ORBi: Detailled Reference

Article (Scientific journals)

Does the Infectious Status of Aphids Influence Their Preference Towards Healthy, Virus-Infected and Endophytically Colonized Plants?

Fingu Mabola, Junior; Martin, Clément; Bawin, Thomas et al.

2020 • In Insects, 11 (7), p. 435

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/257001

DOI
10.3390/insects11070435

Files (2)Send to Details Statistics Bibliography Similar publications

Files

Full Text

insects-11-00435.pdf

Publisher postprint (2.06 MB)

Annexes

insects-11-00435-s001.pdf

Publisher postprint (432.36 kB)

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

biological control; insect–plant–microbe interactions; multitrophic interactions; aphid-borne virus pathosystem; host-finding behavior; endophytic fungus; plant volatile organic compound

Abstract :

[en] Aphids (Hemiptera: Aphididae) cause significant damage and transmit viruses to various crop plants. We aimed to evaluate how the infectious status of aphids influences their interaction with potential hosts. Two aphid (Myzus persicae and Rhopalosiphum padi) and plant (Nicotiana tabacum and Triticum aestivum) species were used. The preferences of aphids towards healthy, virus-infected (Potato Leafroll Virus (PLRV) and Barley Yellow Dwarfvirus (BYDV)), and endophytic entomopathogenic fungi (EEPF)-inoculated (Beauveria bassiana and Metarhizium acridum) plants were investigated in dual-choice tests. The headspace volatiles of the different plant modalities were also sampled and analyzed. Viruliferous and non-viruliferous aphids were more attracted to EEPF-inoculated plants compared to uninoculated plants. However, viruliferous aphids were more attracted to EEPF-inoculated plants compared to virus-infected plants, while non-viruliferous insects exhibited no preference. Fungal-inoculated plants released higher amounts of aldehydes (i.e., heptanal, octanal, nonanal and decanal) compared to other plants, which might explain why viruliferous and non-viruliferous aphids were more abundant in EEPF-inoculated plants. Our study provides an interesting research perspective on how EEPF are involved in behavior of virus vector, depending on the infectious status of the latter.

Disciplines :

Entomology & pest control

Author, co-author :

Fingu Mabola, Junior ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Martin, Clément ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

Bawin, Thomas; UiT The Arctic University of Norway > Department of Arctic and Marine Biology

Verheggen, François ; Université de Liège - ULiège > Département GxABT > Gestion durable des bio-agresseurs

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

Language :

English

Title :

Does the Infectious Status of Aphids Influence Their Preference Towards Healthy, Virus-Infected and Endophytically Colonized Plants?

Publication date :

July 2020

Journal title :

Insects

eISSN :

2075-4450

Publisher :

Multidisciplinary Digital Publishing Institute (MDPI), Switzerland

Volume :

11

Issue :

7

Pages :

435

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.mdpi.com/2075-4450/11/7/435

Available on ORBi :

since 18 February 2021

Statistics

Number of views

91 (4 by ULiège)

Number of downloads

62 (2 by ULiège)

More statistics

Scopus citations^®

12

Scopus citations^®
without self-citations

10

OpenCitations

4

OpenAlex citations

14

Bibliography

Llewellyn, K.S., Loxdale, H.D., Harrington, R., Brookes, C.P., Clark, S.J., Sunnucks, P., Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites (2002) Mol. Ecol, 12, pp. 21-34. , [CrossRef] [PubMed]
Nault, L.R., Arthropod Transmission of Plant Viruses: A New Synthesis (1997) Ann. Entomol. Soc. Am, 90, pp. 521-541. , [CrossRef]
Kamphuis, L.G., Zulak, K., Gao, L.-L., Anderson, J., Singh, K.B., Plant–aphid interactions with a focus on legumes (2013) Funct. Plant Biol, 40, p. 1271. , [CrossRef] [PubMed]
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. , [CrossRef] [PubMed]
Lin, Y., Hussain, M., Avery, P.B., Qasim, M., Fang, D., Wang, L., Volatiles from plants induced by multiple aphid attacks promote conidial performance of Lecanicillium lecanii (2016) PLoS ONE, 11, p. e0151844. , [CrossRef] [PubMed]
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. , [CrossRef]
Döring, T.F., How aphids find their host plants, and how they don’t (2014) Ann. Appl. Biol, 165, pp. 3-26. , [CrossRef]
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. , [CrossRef]
He, X., Xu, H., Gao, G., Zhou, X., Zheng, X., Sun, Y., Yang, Y., Lu, Z., Virus-mediated chemical changes in rice plants impact the relationship between non-vector planthopper Nilaparvata lugens Stål and its egg parasitoid Anagrus nilaparvatae Pang et Wang (2014) PLoS ONE, 9, p. e105373. , [CrossRef]
Ingwell, L.L., Eigenbrode, S.D., Bosque-Pérez, N.A., Plant viruses alter insect behavior to enhance their spread (2012) Sci. Rep, 2, pp. 1-6. , [CrossRef]
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. , [CrossRef] [PubMed]
de Oliveira, R.L., Moscardini, V.F., Gontijo, P.C., Sâmia, R.R., Marucci, R.C., Budia, F., Carvalho, G.A., Life history parameters and feeding preference of the green lacewing Ceraeochrysa cubana fed with virus-free and potato leafroll virus-infected Myzus persicae (2016) BioControl, 61, pp. 671-679. , [CrossRef]
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. , [CrossRef]
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. , [CrossRef]
Calvo, D., Fereres, A., The performance of an aphid parasitoid is negatively affected by the presence of a circulative plant virus (2011) BioControl, 56, pp. 747-757. , [CrossRef]
Jahan, S.M.H., Lee, G.-S., Lee, S., Lee, K.-Y., 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. , [CrossRef]
Vu, V.H., Hong, S., Il, Kim, K., Selection of entomopathogenic fungi for aphid control (2007) J. Biosci. Bioeng, 104, pp. 498-505. , [CrossRef]
Seye, F., Bawin, T., Boukraa, S., Zimmer, J.Y., Ndiaye, M., Delvigne, F., Francis, F., Effect of entomopathogenic Aspergillus strains against the pea aphid, Acyrthosiphon pisum (Hemiptera: Aphididae) (2014) Appl. Entomol. Zool, 49, pp. 453-458. , [CrossRef]
Elliot, S.L., Sabelis, M.W., Janssen, A., Van der Geest, L.P.S., Beerling, E.A.M., Fransen, J., Can plants use entomopathogens as bodyguards? (2000) Ecol. Lett, 3, pp. 228-235. , [CrossRef]
Vega, F.E., Posada, F., Catherine Aime, M., Pava-Ripoll, M., Infante, F., Rehner, S.A., Entomopathogenic fungal endophytes (2008) Biol. Control, 46, pp. 72-82. , [CrossRef]
Parsa, S., Ortiz, V., Vega, F.E., Establishing Fungal Entomopathogens as Endophytes: Towards Endophytic Biological Control (2013) J. Vis. Exp, p. e50360. , [CrossRef] [PubMed]
Biswas, C., Dey, P., Satpathy, S., Satya, P., Establishment of the fungal entomopathogen Beauveria bassiana as a season long endophyte in jute (Corchorus olitorius) and its rapid detection using SCAR marker (2012) BioControl, 57, pp. 565-571. , [CrossRef]
Russo, M.L., Pelizza, S.A., Cabello, M.N., Stenglein, S.A., Scorsetti, A.C., Endophytic colonisation of tobacco, corn, wheat and soybeans by the fungal entomopathogen Beauveria bassiana (Ascomycota, Hypocreales) (2015) Biocontrol Sci. Technol, 25, pp. 475-480. , [CrossRef]
Behie, S.W., Jones, S.J., Bidochka, M.J., Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria (2015) Fungal Ecol, 13, pp. 112-119. , [CrossRef]
McKinnon, A.C., Plant Tissue Preparation for the Detection of an Endophytic Fungus In Planta (2016) Methods in Molecular Biology, 1477, pp. 167-173. , Humana Press: New York, NY, USA, [CrossRef]
Gurulingappa, P., Sword, G.A., Murdoch, G., McGee, P.A., Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta (2010) Biol. Control, 55, pp. 34-41. , [CrossRef]
González-Mas, N., Sánchez-Ortiz, A., Valverde-García, P., Quesada-Moraga, E., Effects of Endophytic Entomopathogenic Ascomycetes on the Life-History Traits of Aphis gossypii Glover and Its Interactions with Melon Plants (2019) Insects, 10, p. 165. , [CrossRef]
Gurulingappa, P., McGee, P.A., Sword, G., Endophytic Lecanicillium lecanii and Beauveria bassiana reduce the survival and fecundity of Aphis gossypii following contact with conidia and secondary metabolites (2011) Crop Prot, 30, pp. 349-353. , [CrossRef]
Clifton, E.H., Jaronski, S.T., Coates, B.S., Hodgson, E.W., Gassmann, A.J., Effects of endophytic entomopathogenic fungi on soybean aphid and identification of Metarhizium isolates from agricultural fields (2018) PLoS ONE, 13, p. e0194815. , [CrossRef]
Jaber, L.R., Araj, S.-E., Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae) (2018) Biol. Control, 116, pp. 53-61. , [CrossRef]
Meister, B., Krauss, J., Härri, S.A., Victoria Schneider, M., Müller, C.B., Fungal endosymbionts affect aphid population size by reduction of adult life span and fecundity (2006) Basic Appl. Ecol, 7, pp. 244-252. , [CrossRef]
Chauzat, M., Faucon, J., Pesticide residues in beeswax samples collected from honey bee colonies (Apis mellifera L.) in France (2007) Pest Manag. Sci, 1106, pp. 1100-1106. , [CrossRef] [PubMed]
Liu, B., Tzeng, Y., Development and applications of destruxins: A review (2012) Biotechnol. Adv, 30, pp. 1242-1254. , [CrossRef] [PubMed]
Jaber, L.R., Ownley, B.H., Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? (2017) Biol. Control, 107, pp. 50-59. , [CrossRef]
Thakur, A., Kaur, S., Kaur, A., Singh, V., Enhanced Resistance to Spodoptera litura in Endophyte Infected Cauliflower Plants (2013) Environ. Entomol, 42, pp. 240-246. , [CrossRef]
Sánchez-Rodríguez, A.R., Raya-Díaz, S., Zamarreño, Á.M., García-Mina, J.M., del Campillo, M.C., Quesada-Moraga, E., An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae (2018) Biol. Control, 116, pp. 90-102. , [CrossRef]
Van Wees, S.C., Van der Ent, S., Pieterse, C.M., Plant immune responses triggered by beneficial microbes (2008) Curr. Opin. Plant Biol, 11, pp. 443-448. , [CrossRef]
Aragón, S.M., (2016) How Entomopathogenic Endophytic Fungi Modulate Plant-Insect Interactions, , Georg-August-University Goettingen: Göttingen, Germany
Jaber, L.R., Vidal, S., Fungal endophyte negative effects on herbivory are enhanced on intact plants and maintained in a subsequent generation (2010) Ecol. Entomol, 35, pp. 25-36. , [CrossRef]
Saikkonen, K., Gundel, P.E., Helander, M., Chemical Ecology Mediated by Fungal Endophytes in Grasses (2013) J. Chem. Ecol, 39, pp. 962-968. , [CrossRef]
Li, T., Blande, J.D., Gundel, P.E., Helander, M., Saikkonen, K., Epichloë Endophytes Alter Inducible Indirect Defences in Host Grasses (2014) PLoS ONE, 9, p. e101331. , [CrossRef]
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. , [CrossRef]
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. , [CrossRef]
Lin, F.-J., Bosquée, E., Liu, Y.-J., Chen, J.-L., Yong, 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. , [CrossRef] [PubMed]
Woodford, J.A.T., Jolly, C.A., Aveyard, C.S., Biological factors influencing the transmission of potato leafroll virus by different aphid species (1995) Potato Res, 38, pp. 133-141. , [CrossRef]
Locust Control and the Making of “Green Muscle”, , http://www.dropdata.org/biopesticides/green_muscle.htm, LUBILOSA. (accessed on 17 June 2020)
Inglis, G.D., Enkerli, J., Goettel, M.S., (2012) Laboratory Techniques Used for Entomopathogenic Fungi BT—Manual of Techniques in Invertebrate Pathology, , 2nd ed.
Elsevier Ltd.: Amsterdam, The Netherlands, [CrossRef]
Rondot, Y., Reineke, A., Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects (2018) Biol. Control, 116, pp. 82-89. , [CrossRef]
Humber, R.A., Fungi (1997) Manual of Techniques in Insect Pathology, pp. 153-185. , Elsevier: Amsterdam, The Netherlands, [CrossRef]
Driver, F., Milner, R.J., Trueman, J.W.H., A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data (2000) Mycol. Res, 104, pp. 134-150. , [CrossRef]
Haas, J., Lozano, E.R., Poppy, G.M., A simple, light clip-cage for experiments with aphids (2018) Agric. For. Entomol, 20, pp. 589-592. , [CrossRef]
Nisbet, A.J., Woodford, J.A., Strang, R.H.C., The effects of azadirachtin on the acquisition and inoculation of potato leafroll virus by Myzus persicae (1996) Crop Prot, 15, pp. 9-14. , [CrossRef]
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, 46, pp. 502-508. , [CrossRef]
Portillo-Estrada, M., Kazantsev, T., Talts, E., Tosens, T., Niinemets, Ü., Emission Timetable and Quantitative Patterns of Wound-Induced Volatiles Across Different Leaf Damage Treatments in Aspen (Populus Tremula) (2015) J. Chem. Ecol, 41, pp. 1105-1117. , [CrossRef]
Verheggen, F.J., Haubruge, E., De Moraes, C.M., Mescher, M.C., Aphid responses to volatile cues from turnip plants (Brassica rapa) infested with phloem-feeding and chewing herbivores (2013) Arthropod. Plant. Interact, 7, pp. 567-577. , [CrossRef]
Zadoks, J.C., Chang, T.T., Konzak, C.F., A decimal code for the growth stages of cereals (1974) Weed Res, 14, pp. 415-421. , [CrossRef]
https://pubchem.ncbi.nlm.nih.gov/, PubChem. (accessed on 2 March 2020)
The Pherobase: Database of Pheromones and Semiochemicals, , https://www.pherobase.com/, (accessed on 2 March 2020)
(2017) NIST Standard Reference Database Number 69, , NIST Chemistry WebBook, Linstrom, P.J.
Mallard, W.G. (Eds) National Institute of Standards and Technology: Gaithersburg, MD, USA
Oksanen, J., Kindt, R., Legendre, P., O’Hara, B., Stevens, M.H.H., Oksanen, M.J., Suggests, M.A.S.S., The vegan package (2007) Community Ecol. Packag, 10, pp. 631-637
Lê, S., Josse, J., Husson, F., FactoMineR: An R Package for Multivariate Analysis (2008) J. Stat. Softw, 25, pp. 1-18. , [CrossRef]
Kassambara, A., Mundt, F., Package ‘factoextra’: Extract and Visualize the Results of Multivariate Data Analyse, , http://www.sthda.com/english/rpkgs/factoextra, (accessed on 2 March 2020)
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, p. 155. , [CrossRef] [PubMed]
Ren, G.W., Wang, X.F., Chen, D., Wang, X.W., Fan, X.J., Liu, X.D., 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. , [CrossRef]
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. , [CrossRef] [PubMed]
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. , [CrossRef] [PubMed]
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. , [CrossRef] [PubMed]
Nikolakakis, N.N., Margaritopoulos, J.T., Tsitsipis, J.A., Performance of Myzus persicae (Hemiptera: Aphididae) clones on different host-plants and their host preference (2003) Bull. Entomol. Res, 93, pp. 235-242. , [CrossRef]
Sharifi, R., Lee, S.-M., Ryu, C.-M., Microbe-induced plant volatiles (2018) New Phytol, 220, pp. 684-691. , [CrossRef]
Quiroz, A., Niemeyer, H.M., Olfactometer-assesed responses of aphid Rhopalosiphum padi to wheat and oat volatiles (1998) J. Chem. Ecol, 24, pp. 113-124. , [CrossRef]
Dheivasigamani, R., Ding, H., Food, U.S., Eigenbrode, S.D., Behavioral Responses of Green Peach Aphid, Myzus persicae (Sulzer), to the Volatile Organic Compound Emissions from Four Potato Varieties (2013) Am. J. Potato Res, 90, pp. 171-178. , [CrossRef]
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. , [CrossRef]
Vidal, S., Jaber, L.R., Entomopathogenic fungi as endophytes: Plant–endophyte–herbivore interactions and prospects for use in biological control (2015) Curr. Sci, 109, pp. 46-54. , [CrossRef]
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. , [CrossRef]
González-Mas, N., Medina, M.C., Sánchez, F.G., Moraga, E.Q., Bottom—Up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon (2019) J. Pest Sci, 92, pp. 1271-1281. , [CrossRef]
Pedrini, N., Crespo, R., Juárez, M.P., Biochemistry of insect epicuticle degradation by entomopathogenic fungi (2007) Comp. Biochem. Physiol. C Toxicol. Pharmacol, 146, pp. 124-137. , [CrossRef]
Bawin, T., Seye, F., Boukraa, S., Zimmer, J.-Y., Delvigne, F., Francis, F., La lutte contre les moustiques (Diptera: Culicidae): Diversité des approches et application du contrôle biologique (2015) Can. Entomol, 147, pp. 476-500. , [CrossRef]
Jaronski, S.T., Mascarin, G.M., Mass Production of Fungal Entomopathogens (2017) Microbial Control of Insect and Mite Pests, pp. 141-155. , Elsevier: Amsterdam, The Netherlands, [CrossRef]

Similar publications