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Geminiviral betasatellites: critical viral ammunition to conquer plant immunity

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Abstract

Geminiviruses have mastered plant cell modulation and immune invasion to ensue prolific infection. Encoding a relatively small number of multifunctional proteins, geminiviruses rely on satellites to efficiently re-wire plant immunity, thereby fostering virulence. Among the known satellites, betasatellites have been the most extensively investigated. They contribute significantly to virulence, enhance virus accumulation, and induce disease symptoms. To date, only two betasatellite proteins, βC1, and βV1, have been shown to play a crucial role in virus infection. In this review, we offer an overview of plant responses to betasatellites and counter-defense strategies deployed by betasatellites to overcome those responses.

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References

  1. Brito AF, Pinney JW (2017) Protein–Protein Interactions in Virus–Host Systems. Front Microbiol 8:

  2. R KC, Ali Z, M TT, et al (2018) Hacking the Cell: Network Intrusion and Exploitation by Adenovirus E1A. mBio 9:e00390-18. https://doi.org/10.1128/mBio.00390-18

    Article  Google Scholar 

  3. Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S (2013) Geminiviruses: masters at redirecting and reprogramming plant processes. Nat Rev Microbiol 11:777–788. https://doi.org/10.1038/nrmicro3117

    Article  CAS  PubMed  Google Scholar 

  4. Gong P, Tan H, Zhao S, et al (2021) Geminiviruses encode additional small proteins with specific subcellular localizations and virulence function. Nat Commun 12:4278. https://doi.org/10.1038/s41467-021-24617-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gupta N, Reddy K, Bhattacharyya D, Chakraborty S (2021) Plant responses to geminivirus infection: guardians of the plant immunity. Virol J 18:143. https://doi.org/10.1186/s12985-021-01612-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Rojas M, Macedo M, Maliano M, et al (2018) World Management of Geminiviruses. Annu Rev Phytopathol 56:637–677. https://doi.org/10.1146/annurev-phyto-080615-100327

    Article  CAS  PubMed  Google Scholar 

  7. Devendran R, Kumar M, Ghosh D, et al (2022) Capsicum-infecting begomoviruses as global pathogens: host–virus interplay, pathogenesis, and management. Trends Microbiol 30:170–184. https://doi.org/10.1016/j.tim.2021.05.007

    Article  CAS  PubMed  Google Scholar 

  8. Zerbini FM, Briddon RW, Idris A, et al (2017) ICTV Virus Taxonomy Profile: Geminiviridae. Journal of General Virology 98:131–133. https://doi.org/10.1099/jgv.0.000738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Fiallo-Olivé E, Lett J-M, Martin D, et al (2021) ICTV Virus Taxonomy Profile: Geminiviridae 2021. Journal of General Virology 102:. https://doi.org/10.1099/jgv.0.001696

  10. Blanc S, Gutiérrez S (2015) The specifics of vector transmission of arboviruses of vertebrates and plants. Curr Opin Virol 15:27–33. https://doi.org/10.1016/j.coviro.2015.07.003

    Article  PubMed  Google Scholar 

  11. Varsani A, Roumagnac P, Fuchs M, et al (2017) Capulavirus and Grablovirus: two new genera in the family Geminiviridae. Arch Virol 162:1819–1831. https://doi.org/10.1007/s00705-017-3268-6

    Article  CAS  PubMed  Google Scholar 

  12. Kishorekumar R, Devendran R, Chakraborty S (2022) Insights into the multifunctional roles of geminivirusencoded proteins in pathogenesis. Arch Virol. https://doi.org/10.1007/s00705-021-05338-x

    Article  Google Scholar 

  13. Dry IB, Krake LR, Rigden JE, Rezaian MA (1997) A novel subviral agent associated with a geminivirus: The first report of a DNA satellite. Proceedings of the National Academy of Sciences 94:7088–7093. https://doi.org/10.1073/pnas.94.13.7088

  14. Saunders K, Bedford I, Stanley J (2002) Adaptation from whitefly to leafhopper transmission of an autonomously replicating nanovirus-like DNA component associated with ageratum yellow vein disease. J Gen Virol 83:907–913. https://doi.org/10.1099/0022-1317-83-4-907

    Article  CAS  PubMed  Google Scholar 

  15. Mansoor S, Zafar Y, Briddon RW (2006) Geminivirus disease complexes: the threat is spreading. Trends Plant Sci 11:209–212. https://doi.org/10.1016/j.tplants.2006.03.003

    Article  CAS  PubMed  Google Scholar 

  16. Nawaz-ul-Rehman MS, Fauquet CM (2009) Evolution of geminiviruses and their satellites. FEBS Lett 583:1825–1832. https://doi.org/10.1016/j.febslet.2009.05.045

    Article  CAS  PubMed  Google Scholar 

  17. Kumar RV, Singh AK, Singh AK, et al (2015) Complexity of begomovirus and betasatellite populations associated with chilli leaf curl disease in India. Journal of General Virology 96:3143–3158. https://doi.org/10.1099/jgv.0.000254

    Article  CAS  PubMed  Google Scholar 

  18. Vinoth Kumar R, Singh D, Singh AK, Chakraborty S (2017) Molecular diversity, recombination and population structure of alphasatellites associated with begomovirus disease complexes. Infection, Genetics and Evolution 49:39–47. https://doi.org/10.1016/j.meegid.2017.01.001

    Article  CAS  PubMed  Google Scholar 

  19. Xiaofeng C, Guixin L, Daowen W, et al (2005) A Begomovirus DNAβ-Encoded Protein Binds DNA, Functions as a Suppressor of RNA Silencing, and Targets the Cell Nucleus. J Virol 79:10764–10775. https://doi.org/10.1128/JVI.79.16.10764-10775.2005

    Article  CAS  Google Scholar 

  20. Saunders K, Briddon RW, 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 89:3165–3172. https://doi.org/10.1099/vir.0.2008/003848-0

    Article  CAS  PubMed  Google Scholar 

  21. Idris A, Shahid MS, Briddon R, et al (2010) An unusual alphasatellite associated with monopartite begomoviruses attenuates symptoms and reduces betasatellite accumulation. J Gen Virol 92:706–717. https://doi.org/10.1099/vir.0.025288-0

    Article  CAS  PubMed  Google Scholar 

  22. 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. https://doi.org/10.1016/j.virol.2010.06.024

    Article  CAS  PubMed  Google Scholar 

  23. Kumar M, Zarreen F, Chakraborty S (2021) Roles of two distinct alphasatellites modulating geminivirus pathogenesis. Virol J 18:249. https://doi.org/10.1186/s12985-021-01718-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhao L, Che X, Wang Z, et al (2022) Functional Characterization of Replication-Associated Proteins Encoded by Alphasatellites Identified in Yunnan Province, China. Viruses 14:222. https://doi.org/10.3390/v14020222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Fiallo-Olivé E, Martínez-Zubiaur Y, Moriones E, Navas-Castillo J (2012) A novel class of DNA satellites associated with New World begomoviruses. Virology 426:1–6. https://doi.org/10.1016/j.virol.2012.01.024

    Article  CAS  PubMed  Google Scholar 

  26. Fiallo-Olivé E, Tovar R, Navas-Castillo J (2016) Deciphering the biology of deltasatellites from the New World: maintenance by New World begomoviruses and whitefly transmission. New Phytologist 212:680–692. https://doi.org/10.1111/nph.14071

    Article  CAS  PubMed  Google Scholar 

  27. Hassan I, Orílio AF, Fiallo-Olivé E, et al (2016) Infectivity, effects on helper viruses and whitefly transmission of the deltasatellites associated with sweepoviruses (genus Begomovirus, family Geminiviridae). Sci Rep 6:30204. https://doi.org/10.1038/srep30204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sivalingam PN, Varma A (2012) Role of betasatellite in the pathogenesis of a bipartite begomovirus affecting tomato in India. Arch Virol 157:1081–1092. https://doi.org/10.1007/s00705-012-1261-7

    Article  CAS  PubMed  Google Scholar 

  29. Zhou X (2013) Advances in Understanding Begomovirus Satellites. Annu Rev Phytopathol 51:357–381. https://doi.org/10.1146/annurev-phyto-082712-102234

    Article  CAS  PubMed  Google Scholar 

  30. Li F, Yang X, Bisaro DM, Zhou X (2018) The βC1 Protein of Geminivirus–Betasatellite Complexes: A Target and Repressor of Host Defenses. Mol Plant 11:1424–1426. https://doi.org/10.1016/j.molp.2018.10.007

    Article  CAS  PubMed  Google Scholar 

  31. Gnanasekaran P, Chakraborty S (2018) Biology of viral satellites and their role in pathogenesis. Curr Opin Virol 33:96–105. https://doi.org/10.1016/j.coviro.2018.08.002

    Article  CAS  PubMed  Google Scholar 

  32. Mansoor S, Khan SH, Bashir A, et al (1999) Identification of a Novel Circular Single-Stranded DNA Associated with Cotton Leaf Curl Disease in Pakistan. Virology 259:190–199. https://doi.org/10.1006/viro.1999.9766

    Article  CAS  PubMed  Google Scholar 

  33. Yang X, Xie Y, Raja P, et al (2011) Suppression of Methylation-Mediated Transcriptional Gene Silencing by βC1-SAHH Protein Interaction during Geminivirus-Betasatellite Infection. PLoS Pathog 7:e1002329-

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Li F, Huang C, Li Z, Zhou X (2014) Suppression of RNA Silencing by a Plant DNA Virus Satellite Requires a Host Calmodulin-Like Protein to Repress RDR6 Expression. PLoS Pathog 10:e1003921-

    Article  PubMed  PubMed Central  Google Scholar 

  35. Bhattacharyya D, Gnanasekaran P, Kumar RK, et al (2015) A geminivirus betasatellite damages the structural and functional integrity of chloroplasts leading to symptom formation and inhibition of photosynthesis. J Exp Bot 66:5881–5895. https://doi.org/10.1093/jxb/erv299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Xueting Z, Qi WZ, Ruyuan X, et al (2017) Mimic Phosphorylation of a βC1 Protein Encoded by TYLCCNB Impairs Its Functions as a Viral Suppressor of RNA Silencing and a Symptom Determinant. J Virol 91:e00300-17. https://doi.org/10.1128/JVI.00300-17

    Article  Google Scholar 

  37. Yang X, Guo W, Li F, et al (2019) Geminivirus-Associated Betasatellites: Exploiting Chinks in the Antiviral Arsenal of Plants. Trends Plant Sci 24:519–529. https://doi.org/10.1016/j.tplants.2019.03.010

    Article  CAS  PubMed  Google Scholar 

  38. Prabu G, Neha G, Kalaiarasan P, Supriya C (2021) Geminivirus Betasatellite-Encoded βC1 Protein Exhibits Novel ATP Hydrolysis Activity That Influences Its DNA-Binding Activity and Viral Pathogenesis. J Virol 95:e00475-21. https://doi.org/10.1128/JVI.00475-21

    Article  Google Scholar 

  39. King AMQ, Lefkowitz EJ, Mushegian AR, et al (2018) Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018). Arch Virol 163:2601–2631. https://doi.org/10.1007/s00705-018-3847-1

    Article  CAS  PubMed  Google Scholar 

  40. Wang N, Zhao P, Wang D, et al (2022) Diverse Begomoviruses Evolutionarily Hijack Plant Terpenoid-Based Defense to Promote Whitefly Performance. Cells 12:149. https://doi.org/10.3390/cells12010149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hu T, Song Y, Wang Y, Zhou X (2020) Functional analysis of a novel βV1 gene identified in a geminivirus betasatellite. Sci China Life Sci 63:688–696. https://doi.org/10.1007/s11427-020-1654-x

    Article  CAS  PubMed  Google Scholar 

  42. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286

    Article  CAS  PubMed  Google Scholar 

  43. Ngou BPM, Ding P, Jones JDG (2022) Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 34:1447–1478. https://doi.org/10.1093/plcell/koac041

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wang Y, Pruitt RN, Nürnberger T, Wang Y (2022) Evasion of plant immunity by microbial pathogens. Nat Rev Microbiol 20:449–464. https://doi.org/10.1038/s41579-022-00710-3

    Article  CAS  PubMed  Google Scholar 

  45. Haasnoot J, Westerhout EM, Berkhout B (2007) RNA interference against viruses: strike and counterstrike. Nat Biotechnol 25:1435–1443. https://doi.org/10.1038/nbt1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833. https://doi.org/10.1038/35081161

    Article  CAS  PubMed  Google Scholar 

  47. Rao M v, Lee H, Creelman RA, et al (2000) Jasmonic Acid Signaling Modulates Ozone-Induced Hypersensitive Cell Death. Plant Cell 12:1633–1646. https://doi.org/10.1105/tpc.12.9.1633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. O’Brien JA, Daudi A, Butt VS, Paul Bolwell G (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779. https://doi.org/10.1007/s00425-012-1696-9

    Article  CAS  PubMed  Google Scholar 

  49. Fu ZQ, Yan S, Saleh A, et al (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486:228–232. https://doi.org/10.1038/nature11162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Xu J, Zhang S (2015) Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends Plant Sci 20:56–64. https://doi.org/10.1016/j.tplants.2014.10.001

    Article  CAS  PubMed  Google Scholar 

  51. Gupta N, Reddy K, Gnanasekaran P, et al (2022) Functional characterization of a new ORF βV1 encoded by radish leaf curl betasatellite. Front Plant Sci 13:

  52. Shen Q, Liu Z, Song F, et al (2011) Tomato SlSnRK1 Protein Interacts with and Phosphorylates βC1, a Pathogenesis Protein Encoded by a Geminivirus β-Satellite. Plant Physiol 157:1394–1406. https://doi.org/10.1104/pp.111.184648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Shen Q, Hu T, Bao M, et al (2016) Tobacco RING E3 Ligase NtRFP1 Mediates Ubiquitination and Proteasomal Degradation of a Geminivirus-Encoded βC1. Mol Plant 9:911–925. https://doi.org/10.1016/j.molp.2016.03.008

    Article  CAS  PubMed  Google Scholar 

  54. Haxim Y, Ismayil A, Jia Q, et al (2017) Autophagy functions as an antiviral mechanism against geminiviruses in plants. Elife 6:e23897. https://doi.org/10.7554/eLife.23897

    Article  PubMed  PubMed Central  Google Scholar 

  55. Ismayil A, Yang M, Haxim Y, et al (2020) Cotton leaf curl Multan virus βC1 Protein Induces Autophagy by Disrupting the Interaction of Autophagy-Related Protein 3 with Glyceraldehyde-3-Phosphate Dehydrogenases. Plant Cell 32:tpc.00759.2019. https://doi.org/10.1105/tpc.19.00759

  56. Macho AP, Zipfel C (2014) Plant PRRs and the Activation of Innate Immune Signaling. Mol Cell 54:263–272. https://doi.org/10.1016/j.molcel.2014.03.028

    Article  CAS  PubMed  Google Scholar 

  57. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10:339–346. https://doi.org/10.1016/j.tplants.2005.05.009

    Article  CAS  PubMed  Google Scholar 

  58. Meng X, Zhang S (2013) MAPK Cascades in Plant Disease Resistance Signaling. Annu Rev Phytopathol 51:245–266. https://doi.org/10.1146/annurev-phyto-082712-102314

    Article  CAS  PubMed  Google Scholar 

  59. Bi G, Zhou J-M (2017) MAP Kinase Signaling Pathways: A Hub of Plant-Microbe Interactions. Cell Host Microbe 21:270–273. https://doi.org/10.1016/j.chom.2017.02.004

    Article  CAS  PubMed  Google Scholar 

  60. Qiu J-L, Zhou L, Yun B-W, et al (2008) Arabidopsis Mitogen-Activated Protein Kinase Kinases MKK1 and MKK2 Have Overlapping Functions in Defense Signaling Mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222. https://doi.org/10.1104/pp.108.120006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Gao M, Liu J, Bi D, et al (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–1198. https://doi.org/10.1038/cr.2008.300

    Article  CAS  PubMed  Google Scholar 

  62. Kong Q, Qu N, Gao M, et al (2012) The MEKK1-MKK1/MKK2-MPK4 Kinase Cascade Negatively Regulates Immunity Mediated by a Mitogen-Activated Protein Kinase Kinase Kinase in Arabidopsis. Plant Cell 24:2225–2236. https://doi.org/10.1105/tpc.112.097253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Asai T, Tena G, Plotnikova J, et al (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983. https://doi.org/10.1038/415977a

    Article  CAS  PubMed  Google Scholar 

  64. Bethke G, Unthan T, Uhrig JF, et al (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proceedings of the National Academy of Sciences 106:8067–8072. https://doi.org/10.1073/pnas.0810206106

  65. Hu T, Huang C, He Y, et al (2019) βC1 protein encoded in geminivirus satellite concertedly targets MKK2 and MPK4 to counter host defense. PLoS Pathog 15:e1007728-

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Wang M-B, Masuta C, Smith NA, Shimura H (2012) RNA Silencing and Plant Viral Diseases. Molecular Plant-Microbe Interactions® 25:1275–1285. https://doi.org/10.1094/MPMI-04-12-0093-CR

    Article  CAS  PubMed  Google Scholar 

  67. Pumplin N, Voinnet O (2013) RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Microbiol 11:745–760. https://doi.org/10.1038/nrmicro3120

    Article  CAS  PubMed  Google Scholar 

  68. Waterhouse PM, Wang M-B, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842. https://doi.org/10.1038/35081168

    Article  CAS  PubMed  Google Scholar 

  69. Pallás V, García J (2011) How do plant viruses induce disease? Interactions and interference with host components. J Gen Virol 92:2691–2705. https://doi.org/10.1099/vir.0.034603-0

    Article  CAS  PubMed  Google Scholar 

  70. Wang M-B, Metzlaff M (2005) RNA silencing and antiviral defense in plants. Curr Opin Plant Biol 8:216–222. https://doi.org/10.1016/j.pbi.2005.01.006

    Article  CAS  PubMed  Google Scholar 

  71. Wang M-B, Masuta C, Smith NA, Shimura H (2012) RNA Silencing and Plant Viral Diseases. Molecular Plant-Microbe Interactions® 25:1275–1285. https://doi.org/10.1094/MPMI-04-12-0093-CR

    Article  CAS  PubMed  Google Scholar 

  72. Lindbo JA, Silva-Rosales L, Proebsting WM, Dougherty WG (1993) Induction of a Highly Specific Antiviral State in Transgenic Plants: Implications for Regulation of Gene Expression and Virus Resistance. Plant Cell 5:1749–1759. https://doi.org/10.1105/tpc.5.12.1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Xiao B, Yang X, Ye C-Y, et al (2014) A diverse set of miRNAs responsive to begomovirus-associated betasatellite in Nicotiana benthamiana. BMC Plant Biol 14:60. https://doi.org/10.1186/1471-2229-14-60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Wang J, Tang Y, Yang Y, et al (2016) Cotton Leaf Curl Multan Virus-Derived Viral Small RNAs Can Target Cotton Genes to Promote Viral Infection. Front Plant Sci 7:

  75. Rishishwar R, Dasgupta I (2019) Suppressors of RNA silencing encoded by geminiviruses and associated DNA satellites. Virusdisease 30:58–65. https://doi.org/10.1007/s13337-018-0418-8

    Article  PubMed  Google Scholar 

  76. Sunter G, Sunter JL, Bisaro DM (2001) Plants Expressing Tomato Golden Mosaic Virus AL2 or Beet Curly Top Virus L2 Transgenes Show Enhanced Susceptibility to Infection by DNA and RNA Viruses. Virology 285:59–70. https://doi.org/10.1006/viro.2001.0950

    Article  CAS  PubMed  Google Scholar 

  77. Xiangli D, Rene van W, John S, Yiguo H (2003) Functional Characterization of the Nuclear Localization Signal for a Suppressor of Posttranscriptional Gene Silencing. J Virol 77:7026–7033. https://doi.org/10.1128/JVI.77.12.7026-7033.2003

    Article  CAS  Google Scholar 

  78. Ramachandran V, Padmanabhan C, S PJ, M FC (2004) Differential Roles of AC2 and AC4 of Cassava Geminiviruses in Mediating Synergism and Suppression of Posttranscriptional Gene Silencing. J Virol 78:9487–9498. https://doi.org/10.1128/JVI.78.17.9487-9498.2004

    Article  CAS  Google Scholar 

  79. Daniela T, Rajeswaran R, Shivaprasad P v, et al (2005) Suppression of RNA Silencing by a Geminivirus Nuclear Protein, AC2, Correlates with Transactivation of Host Genes. J Virol 79:2517–2527. https://doi.org/10.1128/JVI.79.4.2517-2527.2005

    Article  CAS  Google Scholar 

  80. Wang Y, Gong Q, Wu Y, et al (2021) A calmodulin-binding transcription factor links calcium signaling to antiviral RNAi defense in plants. Cell Host Microbe 29:1393–1406.e7. https://doi.org/10.1016/j.chom.2021.07.003

    Article  CAS  PubMed  Google Scholar 

  81. Mubin M, Ijaz S, Nahid N, et al (2020) Journey of begomovirus betasatellite molecules: from satellites to indispensable partners. Virus Genes 56:16–26. https://doi.org/10.1007/s11262-019-01716-5

    Article  CAS  PubMed  Google Scholar 

  82. Gui X, Liu C, Qi Y, Zhou X (2022) Geminiviruses employ host DNA glycosylases to subvert DNA methylation-mediated defense. Nat Commun 13:575. https://doi.org/10.1038/s41467-022-28262-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Voorburg CM, Yan Z, Bergua-Vidal M, et al (2020) Ty-1, a universal resistance gene against geminiviruses that is compromised by co-replication of a betasatellite. Mol Plant Pathol 21:160–172. https://doi.org/10.1111/mpp.12885

    Article  CAS  PubMed  Google Scholar 

  84. Briddon RW, Mansoor S, Bedford ID, et al (2001) Identification of DNA Components Required for Induction of Cotton Leaf Curl Disease. Virology 285:234–243. https://doi.org/10.1006/viro.2001.0949

    Article  CAS  PubMed  Google Scholar 

  85. Amin I, Hussain K, Akbergenov R, et al (2011) Suppressors of RNA Silencing Encoded by the Components of the Cotton Leaf Curl Begomovirus-BetaSatellite Complex. Molecular Plant-Microbe Interactions® 24:973–983. https://doi.org/10.1094/MPMI-01-11-0001

    Article  CAS  PubMed  Google Scholar 

  86. Tiwari N, Sharma PK, Malathi VG (2013) Functional characterization of βC1 gene of Cotton leaf curl Multan betasatellite. Virus Genes 46:111–119. https://doi.org/10.1007/s11262-012-0828-4

    Article  CAS  PubMed  Google Scholar 

  87. Sahu AK, Sanan-Mishra N (2021) Interaction between βC1 of satellite and coat protein of Chili leaf curl virus plays a crucial role in suppression of host RNA silencing. Appl Microbiol Biotechnol 105:8329–8342. https://doi.org/10.1007/s00253-021-11624-0

    Article  CAS  PubMed  Google Scholar 

  88. Eini O (2017) A betasatellite-encoded protein regulates key components of gene silencing system in plants. Mol Biol 51:579–585. https://doi.org/10.1134/S0026893317030037

    Article  CAS  Google Scholar 

  89. Smalle J, Vierstra RD (2004) THE UBIQUITIN 26S PROTEASOME PROTEOLYTIC PATHWAY. Annu Rev Plant Biol 55:555–590. https://doi.org/10.1146/annurev.arplant.55.031903.141801

    Article  CAS  PubMed  Google Scholar 

  90. Sadanandom A, Bailey M, Ewan R, et al (2012) The ubiquitin–proteasome system: central modifier of plant signalling. New Phytologist 196:13–28. https://doi.org/10.1111/j.1469-8137.2012.04266.x

    Article  CAS  PubMed  Google Scholar 

  91. Vierstra RD (2009) The ubiquitin–26S proteasome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397. https://doi.org/10.1038/nrm2688

    Article  CAS  PubMed  Google Scholar 

  92. Üstün S, Sheikh A, Gimenez-Ibanez S, et al (2016) The Proteasome Acts as a Hub for Plant Immunity and Is Targeted by Pseudomonas Type III Effectors. Plant Physiol 172:1941–1958. https://doi.org/10.1104/pp.16.00808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Alcaide-Loridan C, Jupin I (2012) Ubiquitin and Plant Viruses, Let’s Play Together! Plant Physiol 160:72–82. https://doi.org/10.1104/pp.112.201905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Eini O, Dogra S, Selth LA, et al (2009) Interaction with a Host Ubiquitin-Conjugating Enzyme Is Required for the Pathogenicity of a Geminiviral DNA β Satellite. Molecular Plant-Microbe Interactions® 22:737–746. https://doi.org/10.1094/MPMI-22-6-0737

    Article  CAS  PubMed  Google Scholar 

  95. Jia Q, Liu N, Xie K, et al (2016) CLCuMuB βC1 Subverts Ubiquitination by Interacting with NbSKP1s to Enhance Geminivirus Infection in Nicotiana benthamiana. PLoS Pathog 12:e1005668-

    Article  PubMed  PubMed Central  Google Scholar 

  96. Zhou T, Zhang M, Gong P, et al (2021) Selective autophagic receptor NbNBR1 prevents NbRFP1-mediated UPS-dependent degradation of βC1 to promote geminivirus infection. PLoS Pathog 17:e1009956-

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zhang M, Cao B, Zhang H, et al (2022) Geminivirus satellite-encoded βC1 activates UPR, induces bZIP60 nuclear export, and manipulates the expression of bZIP60 downstream genes to benefit virus infection. Sci China Life Sci. https://doi.org/10.1007/s11427-022-2196-y

    Article  PubMed  PubMed Central  Google Scholar 

  98. Islam W, Naveed H, Zaynab M, et al (2019) Plant defense against virus diseases; growth hormones in highlights. Plant Signal Behav 14:1596719. https://doi.org/10.1080/15592324.2019.1596719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Ma K-W, Ma W (2016) Phytohormone pathways as targets of pathogens to facilitate infection. Plant Mol Biol 91:713–725. https://doi.org/10.1007/s11103-016-0452-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Ghosh D, Chakraborty S (2021) Molecular interplay between phytohormones and geminiviruses: a saga of a never-ending arms race. J Exp Bot 72:2903–2917. https://doi.org/10.1093/jxb/erab061

    Article  CAS  PubMed  Google Scholar 

  101. Bhattacharyya D, Chakraborty S (2018) Chloroplast: the Trojan horse in plant–virus interaction. Mol Plant Pathol 19:504–518. https://doi.org/10.1111/mpp.12533

    Article  PubMed  Google Scholar 

  102. Gnanasekaran P, Ponnusamy K, Chakraborty S (2019) A geminivirus betasatellite encoded βC1 protein interacts with PsbP and subverts PsbP-mediated antiviral defence in plants. Mol Plant Pathol 20:943–960. https://doi.org/10.1111/mpp.12804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Nair A, Harshith CY, Narjala A, Shivaprasad P V (2023) Begomoviral βC1 orchestrates organellar genomic instability to augment viral infection. The Plant Journal n/a: https://doi.org/10.1111/tpj.16186

  104. Sun Y-C, Pan L-L, Ying F-Z, et al (2017) Jasmonic acid-related resistance in tomato mediates interactions between whitefly and whitefly-transmitted virus. Sci Rep 7:566. https://doi.org/10.1038/s41598-017-00692-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Yang J-Y, Iwasaki M, Machida C, et al (2008) C1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22:2564–2577. https://doi.org/10.1101/gad.1682208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. ZHANG T, LUAN J-B, QI J-F, et al (2012) Begomovirus–whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol Ecol 21:1294–1304. https://doi.org/10.1111/j.1365-294X.2012.05457.x

    Article  PubMed  Google Scholar 

  107. Stone SL, Hauksdóttir H, Troy A, et al (2005) Functional Analysis of the RING-Type Ubiquitin Ligase Family of Arabidopsis. Plant Physiol 137:13–30. https://doi.org/10.1104/pp.104.052423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Li R, Weldegergis BT, Li J, et al (2014) Virulence Factors of Geminivirus Interact with MYC2 to Subvert Plant Resistance and Promote Vector Performance. Plant Cell 26:4991–5008. https://doi.org/10.1105/tpc.114.133181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Pascal E, Sanderfoot AA, Ward BM, et al (1994) The geminivirus BR1 movement protein binds single-stranded DNA and localizes to the cell nucleus. Plant Cell 6:995–1006. https://doi.org/10.1105/tpc.6.7.995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Stefan H, Christina W, Holger J (2004) Interaction of DNA with the Movement Proteins of Geminiviruses Revisited. J Virol 78:7698–7706. https://doi.org/10.1128/JVI.78.14.7698-7706.2004

    Article  CAS  Google Scholar 

  111. Noueiry AO, Lucas WJ, Gilbertson RL (1994) Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76:925–932. https://doi.org/10.1016/0092-8674(94)90366-2

    Article  CAS  PubMed  Google Scholar 

  112. Lazarowitz SG, Beachy RN (1999) Viral Movement Proteins as Probes for Intracellular and Intercellular Trafficking in Plants. Plant Cell 11:535–548. https://doi.org/10.1105/tpc.11.4.535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Gafni Y, Epel BL (2002) The role of host and viral proteins in intra- and inter-cellular trafficking of geminiviruses. Physiol Mol Plant Pathol 60:231–241. https://doi.org/10.1006/pmpp.2002.0402

    Article  CAS  Google Scholar 

  114. Yanchen Z, R RM, Mi-Ri P, et al (2011) Histone H3 Interacts and Colocalizes with the Nuclear Shuttle Protein and the Movement Protein of a Geminivirus. J Virol 85:11821–11832. https://doi.org/10.1128/JVI.00082-11

    Article  Google Scholar 

  115. Gouveia-Mageste BC, Martins LGC, Dal-Bianco M, et al (2021) A plant-specific syntaxin-6 protein contributes to the intracytoplasmic route for the begomovirus CabLCV. Plant Physiol 187:158–173. https://doi.org/10.1093/plphys/kiab252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Rojas MR, Jiang H, Salati R, et al (2001) Functional Analysis of Proteins Involved in Movement of the Monopartite Begomovirus, Tomato Yellow Leaf Curl Virus. Virology 291:110–125. https://doi.org/10.1006/viro.2001.1194

    Article  CAS  PubMed  Google Scholar 

  117. Gong P, Zhao S, Liu H, et al (2022) Tomato yellow leaf curl virus V3 protein traffics along microfilaments to plasmodesmata to promote virus cell-to-cell movement. Sci China Life Sci 65:1046–1049. https://doi.org/10.1007/s11427-021-2063-4

    Article  CAS  PubMed  Google Scholar 

  118. Li H, Li F, Zhang M, et al (2020) Dynamic Subcellular Localization, Accumulation, and Interactions of Proteins From Tomato Yellow Leaf Curl China Virus and Its Associated Betasatellite. Front Plant Sci 11:

  119. Saeed M, Zafar Y, Randles J, Rezaian M (2007) A monopartite Begomovirus-associated DNA β satellite substitutes for the DNA B of a bipartite begomovirus to permit systemic infection. J Gen Virol 88:2881–2889. https://doi.org/10.1099/vir.0.83049-0

    Article  CAS  PubMed  Google Scholar 

  120. Patil B, Fauquet C (2010) Differential interaction between cassava mosaic geminiviruses and geminivirus satellites. J Gen Virol 91:1871–1882. https://doi.org/10.1099/vir.0.019513-0

    Article  CAS  PubMed  Google Scholar 

  121. Kumar P. P, Usha R, Zrachya A, et al (2006) Protein–protein interactions and nuclear trafficking of coat protein and βC1 protein associated with Bhendi yellow vein mosaic disease. Virus Res 122:127–136. https://doi.org/10.1016/j.virusres.2006.07.007

    Article  CAS  Google Scholar 

  122. Nasim A, Rashid MAR, Hussain K, et al (2022) Interaction estimation of pathogenicity determinant protein βC1 encoded by Cotton leaf curl Multan Betasatellite with Nicotiana benthamiana Nuclear Transport Factor 2. PeerJ 10:e14281. https://doi.org/10.7717/peerj.14281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kamal H, Minhas F ul AA, Tripathi D, et al (2019) βC1, pathogenicity determinant encoded by Cotton leaf curl Multan betasatellite, interacts with calmodulin-like protein 11 (Gh-CML11) in Gossypium hirsutum. PLoS One 14:e0225876. https://doi.org/10.1371/journal.pone.0225876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. GÁLIS I, GAQUEREL E, PANDEY SP, BALDWIN IANT (2009) Molecular mechanisms underlying plant memory in JA-mediated defence responses. Plant Cell Environ 32:617–627. https://doi.org/10.1111/j.1365-3040.2008.01862.x

    Article  CAS  PubMed  Google Scholar 

  125. Guo Y, Jia M, Li S, Li F (2022) Geminiviruses boost active DNA demethylation for counter-defense. Trends Microbiol 30:1121–1124. https://doi.org/10.1016/j.tim.2022.02.002

    Article  CAS  PubMed  Google Scholar 

  126. Zhao P, Yao X, Cai C, et al (2019) Viruses mobilize plant immunity to deter nonvector insect herbivores. Sci Adv 5:eaav9801. https://doi.org/10.1126/sciadv.aav9801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Naqvi AR, Choudhury NR, Mukherjee SK, Haq QMohdR (2011) In silico analysis reveals that several tomato microRNA/microRNA∗ sequences exhibit propensity to bind to tomato leaf curl virus (ToLCV) associated genomes and most of their encoded open reading frames (ORFs). Plant Physiology and Biochemistry 49:13–17. https://doi.org/10.1016/j.plaphy.2010.09.013

    Article  CAS  PubMed  Google Scholar 

  128. Akhtar S, Tahir N, Amin I, Mansoor S (2021) Amplicon-based RNAi construct targeting beta-C1 gene gives enhanced resistance against cotton leaf curl disease. 3 Biotech 11:. https://doi.org/10.1007/s13205-021-02816-6

  129. Ding Z-H, Gao Q, Tong X, et al (2022) MAPKs trigger antiviral immunity by directly phosphorylating a rhabdovirus nucleoprotein in plants and insect vectors. Plant Cell 34:3110–3127. https://doi.org/10.1093/plcell/koac143

    Article  PubMed  PubMed Central  Google Scholar 

  130. Marshall JM, Taylor CE (2009) Malaria Control with Transgenic Mosquitoes. PLoS Med 6:e1000020-

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We acknowledge the facilities supported by DBT BUILDER (grant no. BT/INF/22/SP45382/2022) and DST FIST-II (grant no. SR/FST/LSII-046/2016(C)) to SC. SK acknowledges the University Grants Commission for a JRF fellowship.

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Kumar, S., Gupta, N. & Chakraborty, S. Geminiviral betasatellites: critical viral ammunition to conquer plant immunity. Arch Virol 168, 196 (2023). https://doi.org/10.1007/s00705-023-05776-9

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