1932

Abstract

The transmission of insect-borne plant pathogens, including viruses, bacteria, phytoplasmas, and fungi depends upon the abundance and behavior of their vectors. These pathogens should therefore be selected to influence their vectors to enhance their transmission, either indirectly, through the infected host plant, or directly, after acquisition of the pathogen by the vector. Accumulating evidence provides partial support for the occurrence of vector manipulation by plant pathogens, especially for plant viruses, for which a theoretical framework can explain patterns in the specific effects on vector behavior and performance depending on their modes of transmission. The variability in effects of pathogens on their vectors, however, suggests inconsistency in the occurrence of vector manipulation but also may reflect incomplete information about these systems. For example, manipulation can occur through combinations of specific effects, including direct and indirect effects on performance and behavior, and dynamics in those effects with disease progression or pathogen acquisition that together constitute syndromes that promote pathogen spread. Deciphering the prevalence and forms of vector manipulation by plant pathogens remains a compelling field of inquiry, but gaps and opportunities to advance it remain. A proposed research agenda includes examining vector manipulation syndromes comprehensively within pathosystems, expanding the taxonomic and genetic breadth of the systems studied, evaluating dynamic effects that occur during disease progression, incorporating the influence of biotic and abiotic environmental factors, evaluating the effectiveness of putative manipulation syndromes under field conditions, deciphering chemical and molecular mechanisms whereby pathogens can influence vectors, expanding the use of evolutionary and epidemiological models, and seeking opportunities to exploit these effects to improve management of insect-borne, economically important plant pathogens. We expect this field to remain vibrant and productive in its own right and as part of a wider inquiry concerning host and vector manipulation by plant and animal pathogens and parasites.

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2018-01-07
2024-12-12
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Literature Cited

  1. Ajayi O, Dewar AM. 1.  1983. The effect of barley yellow dwarf virus on field populations of the cereal aphids, Sitobion avenae and Metopolophium dirhodum. Ann. Appl. Biol 103:1–11 [Google Scholar]
  2. Alvarez AE, Garzo E, Verbeek M, Vosman B, Dicke M, Tjallingii WF. 2.  2007. Infection of potato plants with potato leafroll virus changes attraction and feeding behaviour of Myzus persicae. Entomol. Exp. Appl. 125:135–44 [Google Scholar]
  3. Andret-Link P, Fuchs M. 3.  2005. Transmission specificity of plant viruses by vectors. J. Plant Pathol. 87:153–65 [Google Scholar]
  4. Araya JE, Foster JE. 4.  1987. Laboratory study on the effects of Barley yellow dwarf virus on the life cycle of Rhopalosiphum padi (L.). J. Plant Dis. Prot. 94:195–98 [Google Scholar]
  5. Baker PF. 5.  1960. Aphid behavior on healthy and on yellows-virus-infected sugar beet. Ann. Appl. Biol. 48:384–91 [Google Scholar]
  6. Bautista R, Mau R, Cho J, Custer D. 6.  1995. Potential of tomato spotted wilt tospovirus plant hosts in Hawaii as virus reservoirs for transmission by Frankliniella occidentalis (Thysanoptera: Thripidae). Phytopathology 85:953–58 [Google Scholar]
  7. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW. 7.  2005. Herbivore arthropods benefit from vectoring plant viruses. Ecol. Lett. 8:70–79 [Google Scholar]
  8. Belliure B, Janssen A, Sabelis MW. 8.  2008. Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation. Oecologia 156:797–806 [Google Scholar]
  9. Biere A, Honders SC. 9.  2006. Coping with third parties in a nursery pollination mutualism: Hadena bicruris avoids oviposition on pathogen-infected, less rewarding Silene latifolia. New Phytol 169:719–27 [Google Scholar]
  10. Blua MJ, Perring TM. 10.  1992. Alatae production and population increase of aphid vectors on virus-infected host plants. Oecologia 92:65–70 [Google Scholar]
  11. Blua MJ, Perring TM. 11.  1992. Effects of zucchini yellow mosaic virus on colonization and feeding behavior of Aphis gossypii (Homoptera: Aphididae) alatae. Environ. Entomol. 21:578–85 [Google Scholar]
  12. Boquel S, Delayen C, Couty A, Giordanengo P. 12.  2012. Modulation of aphid vector activity by Potato virus Y on in vitro potato plants. Plant Dis 96:82–86 [Google Scholar]
  13. Bosque-Pérez NA, Eigenbrode SD. 13.  2011. The influence of virus-induced changes in plants on aphid vectors: insights from luteovirus pathosystems. Virus Res 159:201–5 [Google Scholar]
  14. Calvo D, Fereres A. 14.  2011. The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus. BioControl 56:747–57 [Google Scholar]
  15. Carmo-Sousa M, Moreno A, Garzo E, Fereres A. 15.  2014. A non-persistently transmitted-virus induces a pull-push strategy in its aphid vector to optimize transmission and spread. Virus Res 186:38–46 [Google Scholar]
  16. Carmo-Sousa M, Moreno A, Plaza M, Garzo E, Fereres A. 16.  2016. Cucurbit aphid-borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Ann. Appl. Biol. 169:284–97 [Google Scholar]
  17. Casteel CL, De Alwis M, Bak A, Dong H, Whitham SA, Jander G. 17.  2015. Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol 169:209–18 [Google Scholar]
  18. Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA, Jander G. 18.  2014. The NIa-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant J 77:653–63 [Google Scholar]
  19. Castle SJ, Berger PH. 19.  1993. Rates of growth and increase of Myzus persicae on virus-infected potatoes according to type of virus-vector relationship. Entomol. Exp. Appl. 69:51–60A classic study that demonstrated that the indirect effects of virus infection on a shared vector (Myzus persicae) differed among viruses that differed in mode of transmission. [Google Scholar]
  20. Castle SJ, Mowry TM, Berger PH. 20.  1998. Differential settling by Myzus persicae (Homoptera: Aphididae) on various virus infected host plants. Ann. Entomol. Soc. Am. 91:661–67Demonstrated differences in host settling behavior consistent with the previously demonstrated effects on performance; first demonstration together with 17 differing vector manipulation syndromes. [Google Scholar]
  21. Chen AYS, Walker GP, Carter D, Ng JCK. 21.  2011. A virus capsid component mediates virion retention and transmission by its insect vector. PNAS 108:16777–82 [Google Scholar]
  22. Chen Y, Lu C, Li M, Wu W, Zhou G, Wei T. 22.  2016. Adverse effects of rice gall dwarf virus upon its insect vector Recilia dorsalis (Hemiptera: Cicadellidae). Plant Dis 100:784–90 [Google Scholar]
  23. Colvin J, Omongo CA, Govindappa MR, Stevenson PC, Maruthi MN. 23.  et al. 2006. Host-plant viral infection effects on arthropod-vector population growth, development and behaviour: management and epidemiological implications. Advances in Virus Research JM Thresh 419–52 San Diego: CA: Academic [Google Scholar]
  24. Costa HS, Brown JK, Byrne DN. 24.  1991. Life history traits of the whitefly, Bemisiatabaci (Homoptera: Aleyrodidae) on six virus-infected or healthy plant species. Environ. Entomol. 20:1102–7 [Google Scholar]
  25. Daugherty MP, Rashed A, Almeida RPP, Perring TM. 25.  2011. Vector preference for hosts differing in infection status: sharpshooter movement and Xylella fastidiosa transmission. Ecol. Entomol. 36:654–62 [Google Scholar]
  26. Davis TS, Bosque-Pérez NA, Foote NE, Magney T, Eigenbrode SD. 26.  2015. Environmentally dependent host–pathogen and vector–pathogen interactions in the Barley yellow dwarf virus pathosystem. J. Appl. Ecol. 52:1392–401 [Google Scholar]
  27. Davis TS, Bosque-Pérez NA, Popova I, Eigenbrode SD. 27.  2015. Evidence for additive effects of virus infection and water availability on phytohormone induction in a staple crop. Front. Ecol. Evol. 3:114 [Google Scholar]
  28. Davis TS, Horton DR, Munyaneza JE, Landolt PJ. 28.  2012. Experimental infection of plants with an herbivore-associated bacterial endosymbiont influences herbivore host selection behavior. PLOS ONE 7:11e49330 [Google Scholar]
  29. Davis TS, Wu Y, Eigenbrode SD. 29.  2017. The effects of Bean leafroll virus on life history traits and host selection behavior of specialized pea aphid (Acyrthosiphon pisum, Hemiptera: Aphididae) genotypes. Environ. Entomol. 46:68–74 [Google Scholar]
  30. de Moraes CM, Stanczyk NM, Betz HS, Pulido H, Sim DG. 30.  et al. 2014. Malaria-induced changes in host odors enhance mosquito attraction. PNAS 111:11079–84 [Google Scholar]
  31. de Oliveira CF, Long EY, Finke DL. 31.  2014. A negative effect of a pathogen on its vector? A plant pathogen increases the vulnerability of its vector to attack by natural enemies. Oecologia 174:1169–77 [Google Scholar]
  32. DeAngelis JD, Sether DM, Rossignol PA. 32.  1993. Survival, development, and reproduction in Western flower thrips (Thysanoptera, Thripidae) exposed to Impatiens necrotic spot virus. Environ. Entomol. 22:1308–12 [Google Scholar]
  33. Donaldson JR, Gratton C. 33.  2007. Antagonistic effects of soybean viruses on soybean aphid performance. Environ. Entomol. 36:918–25 [Google Scholar]
  34. Döring TF, Chittka L. 34.  2007. Visual ecology of aphids—a critical review on the role of colours in host finding. Arthropod-Plant Interact 1:3–16 [Google Scholar]
  35. dos Santos RC, Penaflor M, Sanches PA, Nardi C, Bento JMS. 35.  2016. The effects of Gibberella zeae, Barley Yellow Dwarf Virus, and co-infection on Rhopalosiphum padi olfactory preference and performance. Phytoparasitica 44:47–54 [Google Scholar]
  36. Dötterl S, Jürgens A, Wolfe L, Biere A. 36.  2009. Disease status and population origin effects on floral scent: potential consequences for oviposition and fruit predation in a complex interaction between a plant, fungus, and noctuid moth. J. Chem. Ecol. 35:307–19 [Google Scholar]
  37. Eigenbrode SD, Bosque-Pérez NA. 37.  2016. Chemical ecology of aphid-transmitted plant viruses. Vector-Mediated Transmission of Plant Pathogens JK Brown 3–19 St. Paul, MN: APS Press [Google Scholar]
  38. Eigenbrode SD, Ding H, Shiel P, Berger PH. 38.  2002. Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc. R. Soc. B 269:455–60Demonstrated that volatile organic compounds (VOCs) emitted from infected plants differed among viruses with differing modes of transmission and that settling by vectors in response to these VOCs differed among the viruses. [Google Scholar]
  39. Ellsbury MM, Pratt RG, Knight WE. 39.  1985. Effects of single and combined infection of arrowleaf clover with bean yellow mosaic virus and a Phytophthora sp. on reproduction and colonization by pea aphids (Homoptera, Aphididae). Environ. Entomol. 14:356–359 [Google Scholar]
  40. Fereres A, Kampmeier GE, Irwin ME. 40.  1999. Aphid attraction and preference for soybean and pepper plants infected with potyviridae. Ann. Entomol. Soc. Am. 92:542–48 [Google Scholar]
  41. Fereres A, Moreno A. 41.  2009. Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res 141:158–68 [Google Scholar]
  42. Fereres A, Peñaflor M, Favaro C, Azevedo K, Landi C. 42.  et al. 2016. Tomato infection by whitefly-transmitted circulative and non-circulative viruses induce contrasting changes in plant volatiles and vector behaviour. Viruses 8:225–40Documented differences in vector manipulation of a whitefly. [Google Scholar]
  43. Fiebig M, Poehling H-M, Borgemeister C. 43.  2004. Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions. Entomol. Exp. Appl. 110:11–21 [Google Scholar]
  44. Gandon S. 44.  2017. Evolution and manipulation of vector host choice. bioRxiv 110577. http://doi.org/10.1101/110577 [Crossref]
  45. Garzon A, Budia F, Morales I, Fereres A, Vinuela E, Medina P. 45.  2016. Do Chrysoperla carnea and Adalia bipunctata influence the spread of Cucurbit aphid-borne yellows virus and its vector Aphis gossypii?. Ann. Appl. Biol. 169:106–15 [Google Scholar]
  46. Ghosh A, Das A, Vijayanandraj S, Mandal B. 46.  2016. Cardamom bushy dwarf virus infection in large cardamom alters plant selection preference, life stages, and fecundity of aphid vector, Micromyzus kalimpongensis (Hemiptera: Aphididae). Environ. Entomol 45:178–84 [Google Scholar]
  47. Guo J-Y, Dong S-Z, Yang X-l, Cheng L, Wan F-H. 47.  et al. 2012. Enhanced vitellogenesis in a whitefly via feeding on a begomovirus-infected plant. PLOS ONE 7:e43567 [Google Scholar]
  48. Guo J-Y, Ye G-Y, Dong S-Z, Liu S-S. 48.  2010. An invasive whitefly feeding on a virus-infected plant increased its egg production and realized fecundity. PLOS ONE 5:e11713 [Google Scholar]
  49. Hodge S, Powell G. 49.  2008. Do plant viruses facilitate their aphid vectors by inducing symptoms that alter behavior and performance?. Environ. Entomol. 37:1573–81 [Google Scholar]
  50. Hodge S, Powell G. 50.  2010. Conditional facilitation of an aphid vector, Acyrthosiphon pisum, by the plant pathogen, pea enation mosaic virus. J. Insect Sci. 10:155 [Google Scholar]
  51. Hodgson CJ. 51.  1981. Effects of infection with the cabbage black ringspot strain of turnip mosaic virus on turnip as a host to Myzus persicae and Brevicoryne brassicae. Ann. Appl. Biol. 98:1–14 [Google Scholar]
  52. Holmes JC, Bethel WM. 52.  1972. Modification of intermediate host behaviour by parasites. Behavioral Aspects of Parasite Transmission EU Canning, CA Wright 123–49 New York: Academic [Google Scholar]
  53. Hulcr J, Mann R, Stelinski L. 53.  2011. The scent of a partner: Ambrosia beetles are attracted to volatiles from their fungal symbionts. J. Chem. Ecol. 37:1374–77 [Google Scholar]
  54. Hurd H. 54.  2003. Manipulation of medically important insect vectors by their parasites. Annu. Rev. Entomol. 48:141–61 [Google Scholar]
  55. Imo M, Maixner M, Johannesen J. 55.  2013. Sympatric diversification v. immigration: deciphering host-plant specialization in a polyphagous insect, the stolbur phytoplasma vector Hyalesthes obsoletus (Cixiidae). Mol. Ecol. 22:2188–203 [Google Scholar]
  56. Ingwell LL, Eigenbrode SD, Bosque-Pérez NA. 56.  2012. Plant viruses alter insect behavior to enhance their spread. Sci. Rep. 2:578Demonstrated direct effects of a persistent, nonpropagative virus on its vector, resulting in a switch in preference for infected to healthy plants after virus acquisition by the vector; proposed the vector manipulation hypothesis. [Google Scholar]
  57. Jennersten O. 57.  1988. Insect dispersal of fungal disease: effects of Ustilago infection on pollinator attraction in Viscaria vulgaris. Oikos 51:163–70 [Google Scholar]
  58. Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS. 58.  2004. Life history of the bird cherry-oat aphid, Rhopalosiphum padi (Homoptera: Aphididae), on transgenic and untransformed wheat challenged with Barley yellow dwarf virus. J. Econ. Entomol 97:203–12 [Google Scholar]
  59. Jiménez-Martínez ES, Bosque-Pérez NA, Berger PH, Zemetra RS, Ding H, Eigenbrode SD. 59.  2004. Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ. Entomol. 33:1207–16 [Google Scholar]
  60. Jiu M, Zhou X-P, Tong L, Xu J, Yang X. 60.  et al. 2007. Vector-virus mutualism accelerates population increase of an invasive whitefly. PLOS ONE 2:1e182 [Google Scholar]
  61. Jones RAC. 61.  2014. Plant virus ecology and epidemiology: historical perspectives, recent progress and future prospects. Ann. Appl. Biol. 164:320–47 [Google Scholar]
  62. Kaul C, Seitz A, Maixner M, Johannesen J. 62.  2009. Infection of Bois-Noir tuf-type-I stolbur phytoplasma in Hyalesthes obsoletus (Hemiptera: Cixiidae) larvae and influence on larval size. J. Appl. Entomol. 133:596–601 [Google Scholar]
  63. Kennedy JS. 63.  1951. Benefits to aphids from feeding on galled and virus-infected leaves. Nature 168:825–26This paper provided one of the earliest reports of virus infection of the host plant improving the performance of its vector. [Google Scholar]
  64. Kersch-Becker MF, Thaler JS. 64.  2014. Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores. Oecologia 174:883–92 [Google Scholar]
  65. Khan Z, Saxena C. 65.  1985. Behavior and biology of Nephotettix virescens (Homoptera: Cicadellidae) on Tungro virus-infected rice plants: epidemiology implications. Environ. Entomol. 14:297–304 [Google Scholar]
  66. Lapidot M, Friedmann M, Pilowsky M, Ben-Joseph R, Cohen S. 66.  2001. Effect of host plant resistance to Tomato yellow leaf curl virus (TYLCV) on virus acquisition and transmission by its whitefly vector. Phytopathology 91:1209–13 [Google Scholar]
  67. Lefèvre T, Thomas F. 67.  2008. Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect. Genet. Evol. 8:504–19 [Google Scholar]
  68. Legarrea S, Barman A, Marchant W, Diffie S, Srinivasan R. 68.  2015. Temporal effects of a Begomovirus infection and host plant resistance on the preference and development of an insect vector, Bemisia tabaci, and implications for epidemics. PLOS ONE 10:e0142114 [Google Scholar]
  69. Li M, Liu J, Liu SS. 69.  2011. Tomato yellow leaf curl virus infection of tomato does not affect the performance of the Q and ZHJ2 biotypes of the viral vector Bemisia tabaci. Insect Sci 18:40–49 [Google Scholar]
  70. Liu B, Preisser EL, Chu D, Pan H, Xie W. 70.  et al. 2013. Multiple forms of vector manipulation by a plant-infecting virus: Bemisia tabaci and Tomato yellow leaf curl virus. J. Virol. 87:4929–37 [Google Scholar]
  71. Liu J, Li M, Li J-m, Huang C-j, Zhou X-p. 71.  et al. 2010. Viral infection of tobacco plants improves performance of Bemisia tabaci but more so for an invasive than for an indigenous biotype of the whitefly. J. Zhejiang Univ. Sci. B 11:30–40 [Google Scholar]
  72. Liu J, Zhao H, Jiang K, Zhou X-P, Liu S-S. 72.  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]
  73. Liu X-F, Hu X-S, Keller MA, Zhao H-Y, Wu Y-F, Liu T-X. 73.  2014. Tripartite interactions of Barley yellow dwarf virus, Sitobion avenae and wheat varieties. PLOS ONE 9:9e106639 [Google Scholar]
  74. Lu G, Zhang T, He Y, Zhou G. 74.  2016. Virus altered rice attractiveness to planthoppers is mediated by volatiles and related to virus titre and expression of defence and volatile-biosynthesis genes. Sci. Rep. 6:38581 [Google Scholar]
  75. Luan J-B, Wang X-W, Colvin J, Liu S-S. 75.  2014. Plant-mediated whitefly–begomovirus interactions: research progress and future prospects. Bull. Entomol. Res. 104:267–76 [Google Scholar]
  76. Luan J-B, Yao D-M, Zhang T, Walling LL, Yang M. 76.  et al. 2013. Suppression of terpenoid synthesis in plants by a virus promotes its mutualism with vectors. Ecol. Lett. 16:390–98 [Google Scholar]
  77. Macias W, Mink GI. 77.  1969. Preference of green peach aphids for virus-infected sugarbeet leaves. J. Econ. Entomol. 62:28–29 [Google Scholar]
  78. Maixner M, Albert A, Johannesen J. 78.  2014. Survival relative to new and ancestral host plants, phytoplasma infection, and genetic constitution in host races of a polyphagous insect disease vector. Ecol. Evol. 4:3082–92 [Google Scholar]
  79. Malagnini V, Pedrazzoli F, Gualandri V, Forno F, Zasso R. 79.  et al. 2010. A study of the effects of “Candidatus Phytoplasma mali” on the psyllid Cacopsylla melanoneura (Hemiptera: Psyllidae). J. Invertebr. Pathol. 103:65–67 [Google Scholar]
  80. Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS. 80.  et al. 2012. Induced release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. PLOS Path 8:3e1002610 [Google Scholar]
  81. Mann RS, Sidhu JS, Butter NS. 81.  2009. Settling preference of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae) on healthy versus cotton leaf curl virus-infected cotton plants. Int. J. Trop. Insect Sci. 29:57–61 [Google Scholar]
  82. Maris PC, Joosten NN, Goldbach RW, Peters D. 82.  2004. Tomato spotted wiltvirus infection improves host suitability for its vector Frankliniella occidentalis. Phytopathology 94:706–11 [Google Scholar]
  83. Martini X, Hoffmann M, Coy MR, Stelinski LL, Pelz-Stelinski KS. 83.  2015. Infection of an insect vector with a bacterial plant pathogen increases its propensity for dispersal. PLOS ONE 10:e0129373 [Google Scholar]
  84. Martini X, Pelz-Stelinski KS, Stelinski LL. 84.  2014. Plant pathogen-induced volatiles attract parasitoids to increase parasitism of an insect vector. Front. Ecol. Evol. 2:646–49 [Google Scholar]
  85. Mas F, Vereijssen J, Suckling DM. 85.  2014. Influence of the pathogen Candidatus Liberibacter solanacearum on tomato host plant volatiles and psyllid vector settlement. J. Chem. Ecol. 40:1197–202 [Google Scholar]
  86. Matsuura S, Hoshino S. 86.  2009. Effect of tomato yellow leaf curl disease on reproduction of Bemisia tabaci Q biotype (Hemiptera: Aleyrodidae) on tomato plants. Appl. Entomol. Zool. 44:143–48 [Google Scholar]
  87. Mauck K, Bosque-Pérez NA, Eigenbrode SD, DeMoraes CM, Mescher MC. 87.  2012. Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Funct. Ecol. 26:1162–75Seminal review showing that trends in indirect effects of plant viruses on vectors differed between persistently transmitted and nonpersistently transmitted viruses. [Google Scholar]
  88. Mauck K, De Moraes C, Mescher M. 88.  2014. Evidence of local adaptation in plant virus effects on host–vector interactions. Integr. Comp. Biol. 54:193–209 [Google Scholar]
  89. Mauck KE. 89.  2016. Variation in virus effects on host plant phenotypes and insect vector behavior: What can it teach us about virus evolution?. Curr. Opin. Virol. 21:114–23A review paper describing the effects of genetic and phenotypic variability of host plants and viruses on the specifics of vector manipulation. [Google Scholar]
  90. Mauck KE, De Moraes CM, Mescher MC. 90.  2010. Effects of Cucumber mosaic virus infection on vector and non-vector herbivores of squash. Commun. Integr. Biol. 3:579–82 [Google Scholar]
  91. Mauck KE, De Moraes CM, Mescher MC. 91.  2010. Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. PNAS 107:3600–5Working with the Cucumber mosaic virus–Cucurbita pepo system, the study elucidated for the first time the attract-then-repel strategy of a nonpersistent virus. [Google Scholar]
  92. Mauck KE, De Moraes CM, Mescher MC. 92.  2014. Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host-plant traits that mediate transmission by aphid vectors. Plant Cell Environ 37:1427–39 [Google Scholar]
  93. Mauck KE, Smyers E, De Moraes CM, Mescher MC. 93.  2015. Virus infection influences host plant interactions with non-vector herbivores and predators. Funct. Ecol. 29:662–73 [Google Scholar]
  94. Mayer CJ, Vilcinskas A, Gross J. 94.  2008. Pathogen-induced release of plant allomone manipulates vector insect behavior. J. Chem. Ecol. 34:1518–22 [Google Scholar]
  95. Mayer CJ, Vilcinskas A, Gross J. 95.  2008. Phytopathogen lures its insect vector by altering host plant odor. J. Chem. Ecol. 34:1045–49 [Google Scholar]
  96. Mayer CJ, Vilcinskas A, Gross J. 96.  2011. Chemically mediated multitrophic interactions in a plant–insect vector-phytoplasma system compared with a partially nonvector species. Agric. For. Entomol. 13:25–35 [Google Scholar]
  97. McElhany P, Real LA, Power AG. 97.  1995. Vector preference and disease dynamics: a study of barley yellow dwarf virus. Ecology 76:444–57 [Google Scholar]
  98. McKenzie C. 98.  2002. Effect of tomato mottle virus (ToMoV) on Bemisia tabaci biotype B (Homoptera: Aleyrodidae) oviposition and adult survivorship on healthy tomato. Fla. Entomol. 85:367–68 [Google Scholar]
  99. McLeod G, Gries R, von Reuß SH, Rahe JE, McIntosh R. 99.  et al. 2005. The pathogen causing Dutch elm disease makes host trees attract insect vectors. Proc. R. Soc. B 272:2499–503 [Google Scholar]
  100. Medina-Ortega K, Bosque-Pérez NA, Ngumbi E, Jiménez-Martínez ES, Eigenbrode SD. 100.  2009. Rhopalosiphum padi (Hemiptera: Aphididae) behavioral responses to barley yellow dwarf virus-infected wheat. Environ. Entomol. 38:836–45 [Google Scholar]
  101. Mesfin T, Bosque-Pérez NA. 101.  1998. Feeding behaviour of Cicadulina storeyi China (Homoptera: Cicadellidae) on maize varieties susceptible or resistant to maize streak virus. Afr. Entomol. 6:185–91 [Google Scholar]
  102. Miller JW, Coon BF. 102.  1964. The effect of barley yellow dwarf virus on the biology of its vector, the English grain aphid, Macrosiphum granarium. J. Econ. Entomol. 57:970–74 [Google Scholar]
  103. Montllor CB, Gildow FE. 103.  1986. Feeding responses of two grain aphids to barley yellow dwarf virus-infected oats. Entomol. Exp. Appl. 42:63–69 [Google Scholar]
  104. Moreno-Delafuente A, Garzo E, Moreno A, Fereres A. 104.  2013. A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLOS ONE 8:e61543 [Google Scholar]
  105. Musser RO, Hum-Musser SM, Felton GW, Gergerich RC. 105.  2003. Increased larval growth and preference for virus-infected leaves by the Mexican bean beetle, Epilachnavarivestis Mulsant, a plant virus vector. J. Insect Behav. 16:247–56 [Google Scholar]
  106. Nachappa P, Margolies DC, Nechols JR, Whitfield AE, Rotenberg D. 106.  2013. Tomato spotted wilt virus benefits a non-vector arthropod, Tetranychus urticae, by modulating different plant responses in tomato. PLOS ONE 8:9e75909 [Google Scholar]
  107. Nancarrow N, Constable FE, Finlay KJ, Freeman AJ, Rodoni BC. 107.  et al. 2014. The effect of elevated temperature on Barley yellow dwarf virus-PAV in wheat. Virus Res 186:97–103 [Google Scholar]
  108. Narayandas GK, Alyokhin AV. 108.  2006. Interplant movement of potato aphid (Homoptera: aphididae) in response to environmental stimuli. Environ. Entomol. 35:733–39 [Google Scholar]
  109. Nault LR. 109.  1997. Arthropod transmission of plant viruses: a new synthesis. Ann. Entomol. Soc. Am. 90:521–41 [Google Scholar]
  110. Ng JCK, Perry KL. 110.  2004. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 5:505–11 [Google Scholar]
  111. Ngumbi E, Eigenbrode SD, Bosque-Pérez NA, Ding H, Rodriguez A. 111.  2007. Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato. J. Chem. Ecol. 33:1733–47 [Google Scholar]
  112. Ogada PA, Moualeu DP, Poehling H-M. 112.  2016. Predictive models for Tomato spotted wilt virus spread dynamics, considering Frankliniella occidentalis specific life processes as influenced by the virus. PLOS ONE 11:5e0154533 [Google Scholar]
  113. Pan H, Chu D, Liu B, Shi X, Guo L. 113.  et al. 2013. Differential effects of an exotic plant virus on its two closely related vectors. Sci. Rep. 3:2230 [Google Scholar]
  114. Pelz-Stelinski K, Brlansky R, Ebert T, Rogers M. 114.  2010. Transmission parameters for Candidatus Liberibacter asiaticus by Asian citrus psyllid (Hemiptera: Psyllidae). J. Econ. Entomol. 103:1531–41 [Google Scholar]
  115. Pelz-Stelinski KS, Killiny N. 115.  2016. Better together: Association with ‘Candidatus Liberibacter asiaticus’ increases the reproductive fitness of its insect vector, Diaphorina citri (Hemiptera: Liviidae). Ann. Entomol. Soc. Am. 109:371–76 [Google Scholar]
  116. Perilla-Henao LM, Casteel CL. 116.  2016. Vector-borne bacterial plant pathogens: interactions with hemipteran insects and plants. Front. Plant Sci. 7:1163 [Google Scholar]
  117. Power A. 117.  1996. Competition between viruses in a complex plant-pathogen system. Ecology 77:1004–10 [Google Scholar]
  118. Purcell A. 118.  1988. Increased survival of Dalbulus maidis, a specialist on maize, on non-host plants infected with mollicute plant pathogens. Entomol. Exp. Appl. 46:187–96 [Google Scholar]
  119. Rajabaskar D, Bosque-Pérez NA, Eigenbrode SD. 119.  2014. Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Res 186:32–37 [Google Scholar]
  120. Rajabaskar D, Ding H, Wu Y, Eigenbrode SD. 120.  2013. Different reactions of potato varieties to infection by Potato leafroll virus, and associated responses by its vector, Myzus persicae (Sulzer). J. Chem. Ecol. 39:1027–35 [Google Scholar]
  121. Rajabaskar D, Wu Y, Bosque-Pérez NA, Eigenbrode SD. 121.  2013. Dynamics of Myzus persicae arrestment by volatiles from Potato leafroll virus-infected potato plants during disease progression. Entomol. Exp. Appl. 148:172–81 [Google Scholar]
  122. Roosien BK, Gomulkiewicz R, Ingwell LL, Bosque-Pérez NA, Rajabaskar D, Eigenbrode SD. 122.  2013. Conditional vector preference aids the spread of plant pathogens. Environ. Entomol. 42:1299–308 [Google Scholar]
  123. Roossinck MJ. 123.  2012. Plant virus metagenomics: biodiversity and ecology. Annu. Rev. Genet. 46:357–67 [Google Scholar]
  124. Rostás M, Simon M, Hilker M. 124.  2003. Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl. Ecol. 4:43–62 [Google Scholar]
  125. Rubinstein G, Czosnek H. 125.  1997. Long-term association of tomato yellow leaf curl virus with its whitefly vector Bemisia tabaci, effect of the insect transmission capacity, longevity and fecundity. J. Gen. Virol. 78:2683–89 [Google Scholar]
  126. Salvaudon L, De Moraes CM, Mescher MC. 126.  2013. Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies. Proc. R. Soc. B 280:20122959 [Google Scholar]
  127. Santini A, Faccoli M. 127.  2015. Dutch elm disease and elm bark beetles: a century of association. iForest 8:126–34 [Google Scholar]
  128. Shalileh S, Ogada PA, Moualeu DP, Poehling H-M. 128.  2016. Manipulation of Frankliniella occidentalis (Thysanoptera: Thripidae) by Tomato spotted wilt virus (Tospovirus) via the host plant nutrients to enhance is transmission and spread. Environ. Entomol. 45:1235–42 [Google Scholar]
  129. Shapiro L, De Moraes CM, Stephenson AG, Mescher MC. 129.  2012. Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecol. Lett. 15:1430–38 [Google Scholar]
  130. Shaw AK, Peace A, Power AG, Bosque-Pérez NA. 130.  2017. Vector population growth and condition-dependent movement drive the spread of plant pathogens. Ecology 98:2145–57 [Google Scholar]
  131. Shrestha A, Srinivasan R, Riley DG, Culbreath AK. 131.  2012. Direct and indirect effects of a thrips-transmitted Tospovirus on the preference and fitness of its vector, Frankliniella fusca. Entomol. Exp. Appl. 145:260–71 [Google Scholar]
  132. Sisterson MS. 132.  2008. Effects of insect-vector preference for healthy or infected plants on pathogen spread: insights from a model. J. Econ. Entomol. 101:1–8 [Google Scholar]
  133. Srinivasan R, Alvarez JM. 133.  2007. Effect of mixed viral infections (Potato virus YPotato leaf roll virus) on biology and preference of vectors Myzus persicae and Macrosiphum euphorbiae (Hemiptera: Aphididae). J. Econ. Entomol. 100:646–55 [Google Scholar]
  134. Srinivasan R, Alvarez JM, Bosque-Pérez NA, Eigenbrode SD, Novy RG. 134.  2008. Effect of an alternate weed host, hairy nightshade, Solanum sarrachoides, on the biology of the two most important Potato leafroll virus (Luteoviridae: Polerovirus) vectors, Myzus persicae and Macrosiphum euphorbiae (Aphididae: Homoptera). Environ. Entomol 37:592–600 [Google Scholar]
  135. Srinivasan R, Alvarez JM, Eigenbrode SD, Bosque-Perez NA. 135.  2006. Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae: Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera: Aphididae). Environ. Entomol. 35:546–53 [Google Scholar]
  136. Stafford CA, Walker GP, Ullman DE. 136.  2011. Infection with a plant virus modifies vector feeding behavior. PNAS 108:9350–55Demonstrated that feeding behavior of male thrips, Frankliniella occidentalis, changed (fed more) after virus acquisition; findings based on electronic penetration graph recordings. [Google Scholar]
  137. 137.  Deleted in proof
  138. Su Q, Mescher MC, Wang SL, Chen G, Xie W. 138.  et al. 2016. Tomato yellow leaf curl virus differentially influences plant defence responses to a vector and a non-vector herbivore. Plant Cell Environ 39:597–607 [Google Scholar]
  139. Su Q, Preisser EL, Zhou XM, Xie W, Liu BM. 139.  et al. 2015. Manipulation of host quality and defense by a plant virus improves performance of whitefly vectors. J. Econ. Entomol. 108:11–19 [Google Scholar]
  140. Tasin M, Knudsen G, Pertot I. 140.  2012. Smelling a diseased host: grapevine moth responses to healthy and fungus-infected grapes. Anim. Behav. 83:555–62 [Google Scholar]
  141. Thompson WMO. 141.  2002. Comparison of Bemisia tabaci (Homoptera: Aleyrodidae) development on uninfected cassava plants and cassava plants infected with East African cassava mosaic virus. Ann. Entomol. Soc. Am. 95:387–94 [Google Scholar]
  142. Thompson WMO. 142.  2011. The performance of viruliferous and non-viruliferous cassava biotype Bemisia tabaci on amino acid diets. The Whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) Interaction with Geminivirus-Infected Host Plants WMO Thompson 165–80 Dordrecht, Neth.: Springer [Google Scholar]
  143. Trębicki P, Nancarrow N, Cole E, Bosque-Pérez NA, Constable FE. 143.  et al. 2015. Virus disease in wheat predicted to increase with a changing climate. Glob. Change Biol. 21:3511–19 [Google Scholar]
  144. Trębicki P, Vandegeer RK, Bosque-Pérez NA, Powell KS, Dader B. 144.  et al. 2016. Virus infection mediates the effects of elevated CO2 on plants and vectors. Sci. Rep. 6:22785 [Google Scholar]
  145. Uzest M, Gargani D, Drucker M, Hebrard E, Garzo E. 145.  et al. 2007. A protein key to plant virus transmission at the tip of the insect vector stylet. PNAS 104:17959–64 [Google Scholar]
  146. Weintraub PG, Beanland L. 146.  2006. Insect vectors of phytoplasmas. Annu. Rev. Entomol. 51:91–111 [Google Scholar]
  147. Werner BJ, Mowry TM, Bosque-Pérez NA, Ding H, Eigenbrode SD. 147.  2009. Changes in green peach aphid responses to potato leafroll virus–induced volatiles emitted during disease progression. Environ. Entomol. 38:1429–38 [Google Scholar]
  148. Whitfield AE, Rotenberg D. 148.  2015. Disruption of insect transmission of plant viruses. Curr. Opin. Insect Sci. 8:79–87 [Google Scholar]
  149. Williams CT. 149.  1995. Effects of plant age, leaf age and virus yellows infection on the population dynamics of Myzus persicae (Homoptera: Aphididae) on sugarbeet in field plots. Bull. Entomol. Res. 85:557–67 [Google Scholar]
  150. Wosula EN, Davis JA, Clark CA. 150.  2013. Population dynamics of three aphid species (Hemiptera: Aphididae) on four Ipomoea spp. infected or noninfected with sweetpotato potyviruses. J. Econ. Entomol. 106:1566–73 [Google Scholar]
  151. Wu Y, Davis TS, Eigenbrode SD. 151.  2014. Aphid behavioral responses to virus-infected plants are similar despite divergent fitness effects. Entomol. Exp. Appl. 153:246–55 [Google Scholar]
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