR-mediated amplification of DNA 1: A satellite-like molecule associated with begomovirus-DNA β complexes. Mol Biotechnol. 2003;23:83-86.
Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG. Universal primers for the PCR-mediated amplification of DNA beta: a molecule associated with some monopartite begomoviruses. Mol Biotechnol. 2002;20(3):315-8.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary GeneticsAnalysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-1549.
Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406-425.
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-80.
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015;1(1):vev003. DOI: 10.1093/ve/vev003
Zaidi SS, Martin DP, Amin I, Farooq M, Mansoor S. Tomato leaf curl New Delhi virus: A widespread bipartite begomovirus in the territory of monopartite begomoviruses. Mol Plant Pathol. 2017; 18(7):901-911.
Roberts S, Stanley J. Lethal mutations within the conserved stem–loop of African cassava mosaic virus DNA are rapidly corrected by genomic recombination. J Gen Virol. 1994;75(11):3203-9.
Kikuno R, Toh H, Hayashida H, Miyata T. Sequence similarity between putative gene products of geminiviral DNAs. Nature. 1984;308(5959):562.
Padidam M, Beachy RN, Fauquet CM. Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol. 1995;76(1):25-35.
Fortes IM, Sanchez-Campos S, Fiallo-Olive E, Diaz-Pendon JA, Navas-Castillo J, Moriones E. A novel strain of tomato leaf curl new delhi virus has spread to the mediterranean basin. Viruses. 2016; 8(11):307.
Moriones E, Praveen S, Chakraborty S. tomato leaf curl New Delhi virus: An emerging virus complex threatening vegetable and fiber crops. Viruses. 2017;9(10):264.
Zaidi SS, Martin DP, Amin I, Farooq M, Mansoor S. Tomato leaf curl New Delhi virus: A widespread bipartite begomovirus in the territory of monopartite begomoviruses. Mol Plant Pathol. 2017;18(7):901-911.
Mubin M, Ijaz S, Nahid N, Hassan M, Younus A, Qazi J, Nawaz-Ul-Rehman MS. Journey of begomovirus betasatellite molecules: From satellites to indispensable partners. Virus Genes. 2020;56(1):16-26.
Castillo-Urquiza GP, Beserra Jr JEA, Bruckner FP, Lima ATM, Varsani A, Alfenas-Zerbini P, Zerbini FM. Six novel begomoviruses infecting tomato and associated weeds in Southeastern Brazil. Arch. Virol. 2008;153(10):1985-9.
da Silva SJC, Castillo-Urquiza GP, Hora Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM. High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in northeastern Brazil. Arch. Virol. 2011;156(12):2205-2213.
Ooi K, Ohshita S, Ishii I, Yahara T. Molecular phylogeny of geminivirus infecting wild plants in Japan. Journal of Plant Research. 1997;110:247-257.
Luis-Arteaga M, Alvarez JM, Alonso-Prados JL, Bernal JJ, Garcia- Arenal F, Lavina A, Batlle A, Moriones E. Occurrence, distribution, and relative incidence of mosaic viruses infecting field-grown melon in Spain. Plant Dis. 1998;82(9):979-982.
García-Andrés S, Accotto GP, Navas-Castillo J, Moriones E. Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the Tomato yellow leaf curl disease in the Mediterranean basin. Virology. 2007;359:302-312.
Ferro CG, Silva JP, Xavier CAD, Godinho MT, Lima ATM, Mar TB, Lau D, Zerbini FM. The ever increasing diversity of begomoviruses infecting non-cultivated hosts: new species from Sida spp. and Leonurus sibiricus, plus two New World alphasatellites. Ann Appl Biol. 2017; 170:204-218.
Yao FL, Zheng Y, Huang XY, Ding XL, Zhao JW, Desneux N, He YX, Weng QY. Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005-2014. Sci Rep. 2017; 7:40803.
Palumbo JC, Horowitz AR, Prabhaker N. Insecticidal control and resistance management for Bemisia tabaci. Crop Prot. 2001;20(9):739-765.
Grávalos C, Fernández E, Belando A, Moreno I, Ros C, Bielza P. Cross-resistance and baseline susceptibility of Mediterranean strains of Bemisia tabaci to cyantraniliprole. Pest Manag Sci. 2015; 71:1030-1036.
Raman A, Lau C. Anti-diabetic properties and phytochemistry of Momordica charantia L. Phytomedicine. 1996; 2(4):349-362.
Kubola J, Siriamornpun S. Phenolic contents and antioxidant activities of bitter gourd (Momordica charantia L.) leaf, stem and fruit fraction extracts In vitro. Food Chem. 2008;110(4):881-90.
Efrid JT, Choi YM, Davies SW, Mehra S, Anderson EJ, Katunga LA. Potential for improved glycemic control with dietary Momordica charantia in patients with insulin resistance and pre-diabetes. Int J Environ Res Public Health. 2014;11(2): 2328-2345.
Mahwish, Saeed F, Arshad MS, Nisa MU, Nadeem MT, Arshad MU. Hypoglycemic and hypolipidemic effects of different parts and formulations of bitter gourd (Momordica charantia). Lipids Health Dis. 2017;16(1):211.
Moffat AS. Geminiviruses emerge as serious crop threat. Science. 1999; 286(5446):1835.
Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E, Navas-Castillo J, Rivera-Bustamante R, Roumagnac P, Varsani A. ICTV Virus Taxonomy Profile: Geminiviridae. J Gen Virol. 2017; 98(2):131-133.
Walker PJ, Siddell SG, Lefkowitz EJ, Mushegian AR, Adriaenssens EM, Dempsey DM, Dutilh BE, Harrach B, Harrison RL, Hendrickson RC, Junglen S, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Nibert M, Orton RJ, Rubino L, Sabanadzovic S, Simmonds P, Smith DB, Varsani A, Zerbini FM, Davison AJ. Changes to virus taxonomy and the Statutes ratified by the International Committee on Taxonomy of Viruses Arch Virol. 2020;165(11):2737-2748.
Fiallo-Olivé E, Navas-Castillo J. Begomoviruses: what is the secret(s) of their success? Trends Plant Sci. 2023;S1360-1385(23):00032-8.
Briddon RW, Bull SE, Amin I, Idris AM, Mansoor S, Bedford ID, Dhawan P, Rishi N, Siwatch SS, Abdel-Salam AM, Brown JK, Zafar Y, Markham PG. Diversity of DNA beta, a satellite molecule associated with some monopartite begomoviruses. Virology.2003;312(1):106-21.
Kikuno R, Toh H, Hayashida H, Miyata T. Sequence similarity between putative gene productsof geminiviral DNAs. Nature. 1984;308(5959):562.
Padidam M, Beachy RN, Fauquet CM. Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol. 1995;76(1):25-35.
Gomathi Devi R, Jothika C, Sankari A, Lakshmi S, Malathi VG, Renukadevi P. Seed Transmission of Begomoviruses: A Potential Threat for Bitter Gourd Cultivation. Plants (Basel). 2023;12(6): 1396.
Kiran GVNSM, Nagaraju N, Girish TR, Ashwini BN. Molecular investigations reveal bitter gourd crop is more susceptible to Tomato leaf curl New Delhi virus infection in diverse crop cultivation practices. 3 Biotech. 2021;11(12):500.
Qureshi MA, Lal A, Nawaz-Ul-Rehman MS, Vo TTB, Sanjaya GNPW, Ho PT, Nattanong B, Kil EJ, Jahan SMH, Lee KY, Tsai CW, Dao HT, Hoat TX, Aye TT, Win NK, Lee J, Kim SM, Lee S. Emergence of Asian endemic begomoviruses as a pandemic threat. with some monopartite begomoviruses. Virology. 2003;312(1): 106-21.
Varma A, Malathi VG. Emerging geminivirus problems. A serious threat to crop production. Ann Appl Biol. 2005; 142(2):145-164.
Janssen D, Simón A, Boulares M, Ruiz L. Host Species-Dependent Transmission of Tomato Leaf Curl New Delhi Virus-ES by Bemisia tabaci. Plants (Basel). 2022; 11(3):390.
Kil EJ, Vo TTB, Fadhila C, Ho PH, Lal A, Troiano E, Parrella G, Lee S. Seed Transmission of Tomato Leaf Curl New Delhi Virus from Zucchini Squash in Italy. Plants. 2020;9(5):563.
Nagendran K, Kumar SM, Manoranjitham SK, Karthikeyan G. Molecular detection and characterization of Tomato Leaf Curl New Delhi Virus causing mosaic disease on Bitter Gourd in Tamil Nadu, India. Trends in Biosciences. 2014;7(23):3925-3931.
Tahir M, Haider MS. First report of Tomato leaf curl New Delhi virus infecting bitter gourd in Pakistan. Plant Pathology. 2005;54(6):807.
Rojas MR, Gilbertson RL, Russell DR, Maxwell DP. Use of degenerate primers in the Polymerase Chain Reaction to detect whitefly-transmitted Geminiviruses. Plant Dis. 1993;77:340-347.
Bull SE, Briddon RW, Markham PG. Universal primers for the PCR-mediated amplification of DNA 1: A satellite-like molecule associated with begomovirus-DNA β complexes. Mol Biotechnol. 2003;23:83-86.
Briddon RW, Bull SE, Mansoor S, Amin I, Markham PG. Universal primers for the PCR-mediated amplification of DNA beta: a molecule associated with some monopartite begomoviruses. Mol Biotechnol. 2002;20(3):315-8.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403-410.
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary GeneticsAnalysis across computing platforms. Mol Biol Evol. 2018;35(6):1547-1549.
Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406-425.
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-80.
Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015;1(1):vev003. DOI: 10.1093/ve/vev003
Zaidi SS, Martin DP, Amin I, Farooq M, Mansoor S. Tomato leaf curl New Delhi virus: A widespread bipartite begomovirus in the territory of monopartite begomoviruses. Mol Plant Pathol. 2017; 18(7):901-911.
Roberts S, Stanley J. Lethal mutations within the conserved stem–loop of African cassava mosaic virus DNA are rapidly corrected by genomic recombination. J Gen Virol. 1994;75(11):3203-9.
Kikuno R, Toh H, Hayashida H, Miyata T. Sequence similarity between putative gene products of geminiviral DNAs. Nature. 1984;308(5959):562.
Padidam M, Beachy RN, Fauquet CM. Tomato leaf curl geminivirus from India has a bipartite genome and coat protein is not essential for infectivity. J Gen Virol. 1995;76(1):25-35.
Fortes IM, Sanchez-Campos S, Fiallo-Olive E, Diaz-Pendon JA, Navas-Castillo J, Moriones E. A novel strain of tomato leaf curl new delhi virus has spread to the mediterranean basin. Viruses. 2016; 8(11):307.
Moriones E, Praveen S, Chakraborty S. tomato leaf curl New Delhi virus: An emerging virus complex threatening vegetable and fiber crops. Viruses. 2017;9(10):264.
Zaidi SS, Martin DP, Amin I, Farooq M, Mansoor S. Tomato leaf curl New Delhi virus: A widespread bipartite begomovirus in the territory of monopartite begomoviruses. Mol Plant Pathol. 2017;18(7):901-911.
Mubin M, Ijaz S, Nahid N, Hassan M, Younus A, Qazi J, Nawaz-Ul-Rehman MS. Journey of begomovirus betasatellite molecules: From satellites to indispensable partners. Virus Genes. 2020;56(1):16-26.
Castillo-Urquiza GP, Beserra Jr JEA, Bruckner FP, Lima ATM, Varsani A, Alfenas-Zerbini P, Zerbini FM. Six novel begomoviruses infecting tomato and associated weeds in Southeastern Brazil. Arch. Virol. 2008;153(10):1985-9.
da Silva SJC, Castillo-Urquiza GP, Hora Júnior BT, Assunção IP, Lima GSA, Pio-Ribeiro G, Mizubuti ESG, Zerbini FM. High genetic variability and recombination in a begomovirus population infecting the ubiquitous weed Cleome affinis in northeastern Brazil. Arch. Virol. 2011;156(12):2205-2213.
Ooi K, Ohshita S, Ishii I, Yahara T. Molecular phylogeny of geminivirus infecting wild plants in Japan. Journal of Plant Research. 1997;110:247-257.
Luis-Arteaga M, Alvarez JM, Alonso-Prados JL, Bernal JJ, Garcia- Arenal F, Lavina A, Batlle A, Moriones E. Occurrence, distribution, and relative incidence of mosaic viruses infecting field-grown melon in Spain. Plant Dis. 1998;82(9):979-982.
García-Andrés S, Accotto GP, Navas-Castillo J, Moriones E. Founder effect, plant host, and recombination shape the emergent population of begomoviruses that cause the Tomato yellow leaf curl disease in the Mediterranean basin. Virology. 2007;359:302-312.
Ferro CG, Silva JP, Xavier CAD, Godinho MT, Lima ATM, Mar TB, Lau D, Zerbini FM. The ever increasing diversity of begomoviruses infecting non-cultivated hosts: new species from Sida spp. and Leonurus sibiricus, plus two New World alphasatellites. Ann Appl Biol. 2017; 170:204-218.
Yao FL, Zheng Y, Huang XY, Ding XL, Zhao JW, Desneux N, He YX, Weng QY. Dynamics of Bemisia tabaci biotypes and insecticide resistance in Fujian province in China during 2005-2014. Sci Rep. 2017; 7:40803.
Palumbo JC, Horowitz AR, Prabhaker N. Insecticidal control and resistance management for Bemisia tabaci. Crop Prot. 2001;20(9):739-765.
Grávalos C, Fernández E, Belando A, Moreno I, Ros C, Bielza P. Cross-resistance and baseline susceptibility of Mediterranean strains of Bemisia tabaci to cyantraniliprole. Pest Manag Sci. 2015; 71:1030-1036.
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