1887

Abstract

Alfalfa leaf curl virus (ALCV) is the first geminivirus for which aphid transmission was reported. Transmission by was determined previously to be highly specific and circulative. Using various complementary techniques, the transmission journey of ALCV was monitored from its uptake from infected plant tissues up to the head of its vector. ALCV was shown to be restricted to phloem tissues using fluorescence hybridization (FISH) and electropenetrography (EPG) monitoring of virus acquisition. Furthermore, the virus is heterogeneously distributed in phloem tissues, as revealed by FISH and quantitative PCR of viral DNA acquired by EPG-monitored aphids. Despite the efficient ingestion of viral DNA, about 10 viral DNA copies per insect in a 15 h feeding period on ALCV-infected plants, the individual maximum transmission rate was 12 %. Transmission success was related to a critical viral accumulation, around 1.6×10 viral DNA copies per insect, a threshold that generally needed more than 48 h to be reached. Moreover, whereas the amount of acquired virus did not decrease over time in the whole aphid body, it declined in the haemolymph and heads. ALCV was not detected in progenies of viruliferous aphids and did not affect aphid fitness. Compared to geminiviruses transmitted by whiteflies or leafhoppers, or to luteoviruses transmitted by aphids, the transmission efficiency of ALCV by is low. This result is discussed in relation to the aphid vector of this geminivirus and the agroecological features of alfalfa, a hardy perennial host plant.

Funding
This study was supported by the:
  • Faustine Ryckebusch , Agropolis Fondation , (Award 1504-004)
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001516
2020-11-19
2020-11-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/10.1099/jgv.0.001516/jgv001516.html?itemId=/content/journal/jgv/10.1099/jgv.0.001516&mimeType=html&fmt=ahah

References

  1. Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG. Insect vector interactions with persistently transmitted viruses. Ann Rev Phytopathol 2008; 46:327–359 [CrossRef][PubMed]
    [Google Scholar]
  2. Gray S, Gildow FE. Luteovirus-aphid interactions. Annu Rev Phytopathol 2003; 41:539–566 [CrossRef][PubMed]
    [Google Scholar]
  3. Sicard A, Zeddam J-L, Yvon M, Michalakis Y, Gutiérrez S et al. Circulative nonpropagative aphid transmission of nanoviruses: an oversimplified view. J Virol 2015; 89:9719–9726 [CrossRef][PubMed]
    [Google Scholar]
  4. Czosnek H, Ghanim M. Back to basics: are begomoviruses whitefly pathogens?. J Integr Agric 2012; 11:225–234 [CrossRef]
    [Google Scholar]
  5. Kvarnheden A, Lett J-M, Peterschmitt M. Mastreviruses: tropical and temperate leafhopper-borne geminiviruses. Vector-Mediated Transmission of Plant Pathogens St. Paul, Minnesota, USA: The American Phytopathological Society; 2016 pp 231–241
    [Google Scholar]
  6. Varsani A, Martin DP, Navas-Castillo J, Moriones E, Hernández-Zepeda C et al. Revisiting the classification of curtoviruses based on genome-wide pairwise identity. Arch Virol 2014; 159:1873–1882 [CrossRef][PubMed]
    [Google Scholar]
  7. Varsani A, Navas-Castillo J, Moriones E, Hernández-Zepeda C, Idris A et al. Establishment of three new genera in the family Geminiviridae: Becurtovirus, Eragrovirus and Turncurtovirus. Arch Virol 2014; 159:2193–2203 [CrossRef][PubMed]
    [Google Scholar]
  8. Bejerman N. Geminivirus–Vector Relationship. In Kumar R. editor Geminiviruses Springer; 2019 pp 137–145
    [Google Scholar]
  9. Roumagnac P, Granier M, Bernardo P, Deshoux M, Ferdinand R et al. Alfalfa leaf curl virus: an aphid-transmitted geminivirus. J Virol 2015; 89:9683–9688 [CrossRef][PubMed]
    [Google Scholar]
  10. Ryckebusch F, Sauvion N, Granier M, Roumagnac P, Peterschmitt M. Alfalfa leaf curl virus is transmitted by Aphis craccivora in a highly specific circulative manner. Virology 2020; 546:98–108 [CrossRef][PubMed]
    [Google Scholar]
  11. Susi H, Filloux D, Frilander MJ, Roumagnac P, Laine A-L. Diverse and variable virus communities in wild plant populations revealed by metagenomic tools. PeerJ 2019; 7:e6140 [CrossRef][PubMed]
    [Google Scholar]
  12. Nault LR. Arthropod transmission of plant viruses: a new synthesis. Ann Entomol Soc Am 1997; 90:521–541 [CrossRef]
    [Google Scholar]
  13. Oparka KJ, Turgeon R. Sieve elements and companion cells-traffic control centers of the phloem. Plant Cell 1999; 11:739–750 [CrossRef][PubMed]
    [Google Scholar]
  14. Prado E, Tjallingii WF. Aphid activities during sieve element punctures. Entomol Exp Appl 1994; 72:157–165 [CrossRef]
    [Google Scholar]
  15. Shirasawa-Seo N, Sano Y, Nakamura S, Murakami T, Gotoh Y et al. The promoter of milk vetch dwarf virus component 8 confers effective gene expression in both dicot and monocot plants. Plant Cell Rep 2005; 24:155–163 [CrossRef][PubMed]
    [Google Scholar]
  16. Peter KA, Gildow F, Palukaitis P, Gray SM. The C terminus of the polerovirus P5 readthrough domain limits virus infection to the phloem. J Virol 2009; 83:5419–5429 [CrossRef][PubMed]
    [Google Scholar]
  17. Ryabov EV, Fraser G, Mayo MA, Barker H, Taliansky M. Umbravirus gene expression helps potato leafroll virus to invade mesophyll tissues and to be transmitted mechanically between plants. Virology 2001; 286:363–372 [CrossRef][PubMed]
    [Google Scholar]
  18. Morra MR, Petty IT. Tissue specificity of geminivirus infection is genetically determined. Plant Cell 2000; 12:2259–2270 [CrossRef][PubMed]
    [Google Scholar]
  19. Wang H, Gilbertson RL, Lucas WJ. Spatial and temporal distribution of bean dwarf mosaic geminivirus in Phaseolus vulgaris and Nicotiana benthamiana. Phytopathology 1996; 86:1204–1214 [CrossRef]
    [Google Scholar]
  20. Carr RJ, Kim KS. Evidence that bean golden mosaic virus invades non-phloem tissue in double infections with tobacco mosaic virus. J Gen Virol 1983; 64:2489–2492 [CrossRef]
    [Google Scholar]
  21. Lucy AP, Boulton MI, Davies JW, Maule AJ. Tissue specificity of Zea mays infection by Maize Streak Virus. MPMI 1996; 9:22–31 [CrossRef]
    [Google Scholar]
  22. Storey HH. Investigations of the mechanism of the transmission of plant viruses by insect vectors II. The part played by puncture in transmission. Proc Roy Soc B 1938; 125:455–477
    [Google Scholar]
  23. Lett JM, Granier M, Grondin M, Turpin P, Molinaro F et al. Electrical penetration graphs from Cicadulina mbila on maize, the fine structure of its stylet pathways and consequences for virus transmission efficiency. Entomol Exp Appl 2001; 101:93–109 [CrossRef]
    [Google Scholar]
  24. Reinbold C, Herrbach E, Brault V. Posterior midgut and hindgut are both sites of acquisition of Cucurbit aphid-borne yellows virus in Myzus persicae and Aphis gossypii. J Gen Virol 2003; 84:3473–3484 [CrossRef][PubMed]
    [Google Scholar]
  25. Smith KM. Studies on potato virus diseases: IX Some further experiments on the insect transmission of potato Leaf-Roll. Ann Appl Biol 1931; 18:141–157 [CrossRef]
    [Google Scholar]
  26. Storey HH. Transmission studies of maize streak disease. Ann Appl Biol 1928; 15:1–25 [CrossRef]
    [Google Scholar]
  27. Ghanim M, Morin S, Czosnek H. Rate of tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 2001; 91:188–196 [CrossRef][PubMed]
    [Google Scholar]
  28. Wang Y, Mao Q, Liu W, Mar T, Wei T et al. Localization and distribution of wheat dwarf virus in its vector leafhopper, Psammotettix alienus. Phytopathology 2014; 104:897–904 [CrossRef][PubMed]
    [Google Scholar]
  29. Rosen R, Kanakala S, Kliot A, Cathrin Pakkianathan B, Farich BA et al. Persistent, circulative transmission of begomoviruses by whitefly vectors. Curr Opin Virol 2015; 15:1–8 [CrossRef][PubMed]
    [Google Scholar]
  30. Reynaud B, Peterschmitt M. A study of the mode of transmission of maize streak virus by Cicadulina mbila using an enzyme-linked immunosorbent assay. Ann Appl Biol 1992; 121:85–94 [CrossRef]
    [Google Scholar]
  31. Pakkianathan BC, Kontsedalov S, Lebedev G, Mahadav A, Zeidan M et al. Replication of Tomato yellow leaf curl virus in its whitefly vector, Bemisia tabaci. J Virol 2015; 89:9791–9803 [CrossRef][PubMed]
    [Google Scholar]
  32. He Y-Z, Wang Y-M, Yin T-Y, Fiallo-Olivé E, Liu Y-Q et al. A plant DNA virus replicates in the salivary glands of its insect vector via recruitment of host DNA synthesis machinery. Proc Natl Acad Sci U S A 2020; 117:16928–16937 [CrossRef][PubMed]
    [Google Scholar]
  33. Ghanim M, Morin S, Zeidan M, Czosnek H. Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci. Virology 1998; 240:295–303 [CrossRef][PubMed]
    [Google Scholar]
  34. Wei J, He Y-Z, Guo Q, Guo T, Liu Y-Q et al. Vector development and vitellogenin determine the transovarial transmission of begomoviruses. Proc Natl Acad Sci U S A 2017; 114:6746–6751 [CrossRef][PubMed]
    [Google Scholar]
  35. Rubinstein G, Czosnek H. 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 1997; 78:2683–2689 [CrossRef][PubMed]
    [Google Scholar]
  36. Becker N, Rimbaud L, Chiroleu F, Reynaud B, Thébaud G et al. Rapid accumulation and low degradation: key parameters of Tomato yellow leaf curl virus persistence in its insect vector Bemisia tabaci. Sci Rep 2015; 5:17696 [CrossRef][PubMed]
    [Google Scholar]
  37. Sánchez-Campos S, Rodríguez-Negrete EA, Cruzado L, Grande-Pérez A, Bejarano ER et al. Tomato yellow leaf curl virus: No evidence for replication in the insect vector Bemisia tabaci. Sci Rep 2016; 6:1–6 [CrossRef]
    [Google Scholar]
  38. Bosco D, Mason G, Accotto GP. TYLCSV DNA, but not infectivity, can be transovarially inherited by the progeny of the whitefly vector Bemisia tabaci (Gennadius). Virology 2004; 323:276–283 [CrossRef][PubMed]
    [Google Scholar]
  39. Wang J, Zhao H, Liu J, Jiu M, Qian YJ et al. Low frequency of horizontal and vertical transmission of two begomoviruses through whiteflies exhibits little relevance to the vector infectivity. Ann Appl Biol 2010; 157:125–133 [CrossRef]
    [Google Scholar]
  40. Di Mattia J, Ryckebusch F, Vernerey M-S, Pirolles E, Sauvion N et al. Co-Acquired nanovirus and geminivirus exhibit a contrasted localization within their common aphid vector. Viruses 2020; 12:299 [CrossRef][PubMed]
    [Google Scholar]
  41. Sicard A, Pirolles E, Gallet R, Vernerey MS, Yvon M et al. A multicellular way of life for a multipartite virus. Elife 2019; 8:e43599 [CrossRef][PubMed]
    [Google Scholar]
  42. Boissinot S, Pichon E, Sorin C, Piccini C, Scheidecker D et al. Systemic propagation of a fluorescent infectious clone of a polerovirus following inoculation by agrobacteria and aphids. Viruses 2017; 9:166 [CrossRef][PubMed]
    [Google Scholar]
  43. McLean DL, Kinsey MG. A technique for electronically recording aphid feeding and salivation. Nature 1964; 202:1358–1359 [CrossRef]
    [Google Scholar]
  44. Tjallingii WF. Electronic recording of penetration behaviour by aphids. Entomol Exp Appl 1978; 24:721–730 [CrossRef]
    [Google Scholar]
  45. Tjallingii WF. Electrical recording of stylet penetration activities. In Minks AK, Harrewijn P. (editors) Aphids, Their Biology, Natural Enemies and Control Amsterdam: Elsevier Science Publications; 1988 pp 95–108
    [Google Scholar]
  46. Tjallingii WF. Continuous recording of stylet penetration activities by aphids. In Eikenbary RCR. editor Aphid-Plant Genotype Interactions Amsterdam: Elsevier Science Publishers B.V.; 1990 pp 89–899
    [Google Scholar]
  47. Tjallingii WF, Gabryś B. Anomalous stylet punctures of phloem sieve elements by aphids. Entomol Exp Appl 1999; 91:97–103 [CrossRef]
    [Google Scholar]
  48. Jiménez J, Tjallingii WF, Moreno A, Fereres A. Newly distinguished cell punctures associated with transmission of the semipersistent phloem-limited beet yellows virus. J Virol 2018; 92:e01076–18 [CrossRef][PubMed]
    [Google Scholar]
  49. Jiménez J, Garzo E, Alba-Tercedor J, Moreno A, Fereres A et al. The phloem-pd: a distinctive brief sieve element stylet puncture prior to sieve element phase of aphid feeding behavior. Arthropod Plant Inte 2020; 14:67–78 [CrossRef]
    [Google Scholar]
  50. Jiménez J, Arias-Martín M, Moreno A, Garzo E, Fereres A. Barley yellow dwarf virus can be inoculated during brief intracellular punctures in phloem cells before the sieve element continuous salivation phase. Phytopathology 2020; 110:85–93 [CrossRef][PubMed]
    [Google Scholar]
  51. Johnson DD, Walker GP, Creamer R. Stylet penetration behavior resulting in inoculation of a semipersistently transmitted closterovirus by the whitefly Bemisia argentifolii. Entomol Exp Appl 2002; 102:115–123 [CrossRef]
    [Google Scholar]
  52. Wayadande AC, Nault LR. Leafhopper probing behavior associated with maize chlorotic dwarf virus transmission to maize. Phytopathology 1993; 83:522–526 [CrossRef]
    [Google Scholar]
  53. Tjallingii WF. Salivary secretions by aphids interacting with proteins of phloem wound responses. J Exp Bot 2006; 57:739–745 [CrossRef][PubMed]
    [Google Scholar]
  54. Billy Annan I, Schaefers GA, Tingey WM, Tjallingii WF. Stylet activity of cowpea aphid (Homoptera: Aphididae) on leaf extracts of resistant and susceptible cowpea cultivars. J Insect Behav 1997; 10:603–618 [CrossRef]
    [Google Scholar]
  55. Philippi J, Schliephake E, Jürgens HU, Jansen G, Ordon F. Feeding behavior of aphids on narrow‐leafed lupin (Lupinus angustifolius) genotypes varying in the content of quinolizidine alkaloids. Entomol Exp Appl 2015; 156:37–51 [CrossRef]
    [Google Scholar]
  56. Backus EA, Cline AR, Ellerseick MR, Serrano MS. Lugus hesperus (Hemiptera : Miridae) feeding on cotton: New methods and parameters for analysis of nonsequential electrical penetration graph data. Ann Entomol Soc Am 2007; 100:296–310 [CrossRef]
    [Google Scholar]
  57. Birch LC. The intrinsic rate of natural increase of an insect population. J Anim Ecol 1948; 17:15–26 [CrossRef]
    [Google Scholar]
  58. Wyatt IJ, White PF. Simple estimation of intrinsic increase rates for aphids and tetranychid mites. J Appl Ecol 1977; 14:757–766 [CrossRef]
    [Google Scholar]
  59. Deloach CJ. Rate of increase of populations of cabbage, green peach, and turnip Aphids1 at constant temperatures. Ann Entomol Soc Am 1974; 67:332–340 [CrossRef]
    [Google Scholar]
  60. Efron B, Kotz S. Bootstrap methods: another look at the Jackknife. Breakthroughs in Statistics Springer Series in Statistics (Perspectives in Statistics) 7 New York, NY: Springer; 1979 pp 1–26 [CrossRef]
    [Google Scholar]
  61. R Core TeamR: a language and environment for statistical computing Vienna: R Foundation for Statistical Computing; 2017 https://www.r-project.org;https://www.r-project.org;
  62. Cleveland WS, Devlin SJ. Locally weighted regression: an approach to regression analysis by local fitting. J Am Stat Assoc 1988; 83:596–610 [CrossRef]
    [Google Scholar]
  63. Jacoby WG. Loess: a nonparametric, graphical tool for depicting relationships between variables. Elect Stud 2000; 19:577–613
    [Google Scholar]
  64. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001; 29:1165–1188
    [Google Scholar]
  65. Ghanim M, Brumin M, Popovski S. A simple, rapid and inexpensive method for localization of tomato yellow leaf curl virus and potato leafroll virus in plant and insect vectors. J Virol Methods 2009; 159:311–314 [CrossRef][PubMed]
    [Google Scholar]
  66. Caciagli P, Bosco D. Quantitation over time of tomato yellow leaf curl geminivirus DNA in its whitefly vector. Phytopathology 1997; 87:610–613 [CrossRef][PubMed]
    [Google Scholar]
  67. Gray S, Cilia M, Ghanim M. Circulative,“nonpropagative” virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Adv Virus Res 2014; 89:141–199 [CrossRef][PubMed]
    [Google Scholar]
  68. Lett J-M, Granier M, Hippolyte I, Grondin M, Royer M et al. Spatial and temporal distribution of geminiviruses in leafhoppers of the genus Cicadulina monitored by conventional and quantitative polymerase chain reaction. Phytopathology 2002; 92:65–74 [CrossRef][PubMed]
    [Google Scholar]
  69. Czosnek H. Chapter 2 - Interactions of tomato yellow leaf curl virus with Its whitefly vector. In Czosnek H. editor Springer: Tomato Yellow Leaf Curl Virus Disease; 2007 pp 157–170
  70. Mehta P, Wyman JA, Nakhla MK, Maxwell DP. Transmission of tomato yellow leaf curl Geminivirns by Bemisia tabaci (Homoptera: Aleyrodidae). J Econ Entomol 1994; 87:1291–1297 [CrossRef]
    [Google Scholar]
  71. Bennett CW, Wallace HE. Relation of the curly top virus to the vector, Eutettix tenellus. J Agr Res 1938; 1938:31–52
    [Google Scholar]
  72. Tamada T, Harrison BD. Quantitative studies on the uptake and retention of potato leafroll virus by aphids in laboratory and field conditions. Ann Appl Biol 1981; 98:261–276 [CrossRef]
    [Google Scholar]
  73. Angelella G, Nalam V, Nachappa P, White J, Kaplan I. Endosymbionts differentially alter exploratory probing behavior of a nonpersistent plant virus vector. Microb Ecol 2018; 76:453–458 [CrossRef][PubMed]
    [Google Scholar]
  74. Péréfarres F, Thébaud G, Lefeuvre P, Chiroleu F, Rimbaud L et al. Frequency-Dependent assistance as a way out of competitive exclusion between two strains of an emerging virus. Proc Biol Sci 2014; 281:20133374 [CrossRef][PubMed]
    [Google Scholar]
  75. Kassanis B. Some factors affecting the transmission of leaf‐roll virus by aphids. Ann Appl Biol 1952; 39:157–167 [CrossRef]
    [Google Scholar]
  76. Czosnek H, Hariton-Shalev A, Sobol I, Gorovits R, Ghanim M. The incredible journey of begomoviruses in their whitefly vector. Viruses 2017; 9:273 [CrossRef][PubMed]
    [Google Scholar]
  77. Wang L-L, Wang X-R, Wei X-M, Huang H, Wu J-X et al. The autophagy pathway participates in resistance to tomato yellow leaf curl virus infection in whiteflies. Autophagy 2016; 12:1560–1574 [CrossRef][PubMed]
    [Google Scholar]
  78. Gildow FE, Gray SM. The aphid salivary gland basal lamina as a selective barrier associated with vector-specific transmission of barley yellow dwarf luteovirus. Phytopathology 1993; 83:1293–1302 [CrossRef]
    [Google Scholar]
  79. Wei J, Zhao J-J, Zhang T, Li FF, Ghanim M, Zhou XP et al. Specific cells in the primary salivary glands of the whitefly Bemisia tabaci control retention and transmission of begomoviruses. J Virol 2014; 88:13460–13468 [CrossRef][PubMed]
    [Google Scholar]
  80. Bernardo P, Muhire B, François S, Deshoux M, Hartnady P et al. Molecular characterization and prevalence of two capulaviruses: Alfalfa leaf curl virus from France and Euphorbia caput-medusae latent virus from South Africa. Virology 2016; 493:142–153 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001516
Loading
/content/journal/jgv/10.1099/jgv.0.001516
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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