1932

Abstract

Of the approximately 1,200 plant virus species that have been described to date, nearly one-third are single-stranded DNA (ssDNA) viruses, and all are transmitted by insect vectors. However, most studies of vector transmission of plant viruses have focused on RNA viruses. All known plant ssDNA viruses belong to two economically important families, and , and in recent years, there have been increased efforts to understand whether they have evolved similar relationships with their respective insect vectors. This review describes the current understanding of ssDNA virus–vector interactions, including how these viruses cross insect vector cellular barriers, the responses of vectors to virus circulation, the possible existence of viral replication within insect vectors, and the three-way virus–vector–plant interactions. Despite recent breakthroughs in our understanding of these viruses, many aspects of plant ssDNA virus transmission remain elusive. More effort is needed to identify insect proteins that mediate the transmission of plant ssDNA viruses and to understand the complex virus–insect–plant three-way interactions in the field during natural infection.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-060920-094531
2021-01-07
2024-10-06
Loading full text...

Full text loading...

/deliver/fulltext/en/66/1/annurev-ento-060920-094531.html?itemId=/content/journals/10.1146/annurev-ento-060920-094531&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Alazem M, Lin NS. 2015. Roles of plant hormones in the regulation of host-virus interactions. Mol. Plant Pathol. 16:529–40
    [Google Scholar]
  2. 2. 
    Ammar E, Gargani D, Lett JM, Peterschmitt M 2009. Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila. Arch. Virol 154:255–62
    [Google Scholar]
  3. 3. 
    Becker N, Rimbaud L, Chiroleu F, Reynaud B, Thebaud G, Lett JM 2015. Rapid accumulation and low degradation: key parameters of tomato yellow leaf curl virus persistence in its insect vector Bemisia tabaci. Sci. Rep 5:17696
    [Google Scholar]
  4. 4. 
    Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW 2005. Herbivore arthropods benefit from vectoring plant viruses. Ecol. Lett. 8:70–79
    [Google Scholar]
  5. 5. 
    Blanc S, Drucker M, Uzest M 2014. Localizing viruses in their insect vectors. Annu. Rev. Phytopathol. 52:403–25
    [Google Scholar]
  6. 6. 
    Blanc S, Gutierrez S. 2015. The specifics of vector transmission of arboviruses of vertebrates and plants. Curr. Opin. Virol. 15:27–33
    [Google Scholar]
  7. 7. 
    Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M et al. 2009. The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiol 151:925–35
    [Google Scholar]
  8. 8. 
    Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A et al. 2012. Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. PNAS 109:20124–29
    [Google Scholar]
  9. 9. 
    Bosco D, Mason G, Accotto GP 2004. TYLCSV DNA, but not infectivity, can be transovarially inherited by the progeny of the whitefly vector Bemisia tabaci (Gennadius). Virology 323:276–83
    [Google Scholar]
  10. 10. 
    Brault V, Herrbach E, Reinbold C 2007. Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–12
    [Google Scholar]
  11. 11. 
    Caciagli P, Medina Piles V, Marian D, Vecchiati M, Masenga V et al. 2009. Virion stability is important for the circulative transmission of tomato yellow leaf curl Sardinia virus by Bemisia tabaci, but virion access to salivary glands does not guarantee transmissibility. J. Virol. 83:5784–95
    [Google Scholar]
  12. 12. 
    Chi Y, Pan LL, Bouvaine S, Fan YY, Liu YQ et al. 2019. Differential transmission of Sri Lankan cassava mosaic virus by three cryptic species of the whitefly Bemisia tabaci complex. Virology 540:141–49
    [Google Scholar]
  13. 13. 
    Collum TD, Culver JN. 2016. The impact of phytohormones on virus infection and disease. Curr. Opin. Virol. 17:25–31
    [Google Scholar]
  14. 14. 
    Colvin J, Omongo CA, Govindappa MR, Stevenson PC, Maruthi MN et al. 2006. Host-plant viral infection effects on arthropod-vector population growth, development and behaviour: management and epidemiological implications. Adv. Virus Res. 67:419–52
    [Google Scholar]
  15. 15. 
    Czosnek H, Ghanim M, Ghanim M 2002. The circulative pathway of begomoviruses in the whitefly vector Bemisia tabaci: insights from studies with tomato yellow leaf curl virus. Ann. Appl. Biol. 140:215–31
    [Google Scholar]
  16. 16. 
    Czosnek H, Ghanim M, Morin S, Rubinstein G, Fridman V, Zeidan M 2001. Whiteflies: vectors, and victims (?), of geminiviruses. Adv. Virus Res. 57:291–322
    [Google Scholar]
  17. 17. 
    Czosnek H, Hariton-Shalev A, Sobol I, Gorovits R, Ghanim M 2017. The incredible journey of begomoviruses in their whitefly vector. Viruses 9:273
    [Google Scholar]
  18. 18. 
    De Barro PJ, Liu SS, Boykin LM, Dinsdale AB 2011. Bemisia tabaci: a statement of species status. Annu. Rev. Entomol. 56:1–19
    [Google Scholar]
  19. 19. 
    Di Mattia J, Ryckebusch F, Vernerey MS, Pirolles E, Sauvion N et al. 2020. Co-acquired nanovirus and geminivirus exhibit a contrasted localization within their common aphid vector. Viruses 12:299
    [Google Scholar]
  20. 20. 
    Di Mattia J, Vernerey MS, Yvon M, Pirolles E, Villegas M et al. 2020. Route of a multipartite nanovirus across the body of its aphid vector. J. Virol. 94:9e01998–19
    [Google Scholar]
  21. 21. 
    Eigenbrode SD, Bosque-Perez NA, Davis TS 2018. Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu. Rev. Entomol. 63:169–91
    [Google Scholar]
  22. 22. 
    Fereres A. 2015. Insect vectors as drivers of plant virus emergence. Curr. Opin. Virol. 10:42–46
    [Google Scholar]
  23. 23. 
    Fiallo-Olivé E, Pan LL, Liu SS, Navas-Castillo J 2020. Transmission of begomoviruses and other whitefly-borne viruses: dependence on the vector species. Phytopathology 110:10–17
    [Google Scholar]
  24. 24. 
    Franz A, Makkouk KM, Vetten HJ 1998. Acquisition, retention and transmission of faba bean necrotic yellows virus by two of its aphid vectors, Aphis craccivora (Koch) and Acyrthosiphon pisum (Harris). J. Phytopathol. 146:347–55
    [Google Scholar]
  25. 25. 
    Franz AW, van der Wilk F, Verbeek M, Dullemans AM, van den Heuvel JF 1999. Faba bean necrotic yellows virus (genus Nanovirus) requires a helper factor for its aphid transmission. Virology 262:210–19
    [Google Scholar]
  26. 26. 
    Geng L, Qian LX, Shao RX, Liu YQ, Liu SS, Wang XW 2018. Transcriptome profiling of whitefly guts in response to tomato yellow leaf curl virus infection. Virol. J. 15:14
    [Google Scholar]
  27. 27. 
    Ghanim M, Morin S, Czosnek H 2001. Rate of tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91:188–96
    [Google Scholar]
  28. 28. 
    Ghanim M, Morin S, Zeidan M, Czosnek H 1998. Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci. Virology 240:295–303
    [Google Scholar]
  29. 29. 
    Goetz M, Popovski S, Kollenberg M, Gorovits R, Brown JK et al. 2012. Implication of Bemisia tabaci heat shock protein 70 in begomovirus-whitefly interactions. J. Virol. 86:13241–52
    [Google Scholar]
  30. 30. 
    Gottlieb Y, Zchori-Fein E, Mozes-Daube N, Kontsedalov S, Skaljac M et al. 2010. The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J. Virol. 84:9310–17
    [Google Scholar]
  31. 31. 
    Gray S, Cilia M, Ghanim M 2014. Circulative, “nonpropagative” virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Adv. Virus Res. 89:141–99
    [Google Scholar]
  32. 32. 
    Gray SM, Gildow FE. 2003. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 41:539–66
    [Google Scholar]
  33. 33. 
    Grigoras I, Gronenborn B, Vetten HJ 2010. First report of a nanovirus disease of pea in Germany. Plant Dis 94:642
    [Google Scholar]
  34. 34. 
    Grigoras I, Vetten HJ, Commandeur U, Ziebell H, Gronenborn B, Timchenko T 2018. Nanovirus DNA-N encodes a protein mandatory for aphid transmission. Virology 522:281–91
    [Google Scholar]
  35. 35. 
    Gronenborn B. 2004. Nanoviruses: genome organisation and protein function. Vet. Microbiol. 98:103–9
    [Google Scholar]
  36. 36. 
    Guo JY, Ye GY, Dong SZ, Liu SS 2010. An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity. PLOS ONE 5:e11713
    [Google Scholar]
  37. 37. 
    Guo Q, Shu Y, Liu C, Chi Y, Liu Y, Wang X 2019. Transovarial transmission of tomato yellow leaf curl virus by seven species of the Bemisia tabaci complex indigenous to China: Not all whiteflies are the same. Virology 531:240–47
    [Google Scholar]
  38. 38. 
    Guo T, Zhao J, Pan LL, Geng L, Lei T et al. 2018. The level of midgut penetration of two begomoviruses affects their acquisition and transmission by two species of Bemisia tabaci. Virology 515:66–73
    [Google Scholar]
  39. 39. 
    Hanley-Bowdoin L, Bejarano ER, Robertson D, Mansoor S 2013. Geminiviruses: masters at redirecting and reprogramming plant processes. Nat. Rev. Microbiol. 11:777–88
    [Google Scholar]
  40. 40. 
    Harrison BD, Swanson MM, Fargette D 2002. Begomovirus coat protein: serology, variation and functions. Physiol. Mol. Plant Pathol. 60:257–71
    [Google Scholar]
  41. 41. 
    Hasegawa DK, Chen W, Zheng Y, Kaur N, Wintermantel WM et al. 2018. Comparative transcriptome analysis reveals networks of genes activated in the whitefly, Bemisia tabaci when fed on tomato plants infected with tomato yellow leaf curl virus. Virology 513:52–64
    [Google Scholar]
  42. 42. 
    He WB, Li J, Liu SS 2015. Differential profiles of direct and indirect modification of vector feeding behaviour by a plant virus. Sci. Rep. 5:7682
    [Google Scholar]
  43. 43. 
    He YZ, Wang YM, Yin TY, Fiallo-Olivé E, Liu YQ et al. 2020. A plant DNA virus replicates in the salivary glands of its insect vector via recruitment of host DNA synthesis machinery. PNAS 117:16928–37
    [Google Scholar]
  44. 44. 
    Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG 2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327–59
    [Google Scholar]
  45. 45. 
    Jia Q, Liu N, Xie K, Dai Y, Han S et al. 2016. CLCuMuB βC1 subverts ubiquitination by interacting with NbSKP1s to enhance geminivirus infection in Nicotiana benthamiana. PLOS Pathog 12:e1005668
    [Google Scholar]
  46. 46. 
    Jiu M, Zhou XP, Tong L, Xu J, Yang X et al. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLOS ONE 2:e182
    [Google Scholar]
  47. 47. 
    Kanakala S, Ghanim M. 2016. Implication of the whitefly Bemisia tabaci cyclophilin B protein in the transmission of tomato yellow leaf curl virus. Front. Plant Sci. 7:1702
    [Google Scholar]
  48. 48. 
    Kazan K, Lyons R. 2014. Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26:2285–309
    [Google Scholar]
  49. 49. 
    Kumar PL, Selvarajan R, Iskra-Caruana ML, Chabannes M, Hanna R 2015. Biology, etiology, and control of virus diseases of banana and plantain. Adv. Virus Res. 91:229–69
    [Google Scholar]
  50. 50. 
    Le Trionnaire G, Tanguy S, Hudaverdian S, Gleonnec F, Richard G et al. 2019. An integrated protocol for targeted mutagenesis with CRISPR-Cas9 system in the pea aphid. Insect Biochem. Mol. Biol. 110:34–44
    [Google Scholar]
  51. 51. 
    Leshkowitz D, Gazit S, Reuveni E, Ghanim M, Czosnek H et al. 2006. Whitefly (Bemisia tabaci) genome project: analysis of sequenced clones from egg, instar, and adult (viruliferous and non-viruliferous) cDNA libraries. BMC Genom 7:79
    [Google Scholar]
  52. 52. 
    Li P, Liu C, Deng WH, Yao DM, Pan LL et al. 2019. Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors. PLOS Pathog 15:e1007607
    [Google Scholar]
  53. 53. 
    Li P, Shu YN, Fu S, Liu YQ, Zhou XP et al. 2017. Vector and nonvector insect feeding reduces subsequent plant susceptibility to virus transmission. New Phytol 215:699–710
    [Google Scholar]
  54. 54. 
    Li R, Weldegergis BT, Li J, Jung C, Qu J et al. 2014. Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell 26:4991–5008
    [Google Scholar]
  55. 55. 
    Liu J, Zhao H, Jiang K, Zhou XP, Liu SS 2009. Differential indirect effects of two plant viruses on an invasive and an indigenous whitefly vector: implications for competitive displacement. Ann. Appl. Biol. 155:439–48
    [Google Scholar]
  56. 56. 
    Liu SS, Colvin J, De Barro PJ 2012. Species concepts as applied to the whitefly Bemisia tabaci systematics: How many species are there. J. Integr. Agric. 11:176–86
    [Google Scholar]
  57. 57. 
    Lu G, Li S, Zhou C, Qian X, Xiang Q et al. 2019. Tenuivirus utilizes its glycoprotein as a helper component to overcome insect midgut barriers for its circulative and propagative transmission. PLOS Pathog 15:e1007655
    [Google Scholar]
  58. 58. 
    Luan JB, Li JM, Varela N, Wang YL, Li FF et al. 2011. Global analysis of the transcriptional response of whitefly to tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. J. Virol. 85:3330–40
    [Google Scholar]
  59. 59. 
    Luan JB, Wang XW, Colvin J, Liu SS 2014. Plant-mediated whitefly-begomovirus interactions: research progress and future prospects. Bull. Entomol. Res. 104:267–76
    [Google Scholar]
  60. 60. 
    Luan JB, Yao DM, Zhang T, Walling LL, Yang M et al. 2013. Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol. Lett. 16:390–98
    [Google Scholar]
  61. 61. 
    Makkouk KM, Kumari SG. 2009. Epidemiology and integrated management of persistently transmitted aphid-borne viruses of legume and cereal crops in West Asia and North Africa. Virus Res 141:209–18
    [Google Scholar]
  62. 62. 
    Mauck K, Bosque-Pérez NA, Eigenbrode SD, De Moraes CM, Mescher MC, Fox C 2012. Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct. Ecol. 26:1162–75
    [Google Scholar]
  63. 63. 
    Mehta P, Wyman JA, Nakhla MK, Maxwell DP 1994. Transmission of tomato yellow leaf curl geminivirus by Bemisia tabaci (Homoptera, Aleyrodidae). J. Econ. Entomol. 87:1291–97
    [Google Scholar]
  64. 64. 
    Moreno-Delafuente A, Garzo E, Moreno A, Fereres A 2013. A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLOS ONE 8:e61543
    [Google Scholar]
  65. 65. 
    Morin S, Ghanim M, Zeidan M, Czosnek H, Verbeek M, van den Heuvel J 1999. A GroEL homologue from endosymbiotic bacteria of the whitefly Bemisia tabaci is implicated in the circulative transmission of tomato yellow leaf curl virus. Virology 256:75–84
    [Google Scholar]
  66. 66. 
    Navas-Castillo J, Fiallo-Olivé E, Sanchez-Campos S 2011. Emerging virus diseases transmitted by whiteflies. Annu. Rev. Phytopathol. 49:219–48
    [Google Scholar]
  67. 67. 
    Ohnesorge S, Bejarano ER. 2009. Begomovirus coat protein interacts with a small heat-shock protein of its transmission vector (Bemisia tabaci). Insect Mol. Biol. 18:693–703
    [Google Scholar]
  68. 68. 
    Ohnishi J, Kitamura T, Terami F, Honda K 2009. A selective barrier in the midgut epithelial cell membrane of the nonvector whitefly Trialeurodes vaporariorum to tomato yellow leaf curl virus uptake. J. Gen. Plant Pathol. 75:131–39
    [Google Scholar]
  69. 69. 
    Pakkianathan BC, Kontsedalov S, Lebedev G, Mahadav A, Zeidan M et al. 2015. Replication of tomato yellow leaf curl virus in its whitefly vector. Bemisia tabaci. J. Virol. 89:9791–803
    [Google Scholar]
  70. 70. 
    Pan LL, Chen QF, Guo T, Wang XR, Li P et al. 2018. Differential efficiency of a begomovirus to cross the midgut of different species of whiteflies results in variation of virus transmission by the vectors. Sci. China Life Sci. 61:1254–65
    [Google Scholar]
  71. 71. 
    Pan LL, Chen QF, Zhao JJ, Guo T, Wang XW et al. 2017. Clathrin-mediated endocytosis is involved in tomato yellow leaf curl virus transport across the midgut barrier of its whitefly vector. Virology 502:152–59
    [Google Scholar]
  72. 72. 
    Pan LL, Cui XY, Chen QF, Wang XW, Liu SS 2018. Cotton leaf curl disease: Which whitefly is the vector. Phytopathology 108:1172–83
    [Google Scholar]
  73. 73. 
    Pirone TP, Blanc S. 1996. Helper-dependent vector transmission of plant viruses. Annu. Rev. Phytopathol. 34:227–47
    [Google Scholar]
  74. 74. 
    Ponsen MB. 1972. The Site of Potato Leafroll Virus Multiplication in its Vector, Myzus persicae: An Anatomical Study Wageningen, Neth: H. Veenman & Zonen N.V.
    [Google Scholar]
  75. 75. 
    Rana VS, Popli S, Saurav GK, Raina HS, Chaubey R et al. 2016. A Bemisia tabaci midgut protein interacts with begomoviruses and plays a role in virus transmission. Cell. Microbiol. 18:663–78
    [Google Scholar]
  76. 76. 
    Rana VS, Popli S, Saurav GK, Raina HS, Jamwal R et al. 2019. Implication of the whitefly, Bemisia tabaci, collagen protein in begomoviruses acquisition and transmission. Phytopathology 109:1481–93
    [Google Scholar]
  77. 77. 
    Rana VS, Shalini T, Priya NG, Kumar J, Rajagopal R 2012. Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLOS ONE 7:e42168
    [Google Scholar]
  78. 78. 
    Rojas MR, Macedo MA, Maliano MR, Soto-Aguilar M, Souza JO et al. 2018. World management of geminiviruses. Annu. Rev. Phytopathol. 56:637–77
    [Google Scholar]
  79. 79. 
    Rosen R, Kanakala S, Kliot A, Pakkianathan BC, Abu Farich B et al. 2015. Persistent, circulative transmission of begomoviruses by whitefly vectors. Curr. Opin. Virol. 15:1–8
    [Google Scholar]
  80. 80. 
    Roumagnac P, Granier M, Bernardo P, Deshoux M, Ferdinand R et al. 2015. Alfalfa leaf curl virus: an aphid-transmitted geminivirus. J. Virol. 89:9683–88
    [Google Scholar]
  81. 81. 
    Rubinstein G, Czosnek H. 1997. Long-term association of tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci: effect on the insect transmission capacity, longevity and fecundity. J. Gen. Virol. 78:2683–89
    [Google Scholar]
  82. 82. 
    Ryckebusch F, Sauvion N, Granier M, Roumagnac P, Peterschmitt M 2020. Alfalfa leaf curl virus is transmitted by Aphis craccivora in a highly specific circulative manner. Virology 546:98–108
    [Google Scholar]
  83. 83. 
    Sánchez-Campos S, Rodríguez-Negrete EA, Cruzado L, Grande-Pérez A, Bejarano ER et al. 2016. Tomato yellow leaf curl virus: no evidence for replication in the insect vector Bemisia tabaci. Sci. Rep 6:30942
    [Google Scholar]
  84. 84. 
    Santner A, Estelle M. 2009. Recent advances and emerging trends in plant hormone signalling. Nature 459:1071–78
    [Google Scholar]
  85. 85. 
    Saurav GK, Rana VS, Popli S, Daimei G, Rajagopal R 2019. A thioredoxin-like protein of Bemisia tabaci interacts with coat protein of begomoviruses. Virus Genes 55:356–67
    [Google Scholar]
  86. 86. 
    Savory FR, Ramakrishnan U. 2015. Cryptic diversity and habitat partitioning in an economically important aphid species complex. Infect. Genet. Evol. 30:230–37
    [Google Scholar]
  87. 87. 
    Shalev AH, Sobol I, Ghanim M, Liu SS, Czosnek H 2016. The whitefly Bemisia tabaci Knottin-1 gene is implicated in regulating the quantity of tomato yellow leaf curl virus ingested and transmitted by the insect. Viruses 8:205
    [Google Scholar]
  88. 88. 
    Shatters RG Jr., McKenzie CL, Boykin LM, Gazit S, Sinisterra X et al. 2008. A knottin-like putative antimicrobial gene family in the whitefly Bemisia tabaci biotype B: cloning and transcript regulation. J. Insect Sci. 8:44–45
    [Google Scholar]
  89. 89. 
    Sicard A, Yvon M, Timchenko T, Gronenborn B, Michalakis Y et al. 2013. Gene copy number is differentially regulated in a multipartite virus. Nat. Commun. 4:2248
    [Google Scholar]
  90. 90. 
    Sicard A, Zeddam JL, Yvon M, Michalakis Y, Gutierrez S, Blanc S 2015. Circulative nonpropagative aphid transmission of nanoviruses: an oversimplified view. J. Virol. 89:9719–26
    [Google Scholar]
  91. 91. 
    Sinisterra XH, McKenzie CL, Hunter WB, Powell CA, Shatters RG 2005. Differential transcriptional activity of plant-pathogenic begomoviruses in their whitefly vector (Bemisia tabaci, Gennadius: Hemiptera Aleyrodidae). J. Gen. Virol. 86:1525–32
    [Google Scholar]
  92. 92. 
    Stainton D, Martin DP, Muhire BM, Lolohea S, Halafihi M et al. 2015. The global distribution of banana bunchy top virus reveals little evidence for frequent recent, human-mediated long distance dispersal events. Virus Evol 1:vev009
    [Google Scholar]
  93. 93. 
    Uchibori M, Hirata A, Suzuki M, Ugaki M 2013. Tomato yellow leaf curl virus accumulates in vesicle-like structures in descending and ascending midgut epithelial cells of the vector whitefly, Bemisia tabaci, but not in those of nonvector whitefly Trialeurodes vaporariorum. J. Gen. Plant Pathol 79:115–22
    [Google Scholar]
  94. 94. 
    Wang LL, Wang XR, Wei XM, Huang H, Wu JX et al. 2016. The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies. Autophagy 12:1560–74
    [Google Scholar]
  95. 95. 
    Wang YM, He YZ, Ye XT, He WZ, Liu SS, Wang XW 2020. Whitefly HES1 binds to the intergenic region of tomato yellow leaf curl China virus and promotes viral gene transcription. Virology 542:54–62
    [Google Scholar]
  96. 96. 
    Wang ZZ, Bing XL, Liu SS, Chen XX 2017. RNA interference of an antimicrobial peptide, Btdef, reduces tomato yellow leaf curl China virus accumulation in the whitefly Bemisia tabaci. Pest Manag. Sci 73:1421–27
    [Google Scholar]
  97. 97. 
    Wang ZZ, Shi M, Huang YC, Wang XW, Stanley D, Chen XX 2016. A peptidoglycan recognition protein acts in whitefly (Bemisia tabaci) immunity and involves in begomovirus acquisition. Sci. Rep. 6:37806
    [Google Scholar]
  98. 98. 
    Watanabe S, Bressan A. 2013. Tropism, compartmentalization and retention of banana bunchy top virus (Nanoviridae) in the aphid vector Pentalonia nigronervosa. J. Gen. Virol 94:209–19
    [Google Scholar]
  99. 99. 
    Watanabe S, Greenwell AM, Bressan A 2013. Localization, concentration, and transmission efficiency of banana bunchy top virus in four asexual lineages of Pentalonia aphids. Viruses 5:758–76
    [Google Scholar]
  100. 100. 
    Wei J, He YZ, Guo Q, Guo T, Liu YQ et al. 2017. Vector development and vitellogenin determine the transovarial transmission of begomoviruses. PNAS 114:6746–51
    [Google Scholar]
  101. 101. 
    Wei J, Zhao JJ, Zhang T, Li FF, Ghanim M et al. 2014. Specific cells in the primary salivary glands of the whitefly Bemisia tabaci control retention and transmission of begomoviruses. J. Virol. 88:13460–68
    [Google Scholar]
  102. 102. 
    Xia WQ, Liang Y, Chi Y, Pan LL, Zhao J et al. 2018. Intracellular trafficking of begomoviruses in the midgut cells of their insect vector. PLOS Pathog 14:e1006866
    [Google Scholar]
  103. 103. 
    Yang JY, Iwasaki M, Machida C, Machida Y, Zhou X, Chua NH 2008. Beta C1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev 22:2564–77
    [Google Scholar]
  104. 104. 
    Yang XL, Wang B, Luan JB, Xie Y, Liu SS, Zhou XP 2017. Molecular variation of tomato yellow leaf curl virus in the insect vector Bemisia tabaci. Sci. Rep 7:16427
    [Google Scholar]
  105. 105. 
    Ye XQ, Shi M, Huang JH, Chen XX 2018. Parasitoid polydnaviruses and immune interaction with secondary hosts. Dev. Comp. Immunol. 83:124–29
    [Google Scholar]
  106. 106. 
    Zerbini FM, Briddon RW, Idris A, Martin DP, Moriones E et al. 2017. ICTV virus taxonomy profile: Geminiviridae. J. Gen. Virol. 98:131–33
    [Google Scholar]
  107. 107. 
    Zhang T, Luan JB, Qi JF, Huang CJ, Li M et al. 2012. Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Mol. Ecol. 21:1294–304
    [Google Scholar]
  108. 108. 
    Zhao J, Chi Y, Zhang XJ, Lei T, Wang XW, Liu SS 2019. Comparative proteomic analysis provides new insight into differential transmission of two begomoviruses by a whitefly. Virol. J. 16:32
    [Google Scholar]
  109. 109. 
    Zhao J, Chi Y, Zhang XJ, Wang XW, Liu SS 2019. Implication of whitefly vesicle associated membrane protein-associated protein B in the transmission of tomato yellow leaf curl virus. Virology 535:210–17
    [Google Scholar]
  110. 110. 
    Zhao P, Yao X, Cai C, Li R, Du J et al. 2019. Viruses mobilize plant immunity to deter nonvector insect herbivores. Sci. Adv. 5:eaav9801
    [Google Scholar]
  111. 111. 
    Zhou XP. 2013. Advances in understanding begomovirus satellites. Annu. Rev. Phytopathol. 51:357–81
    [Google Scholar]
/content/journals/10.1146/annurev-ento-060920-094531
Loading
/content/journals/10.1146/annurev-ento-060920-094531
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error