Aphid–Plant–Phytovirus Pathosystems: Influencing Factors from Vector Behaviour to Virus Spread

[en] Aphids are responsible for the spread of more than half of the known phytovirus species. Virus transmission within the plant–aphid–phytovirus pathosystem depends on vector mobility which allows the aphid to reach its host plant and on vector efficiency in terms of ability to transmit phytoviruses. However, several other factors can influence the phytoviruses transmission process and have significant epidemiological consequences. In this review, we aimed to analyse the aphid behaviours and influencing factors affecting phytovirus spread. We discussed the impact of vector host‐seeking and dispersal behaviours mostly involved in aphid‐born phytovirus spread but also the effect of feeding behaviours and life history traits involved in plant–aphid–phytovirus relationships on vector performances. We also noted that these behaviours are influenced by factors inherent to the interactions between pathosystem components (mode of transmission of phytoviruses, vector efficiency, plant resistance, …) and several biological, biochemical, chemical or physical factors related to the environment of these pathosystem components, most of them being manipulated as means to control vector‐borne diseases in the crop fields.

Disciplines :

Entomology & pest control

Author, co-author :

Fingu Mabola, Junior Corneille ; Université de Liège - ULiège > Terra

Francis, Frédéric ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Language :

English

Title :

Aphid–Plant–Phytovirus Pathosystems: Influencing Factors from Vector Behaviour to Virus Spread

Publication date :

29 May 2021

Journal title :

Agriculture

eISSN :

2077-0472

Publisher :

MDPI AG, Switzerland

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 07 June 2021

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57 (8 by ULiège)

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84 (17 by ULiège)

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Bibliography

Yvon, M., Vile, D., Brault, V., Blanc, S., van Munster, M., Drought reduces transmission of turnip yellows virus, an insect‐vectored circulative virus (2017) Virus Res, 241, pp. 131-136
Mulot, M., Monsion, B., Boissinot, S., Rastegar, M., Meyer, S., Bochet, N., Brault, V., Transmission of turnip yellows virus by Myzus persicae is reduced by feeding aphids on double‐stranded RNA targeting the ephrin receptor protein (2018) Front. Microbiol, 9
Carmo‐Sousa, M., Moreno, A., Garzo, E., Fereres, A., A non‐persistently transmitted‐virus induces a pull‐push strategy in its aphid vector to optimize transmission and spread (2014) Virus Res, 186, pp. 38-46
Safari, M., Ferrari, M.J., Roossinck, M.J., Manipulation of aphid behavior by a persistent plant virus (2019) J. Virol, 93
Fereres, A., Moreno, A., Behavioural aspects influencing plant virus transmission by homopteran insects (2009) Virus Res, 141, pp. 158-168
Carmo‐Sousa, M., Moreno, A., Plaza, M., Garzo, E., Fereres, A., Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread (2016) Ann. Appl. Biol, 169, pp. 284-297
Bragard, C., Caciagli, P., Lemaire, O., Lopez‐Moya, J.J., MacFarlane, S., Peters, D., Susi, P., Torrance, L., Status and prospects of plant virus control through interference with vector transmission (2013) Annu. Rev. Phytopathol, 51, pp. 177-201
Dáder, B., Moreno, A., Viñuela, E., Fereres, A., Spatio‐temporal dynamics of viruses are differentially affected by parasitoids depending on the mode of transmission (2012) Viruses, 4, pp. 3069-3089
Boquel, S., Ameline, A., Giordanengo, P., Assessing aphids potato virus Y‐transmission efficiency: A new approach (2011) J. Virol. Methods, 178, pp. 63-67
Powell, G., Hardie, J., The chemical ecology of aphid host alternation: How do return migrants find the primary host plant? (2001) Appl. Entomol. Zool, 36, pp. 259-267
Watson, M.A., Epidemiology of aphid‐transmitted plant‐virus diseases (1967) Outlook Agric, 5, pp. 155-166
Lin, F., ‐, J.J., Bosquée, E., Liu, Y, ‐, J.J., Chen, J, ‐, L.L., Francis, F., Impact of aphid alarm pheromone release on virus transmission efficiency: When pest control strategy could induce higher virus dispersion (2016) J. Virol. Methods, 235, pp. 34-40
Capinera, J.L., Green Peach Aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) (2008) Encyclopedia of Entomology, pp. 1727-1730. , Capinera, J.L., Ed.
Springer: Dordrecht, The Netherlands
Prado, E.C., (1997) Aphid‐Plant Interactions at Phloem Level, a Behavioural Study, , Landbouwuniversiteit: Wageningen, The Netherlands
Ishikawa, A., Miura, T., Morphological differences between wing morphs of two Macrosiphini aphid species, Acyrthosiphon pisum and Megoura crassicauda (Hemiptera, Aphididae) (2007) Sociobiology, 50, pp. 881-893
Chen, Y., Martin, C., Fingu‐Mabola, J.C., Verheggen, F., Wang, Z., He, K., Francis, F., Effects of host plants reared under elevated CO2 concentrations on the foraging behavior of different stages of corn leaf aphids Rhopalosiphum maidis (2019) Insects, 10, p. 182
Quiroz, A., Niemeyer, H.M., Olfactometer‐assessed responses of aphid Rhopalosiphum padi to wheat and oat volatiles (1998) J. Chem. Ecol, 24, pp. 113-124
Congdon, B.S., Coutts, B.A., Renton, M., Flematti, G.R., Jones, R.A.C., Establishing alighting preferences and species transmission differences for pea seed‐borne mosaic virus aphid vectors (2017) Virus Res, 241, pp. 145-155
Döring, T.F., Chittka, L., Visual ecology of aphids—a critical review on the role of colours in host finding (2007) Arthropod. Plant. Interact, 1, pp. 3-16
dos Santos, R.C., Peñaflor, M.F.G.V., Sanches, P.A., Nardi, C., Bento, J.M.S., The effects of Gibberella zeae, barley yellow dwarf virus, and co‐infection on Rhopalosiphum padi olfactory preference and performance (2016) Phytoparasitica, 44, pp. 47-54
Lacroix, C., Jolles, A., Seabloom, E.W., Power, A.G., Mitchell, C.E., Borer, E.T., Non‐random biodiversity loss underlies predictable increases in viral disease prevalence (2014) J. R. Soc. Interface, 11, p. 20130947
Cilia, M., Peter, K.A., Bereman, M.S., Howe, K., Fish, T., Smith, D., Gildow, F., Gray, S.M., Discovery and targeted LC‐MS/MS of purified polerovirus reveals differences in the virus‐host interactome associated with altered aphid transmission (2012) PLoS ONE, 7, p. e48177
Mauck, K.E., De Moraes, C.M., Mescher, M.C., Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts (2010) Proc. Natl. Acad. Sci. USA, 107, pp. 3600-3605
Hodge, S., Powell, G., Complex interactions between a plant pathogen and insect parasitoid via the shared vector‐host: Consequences for host plant infection (2008) Oecologia, 157, pp. 387-397
Gadhave, K.R., Dutta, B., Coolong, T., Srinivasan, R., A non‐persistent aphid‐transmitted Potyvirus differentially alters the vector and non‐vector biology through host plant quality manipulation (2019) Sci. Rep, 9, p. 2503
Jahan, S.M.H., Lee, G., ‐, S., Lee, S., Lee, K, Acquisition of tomato yellow leaf curl virus enhances attraction of Bemisia tabaci to green light emitting diodes (2014) J. Asia Pac. Entomol, 17, pp. 79-82. , Y
Döring, T.F., Archetti, M., Hardie, J., Autumn leaves seen through herbivore eyes (2009) Proc. R. Soc. B Biol. Sci, 276, pp. 121-127
Rajabaskar, D., Bosque‐Pérez, N.A., Eigenbrode, S.D., Preference by a virus vector for infected plants is reversed after virus acquisition (2014) Virus Res, 186, pp. 32-37
Eigenbrode, S.D., Ding, H., Shiel, P., Berger, P.H., Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae) (2002) Proc. R. Soc. London. Ser. B Biol. Sci, 269, pp. 455-460
Rajabaskar, D., Ding, H., Wu, Y., Eigenbrode, S.D., Different reactions of potato varieties to infection by potato leafroll virus, and associated responses by its vector, Myzus persicae (Sulzer) (2013) J. Chem. Ecol, 39, pp. 1027-1035
Mauck, K.E., De Moraes, C.M., Mescher, M.C., Evidence of local adaptation in plant virus effects on host‐vector interactions (2014) Integr. Comp. Biol, 54, pp. 193-209
Mwando, N.L., Tamiru, A., Nyasani, J.O., Obonyo, M.A., Caulfield, J.C., Bruce, T.J.A.A., Subramanian, S., Maize chlorotic mottle virus induces changes in host plant volatiles that attract vector thrips species (2018) J. Chem. Ecol, 44, pp. 681-689
Ngumbi, E., Eigenbrode, S.D., Bosque‐Pérez, N.A., Ding, H., Rodriguez, A., Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of plrv‐infected potato (2007) J. Chem. Ecol, 33, pp. 1733-1747
Medina‐Ortega, K.J., Bosque‐Pérez, N.A., Ngumbi, E., Jiménez‐Martínez, E.S., Eigenbrode, S.D., Medina‐ortega, A.K.J., Bosque‐ Pérez, N.A., Ngumbi, E., Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from barley yellow dwarf virus‐infected wheat (2009) Environ. Entomol, 38, pp. 836-845
Webster, B., The role of olfaction in aphid host location (2012) Physiol. Entomol, 37, pp. 10-18
Powell, G., Tosh, C.R., Hardie, J., Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives (2006) Annu. Rev. Entomol, 51, pp. 309-330
Westwood, J.H., Stevens, M., Resistance to aphid vectors of virus disease (2010) Natural and Engineered Resistance to Plant Viruses, Part B, 76, pp. 179-210. , Elsevier Inc.: Amsterdam, The Netherlands
Prado, E., Tjallingii, W.F., Effects of previous plant infestation on sieve element acceptance by two aphids (1997) Entomol. Exp. Appl, 82, pp. 189-200
Wamonje, F.O., Donnelly, R., Tungadi, T.D., Murphy, A.M., Pate, A.E., Woodcock, C., Caulfield, J., Gilligan, C.A., Different plant viruses induce changes in feeding behavior of specialist and generalist aphids on common bean that are likely to enhance virus transmission (2020) Front. Plant Sci, 10, p. 1811
Giordanengo, P., Brunissen, L., Rusterucci, C., Vincent, C., van Bel, A., Dinant, S., Girousse, C., Bonnemain, J, Compatible plant‐aphid interactions: How aphids manipulate plant responses (2010) C. R. Biol, 333, pp. 516-523. , L
Ziegler‐Graff, V., Molecular insights into host and vector manipulation by plant viruses (2020) Viruses, 12, p. 263
Bosque‐Pérez, N.A., Eigenbrode, S.D., The influence of virus‐induced changes in plants on aphid vectors: Insights from luteovirus pathosystems (2011) Virus Res, 159, pp. 201-205
Alvarez, A.E., Broglia, V.G., Alberti D’Amato, A.M., Wouters, D., van der Vossen, E., Garzo, E., Tjallingii, W.F., Vosman, B., Comparative analysis of Solanum stoloniferum responses to probing by the green peach aphid Myzus persicae and the potato aphid Macrosiphum euphorbiae (2013) Insect Sci, 20, pp. 207-227
Chesnais, Q., Mauck, K.E., Bogaert, F., Bamière, A., Catterou, M., Spicher, F., Brault, V., Ameline, A., Virus effects on plant quality and vector behavior are species specific and do not depend on host physiological phenotype J. Pest Sci. (2004), 92, pp. 791-804. , 2019
Döring, T.F., How aphids find their host plants, and how they don’t (2014) Ann. Appl. Biol, 165, pp. 3-26
Boquel, S., Giordanengo, P., Ameline, A., Vector activity of three aphid species (Hemiptera: Aphididae) modulated by host plant selection behaviour on potato (Solanales: Solanaceae) (2014) Ann. Soc. Entomol. Fr, 50, pp. 141-148
Tjallingii, W.F., Prado, E., Analysis of circulative transmission by electrical penetration graphs (2001) Virus‐Insect‐Plant Interactions, pp. 69-85. , Academic Press: Cambridge, Massachusetts
Garzo, E., Moreno, A., Plaza, M., Fereres, A., Feeding behavior and virus‐transmission ability of insect vectors exposed to systemic insecticides (2020) Plants, 9, p. 895
Giordanengo, P., EPG‐Calc: A PHP‐based script to calculate electrical penetration graph (EPG) parameters (2014) Arthropod. Plant. Interact, 8, pp. 163-169
Tjallingiil, W.E., Mayoral, A., (1992) Criteria for Host Plant Acceptance by Aphids, pp. 280-281. , Springer: Dordrecht, The Netherlands
Martín, B., Collar, J.L., Tjallingii, W.F., Fereres, A., Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non‐persistently transmitted plant viruses (1997) J. Gen. Virol, 78, pp. 2701-2705. , Pt 10
Collar, J.L., Avilla, C., Fereres, A., New correlations between aphid stylet paths and nonpersistent virus transmission (1997) Environ. Entomol, 26, pp. 537-544
Powell, G., Intracellular salivation is the aphid activity associated with inoculation of non‐persistently transmitted viruses (2005) J. Gen. Virol, 86, pp. 469-472
Angelella, G., Nalam, V., Nachappa, P., White, J., Kaplan, I., Endosymbionts differentially alter exploratory probing behavior of a nonpersistent plant virus vector (2018) Microb. Ecol, 76, pp. 453-458
Boquel, S., Giordanengo, P., Ameline, A., Divergent effects of PVY‐infected potato plant on aphids (2011) Eur. J. Plant Pathol, 129, pp. 507-510
Mauck, K.E., De Moraes, C.M., Mescher, M.C., Effects of pathogens on sensory‐mediated interactions between plants and insect vectors (2016) Curr. Opin. Plant Biol, 32, pp. 53-61
Ghosh, A., Das, A., Vijayanandraj, S., Mandal, B., Cardamom bushy dwarf virus infection in large cardamom alters plant selection preference, life stages, and fecundity of aphid vector, Micromyzus kalimpongensis (Hemiptera: Aphididae) (2016) Environ. Entomol, 45, pp. 178-184
Van Munster, M., Yvon, M., Vile, D., Dader, B., Fereres, A., Blanc, S., Water deficit enhances the transmission of plant viruses by insect vectors (2017) PLoS ONE, 12, p. e0174398
Ingwell, L.L., Eigenbrode, S.D., Bosque‐Pérez, N.A., Plant viruses alter insect behavior to enhance their spread (2012) Sci. Rep, 2, p. 578
Mauck, K.E., Chesnais, Q., Shapiro, L.R., Evolutionary determinants of host and vector manipulation by plant viruses (2018) Environmental Virology and Virus Ecology, pp. 189-250. , Malmstrom, C.M., Ed.
Academic Press: Amsterdam, The Netherlands
Hodge, S., Powell, G., Conditional facilitation of an aphid vector, Acyrthosiphon pisum, by the plant pathogen, Pea enation mosaic virus (2010) J. Insect Sci, 10, pp. 1-14
Westwood, J.H., Groen, S.C., Du, Z., Murphy, A.M., Anggoro, D.T., Tungadi, T., Luang‐In, V., Powell, G., A trio of viral proteins tunes aphid‐plant interactions in Arabidopsis thaliana (2013) PLoS ONE, 8, p. e83066
Carr, J.P., Tungadi, T., Donnelly, R., Bravo‐Cazar, A., Rhee, S.‐J., Watt, L.G., Mutuku, J.M., Arinaitwe, W., Modelling and manipulation of aphid‐mediated spread of non‐persistently transmitted viruses (2020) Virus Res, 277, p. 197845
Donnelly, R., Cunniffe, N.J., Carr, J.P., Gilligan, C.A., Pathogenic modification of plants enhances long‐distance dispersal of nonpersistently transmitted viruses to new hosts (2019) Ecology, 100
Belliure, B., Amorós‐Jiménez, R., Fereres, A., Marcos‐García, M.Á., Antipredator behaviour of Myzus persicae affects transmission efficiency of broad bean wilt virus 1 (2011) Virus Res, 159, pp. 206-214
Boquel, S., Delayen, C., Couty, A., Giordanengo, P., Ameline, A., Modulation of aphid vector activity by potato virus Y on in vitro potato plants (2012) Plant Dis, 96, pp. 82-86
Andret‐Link, P., Fuchs, M., Transmission specificity of plant viruses by vectors (2005) J. Plant Pathol, 87, pp. 153-165
Ng, J.C.K., Perry, K.L., Transmission of plant viruses by aphid vectors (2004) Mol. Plant Pathol, 5, pp. 505-511
Blanc, S., Drucker, M., Uzest, M., Localizing viruses in their insect vectors (2014) Annu. Rev. Phytopathol, 52, pp. 403-425
Whitfield, A.E., Falk, B.W., Rotenberg, D., Insect vector‐mediated transmission of plant viruses (2015) Virology, , 479–480, 278–289
Cervantes, F.A., Alvarez, J.M., Within plant distribution of potato virus Y in hairy nightshade (Solanum sarrachoides): An inoculum source affecting PVY aphid transmission (2011) Virus Res, 159, pp. 194-200
Verbeek, M., Piron, P.G.M., Dullemans, A.M., Cuperus, C., Van Der Vlugt, R.A.A., Determination of aphid transmission efficiencies for N, NTN and Wilga strains of potato virus Y (2010) Ann. Appl. Biol, 156, pp. 39-49
Kersch‐Becker, M.F., Thaler, J.S., Virus strains differentially induce plant susceptibility to aphid vectors and chewing herbivores (2014) Oecologia, 174, pp. 883-892
van den Heuvel, J.F.J.M., Boerma, T.M., Peters, D., Transmission of potato leafroll virus from plants and artificial diets by Myzus persicae (1991) Phytopathology, 81, pp. 150-154
Collar, J.L., Fereres, A., Nonpersistent virus transmission efficiency determined by aphid probing behavior during intracellular punctures (1998) Environ. Entomol, 27, pp. 583-591
Sylvester, E.S., Aphid transmission of nonpersistent plant viruses with special reference to the brassica nigra virus (1954) Hilgardia, 23, pp. 53-98
Robert, Y., Bourdin, D., Aphid transmission of potato viruses (2001) Virus and Virus‐like Diseases of Potatoes and Production of Seed‐Potatoes, pp. 195-225. , Loebenstein, G., Berger, P.H., Brunt, A.A., Lawson, R.H., Eds.
Springer: Dordrecht, The Netherlands
Sadeghi, E., Dedryver, C., Gauthier, J., Role of acquisition and inoculation time in the expression of clonal variation for BYDV‐ PAV transmission in the aphid species Rhopalosiphum padi (1997) Plant Pathol, pp. 502-508
Ren, G., Wang, X., Chen, D., Wang, X., Fan, X., Liu, X., Potato virus Y‐infected tobacco affects the growth, reproduction, and feeding behavior of a vector aphid, Myzus persicae (Hemiptera: Aphididae) (2015) Appl. Entomol. Zool, 50, pp. 239-243
McMenemy, L.S., Hartley, S.E., MacFarlane, S.A., Karley, A.J., Shepherd, T., Johnson, S.N., Raspberry viruses manipulate the behaviour of their insect vectors (2012) Entomol. Exp. Appl, 144, pp. 56-68
Albittar, L., Ismail, M., Lohaus, G., Ameline, A., Visser, B., Bragard, C., Hance, T., Bottom‐up regulation of a tritrophic system by beet yellows virus infection: Consequences for aphid‐parasitoid foraging behaviour and development (2019) Oecologia, 191, pp. 113-125
de Oliveira, C.F., Long, E.Y., Finke, D.L., A negative effect of a pathogen on its vector? A plant pathogen increases the vulnerability of its vector to attack by natural enemies (2014) Oecologia, 174, pp. 1169-1177
Long, E.Y., Finke, D.L., Predators indirectly reduce the prevalence of an insect‐vectored plant pathogen independent of predator diversity (2015) Oecologia, 177, pp. 1067-1074
González‐Mas, N., Quesada‐Moraga, E., Plaza, M., Fereres, A., Moreno, A., Changes in feeding behaviour are not related to the reduction in the transmission rate of plant viruses by Aphis gossypii (Homoptera: Aphididae) to melon plants colonized by Beauveria bassiana (Ascomycota: Hypocreales) (2019) Biol. Control, 130, pp. 95-103
Bayendi Loudit, S.M., Boullis, A., Verheggen, F., Francis, F., Identification of the alarm pheromone of cowpea aphid, and comparison with two other aphididae species (2018) J. Insect Sci, 18
Laney, A.G., Chen, P., Korth, K.L., Interactive effects of aphid feeding and virus infection on host gene expression and volatile compounds in salt‐stressed soybean, Glycine max (L.) Merr (2018) Arthropod. Plant. Interact, 12, pp. 401-413
Nachappa, P., Culkin, C.T., Saya, P.M., Han, J., Nalam, V.J., Water Stress Modulates Soybean Aphid Performance, Feeding Behavior, and Virus Transmission in Soybean (2016) Front. Plant Sci, 7, p. 552
del Toro, F.J., Choi, K.S., Rakhshandehroo, F., Aguilar, E., Tenllado, F., Canto, T., Ambient conditions of elevated temperature and CO2 levels are detrimental to the probabilities of transmission by insects of a potato virus Y isolate and to its simulated prevalence in the environment (2019) Virology, 530, pp. 1-10
Khelifa, M., Possible induction of potato plant defences against potato virus Y by mineral oil application (2017) Eur. J. Plant Pathol, 147, pp. 339-348