Bacterial plant pathogens affect the locomotor behavior of the insect vector: a case study of Citrus volkameriana–Triozae erytreae–Candidatus Liberibacter asiaticus system

Abstract

Plant pathogens can alter the behavior of their insect vectors as well as their survival and reproduction. The African psyllid, Trioza erytreae, is one of the vectors of Huanglongbing, a citrus disease caused mainly by “Candidatus Liberibacter asiaticus” (CLas). The purpose of this study was to characterize the effects of CLas on the psyllid, T. erytreae using Citrus volkamerina plants as the study system. The study focused more specifically on the CLas effects prior to and after its acquisition by the psyllid T. erytreae. Our results did not support the hypothesis that CLas effects psyllid probing behavior prior to acquisition; few differences were observed between uninfected T. erytrea feeding on CLas-infected versus control plants. On the other hand, compared to psyllids that had completed their development on control plants, the ones that had completed their development on a CLas-infected plant exhibited changes in their behavior (greater velocity), physiology (smaller mass) and biochemistry (lower water and lipid content). Altogether, our results confirm the existence of a marked postacquisition effect on the vector locomotor behavior and a minor preacquisition effect of CLas on the vector behavior, which can be partially explained by physiological and biochemical changes.

Keywords

electrical penetration graph / Huanglongbing / locomotory behavior / lipid biomass / probing behavior / vector manipulation

References

[1] Ajene,I.J., Khamis, F., Mohammed,S., Rasowo,B., Ombura, F.L., Pietersen,G. et al. (2019) First report of field population of Trioza erytreae carrying the huanglongbing-associated pathogen, “Candidatus Liberibacter asiaticus,” in Ethiopia. Plant Disease, 103, 1766.

[2] Ammar,E.-D., Ramos,J.E., Hall,D.G., Dawson, W.O. and Shatters Jr,R.G. (2016) Acquisition, replication and inoculation of Candidatus Liberibacter asiaticus following various acquisition periods on huanglongbing-infected citrus by nymphs and adults of the Asian citrus psyllid. PLoS ONE, 11, e0159594.

[3] Antolinez,C.A., Moreno, A., Appezzato-da-Gloria,B. and Fereres,A. (2017) Characterization of the electrical penetration graphs of the psyllid Bactericera trigonica on carrots. Entomologia Experimentalis et Applicata, 163, 127–139.

[4] Benhadi-Marín,J., Garzo,E., Moreno, A., Pereira,J.A. and Fereres,A. (2021) Host plant preference of Trioza erytreae on lemon and bitter orange plants. Arthropod-Plant Interactions, 15, 887–896.

[5] Bonani,J.P., Fereres, A., Garzo,E., Miranda,M.P., Appezzato-Da-Gloria, B. and Lopes,J.R.S. (2010) Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings. Entomologia Experimentalis et Applicata, 134, 35–49.

[6] Bové,J.M. (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology, 88, 7–37.

[7] Caillaud,M. and Via, S. (2000) Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. American Naturalist, 156, 606–621.

[8] Cen,Y., Yang,C., Holford,P., Beattie, G.A.C., Spooner-Hart,R.N., Liang,G. et al. (2012) Feeding behaviour of the Asiatic citrus psyllid, Diaphorina citri, on healthy and huanglongbing-infected citrus. Entomologia Experimentalis et Applicata, 143, 13–22.

[9] Chesnais,Q., Caballero Vidal, G., Coquelle,R., Yvon,M., Mauck,K., Brault,V. et al. (2020) Post-acquisition effects of viruses on vector behavior are important components of manipulation strategies. Oecologia, 194, 429–440.

[10] Chin,E.L., Ramsey, J.S., Mishchuk,D.O., Saha,S., Foster, E., Chavez,J.D. et al. (2020) Longitudinal transcriptomic, proteomic, and metabolomic analyses of Citrus sinensis (L.) Osbeck graft-inoculated with “Candidatus Liberibacter asiaticus.” Journal of Proteome Research, 19, 719–732.

[11] Dobson,A.P. (1988) The population biology of parasite-induced changes in host behavior. The Quarterly Review of Biology, 63, 139–165.

[12] Etxeberria,E., Gonzalez, P., Achor,D. and Albrigo,G. (2009) Anatomical distribution of abnormally high levels of starch in HLB-affected Valencia orange trees. Physiological and Molecular Plant Pathology, 74, 76–83.

[13] Fereres,A. and Moreno, A. (2009) Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research, 141, 158–168.

[14] Fiebig,M., Poehling, H.-M. and Borgemeister,C. (2004) Barley yellow dwarf virus, wheat, and Sitobion avenae: a case of trilateral interactions. Entomologia Experimentalis et Applicata, 110, 11–21.

[15] Garnier,M., Jagoueix, S., Toorawa,P., Grisoni,M., Mallessard, R., Dookun,A. et al. (1996) Both Huanglongbing (Greening) Liberobacter species are present in Mauritius and Reunion. International Organization of Citrus Virologists Conference Proceedings (1957–2010), 13, 392–394.

[16] Giordanengo,P. (2014) EPG-Calc: a PHP-based script to calculate electrical penetration graph (EPG) parameters. Arthropod-Plant Interactions, 8, 163–169.

[17] Hijaz,F.M., Manthey, J.A., Folimonova,S.Y., Davis,C.L., Jones,S.E. and Reyes-De-Corcuera,J.I. (2013) An HPLC-MS characterization of the changes in sweet orange leaf metabolite profile following infection by the bacterial pathogen Candidatus Liberibacter asiaticus. PLoS ONE, 8, e79485.

[18] Hodge,S. and Powell, G. (2010) Conditional facilitation of an aphid vector, Acyrthosiphon pisum, by the plant pathogen, pea enation mosaic virus. Journal of Insect Science, 10, 155.

[19] Ingwell,L.L., Eigenbrode, S.D. and Bosque-Pérez,N.A. (2012) Plant viruses alter insect behavior to enhance their spread. Scientific Reports, 2, 578.

[20] Irwin,M.E., Kampmeier, G.E. and Weisser,W.W. (2007) Aphid movement: process and consequences. In Aphids as Crop Pests (eds. H.F.van Emden & R.Harrington), pp. 153–186. CABI Books.

[21] Kim,J.-S., Sagaram, U.S., Burns,J.K., Li,J.-L. and Wang, N. (2009) Response of sweet orange (Citrus sinensis) to “Candidatus Liberibacter asiaticus” infection: microscopy and microarray analyses. Phytopathology, 99, 50–57.

[22] Lafferty,K.D. and Kuris, A.M. (2012) Ecological consequences of manipulative parasites. In Host Manipulation by Parasites (eds. D.P. Hughes, J.Brodeur & F.Thomas), pp. 158–168. Oxford University Press.

[23] Lopes,S.A. and Cifuentes-Arenas, J.C. (2021) Protocol for successful transmission of ‘Candidatus liberibacter asiaticus’ from citrus to citrus using Diaphorina citri. Phytopathology, 111, 2367–2374.

[24] Liquido,N.J. and Irwin, M.E. (1986) Longevity, fecundity, change in degree of gravidity and lipid content with adult age, and lipid utilisation during tethered flight of alates of the corn leaf aphid, Rhopalosiphum maidis. Annals of Applied Biology, 108, 449–459.

[25] Liu,Z., Gong,P., Wu,K., Wei, W., Sun,J. and Li,D. (2007) Effects of larval host plants on over-wintering preparedness and survival of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Journal of Insect Physiology, 53, 1016–1026.

[26] Martini,X., Hoffmann, M., Coy,M.R., Stelinski,L.L. and Pelz-Stelinski, K.S. (2015) Infection of an insect vector with a bacterial plant pathogen increases its propensity for dispersal. PLoS ONE, 10, e0129373.

[27] Martini,X., Kuhns,E., Hoyte,A. and Stelinski, L. (2014) Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host suitability on a spatial scale. Arthropod-Plant Interactions, 8, 453–460.

[28] Mauck,K.E. and Chesnais, Q. (2020) A synthesis of virus-vector associations reveals important deficiencies in studies on host and vector manipulation by plant viruses. Virus Research, 285, 197957.

[29] Moiroux,J., Chesnais, Q., Spicher,F., Verrier,E., Ameline, A. and Couty,A. (2018) Plant virus infection influences bottom-up regulation of a plant-aphid-parasitoid system. Journal of Pest Science, 91, 361–372.

[30] Moreno-Delafuente,A., Garzo, E., Moreno,A. and Fereres,A. (2013) A plant virus manipulates the behavior of its whitefly vector to enhance its transmission efficiency and spread. PLoS ONE, 8, e61543.

[31] Oke,A.O., Oladigbolu, A.A., Kunta,M., Alabi,O.J. and Sétamou, M. (2020) First report of the occurrence of Asian citrus psyllid Diaphorina citri (Hemiptera: Liviidae), an invasive species in Nigeria, West Africa. Scientific Reports, 10, 9418.

[32] Padhi,E.M.T., Araujo, K.J., Mitrovic,E., Polek,M., Godfrey, K.E. and Slupsky,C.M. (2022) The impact of Diaphorina citri-vectored “Candidatus Liberibacter asiaticus” on Citrus metabolism. Phytopathology, 112, 197–204.

[33] Pandey,S.S., Vasconcelos N.D.C. F. and Wang,N. (2021) Spatiotemporal Dynamics of “Candidatus Liberibacter asiaticus” colonization inside Citrus plant and huanglongbing disease development. Phytopathology, 111, 921–928.

[34] Ren,S.L., Li,Y.H., Zhou,Y.T., Xu, W.M., Cuthbertson,A.G.S., Guo,Y.J. et al. (2016) Effects of Candidatus Liberibacter asiaticus on the fitness of the vector Diaphorina citri. Journal of Applied Microbiology, 121, 1718–1726.

[35] Reynaud,B., Turpin, P., Molinari,F.M., Grondin,M., Roque,S., Chiroleu,F. et al. (2022) The African citrus psyllid Trioza erytreae: an efficient vector of Candidatus Liberibacter asiaticus. Frontiers in Plant Science, 13, 1089762.

[36] Silva,J.R. da, Boaretto, R.M., Lavorenti,J.A.L., dos Santos,B.C.F., Coletta-Filho, H.D. and Mattos,D. (2021) Effects of deficit irrigation and Huanglongbing on sweet orange trees. Frontiers in Plant Science, 12, 731734.

[37] Tjallingii,W.F. (1988) Electrical recording of stylet penetration activities. In Aphids, Their Biology, Natural Enemies and Control (eds. A.K.Minks & P. Harrewijn), pp. 95–108. Elsevier.

[38] Tjallingii,W.F. (1978) Electronic recording of penetration behaviour by aphids. Entomologia Experimentalis et Applicata, 24, 721–730.

[39] Yao,I. and Katagiri, C. (2011) Comparing wing loading, flight muscle and lipid content in ant-attended and non-attended Tuberculatus aphid species. Physiological Entomology, 36, 327–334.

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2023 2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.