Densovirus infection facilitates plant-virus transmission by an aphid.
Myzus persicae
Myzus persicae nicotianae densovirus
Potato virus Y
(E)‐β‐farnesene
locomotor activity
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
Aug 2024
Aug 2024
Historique:
received:
05
04
2024
accepted:
29
05
2024
medline:
18
7
2024
pubmed:
18
7
2024
entrez:
18
7
2024
Statut:
ppublish
Résumé
The interactions among plant viruses, insect vectors, and host plants have been well studied; however, the roles of insect viruses in this system have largely been neglected. We investigated the effects of MpnDV infection on aphid and PVY transmission using bioassays, RNA interference (RNAi), and GC-MS methods and green peach aphid (Myzus persicae (Sulzer)), potato virus Y (PVY), and densovirus (Myzus persicae nicotianae densovirus, MpnDV) as model systems. MpnDV increased the activities of its host, promoting population dispersal and leading to significant proliferation in tobacco plants by significantly enhancing the titer of the sesquiterpene (E)-β-farnesene (EβF) via up-regulation of expression levels of the MpFPPS1 gene. The proliferation and dispersal of MpnDV-positive individuals were faster than that of MpnDV-negative individuals in PVY-infected tobacco plants, which promoted the transmission of PVY. These results combined showed that an insect virus may facilitate the transmission of a plant virus by enhancing the locomotor activity and population proliferation of insect vectors. These findings provide novel opportunities for controlling insect vectors and plant viruses, which can be used in the development of novel management strategies.
Substances chimiques
Sesquiterpenes
0
beta-farnesene
18794-84-8
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1539-1553Subventions
Organisme : Agricultural Science and Technology Innovation Program
ID : ASTIP-TRIC04
Organisme : Agricultural Science and Technology Innovation Program
ID : KLTPMIMT2022-01
Organisme : Major special projects for green pest control
ID : 110202101028(LS-03)
Organisme : Major special projects for green pest control
ID : 110202201017(LS-01)
Organisme : Major special projects for green pest control
ID : SCYC202314
Informations de copyright
© 2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.
Références
Amuzu HE, Tsyganov K, Koh C, Herbert RI, Powell DR, McGraw EA. 2018. Wolbachia enhances insect‐specific flavivirus infection in Aedes aegypti mosquitoes. Ecology and Evolution 8: 5441–5454.
Blackman RL, Eastop VF. 2000. Aphids on the world's crops, an identification and information guide, 2ndedn. Chichester, UK: John Wiley & Sons Ltd.
Blua MJ, Perring TM. 1992. Alatae production and population increase of aphid vectors on virus‐infected host plants. Oecologia 92: 65–70.
Buchfink B, Xie C, Huson DH. 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods 12: 59–60.
Carmo‐Sousa M, Moreno A, Plaza M, Garzo E, Fereres A. 2016. Cucurbit aphid‐borne yellows virus (CABYV) modifies the alighting, settling and probing behaviour of its vector Aphis gossypii favouring its own spread. Annals of Applied Biology 169: 284–297.
Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA, Jander G. 2014. The NIa‐pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). The Plant Journal 77: 653–663.
Chen X, Liu J, Xu P, Liu Y, Dong Y, Zang Y, Cai X, Ren G. 2020. Changes in the nutrient composition of tobacco plants after Potato virus Y infection and their effects on the growth and development of the vector Myzus persicae (Hemiptera: Aphidiae). Acta Entomologica Sinica 63: 181–190.
Chen Y, Evans J, Feldlaufer M. 2006. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. Journal of Invertebrate Pathology 92: 152–159.
Cheng Y, Li Z. 2019. Both farnesyl diphosphate synthase genes are involved in the production of alarm pheromone in the green peach aphid Myzus persicae. Archives of Insect Biochemistry and Physiology 100: e21530.
Clem RJ, Passarelli AL. 2013. Baculoviruses: sophisticated pathogens of insects. PLoS Pathogens 9: e1003729.
Conesa A, Götz S, García‐Gómez JM, Terol J, Talón M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674–3676.
Dietzgen RG, Mann KS, Johnson KN. 2016. Plant virus–insect vector interactions: current and potential future research directions. Viruses 8: 303.
Eddy SR. 2011. Accelerated profile HMM searches. PLoS Computational Biology 7: e1002195.
van Emden HF, Eastop VF, Hughes RD, Way MJ. 1969. The ecology of Myzus persicae. Annual Review of Entomology 14: 197–270.
Fereres A, Moreno A. 2009. Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Research 141: 158–168.
Gadhave KR, Gautam S, Rasmussen DA, Srinivasan R. 2020. Aphid transmission of Potyvirus: the largest plant‐infecting RNA virus genus. Viruses 12: 773.
Gallois P, Marinho P. 1995. Leaf disk transformation using Agrobacterium tumefaciens‐expression of heterologous genes in tobacco. Methods in Molecular Biology 49: 39–48.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al. 2011. Full‐length transcriptome assembly from RNA‐Seq data without a reference genome. Nature Biotechnology 29: 644–652.
Graham RI, Grzywacz D, Mushobozi WL, Wilson K. 2012. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecology Letters 15: 993–1000.
Guo J, Ye G, Dong S, Liu S. 2010. An invasive whitefly feeding on a virus‐infected plant increased its egg production and realized fecundity. PLoS ONE 5: e11713.
Haase S, Sciocco‐Cap A, Romanowski V. 2015. Baculovirus insecticides in Latin America: historical overview, current status and future perspectives. Viruses 7: 2230–2267.
Hayes AM, Lavine MD, Gotoh H, Lin X, Lavine LC. 2019. Mechanisms regulating phenotypic plasticity in wing polyphenic insects. Advances in Insect Physiology 56: 43–72.
He Y, Wang Y, Yin T, Cuellar WJ, Liu S, Wang X. 2021. Gut‐expressed vitellogenin facilitates the movement of a plant virus across the midgut wall in its insect vector. mSystems 6: e0058121.
Hoffmann AA, Montgomery BL, Popovici J, Iturbe‐Ormaetxe I, Johnson PH, Muzzi F, Greenfield M, Durkan M, Leong YS, Dong Y et al. 2011. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476: 454–457.
Ibarra JE, Del Rincón‐Castro MC. 2009. Insect viruses diversity, biology, and use as bioinsecticides. In: Del Claro K, Oliveira PS, Gray VR, eds. Tropical biology and conservation management. Oxford, UK: Eolss Publishers, 304.
Islam W, Noman A, Naveed H, Alamri SA, Hashem M, Huang Z, Chen HYH. 2020. Plant‐insect vector‐virus interactions under environmental change. Science of the Total Environment 701: 135044.
Jagdale SS, Joshi RS. 2019. Facilitator roles of viruses in enhanced insect resistance to biotic stress. Current Opinion in Insect Science 33: 111–116.
Käfer S, Paraskevopoulou S, Zirkel F, Wieseke N, Donath A, Petersen M, Jones TC, Liu S, Zhou X, Middendorf M et al. 2019. Re‐assessing the diversity of negative strand RNA viruses in insects. PLoS Pathogens 15: e1008224.
Kennedy J, Day M, Eastop V. 1962. A conspectus of aphids as vector of plant viruses. London, UK: Commonwealth Institute of Entomology.
Kliot A, Kontsedalov S, Lebedev G, Czosnek H, Ghanim M. 2019. Combined infection with tomato yellow leaf curl virus and Rickettsia influences fecundity, attraction to infected plants and expression of immunity‐related genes in the whitefly Bemisia tabaci. Journal of General Virology 100: 721–731.
Kunert G, Otto S, Roese U, Gershenzon J, Weisser W. 2005. Alarm pheromone mediates production of dispersal morphs in aphids. Ecology Letters 8: 596–603.
Lacey LA, Grzywacz D, Shapiro‐Ilan DI, Frutos R, Brownbridge M, Goettel MS. 2015. Insect pathogens as biological control agents: back to the future. Journal of Invertebrate Pathology 132: 1–41.
Li P, Liu C, Deng W, Yao D, Pan L, Li Y, Liu Y, Liang Y, Zhou X, Wang X. 2019. Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors. PLoS Pathogens 15: e1007607.
Li T, Li H, Wu Y, Li S, Yuan G, Xu P. 2022. Identification of a novel densovirus in aphid, and uncovering the possible antiviral process during its infection. Frontiers in Immunology 13: 905628.
Li T, Xiao J, Xu Z, Murphy RW, Huang D. 2011. Cellular tropism, population dynamics, host range and taxonomic status of an aphid secondary symbiont, SMLS (Sitobion miscanthi L type symbiont). PLoS ONE 6: e21944.
Lin F, Bosquée E, Liu Y, Chen J, Yong L, Francis F. 2016. Impact of aphid alarm pheromone release on virus transmission efficiency: when pest control strategy could induce higher virus dispersion. Journal of Virological Methods 235: 34–40.
Liu J, Liu Y, Donkersley P, Dong Y, Chen X, Zang Y, Xu P, Ren G. 2019. Preference of the aphid Myzus persicae (Hemiptera: Aphididae) for tobacco plants at specific stages of potato virus Y infection. Archives of Virology 164: 1567–1573.
Ma E, Zhu Y, Liu Z, Wei T, Wang P, Cheng G. 2021. Interaction of viruses with the insect intestine. Annual Review of Virology 8: 115–131.
Medina‐Ortega KJ, Bosque‐Pérez NA, Ngumbi E, Jiménez‐Martínez ES, Eigenbrode SD. 2009. Rhopalosiphum padi (Hemiptera: Aphididae) responses to volatile cues from barley yellow dwarf virus–infected wheat. Environmental Entomology 38: 836–845.
Mondotte JA, Saleh MC. 2018. Antiviral Immune Response and the Route of Infection in Drosophila melanogaster. Advances in Virus Research 100: 247–278.
Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. 2007. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research 35: W182–W185.
Mostafavi R, Henning JA, Gardea‐Torresday J, Ray IM. 1996. Variation in aphid alarm pheromone content among glandular and eglandular‐haired Medicag accessions. Journal of Chemical Ecology 22: 1629–1638.
van Munster M, Dullemans AM, Verbeek M, van den Heuvel JFJM, Reinbold C, Brault V, Clérivet A, van der Wilk F. 2003. Characterization of a new densovirus infecting the green peach aphid Myzus persicae. Journal of Invertebrate Pathology 84: 6–14.
Musser RO, Hum‐Musser SM, Felton GW, Gergerich RC. 2003. Increased larval growth and preference for virus‐infected leaves by the Mexican bean beetle, Epilachna varivestis mulsant, a plant virus vector. Journal of Insect Behavior 16: 247–256.
Ng JCK, Perry KL. 2004. Transmission of plant viruses by aphid vectors. Molecular Plant Pathology 5: 505–511.
Palmer W, Medd N, Beard P, Obbard D. 2018. Isolation of a natural DNA virus of Drosophila melanogaster, and characterisation of host resistance and immune responses. PLoS Pathogens 14: e1007050.
Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS, Xi Z. 2012. Wolbachia induces reactive oxygen species (ROS)‐dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proceedings of the National Academy of Sciences, USA 109: E23–E31.
Pinheiro PV, Wilson JR, Xu Y, Zheng Y, Rebelo AR, Fattah‐Hosseini S, Kruse A, Dos Silva RS, Xu Y, Kramer M et al. 2019. Plant viruses transmitted in two different modes produce differing effects on small RNA‐mediated processes in their aphid vector. Phytobiomes Journal 3: 71–81.
Possee RD, King LA. 2014. Insect viruses. Chichester, UK: John Wiley & Sons, Ltd.
Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. 2005. InterProScan: protein domains identifier. Nucleic Acids Research 33: W116–W120.
Rajabaskar D, Wu Y, Bosque‐Pérez NA, Eigenbrode SD. 2013. Dynamics of Myzus persicae arrestment by volatiles from potato leafroll virus‐infected potato plants during disease progression. Entomologia Experimentalis et Applicata 148: 172–181.
Rancès E, Ye Y, Woolfit M, McGraw EA, O'Neill SL. 2012. The relative importance of innate immune priming in wolbachia‐mediated dengue interference. PLoS Pathogens 8: e1002548.
Ryabov EV, Keane G, Naish N, Evered C, Winstanley D. 2009. Densovirus induces winged morphs in asexual clones of the rosy apple aphid, Dysaphis plantaginea. Proceedings of the National Academy of Sciences, USA 106: 8465–8470.
Shi M, Lin X, Chen X, Tian J, Chen L, Li K, Wang W, Eden JS, Shen J, Liu L et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556: 197–202.
Shi M, Lin X, Tian J, Chen L, Chen X, Li C, Qin X, Li J, Cao J, Eden JS et al. 2016. Redefining the invertebrate RNA virosphere. Nature 540: 539–543.
Tang S, Song X, Xue L, Wang X, Wang X, Xu P, Ren G. 2016. Characterization and distribution analysis of a densovirus infecting Myzus persicae nicotianae (Hemiptera: Aphididae). Journal of Economic Entomology 109: 580–587.
Tian Y, Valkonen JP. 2015. Recombination of strain O segments to HCpro‐encoding sequence of strain N of Potato virus Y modulates necrosis induced in tobacco and in potatoes carrying resistance genes Ny or Nc. Molecular Plant Pathology 16: 735–747.
de Vos M, Cheng W, Summers HE, Raguso RA, Jander G. 2010. Alarm pheromone habituation in Myzus persicae has fitness consequences and causes extensive gene expression changes. Proceedings of the National Academy of Sciences, USA 107: 14673–14678.
Wan J, Liang Q, Zhang R, Cheng Y, Wang X, Wang H, Zhang J, Jia D, Du Y, Zheng W et al. 2023. Arboviruses and symbiotic viruses cooperatively hijack insect sperm‐specific proteins for paternal transmission. Nature Communications 14: 1289.
Wang B, Dong W, Li H, D'Onofrio C, Bai P, Chen R, Yang L, Wu J, Wang X, Wang B et al. 2022. Molecular basis of (E)‐β‐farnesene‐mediated aphid location in the predator Eupeodes corollae. Current Biology 32: 951–962.
Wang G, Yu X, Fan J, Wang C‐S, Xia L. 2015. Expressing an (E)‐β‐farnesene synthase in the chloroplast of tobacco affects the preference of green peach aphid and its parasitoid. Journal of Integrative Plant Biology 57: 770–782.
Wang X, Blanc S. 2021. Insect transmission of plant single‐stranded DNA viruses. Annual Review of Entomology 66: 389–405.
Whitfield AE, Falk BW, Rotenberg D. 2015. Insect vector‐mediated transmission of plant viruses. Virology 479‐480: 278–289.
Wu H, Pang R, Cheng T, Xue L, Zeng H, Lei T, Chen M, Wu S, Ding Y, Zhang J et al. 2020. Abundant and diverse RNA viruses in insects revealed by RNA‐seq analysis: ecological and evolutionary implications. mSystems 5: e00039.
Xu P, Liu Y, Graham RI, Wilson K, Wu K. 2014. Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide. PLoS Pathogens 10: e1004490.
Xu P, Yang L, Yang X, Li T, Graham RI, Wu K, Wilson K. 2020. Novel partiti‐like viruses are conditional mutualistic symbionts in their normal lepidopteran host, African armyworm, but parasitic in a novel host, fall armyworm. PLoS Pathogens 16: e1008467.
Yang X, Xu P, Yuan H, Graham RI, Wilson K, Wu K. 2019. Discovery and characterization of a novel picorna‐like RNA virus in the cotton bollworm Helicoverpa armigera. Journal of Invertebrate Pathology 160: 1–7.
Ye X, Shi M, Huang J, Chen X. 2018. Parasitoid polydnaviruses and immune interaction with secondary hosts. Developmental and Comparative Immunology 83: 124–129.
Zhang C, Brisson JA, Xu H. 2019. Molecular mechanisms of wing polymorphism in insects. Annual Review of Entomology 64: 297–314.
Zhang R, Wang B, Grossi G, Falabella P, Liu Y, Yan S, Lu J, Xi J, Wang G. 2017. Molecular basis of alarm pheromone detection in aphids. Current Biology 27: 55–61.