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Banana Tree Infected with Banana Bunchy Top Virus Attracts Pentalonia nigronervosa Aphids Through Increased Volatile Organic Compounds Emission

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Abstract

Banana plants are affected by various viral diseases, among which the most devastating is the "bunchy top", caused by the Banana bunchy top virus (BBTV) and transmitted by the aphid Pentalonia nigronervosa Coquerel. The effect of BBTV on attraction mechanisms of dessert and plantain banana plants on the vector remains far from elucidated. For that, attractiveness tests were carried out using a two columns olfactometer for apterous aphids, and a flight cage experiment for alate aphids. Volatile Organic Compounds (VOCs) emitted by either healthy or BBTV-infected banana plants were identified using a dynamic extraction system and gas-chromatography mass-spectrometry (GC–MS) analysis. Behavioral results revealed a stronger attraction of aphids towards infected banana plants (independently from the variety), and towards the plantain variety (independently from the infection status). GC–MS results revealed that infected banana plants produced VOCs of the same mixture as healthy banana plants but in much higher quantities. In addition, VOCs produced by dessert and plantain banana plants were different in nature, and plantains produced higher quantities than dessert banana trees. This work opens interesting opportunities for biological control of P. nigronervosa, for example by luring away the aphid from banana plants through manipulation of olfactory cues.

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References

  • Abadie C, Bakry F, Carlier J, Caruana ML, Cote F, Ganry J, Lescot T, Marie P, Sarah JL (2003) Bananes forever. Dossier du mois Février. FruitTrop 99:4–11

    Google Scholar 

  • Allmann S, Baldwin IT (2010) Insects betray themselves in nature to predators by rapid isomerization of Green Leaf Volatiles. Science 329:1075–1078. https://doi.org/10.1126/science.1191634

    Article  CAS  PubMed  Google Scholar 

  • Anhalt MD, Almeida RPP (2008) Effect of temperature, vector life stage and plant access period on transmission of Banana bunchy top virus to banana. Arch Virol 153:135–146

    CAS  Google Scholar 

  • Arimura G-I, Ozawa R, Kugimiya S, Takabayashi J, Bohlmann J (2004) Herbivore-induced defense response in a model legume. Two-spotted spider mites induce emission of (E)-ocimene and transcript accumulation of (E)-ocimene synthase in Lotus japonicus. Plant Physiol 135:1976–1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW (2005) Herbivore arthropods benefit from vectoring plant viruses. Ecol Lett 8:70–79

    Article  Google Scholar 

  • Berenbaum MR (1995) The chemistry of defense: theory and practice. Proc Natl Acad Sci 92:2–8. https://doi.org/10.1073/pnas.92.1.2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berhal C, De Clerck C, Fauconnier ML, Levicek C, Boullis A, Kaddes A, Jijakli HM, Verheggen F, Massart S (2017) First characterisation of volatile organic compounds emitted by banana plants. Nat Publ Group 1:1–7. https://doi.org/10.1038/srep46400

    Article  CAS  Google Scholar 

  • Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol Exp Appl 87:133–142

    Article  CAS  Google Scholar 

  • Bosque-Pérez NA, Eigenbrode SD (2011) The infuence of virus-induced changes in plants on aphid vectors: insights from Luteovirus pathosystems. Virus Res 159:201–205

    Article  PubMed  CAS  Google Scholar 

  • Braendle C, Davis GK, Brisson JA, Stern DL (2006) Wing dimorphism in aphids. Heredity 97:192–199

    Article  CAS  PubMed  Google Scholar 

  • Burns RM, Dale HJL (1995) The genome organization of Banana bunchy top virus: analysis of six DNAss components. J Gen Virol 76:1471–1482

    Article  CAS  PubMed  Google Scholar 

  • Byers JA, Wood DL, Browne LE, Fish R, Piatek B, Hendry LB (1979) Relationship between a host plant compound, myrcene and pheromone production in the bark beetle, Ips paraconfusus. J Insect Physiol 25:477–482

    Article  CAS  Google Scholar 

  • CABI (2021) Invasive species compendium https://www.cabi.org/isc/. Consulted le 26 May 2021

  • Carmo-Sousa M, Moreno A, Garzo E, Fereres A (2014) A non-persistently transmitted-virus induces a pull-push strategy in its aphid vector to optimize transmission and sprea. Virus Res 186:38–46. https://doi.org/10.1016/j.virusres.2013.12.012

    Article  CAS  PubMed  Google Scholar 

  • 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. Ann Appl Biol 169:284–297

    Article  CAS  Google Scholar 

  • Chabannes M, Baurens FC, Duroy PO, Bocs S, Vernerey M-S, Rodier-Goud M, Barbe V, Gayral P, Iskra-Caruana ML (2013) Three infectious viral species lying in wait in the banana genome. J Virol 87(15):8624–8637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrassekar A, Kalaiponnani K, Elayabalan S, Kumar KK, Angappan K, Balasubramanian P (2011) Screening of Banana bunchy top virus through multiplex PCR approach. Arch Phytopathol Plant Prot 44:1920–2192. https://doi.org/10.1080/03235408.2010.522820

    Article  CAS  Google Scholar 

  • Chaudhry Z, Fujimoto S, Satoh S, Yoshioka T, Hase S, Ehara Y (1998) Stimulated ethylene production in Tobacco (Nicotiana Tabacum L., Cv. Ky 57) leaves infected systemically with Cucumber Mosaic Virus yellow strain. Plant Sci 131:123–130

    Article  CAS  Google Scholar 

  • Chesnais Q, Couty A, Uzest M, Brault V, Ameline A (2019a) Plant infection by two different viruses induce contrasting changes of vectors fitness and behavior. Insect Sci 26:86–96. https://doi.org/10.1111/1744-7917.12508

    Article  CAS  PubMed  Google Scholar 

  • Chesnais Q, Mauck QE, Bogaert F, Bamière A, Catterou MF, Brault V, Tepfer M, Ameline A (2019b) Virus effects on plant quality and vector behavior are species specific and do not depend on host physiological phenotype. J Pest Sci 92:791–804

    Article  Google Scholar 

  • De Backer L, Megido RC, Fauconnier ML, Brostaux Y, Francis F, Verheggen F (2015) Tuta absoluta-induced plant volatiles: attractiveness towards the generalist predator Macrolophus pygmaeus. Interact Arthropode-Plante 9:465–476. https://doi.org/10.1002/9780470015902.A0021525.a0000760.pub2

    Article  Google Scholar 

  • Döring TF (2014) How aphids find their host plants, and how they don’t. Ann Appl Biol 165:3–26

    Article  Google Scholar 

  • Dowiya NB, Rweyemamu CI, Maerere AP (2009) Banana (Musa spp. Colla) cropping systems, production constraints and cultivar preferences in eastern Democratic Republic of Congo. J Anim Plant Sci 4(2):341–356

    Google Scholar 

  • Edwards FL, Tchounwou P (2005) Environmental toxicology and health effects associated with methyl parathion exposure—a scientific review. Int J Environ Res Public Health 2(3):430–441

    Article  CAS  PubMed  Google Scholar 

  • Eigenbrode SD, Ding H, Shiel P, Berger PH (2002) Volatiles from potato plants infected with potato leafroll virus attract and arrest the virus vector, Myzus persicae (Homoptera: Aphididae). Proc R Soc Lond B 269:455–460

    Article  CAS  Google Scholar 

  • Eigenbrode SD, Bosque-Pérez NA, Davis TS (2018) Insect-borne plant pathogens and their vectors: ecology, evolution, and complex interactions. Annu Rev Entomol 63:169–191

    Article  CAS  PubMed  Google Scholar 

  • Fereres A, Raccah B (2015) Plant virus transmission by insects. Encyclopedia of life sciences

  • Francis F, Vandermoten S, Verheggen F, Lognay G, Haubruge E (2005) Is the (E)-β-farnesene only volatile terpenoid in aphids? J Appl Entomol 129:6–11

    Article  CAS  Google Scholar 

  • Gatsinzi F (1987) Les Principales Maladies et Ravageurs du Bananier au sein de la CEPGL in Séminaire sur les maladies et ravageurs des principales cultures vivrières d’Afrique centrale. Iraz, CTA, Bujumbura

  • Gray S, Cilia M, Ghanim M (2014) Circulative, “non propagative” virus transmission: an orchestra of virus-, insect-, and plant-derived instruments. Adv Virus Res 89:141–199

    Article  PubMed  Google Scholar 

  • Hafner GJ, Harding RM, Dale JL (1995) Movement and transmission of Banana bunchy top virus DNA component one in banana. J Gen Virol 76:2279–2285

    Article  CAS  PubMed  Google Scholar 

  • Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT (2008) Shared signals—alarm calls from plants increase apparency to herbivores and their enemies in nature. Ecol Lett 11:24–34

    PubMed  Google Scholar 

  • Hardie J, Visser JH, Piron PGM (1995) Peripheral odour perception by adult aphid forms with the same genotype but different host-plant preferences. J Insect Physiol 41:91–97

  • Harris KF (1977) An ingestion-egestion hypothesis of non circulative virus transmission. In: Harris KF et al (eds) Aphids as virus vectors. Academic Press, New York, pp 166–208

    Google Scholar 

  • Herrbach E (1985) Rôle des semiochimiques dans les relations pucerons-plantes II - Les substances allelochimiques. Agron EDP Sci 5:375–384

    Google Scholar 

  • Hoballah ME, Turlings TCJ (2005) The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J Chem Ecol 31:2003–2018

    Article  CAS  PubMed  Google Scholar 

  • Hooks CRR, Manandhar R, Perez EP, Wang KH, Almeida RPP (2009) Comparative susceptibility of two banana cultivars to banana bunchy top virus under laboratory and field environments. J Econ Entomol 102(3):897–904. https://doi.org/10.1603/029.102.0306

    Article  CAS  PubMed  Google Scholar 

  • Hullé M, Ighil ET-A, Robert Y, Monnet Y (1999) Les pucerons des plantes maraîchères. Cycles biologiques et activités de vol. INRA édit

  • Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Science 2:578

    Google Scholar 

  • Iskra-Caruana M-L (2003) Banana bunchy top virus—BBTV, Analyse du risque Phytosanitaire (ARP). CIRAD, BAN, p 31

  • James DG (2003) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J Chem Ecol 29:1601–1609

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628

    Article  CAS  PubMed  Google Scholar 

  • Jimenez-Martinez ES, Bosque-Perez NA, Berger PH, Zemetra RS, Ding H, Eigenbrode SD (2004) Volatile cues influence the reponse of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environ Entomol 33(5):1207–1216. https://doi.org/10.1603/0046-225X-33.5.1207

    Article  CAS  Google Scholar 

  • Kassambara A, Mundt F (2017) Package ‘factoextra’. Extract and visualize the results of multivariate data analyses, 76

  • Kumar LP, Selvarajan R, Iskra- Caruana M-L, Chabannes M, Hanna R (2015) Biology, etiology and control of virus diseases of banana and plantain. Adv Virus Res 91:229–269

    Article  CAS  PubMed  Google Scholar 

  • Kwa M (2003) Activation de bourgeons latents et utilisation de fragments de tige du bananier pour la propagation en masse de plants en conditions horticoles in vivo. Fruits 58:315–328. https://doi.org/10.1051/fruits:2003018

    Article  Google Scholar 

  • Kwa M (2009) La culture et la multiplication des plants de bananier (Musa sp.), Connaissances et techniques de base. CARBAP, RD Congo

  • Leather SR (2014) What attracts aphids—Kennedy, Booth and Kershaw (1961): host finding by aphids in the field III. Visual attraction—a top 20 paper in the Annals of Applied Biology. Ann Appl Biol 165:1–2. https://doi.org/10.1111/aab.12140

    Article  Google Scholar 

  • Lepoivre P (2003) Phytopathologie. Ed. De Broek

  • Lípez MF, Cano-Ramírez C, Shibayama M, Zúñiga G (2011) α-pinene et myrcene induce ultrastructural changes in the midgut of Dendroctonus valens (Coleoptera: Curculionidae: Scolytinae). Ann Entomol Soc Am 104:553–561. https://doi.org/10.1603/AN10023

    Article  CAS  Google Scholar 

  • Lorenzen J, Tenkouano A, Bandyopadhyay R, Vroh B, Coyne D, Tripathi L (2010) Overview of banana and plantain (Musa spp.) Improvement in Africa: past and future. Acta Hortic 879:595–603

    Article  Google Scholar 

  • Mauck KE, Chesnais Q (2020) A synthesis of virus-vector associations reveals important deficiencies in studies on host and vector manipulation by plant viruses. Virus Res 285:197957. https://doi.org/10.1016/j.virusres.2020.197957

  • Mauck KE, De Moraes CM, Mescher MC (2010) Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. PNAS 107(8):3600–3605. https://doi.org/10.1073/pnas.0907191107

    Article  PubMed  PubMed Central  Google Scholar 

  • Mauck KE, Bosque-Pérez NA, Eigenbrode SD, De Moraes C, Mescher MC (2012) Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses (ed C Fox). Funct Ecol 26:1162–1175. https://doi.org/10.1111/j.1365-2435.2012.02026.x

    Article  Google Scholar 

  • Mauck KE, Chesnais Q, Shapiro LR, Seven C (2018) Evolutionary determinants of host and vector manipulation by plant viruses. Adv Virus Res 101:189–250. https://doi.org/10.1016/bs.aivir.2018.02.007

    Article  PubMed  Google Scholar 

  • Mbunzu BBN, Ngbengbu N, Ngongo MK (2019) Evaluation du potentiel de prolifération d’explants de différentes dimensions de bananier plantain (Musa sp. cv. AAB) par la macropropagation en conditions semicontrôlées. Revue Africaine D’environnement Et D’agriculture 2:25–31

    Google Scholar 

  • Meutchieye F (2009) Fiche Technique de multiplication des bananiers par la méthode de PIF. SECAAR, Lomé, Togo

  • Mobambo P, Staver C, Hauser S, Dheda B, Vangu G (2010) An Innovation Capacity Analysis to identify Strategies for improving plantain and banana (Musa spp.) productivity and value addition in the Democratic Republic of Congo. Acta Hort 879:821–828

    Article  Google Scholar 

  • Mukwa LFT, Muengula M, Zinga I, Kalonji A, Iskra-Caruana ML, Bragard C (2014) Occurrence and distribution of Banana bunchy top virus related Agro-Ecosystem in South Wewtern, Democratic Republic of Congo. Am J Plant Sci 5:647–658

    Article  Google Scholar 

  • Mukwa LFT, Gillis A, Vanhese V, Romay G, Galzi S, Laboureau N, Kalonji-Mbuyi A, Iskra-Caruana L, Bragard C (2016) Low genetic diversity of Banana bunchy top virus, with a sub-regional pattern of variation, in Democratic Republic of Congo. Virus Genes 52(6):900–905

    Article  CAS  PubMed  Google Scholar 

  • Natale D, Mattiacci L, Hern A, Pasqualini E, Dorn S (2003) Response of female Cydia molesta (Lepidoptera: Tortricidae) to plant derived volatiles. Bull Entomol Res 93:335–342

    Article  CAS  PubMed  Google Scholar 

  • Peccoud J, Simon J-C, von Dohlen C, Coeur d’acier A, Plantegenest M, Vanlerberghe-Masutti F, Jousselin E (2010) Evolutionary history of aphid-plant associations and their role in aphid diversification. C R Biol 333:474–487. https://doi.org/10.1016/j.crvi.2010.03.004

    Article  PubMed  Google Scholar 

  • Penrose L, Thwaite WG, Bower CC (1994) Rating index as a basis for decision making on pesticide use reduction and for accreditation of fruit produced under integrated pest-management. Crop Prot 13(2):146–152

    Article  Google Scholar 

  • Pherobase. Pherobase. http://www.pherobase.com/. Accessed 6 Jan 2021

  • Pickett JA, Allemann RK, Birkett MA (2013) The semiochemistry of aphids. Nat Prod Rep 30:1277–1283

    Article  CAS  PubMed  Google Scholar 

  • Piesik D, Pańka D, Jeske M, Wenda-Piesik A, Delaney KJ, Weaver DK (2013) Volatile induction of infected and neighbouring uninfected plants potentially influence attraction/repellence of a cereal herbivore. J Appl Entomol 137:296–309

    Article  CAS  Google Scholar 

  • Ploetz RC (2015) Management of Fusarium wilt of banana: a review with special reference to tropical race 4. Crop Prot 73:7–15. https://doi.org/10.1016/j.cropro.2015.01.007

    Article  CAS  Google Scholar 

  • Qazi J (2016) Virus du Bunchy top de la banane et maladie du bunchy top. J Gen Plant Pathol 82:2–11

    Article  Google Scholar 

  • Raccah B, Fereres A (2009) Plant virus transmission by insects. In: Encyclopedia of life sciences (ELS). Wiley, Chichester

  • Rajabaskar D, Bosque-Perez NA, Eigenbrode SD (2014) Preference by a virus vector for infected plants is reversed after virus acquisition. Virus Res 186:32–37

    Article  CAS  PubMed  Google Scholar 

  • Roosien BK, Gomulkiewicz R, Ingwell LL, Bosque-Perez NA, Rajabaskar D, Eigenbrode SD (2013) Conditional vector preference aids the spread of plant pathogens: results from a model. Environ Entomol 42:1299–1308

    Article  PubMed  Google Scholar 

  • Ruther J, Kleier S (2005) Plant-plant signaling: ethylene synergizes volatile emission in: Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222. https://doi.org/10.1007/s10886-005-6413-8

    Article  CAS  PubMed  Google Scholar 

  • Sadom L, Tomekpé K, Folliot M, Côte F-X (2010) Comparaison de l’efficacité de deux méthodes de multiplication rapide de plants de bananier à partir de l’étude des caractéristiques agronomiques d’un hybride de bananier plantain (Musa spp.). Fruits 65:3–9. https://doi.org/10.1051/fruits/2009036

    Article  Google Scholar 

  • Shapiro L, De Moraes CM, Stephenson AG, Mescher MC (2012) Pathogen effects on vegetative and floral odours mediate vector attraction and host exposure in a complex pathosystem. Ecol Lett 15:1430–1438

    Article  PubMed  Google Scholar 

  • Shiragi H, Baque A, Nasiruddin K (2010) Eradication of Banana bunchy top virus (BBTV) through meristem culture of infected plant banana cv. Sabri. Horticult Environ Biotechnol 51:212–221

    CAS  Google Scholar 

  • Simmonds NW (1962) The evolution of the bananas. Tropical Science Series, Longmans, London (GBR)

  • Sisterson MS (2008) Effects of insect-vector preference for healthy or infected plants on pathogen spread: insights from a model. J Econ Entomol 101:1–8

    Article  PubMed  Google Scholar 

  • Smith RH (1965) Effect of monoterpene vapors on the western pine beetle. J Econ Entomo 58:509–510

    Article  CAS  Google Scholar 

  • Srinivasan R, Alvarez JM, Eigenbrode SD, Bosque-pérez NA (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 35:546–553. https://doi.org/10.1603/0046-225X-35.2.546

    Article  Google Scholar 

  • Stainton D, Martin DP, Muhire BM, Lolohea S, Halafihi M, Lepoint P, Blomme G, Crew KS, Sharman M, Kraberger S, Dayaram A, Walters M, Collings DA, Mabvakure B, Lemey P, Harkins GW, Thomas JE, Varsani A (2015) The global distribution of Banana bunchy top virus reveals little evidence for frequent recent, human-mediated long distance dispersal events. Virus Evol 1(1):vev009. https://doi.org/10.1093/ve/vev009

    Article  PubMed  PubMed Central  Google Scholar 

  • Stenberg JA, Heil M, Åhman I, Björkman C (2015) Optimizing crops for biocontrol of pests and disease. Trends Plant Sci 20:698–712

    Article  CAS  PubMed  Google Scholar 

  • Su HJ, Wu RY, Tsao LY (1992) Ecology of banana bunchy top virus desease. In: Proceedings of the international symptosium on recent development in banana cultivation technology. INIBAP-ASPNET, Los Bonos, Philippines, p 308–312

  • Syed Z, Leal WS (2009) Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proc Natl Acad Sci USA 106(44):18803–18808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas JE, Iskra Caruana ML (1999) Bunchy top. In: Jones DR (ed) Deseases of, abaca and enset. CABI, London, pp 241–253

    Google Scholar 

  • Thomas JE, Iskra-Caruana ML (2000) Bunchy top. In: Jones DR (ed) Diseases of banana, Abaca and Ensete. CAB International, Wallingford, pp 241–253

    Google Scholar 

  • Thomas JE, Iskra-Caruana ML, Jones DR (1994) Maladies des Musa – Le bunchy top du Bananier. Fiche technique N° 4, INIBA, Montpellier, France

  • Thomas F, Adamo S, Moore J (2005) Parasitic manipulation: where are we and where should we go? Behav Proc 68(3):185–199

    Article  Google Scholar 

  • Timchenko T, Bernadi F (2007) Nanoviruses, small plant viruses: similarities and differences with geminiviruses. Virology 11:27–42

    Google Scholar 

  • Toby JAB, Wadhams LJ, Woodcock CM (2005) Insect host location a volatile situation. Trends Plant Sci 10:269–274

    Article  CAS  Google Scholar 

  • Tungadi T, Groen SC, Murphy AM, Pate AE, Iqbal J, Bruce TJA, Cunniffe NJ, Carr JP (2017) Cucumber mosaic virus and its 2b protein alter emission of host volatile organic compounds but not aphid vector settling in tobacco. Virol J 14:91. https://doi.org/10.1186/s12985-017-0754-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Emden HF (1973) Aphid host plant relationships, some recent studies. ln: A. D. Lowe: Perspectives in aphid biology. Bull Entomol Soc N Z 2:54–64

    Google Scholar 

  • van Regenmortel, MHV, Fauquet CM, Bishop DHL, Carstens EB, Estes MK, Lemon SM, Maniloff J, Mayo MA, McGeoch DJ, Pringle CR and Wickner RB (2000) Virus taxonomy: classification and nomenclature of viruses. In: Seventh report of the International Committee on Taxonomy of Viruses, San Diego, San Francisco, New York, Boston, London, Sydney and Tokyo, Academic Press

  • Verheggen FJ, Haubruge E, De Moraes CM, Mescher MC (2009) Social enviroment influences aphid production of alarm pheromone. Behav Ecol 20:283–288

    Article  Google Scholar 

  • Visser JH, Piron PGM, Hardie J (1996) The aphids’ peripheral perception of plant volatiles. In: Städler E, Rowell-Rahier M, Bauer R (eds) Proceedings of the 9th international symposium on insect-plant relationships. Series entomologica, vol 53, Springer, Dordrecht. https://doi.org/10.1007/978-94-009-1720-0_8

  • Walangululu MJ, Matara MR, Bahati L, Niyongere C, Lepoint P, Blomme G (2010) Assessing the spread and seasonal influence of fruit peel disease and banana bunchy top disease in South Kivu, Eastern DR-Congo. Tree Fort Sci Biotechnol 4(46):52

    Google Scholar 

  • Whittaker RH, Feeny PP (1971) Allelochemics: chemical interactions between species. Science 17:757–770. https://doi.org/10.1126/science.171.3973.757

    Article  Google Scholar 

  • Williams IS, Dixon AFG (2007) Life cycles and polymorphism. In: van Emden HF, Harrington R (eds) Aphid as crop pests. CABI, Wallington, pp 69–85

    Chapter  Google Scholar 

  • Xu Q, Hatt S, Lopes T, Zhang Y, Bodson B, Chen J, Francis F (2018) A push-pull strategy to control aphids combines intercropping with semiochemical releases. J Pest Sci 91:93–103. https://doi.org/10.1007/s10340-017-0888-2

    Article  Google Scholar 

  • Xu H, Zhou G, Dötterl S, Schäffler I, Degen T, Chen L, Turlings TCJ (2020) Distinct roles of cuticular aldehydes as pheromonal cues in two Cotesia parasitoids. J Chem Ecol 46:128–137

    Article  CAS  PubMed  Google Scholar 

  • Yongjun D, Fushun Y, Jue T (1995) Structure and function of olfactory sensilla on the antennae of soybean aphids, Aphis glycines. Acta Entomol Sin 38:1–7

    Google Scholar 

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Acknowledgements

We thank Franck Michels and Matthieu Leclercq for having introduced us to chromatographic analyzes. We also thank the International Institute of Tropical Agriculture—IITA/Kalambo (Bukavu, Democratic Republic of Congo) and the head of the Kinshasa Plant Clinic, Lyna Mukwa Fama Tongo, for their supports and advice regarding healthy and infected banana collection. We thank anonymous reviewers for their work on an earlier version of this manuscript. This paper is the publication BRC 372 of the Earth and Life Institute, UCLouvain.

Funding

Ignace Murhububa Safari was supported by the Conseil de l'action internationale (CAI) of the UCLouvain. Kévin Tougeron was supported by the F.R.S.-FNRS. The "attractiveness" section of this study was supported by the Academy of Research and Higher Education (ARES). The "VOC extraction and identification" section was funded by the UCLouvain.

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Authors and Affiliations

  1. Earth and Life Institute, Ecology and Biodiversity, UCLouvain, Croix du sud 4-5/L7.07.04, 1348, Louvain-la-Neuve, Belgium

    Ignace Safari Murhububa, Kévin Tougeron & Thierry Hance

  2. Faculté Des Sciences Agronomiques, Université Catholique de Bukavu, Bukavu, Democratic Republic of the Congo

    Ignace Safari Murhububa, Espoir Bisimwa Basengere & Jean Walangululu Masamba

  3. UMR CNRS 7058 EDYSAN (Écologie et Dynamique des Systèmes Anthropisés), Université de Picardie Jules Verne, 33 rue St Leu, 80039, Amiens Cedex,, France

    Kévin Tougeron

  4. Earth and Life Institute, Applied Microbiology, UCLouvain, Croix du sud 2/L7.05.03, 1348, Louvain-la-Neuve, Belgium

    Claude Bragard

  5. General and Organic Chemistry Laboratory, Gembloux Agro-Bio Tech, Université de Liège, Gembloux, Belgium

    Marie-Laure Fauconnier

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  1. Ignace Safari Murhububa
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Contributions

IMS performed the experiments and wrote a first draft of the manuscript. IMS and KT analysed data. TH secured funding and supervised the project. All coauthors significantly contributed to the realization of the study and in the revision of the manuscript.

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Correspondence to Ignace Safari Murhububa.

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Safari Murhububa, I., Tougeron, K., Bragard, C. et al. Banana Tree Infected with Banana Bunchy Top Virus Attracts Pentalonia nigronervosa Aphids Through Increased Volatile Organic Compounds Emission. J Chem Ecol 47, 755–767 (2021). https://doi.org/10.1007/s10886-021-01298-3

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  • DOI: https://doi.org/10.1007/s10886-021-01298-3

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