Vol. 65 No. 1 (2026)
Articles

Spatial distribution and molecular characterization of persistently aphid-transmitted viruses causing yellowing and stunting in faba bean and chickpea crops in Tunisia

PDF
  • Mghandef SAMIA,
  • Safaa KUMARI,
  • Abdulrahman MOUKAHEL,
  • Imen HAMDI,
  • Arvind VARSANI,
  • Asma NAJAR
Mghandef SAMIA
Institut National de la Recherche Agronomique de Tunisie (INRAT), Tunis, Tunisie
Safaa KUMARI
Seed Health/Virology Laboratory, International Center for Agricultural Research in the Dry Areas (ICARDA), Terbol Station, Zahle, Lebanon
Abdulrahman MOUKAHEL
Seed Health/Virology Laboratory, International Center for Agricultural Research in the Dry Areas (ICARDA), Terbol Station, Zahle, Lebanon
Imen HAMDI
Institut National de la Recherche Agronomique de Tunisie (INRAT), Tunis, Tunisie
Arvind VARSANI
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, Arizona, United States of America
Asma NAJAR
Institut National de la Recherche Agronomique de Tunisie (INRAT), Tunis, Tunisie
DOI: https://doi.org/10.36253/phyto-16680
Categories

Published 2026-05-14

Keywords

  • CpCSV,
  • BWYV,
  • BLRV,
  • mixed infections,
  • sequencing,
  • phylogenetic analysis
    • ...More
    Less

How to Cite

[1]
M. SAMIA, S. KUMARI, A. MOUKAHEL, I. HAMDI, A. VARSANI, and A. NAJAR, “Spatial distribution and molecular characterization of persistently aphid-transmitted viruses causing yellowing and stunting in faba bean and chickpea crops in Tunisia”, Phytopathol. Mediterr., vol. 65, no. 1, pp. 165–184, May 2026.

Copyright (c) 2026 Mghandef SAMIA, Safaa KUMARI, Abdulrahman MOUKAHEL, Imen HAMDI, Arvind VARSANI, Asma NAJAR

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Field surveys were conducted in the northeastern and northwestern regions of Tunisia between 2013/2014 and 2018/2019 growing seasons to identify viruses that infect faba bean and chickpea crops. Field observations showed that 18.8% of the faba bean and 21.0% of the chickpea fields surveyed had virus-like symptoms. These rates exceeded 20% during the growing seasons from 2013/2014 to 2018/2019, and were most common in the 2014/2015 growing season (28.6% of surveyed faba bean fields and 37.5% of chickpea fields showed virus-like symptoms in more than 20%). Totals of 1,538 faba bean and 1,511 chickpea plant samples showing yellowing and stunting symptoms were collected from 144 faba bean and 124 chickpea fields, . All collected samples were tested by tissue blot immunoassay (TBIA) using six monoclonal antibodies. These results showed that chickpea chlorotic stunt virus (CpCSV; Polerovirus CPCSV) was the most prevalent in faba bean and chickpea, with incidences of 20.2% and 37.6%, respectively, followed by beet western yellows virus (BWYV; Polerovirus BWYV) (13.5 and 9.7%), bean leafroll virus (BLRV; Luteovirus phaseoli) (3.7 and 3.3%), and faba bean necrotic yellows virus (FBNYV; Nanovirus necroflaviviciae) detected only in faba bean (6.6% of faba bean samples tested). In addition, TBIA results indicated that single virus infections were more prevalent than mixed infections in both crops. Mixed infections were predominantly co-infections involving viruses in Polerovirus (Solemoviridae), particularly CpCSV and BWYV (93% in faba bean and 69% in chickpea). Twenty-six samples that reacted positively with different monoclonal antibodies were assessed with reverse transcription-polymerase chain reaction (RT-PCR) using generic and specific primers followed by sequencing of the partial coat protein (CP) gene. The sequence analyses confirmed presence of CpCSV, BWYV, BLRV, brassica yellows virus (BrYV; Polerovirus TUYV), and turnip yellows virus (TuYV; Polerovirus TUYV). Comparative sequence analyses of the Tunisian isolates indicated that 13 CpCSV sequences had nucleotide sequence similarities of 95 to 99% with the reference isolate (EU541266) belonging to serotype I, and six BLRV isolates had similarities of 96 to 99% with BLRV reference isolate (PP333098). One sample (TuCp265-19) had a mixed infection with CpCSV and BLRV. Six isolates initially detected using BWYV-specific primers were sequenced and analyzed. BLASTn results showed that only three isolates were closely related (98 to 100%) to BWYV (OM419176), while the remaining four isolates were identified as Polerovirus TUYV and showed greatest similarity to BrYV (LC428361) and TuYV (OP699039), indicating co-occurrence of two distinct Polerovirus species within the analyzed samples. There is no information on the genetic variability of legume viruses in Tunisia, so this study shows that these viruses should be considered when developing disease management strategies to improve faba bean and chickpea production in Tunisia.

PDF

Downloads

Download data is not yet available.

References

  1. Abraham A.D., 2025. Virus diseases of economic importance on food legumes in Africa and their control. Viruses 17(12): 1555. https://doi.org/10.3390/v17121555
  2. Abraham A.D., Menzel W., Lesemann D.E., Varrelmann M., Vetten H.J., 2006. Chickpea chlorotic stunt virus: a new polerovirus infecting cool-season food legumes in Ethiopia. Phytopathology 96: 437–446. https://doi.org/10.1094/PHYTO-96-0437
  3. Abraham A.D., Menzel W., Varrelmann M., Vetten H.J., 2009. Molecular, serological and biological variation among chickpea chlorotic stunt virus isolates from five countries of North Africa and West Asia. Archives of virology 154: 791–799. https://doi.org/10.1007/s00705-009-0374-0
  4. Abraham A.D., Varrelmann M., Vetten H.J., 2008. Molecular evidence for the occurrence of two new luteoviruses in cool-season food legumes in northeast Africa. African Journal of Biotechnology 7(4): 414–420.
  5. Abraham A., Vetten H.J., 2022. Chickpea chlorotic stunt virus: a threat to cool-season food legumes. Archives of virology 167: 21–30. https://doi.org/10.1007/s00705-021-05288-4
  6. Ademe A., Kumari S.G., Moukahel A., Alemu T., Abraham A., … Kemal S.A., 2025. Phylogenetic analysis, mixed infection and seed transmission of Pea seed‑borne mosaic virus in Ethiopia. Physiological and Molecular Plant Pathology 136: 102531. https://doi.org/10.1016/j.pmpp.2024.102531
  7. Aguiar R.W.S., Alves G.B., Queiroz A.P., Nascimento I.R., Lima, M.F., 2018. Evaluation of weeds as virus reservoirs in watermelon crops. Planta Daninha 36. https://doi.org/10.1590/S0100-83582018360100032
  8. Altschul S.F., Madden T.L., Schaffer A.A., Zhang Z.H., Zhang Z., … Lippman D.J., 1997. Gapped BLAST and PSIBLAST: A new generation of protein database search programs. Nucleic Acids Research 25(17): 3389–3402. https://doi.org/10.1093/nar/25.17.3389
  9. Altschul S.F., Wootton J.C., Gertz E.M., Agarwala R., Morgulis A., … Yu Y-K., 2005. Protein database searches using compositionally adjusted substitution matrices. FEBS Journal 272(20): 5101–5109. https://doi.org/10.1111/j.1742-4658.2005.04945.x
  10. Asaad N.Y., Kumari S.G., Haj-Kassem A.A., Shalaby A.A., Al-Shaabi S., Malhotra R.S., 2009. Detection and characterisation of chickpea chlorotic stunt virus in Syria. Journal of Phytopathology 157(11-12): 756–761. https://doi.org/10.1111/j.1439-0434.2009.01574.x
  11. Blackman R.L., Eastop V.F., 2000. Aphids on the World’s Crops: an Identification and Information Guide. 2nd ed. John Wiley & Sons, Ltd.: Chichester, UK.
  12. Boukhris-Bouhachem S., Souissi R., Turpeau E., Rouzé-Jouan J., Fahem M., … Hulle M., 2007. Aphid (Hemiptera: Aphidoidea) diversity in Tunisia in relation to seed potato production. Annales de la Société Entomologique de France 43(3): 311–318. https://doi.org/10.1080/00379271.2007.10697526
  13. Boukhris-Bouhachem S., Rouzé-Jouan J., Souissi R., Glais L., Hullé M., 2011. Transmission efficiency of the strain PVYNTN by commonly captured aphids in Tunisian potato fields. Plant Pathology Journal 10(1): 22–28. https://doi.org/10.3923/ppj.2011.22.28
  14. Charaabi K., Boukhris‐Bouhachem S., Makni M., Fenton B., Denholm I., 2016. Genetic variation in target‐site resistance to pyrethroids and pirimicarb in Tunisian populations of the peach potato aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Pest Management Science 72(12): 2313–2320. https://doi.org/10.1002/ps.4276
  15. Chiquito-Almanza E., Acosta-Gallegos J.A., García-Álvarez N.C., Garrido-Ramírez E.R., Montero-Tavera V., Anaya López J.L., 2017. Simultaneous detection of both RNA and DNA viruses infecting dry bean and occurrence of mixed infections by BGYMV, BCMV and BCMNV in the Central-West region of Mexico. Viruses 9(4): 63. https://doi.org/10.3390/v9040063
  16. D’Arcy C.J., Domier L.L., 2005. Luteoviridae. In: Virus Taxonomy. Eight Report of the International Committee on Taxonomy of Viruses (C.M. Faugnet, M.A. Mayo, J. Maniloff, U. Desselberger, L.A. Ball, ed.), Elsevier Academic Press, London, UK, 343–352.
  17. Deb M., Anderson J.M., 2008. Development of a multiplexed PCR detection method for Barley and Cereal yellow dwarf viruses, Wheat spindle streak virus, Wheat streak mosaic virus and Soil-borne wheat mosaic virus. Journal of Virological Methods 148(1-2): 17–24. https://doi.org/10.1016/j.jviromet.2007.10.015
  18. FAOSTAT. 2026. United Nations Food and Agriculture Organization, Statistics Division, Rome, Italy. Available at: https://www.fao.org/faostat/en/#data/QCL. Accessed April 2, 2026.
  19. Filardo F., Nancarrow N., Kehoe M., McTaggart A.R., Congdon, B., … Sharman, M., 2021. Genetic diversity and recombination between turnip yellows virus strains in Australia. Archives of Virology 166(3): 813–829. https://doi.org/10.1007/s00705-020-04931-w
  20. Fortass M., van der Wilk F., van den Heuvel J.F.J.M., Goldbach R.W., 1997. Molecular evidence for the occurrence of beet western yellows virus on chickpea in Morocco. European Journal of Plant Pathology 103: 481–484. https://doi.org/10.1023/A:1008687629522
  21. Franz A., Makkouk K.M., Katul L., Vetten H.J., 1996. Monoclonal antibodies for the detection and differentiation of faba bean necrotic yellows virus isolates. Annals of Applied Biology 128(2): 255–2268. https://doi.org/10.1111/j.1744-7348.1996.tb07321.x
  22. Ghorbani S.G.M., Shahraeena N., Elahinia S.A., 2010. Distribution and impact of virus associated diseases of common bean (Phaseolus vulgaris L.) in northern Iran. Archives of Phytopathology and Plant Protection 43(12): 1183–1189. https://doi.org/10.1080/03235400802366834
  23. Guesmi J., Ben Halima K.M., Almohandes-Dridi B., 2010. Identification and population evolution of aphids infesting artichoke in Tunisia. Tunisian Journal of Plant Protection 5: 83–89.
  24. Hajiyusef T., Shahraeen N., Maleki M., 2017. Serological and molecular detection of Bean leaf roll and Chickpea chlorotic stunt luteoviruses in chickpea from Iran. Journal of Plant Protection Research 57(2): 136–143. https://doi.org/10.1515/jppr-2017-0018
  25. Hauser S., Stevens M., Mougel C., Smith H.G., Fritsch C., … Lemaire O., 2000. Biological, serological, and molecular variability suggest three distinct Polerovirus species infecting beet or rape. Phytopathology 90(5): 460–466. https://doi.org/10.1094/PHYTO.2000.90.5.460
  26. Hauser S., Stevens M., Beuve M., Lemaire O., 2002. Biological properties and molecular characterization of beet chlorosis virus (BChV). Archives of Virology 147: 745–762. https://doi.org/10.1007/s007050200023
  27. Hlaoui A., Boukhris-Bouhachem S., Sepúlveda D.A., Correa M.C., Briones L.M., … Figueroa C.C., 2019. Spatial and temporal genetic diversity of the peach potato aphid Myzus persicae (Sulzer) in Tunisia. Insects 10(10): 330. https://doi.org/10.3390/insects10100330
  28. Hlaoui A., Chiesa O., Figueroa C.C., Souissi R., Mazzoni E., Boukhris‐Bouhachem S., 2022. Target site mutations underlying insecticide resistance in Tunisian populations of Myzus persicae (Sulzer) on peach orchards and potato crops. Pest Management Science 78(4): 1594–1604. https://doi.org/10.1002/ps.6778
  29. Hussein Aliyu T.H., Takim F.O., Olatinwo L.K., Arogundade O., Funmilayo Omotesho K.F., Oladoja D.A., 2021. Severity of viral diseases and types of weeds as alternative viral hosts in Dioscorea fields in southern guinea savannah agroecology of Nigeria. Journal of Food and Agriculture, 14(2): 1–16. https://doi.org/10.4038/jfa.v14i2.5242
  30. Irwin M.E., Thresh J.M., 1988. Long-range aerial dispersal of cereal aphids as virus vectors in North America. Philosophical Transactions of the Royal Society of London. B, Biological Sciences, 321(1207): 421–446. http://www.jstor.org/stable/2396815
  31. Jones R.A.C., 2016. Future scenarios for plant virus pathogens as climate change progresses. Advances in Virus Research 95: 87–147. https://doi.org/10.1016/bs.aivir.2016.02.004
  32. Jones R. A., Barbetti M.J., 2012. Influence of climate change on plant disease infections and epidemics caused by viruses and bacteria. CABI Reviews 1–13. https://doi.org/10.1079/PAVSNNR20127022
  33. Jukes T.H., Cantor C.R., 1969. Evolution of protein molecules. In: Mammalian Protein Metabolism (H.N. Munro, ed.), Academic Press, New York, 21–132.
  34. Katul L., 1992. Serological and Molecular Characterization of Bean leaf roll virus (BLRV) and Faba bean necrotic yellows virus (FBNYV). PhD Thesis, University of Göttingen, Germany, 115 pp.
  35. Kazinczi G., Horvath J., Takacs A., 2007. Toposviruses on ornamental plants. Plant Viruses 2: 142– 162.
  36. Keremane M., Singh K., Ramadugu C., Krueger R.R., Skaggs T.H., 2024. Next generation sequencing, and development of a pipeline as a tool for the detection and discovery of citrus pathogens to facilitate safer germplasm exchange. Plants 13(3): 411. https://doi.org/10.3390/plants13030411
  37. Kidanemariam D., Abraham A., 2023. Luteoviruses. In: Plant RNA Viruses (R.K. Gaur, B.P. Patil, R. Selvarajan, ed.), London: Academic Press, 57–77.
  38. Kumar P.L., Kumari S.G., Waliyar F., 2008. Virus diseases of chickpea. In: Characterization, Diagnosis and Management of Plant Viruses: Vegetable and Pulse Crops, Vol 3 (G.P. Rao, P.L. Kumar, R.J.H. Penna, ed.), Texas, USA: Studium Press LLC, 213–234.
  39. Kumar S., Stecher G., Li M., Knyaz C., Tamura K., 2018. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution 35(6): 1547–1549. https://doi.org/10.1093/molbev/msy096
  40. Kumari S.G., Makkouk K.M., 2007. Virus diseases of faba bean (Vicia faba L.) in Asia and Africa. Plant Viruses 1(1): 93–105. https://www.globalsciencebooks.info/Online/GSBOnline/images/0706/PV_1(1)/PV_1(1)93-105o.pdf
  41. Kumari S.G., Makkouk K.M., Asaad N., Attar N., Hlaing Loh M., 2007. Chickpea chlorotic stunt virus affecting cool-season food legumes in West Asia and North Africa. In: Abstract book of 10th International Plant Virus Epidemiology Symposium, on the theme “Controlling Epidemics of Emerging and Established Plant Virus Diseases—The Way Forward”, 15–19 October 2007, Hyderabad, India, 157 (abstract).
  42. Kumari S.G., Makkouk K.M., Loh M.H., Negassi K., Tsegay S., … Tesfatsion, Y., 2008. Viral diseases affecting chickpea crops in Eritrea. Phytopathologia Mediterranea 47(1): 42–49. https://www.jstor.org/stable/26463297
  43. Kumari S.G., Larsen R., Makkouk K.M., Bashir M., 2009. Virus diseases of lentil and their control. In: The Lentil: Botany, Production and Uses (W. Erskine, F.J. Muehlbauer, A. Sarker, B. Sharma, ed.). CABI, UK, 306–325.
  44. Kumari S.G., Najar A., Timoumi S., Male M.F., Kraberger S., Varsani A., 2015. First report of Chickpea chlorotic dwarf virus naturally infecting chickpea in Tunisia. New Disease Reports 32(1): 16. https://doi.org/10.5197/j.2044-0588.2015.032.016
  45. Kumari S.G., Moukahel A.R., Hamed A.A., Sharman M., 2018. First report of Cucurbit aphid-borne yellows virus affecting chickpea (Cicer arietinum L.) in Sudan. Plant Disease 102(10): 2048. https://doi.org/10.1094/PDIS-02-18-0347-PDN
  46. Lei, J., Yuan J., Chen M., Mao Q., 2025. Insect-specific viruses and their emerging role in plant disease mitigation. Viruses 17(9): 1269. https://doi.org/10.3390/v17091269
  47. Maina S., Jones R.A.C., 2023. Enhancing biosecurity against virus disease threats to Australian grain crops: current situation and future prospects. Frontiers in Horticulture 2: 1263604. https://doi.org/10.3389/fhort.2023.1263604
  48. Makkouk K.M., 2020. Plant pathogens which threaten food security: viruses of chickpea and other cool season legumes in West Asia and North Africa. Food Security 12: 495–502. https://doi.org/10.1007/s12571-020-01017-y
  49. Makkouk K.M., Kumari S.G., 1996. Detection of ten viruses by the tissue-blot immunoassay (TBIA). Arab Journal of Plant Protection 14(1): 3–9 (in Arabic).
  50. Makkouk, K.M., Vetten, H.J., Katul, L., Franz, A., Madkour, M.A., 1998. Epidemiology and control of faba bean necrotic yellows virus. (Chapter 40). In: Plant Virus Disease Control (A. Hadidi, R.K. Khetarpal, H. Koganezawa, ed.). APS Press, The American Phytopathological Society, St. Paul, Minnesota, USA, 534–540
  51. Makkouk K.M., Kumari S.G., Hughes J.d’A., Muniyappa V., Kulkarni N.K., 2003. Other legumes: Faba bean, chickpea, lentil, pigeonpea, mungbean, blackgram, lima bean, horegram, bambara groundnut and winged bean. In: Virus and Virus-like Diseases of Major Crops in Developing Countries (G. Loebenstein, G. Thottappilly, ed.). Kluwer Academic Publishers, Dordrecht, The Netherlands, 447–476.
  52. Makkouk K.M., Kumari S.G., van Leur J.A., Jones R.A., 2014. Control of plant virus diseases in cool-season grain legume crops. Advances in Virus Research 90: 207–253. https://doi.org/10.1016/B978-0-12-801246-8.00004-4
  53. Martin R.R., D’Arcy C.J., 1990. Relationships among luteoviruses based on nucleic acid hybridization and serological studies. Intervirology 31(1): 23–30. https://doi.org/10.1159/000150130
  54. Mdellel L., Ben Halima M.K., 2012. Aphids on almond and peach: preliminary results about biology in different areas of Tunisia. REDIA 95: 3–8.
  55. Mdellel L., Kamel M.B.H. 2014. Effects of different varieties of pepper (Capsicum annum L.) on the biological parameters of the green peach aphid Myzus persicae Sulzer (Hemiptera, Aphididae) in Tunisia. European Journal of Environmental Sciences 4(2): 102–105. https://doi.org/10.14712/23361964.2014.4
  56. Moreno A.B., López-Moya J.J., 2020. When viruses play team sports: mixed infections in plants. Phytopathology 110(1): 29–48. https://doi.org/10.1094/PHYTO-07-19-0250-FI
  57. Moukahel A., Kumari S., Hamed A., Sharman M., Kemal S., 2021. Distribution and identification of luteovirids affecting chickpea in Sudan. Phytopathologia Mediterranea 60(2): 199–214. https://doi.org/10.36253/phyto-12135
  58. Muhire B.M., Varsani A., Martin D.P., 2014. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLOS ONE 9: e108277. https://doi.org/10.1371/journal.pone.0108277
  59. Mulenga R.M., Miano D.W., Al Rwahnih M., Kaimoyo E., Akello J., … Alabi O.J., 2022. Survey for Virus Diversity in Common Bean (Phaseolus vulgaris) Fields and the Detection of a Novel Strain of Cowpea polerovirus 1 in Zambia. Plant Disease 106(9): 2380–2391. https://doi.org/10.1094/PDIS-11-21-2533-RE
  60. Najar A., Kumari S.G., Makkouk K.M., Daaloul A., 2003. A survey of viruses affecting faba bean (Vicia faba) in Tunisia includes first record of Soybean dwarf virus. Plant Disease 87(9): 1151. https://doi.org/10.1094/PDIS.2003.87.9.1151B
  61. Najar A., Kumari S.G., Attar N., Lababidi S., 2011. Present status of some virus diseases affecting legume crops in Tunisia and partial characterization of Chickpea chlorotic stunt virus. Phytopathologia Mediterranea 50(2): 310–315. https://www.jstor.org/stable/26458704
  62. Najar A., Makkouk K.M., Boudhir H., Kumari S.G., Zarouk R., … Ben Othman F., 2000a. Viral diseases of cultivated legume and cereal crops in Tunisia. Phytopathologia Mediterranea 39: 423–432. https://www.jstor.org/stable/26456574
  63. Najar A., Makkouk K.M., Kumari S.G., 2000b. First record of Faba bean necrotic yellows virus and Beet western yellows virus infecting faba bean in Tunisia. Plant Disease 84(9): 1046. https://doi.org/10.1094/PDIS.2000.84.9.1046A
  64. Ng J.C.K., Perry, K.L., 2004. Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5(5): 505–511. https://doi.org/10.1111/j.1364-3703.2004.00240.x
  65. Oshima K., Inoue A.K., Ishikawa Y., Shikata E., Takashi H., 1990. Production and application of monoclonal antibodies specific to ordinary strain and necrotic strain of potato virus Y. Japanese Journal of Phytopathology 56(4): 508–514. https://doi.org/10.3186/jjphytopath.56.508 (in Japanese).
  66. Peng Q., Li W., Zhou X., Sun C., Hou Y., … Lei L., 2023. Genetic diversity analysis of Brassica yellows virus causing aberrant color symptoms in oilseed rape. Plants 12(5): 1008. https://doi.org/10.3390/plants12051008
  67. Pierre H., Ellen E., Elisabeth D., Pauline R., Yordan M., … Stéphan S., 2026. Comparative analysis of beet western yellows virus detection methods: Development and validation of a novel real-time RT-PCR assay also targeting beet leaf yellowing virus. Journal of Virological Methods 342: 115352. https://doi.org/10.1016/j.jviromet.2026.115352
  68. Puthanveed V., Singh K., Poimenopoulou E., Pettersson J., Siddique A.B., … Kvarnheden A., 2023. Milder autumns may increase risk for infection of crops with Turnip yellows virus. Phytopathology 113(9): 1788–1798. https://doi.org/10.1094/PHYTO-11-22-0446-V
  69. Robert Y., Lemaire O., 1999. Epidemiology and control strategies. In: The Luteoviridae. H.J. Smith and H. Barker (ed.). CABI Publishing, UK. Pp 211–219.
  70. Rozas, J., Ferrer-Mata A., Sánchez-DelBarrio J.C., Guirao-Rico S., Librado P., Ramos-Onsins S.E., Sánchez-Gracia A., 2017. DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Molecular Biology and Evolution 34(12): 3299–3302. https://doi.org/10.1093/molbev/msx248
  71. Roonjha M.A., Roonjho R., Ali M., Anas M., Khalid H., Jan A., 2025. Aphid-transmitted plant viruses: Epidemiology and integrated vector management. International Journal of Agricultural Innovations and Cutting-Edge Research 3(3): 109–126. https://jai.bwo-researches.com/index.php/jwr/article/view/157
  72. Sánchez-Tovar M.R., Rivera-Bustamante R.F., Saavedra-Trejo D.L., Guevara-González R.G., Torres-Pacheco I., 2025. Mixed plant viral infections: complementation, interference and their effects, a review. Agronomy 15(3): 620. https://doi.org/10.3390/agronomy15030620
  73. Simon J.C., Rispe C., Sunnucks P., 2002. Ecology and evolution of sex in aphids. Trends in Ecology & Evolution 17(1): 34–39. https://doi.org/10.1016/S0169-5347(01)02331-X
  74. Stevens M., Freeman B., Liu H.Y., Herrbach E., Lemaire O., 2005. Beet poleroviruses: close friends or distant relatives?. Molecular Plant Pathology 6(1): 1–9. https://doi.org/10.1111/j.1364-3703.2004.00258.x
  75. Tajima F., 1989. Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123(3): 585–595. https://doi.org/10.1093/genetics/123.3.585
  76. Trebicki P., 2020. Climate change and plant virus epidemiology. Virus Research 286: 198059. https://doi.org/10.1016/j.virusres.2020.198059
  77. Venkataravanappa V., Ashwathappa K.V., Hiremath S., Manjunatha L., Shankarappa K.S., … Lakshminarayana Reddy C.N., 2023. Begomovirus and DNA-satellites association with mosaic and leaf curl disease of Solanum nigrum and Physalis minima: the new hosts for chilli leaf curl virus. VirusDisease 34(4): 504–513. https://doi.org/10.1007/s13337-023-00850-x
  78. Wisler G.C., Norris R.F., 2005. Interactions between weeds and cultivated plants as related to management of plant pathogens. Weed Science 53(6): 914–917. https://doi.org/10.1614/WS-04-051R.1
  79. Yoshida N., Tamada T., 2019. Host range and molecular analysis of Beet leaf yellowing virus, Beet western yellows virus-JP and Brassica yellows virus in Japan. Plant Pathology 68(6): 1045–1058. https://doi.org/10.1111/ppa.13023
  80. Yazdkhasti E., Hopkins R.J., Kvarnheden A., 2021. Reservoirs of plant virus disease: Occurrence of Wheat dwarf virus and Barley/Cereal yellow dwarf viruses in Sweden. Plant Pathology 70(11): 1552–1561. https://doi.org/10.1111/ppa.13414

Most read articles by the same author(s)