دورية أكاديمية
Effects of root inoculation of entomopathogenic fungi on olfactory-mediated behavior and life-history traits of the parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae).
| العنوان: | Effects of root inoculation of entomopathogenic fungi on olfactory-mediated behavior and life-history traits of the parasitoid Aphidius ervi (Haliday) (Hymenoptera: Braconidae). |
|---|---|
| المؤلفون: | Wilberts L; CMPG Laboratory for Process Microbial Ecology and Bioinspirational Management, Department of Microbial and Molecular Systems, KU Leuven, Leuven, Belgium.; Leuven Plant Institute, KU Leuven, Leuven, Belgium., Vuts J; Protecting Crops and the Environment, Rothamsted Research, Harpenden, UK., Caulfield JC; Protecting Crops and the Environment, Rothamsted Research, Harpenden, UK., Thomas G; Protecting Crops and the Environment, Rothamsted Research, Harpenden, UK., Withall DM; Protecting Crops and the Environment, Rothamsted Research, Harpenden, UK., Wäckers F; Biobest, Westerlo, Belgium.; Lancaster Environment Centre, Lancaster University, Lancaster, UK., Birkett MA; Protecting Crops and the Environment, Rothamsted Research, Harpenden, UK., Jacquemyn H; Leuven Plant Institute, KU Leuven, Leuven, Belgium.; Laboratory of Plant Conservation and Population Biology, Biology Department, KU Leuven, Leuven, Belgium., Lievens B; CMPG Laboratory for Process Microbial Ecology and Bioinspirational Management, Department of Microbial and Molecular Systems, KU Leuven, Leuven, Belgium.; Leuven Plant Institute, KU Leuven, Leuven, Belgium. |
| المصدر: | Pest management science [Pest Manag Sci] 2024 Feb; Vol. 80 (2), pp. 307-316. Date of Electronic Publication: 2023 Sep 23. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Published for SCI by Wiley Country of Publication: England NLM ID: 100898744 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1526-4998 (Electronic) Linking ISSN: 1526498X NLM ISO Abbreviation: Pest Manag Sci Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: West Sussex, UK : Published for SCI by Wiley, c2000- |
| مواضيع طبية MeSH: | Parasites* , Wasps*/physiology , Aphids*/physiology , Capsicum*, Animals ; Pest Control, Biological ; Plants ; Nicotiana |
| مستخلص: | Background: Although most biological control programs use multiple biological agents to manage pest species, to date only a few programs have combined the use of agents from different guilds. Using sweet pepper (Capsicum annuum L.), the entomopathogenic fungus Akanthomyces muscarius ARSEF 5128, the tobacco peach aphid Myzus persicae var. nicotianae and the aphid parasitoid Aphidius ervi as the experimental model, we explored whether root inoculation with an entomopathogenic fungus is compatible with parasitoid wasps for enhanced biocontrol of aphids. Results: In dual-choice behavior experiments, A. ervi was significantly attracted to the odor of M. persicae-infested C. annuum plants that had been inoculated with A. muscarius, compared to noninoculated infested plants. There was no significant difference in attraction to the odor of uninfested plants. Myzus persicae-infested plants inoculated with A. muscarius emitted significantly higher amounts of indole, (E)-nerolidol, (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene and one unidentified terpene compared to noninoculated infested plants. Coupled gas chromatography-electroantennography, using the antennae of A. ervi, confirmed the physiological activity of these elevated compounds. Inoculation of plants with A. muscarius did not affect parasitism rate nor parasitoid longevity, but significantly increased the speed of mummy formation in parasitized aphids on fungus-inoculated plants. Conclusion: Our data suggest that root inoculation of C. annuum with A. muscarius ARSEF 5128 alters the olfactory-mediated behavior of parasitoids, but has little effect on parasitism efficiency or life-history parameters. However, increased attraction of parasitoids towards M. persicae-infested plants when inoculated by entomopathogenic fungi can accelerate host localization and hence improve biocontrol efficacy. © 2023 Society of Chemical Industry. (© 2023 Society of Chemical Industry.) |
| References: | Mohammed AA and Hatcher PE, Combining entomopathogenic fungi and parasitoids to control the green peach aphid Myzus persicae. Biol Control 110:44-55 (2017). Aqueel MA and Leather SR, Virulence of verticillium lecanii (Z.) against cereal aphids; does timing of infection affect the performance of parasitoids and predators? Pest Manag Sci 69:493-498 (2013). Miranda-Fuentes P, Quesada-Moraga E, Aldebis HK and Yousef-Naef M, Compatibility between the endoparasitoid Hyposoter didymator and the entomopathogenic fungus Metarhizium brunneum: a laboratory simulation for the simultaneous use to control Spodoptera littoralis. Pest Manag Sci 76:1060-1070 (2020). van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ and Urbaneja A, Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39-59 (2018). Bale JS, Van Lenteren JC and Bigler F, Biological control and sustainable food production. Philos Trans R Soc B Biol Sci 363:761-776 (2008). Wu S, Xie H, Li M, Xu X and Lei Z, Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Exp Appl Acarol 70:421-435 (2016). Michereff-Filho M, Navia D, Alexopoulos Quevedo I, de Almeida Magalhães M, Wagner da Silva Melo J and Biaggioni Lopes R, The effect of spider mite-pathogenic strains of Beauveria bassiana and humidity on the survival and feeding behavior of Neoseiulus predatory mite species. Biol Control 176:105083 (2022). Ferguson KI and Stiling P, Non-additive effects of multiple natural enemies on aphid populations. Oecologia 108:375-379 (1996). Malo S, Arnó J and Gabarra R, Intraguild interactions between the predator Macrolophus pygmaeus and the parasitoid Eretmocerus mundus, natural enemies of Bemisia tabaci. Biocontrol Sci Technol 22:1059-1073 (2012). Fazeli-Dinan M, Talaei-Hassenloui R and Goettel M, Virulence of the entomopathogenic fungus Lecanicillium longisporum against the greenhouse whitefly, Trialeurodes vaporariorum and its parasitoid Encarsia Formosa. Int J Pest Manag 62:251-260 (2016). Oreste M, Baser N, Bubici G and Tarasco E, Effect of Beauveria bassiana strains on the Ceratitis capitata-Psyttalia concolor system. Bull Insectology 68:265-272 (2015). Lovett B and St. Leger RJ, The insect pathogens. Microbiol Spectr 5:1-19 (2017). de Faria MR and Wraight SP, Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237-256 (2007). Gange AC, Koricheva J, Currie AF, Jaber LR and Vidal S, Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol 223:2002-2010 (2019). Jaber LR and Ownley BH, Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36-45 (2018). Vega FE, The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110:4-30 (2018). Vidal S and Jaber LR, Entomopathogenic fungi as endophytes: plant-endophyte-herbivore interactions and prospects for use in biological control. Curr Sci 109:46-54 (2015). Bamisile BS, Dash CK, Akutse KS, Keppanan R and Wang L, Fungal endophytes: beyond herbivore management. Front Microbiol 9:544 (2018). Kuzhuppillymyal-Prabhakarankutty L, Tamez-Guerra P, Gomez-Flores R, Rodriguez-Padilla MC and Ek-Ramos MJ, Endophytic Beauveria bassiana promotes drought tolerance and early flowering in corn. World J Microbiol Biotechnol 36:47 (2020). Lopez DC and Sword GA, The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea). Biol Control 89:53-60 (2015). Tall S and Meyling NV, Probiotics for plants? Growth promotion by the entomopathogenic fungus Beauveria bassiana depends on nutrient availability. Microb Ecol 76:1002-1008 (2018). Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño ÁM, García-Mina JM, del Campillo MC and 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. Biol Control 116:90-102 (2018). Sword GA, Tessnow A and Ek-Ramos MJ, Endophytic fungi alter sucking bug responses to cotton reproductive structures. Insect Sci 24:1003-1014 (2017). Rondot Y and Reineke A, Endophytic Beauveria bassiana activates expression of defence genes in grapevine and prevents infections by grapevine downy mildew Plasmopara viticola. Plant Pathol 68:1719-1731 (2019). Klieber J and Reineke A, The entomopathogen Beauveria bassiana has epiphytic and endophytic activity against the tomato leaf miner Tuta absoluta. J Appl Entomol 140:580-589 (2016). Wilberts L, Vuts J, Caulfield JC, Thomas G, Birkett MA, Herrera-Malaver B et al., Impact of endophytic colonization by entomopathogenic fungi on the behavior and life history of the tobacco peach aphid Myzus persicae var. nicotianae. PLoS One 17:e0273791 (2022). Vega FE, Insect pathology and fungal endophytes. J Invertebr Pathol 98:277-279 (2008). Vega FE, Posada F, Catherine Aime M, Pava-Ripoll M, Infante F and Rehner SA, Entomopathogenic fungal endophytes. Biol Control 46:72-82 (2008). van Lenteren JC, The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:1-20 (2012). Wajnberg E, Roitberg BD and Boivin G, Using optimality models to improve the efficacy of parasitoids in biological control programmes. Entomol Exp Appl 158:2-16 (2016). Rehman A and Powell W, Host selection behaviour of aphid parasitoids (Aphidiidae: Hymenoptera). J Plant Breed Crop Sci 2:299-311 (2010). Heimpel GE and Asplen MK, A ‘Goldilocks’ hypothesis for dispersal of biological control agents. BioControl 56:441-450 (2011). González-Mas N, Gutiérrez-Sánchez F, Sánchez-Ortiz A, Grandi L, Turlings TCJ, Manuel Muñoz-Redondo J et al., Endophytic colonization by the entomopathogenic fungus Beauveria Bassiana affects plant volatile emissions in the presence or absence of chewing and sap-sucking insects. Front Plant Sci 12:660460 (2021). Jensen RE, Cabral C, Enkegaard A and Steenberg T, Influence of the plant interacting entomopathogenic fungus Beauveria bassiana on parasitoid host choice-behavior, development, and plant defense pathways. PLoS One 15:e0238943 (2020). González-Mas N, Cuenca-Medina M, Gutiérrez-Sánchez F and Quesada-Moraga E, Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. J Pest Sci 92:1271-1281 (2019). Jaber LR and Araj SE, 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). Biol Control 116:53-61 (2018). Francis F, Fingu-Mabola JC and Ben Fekih I, Direct and endophytic effects of fungal entomopathogens for sustainable aphid control: a review. Agriculture 12:2081 (2022). Dedryver CA, Le Ralec A and Fabre F, The conflicting relationships between aphids and men: a review of aphid damage and control strategies. C R Biol 333:539-553 (2010). Van Emden HF and Harrington R, Aphids as Crop Pests. CABI Publishing, Wallingford, United Kingdom (2007). Clements KM, Sorenson CE, Wiegmann BM, Neese PA and Roe RM, Genetic, biochemical, and behavioral uniformity among populations of Myzus nicotianae and Myzus persicae. Entomol Exp Appl 95:269-281 (2000). Hall RA, Control of whitefly, Trialeurodes vaporariorum and cotton aphid, Aphis gossypii in glasshouses by two isolates of the fungus, Verticillium lecanii. Ann Appl Biol 101:1-11 (1982). Landa BB, López-Díaz C, Jiménez-Fernández D, Montes-Borrego M, Muñoz-Ledesma FJ, Ortiz-Urquiza A et al., In-planta detection and monitorization of endophytic colonization by a Beauveria bassiana strain using a new-developed nested and quantitative PCR-based assay and confocal laser scanning microscopy. J Invertebr Pathol 114:128-138 (2013). Gardes M and Bruns TD, ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113-118 (1993). Sen SE and Garvin GM, Substrate requirements for Lepidopteran farnesol dehydrogenase. J Agric Food Chem 43:820-825 (1995). Osei-owusu J, Vuts J, Caulfield JC, Woodcock CM, Withall DM, Hooper AM et al., Identification of semiochemicals from cowpea, Vigna unguiculata, for low-input management of the legume pod borer, Maruca vitrata. J Chem Ecol 46:288-298 (2020). Goelen T, Sobhy IS, Vanderaa C, de Boer JG, Delvigne F, Francis F et al., Volatiles of bacteria associated with parasitoid habitats elicit distinct olfactory responses in an aphid parasitoid and its hyperparasitoid. Funct Ecol 34:507-520 (2020). Wadhams LJ, The use of coupled gas chromatography: electrophysiological techniques in the identification of insect pheromones, in Chromatography and Isolation of Insect Hormones and Pheromones, ed. by McCaffery AR and Wilson ID. Plenum Press, New York, USA, pp. 289-298 (1990). Sobhy IS, Baets D, Goelen T, Herrera-Malaver B, Bosmans L, van den Ende W et al., Sweet scents: nectar specialist yeasts enhance nectar attraction of a generalist aphid parasitoid without affecting survival. Front Plant Sci 9:1009 (2018). Nyabuga FN, Outreman Y, Simon JC, Heckel DG and Weisser WW, Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. Entomol Exp Appl 136:243-253 (2010). Oksanen AJ, Blanchet FG, Friendly M, Kindt R, Legendre P, Mcglinn D et al., vegan: Community Ecology Package. R package Version 2.5-5 (2019). https://CRAN.R-project.org/package=vegan. R Core Team, R: A language and environment for statistical computing R foundation for statistical computing (2019). Wilberts L, Preciado NR, Jacquemyn H and Lievens B, Fungal strain and crop cultivar affect growth of sweet pepper plants after root inoculation with entomopathogenic fungi. Front Plant Sci 14:1196765 (2023). Allegrucci N, Velazquez MS, Russo ML, Perez E and Scorsetti AC, Endophytic colonisation of tomato by the entomopathogenic fungus Beauveria bassiana: the use of different inoculation techniques and their effects on the tomato leafminer Tuta absoluta (lepidoptera: Gelechiidae). J Plant Prot 57:331-337 (2017). Gurulingappa P, Sword GA, Murdoch G and McGee PA, Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34-41 (2010). Posada F, Aime MC, Peterson SW, Rehner SA and Vega FE, Inoculation of coffee plants with the fungal entomopathogen Beauveria bassiana (Ascomycota: Hypocreales). Mycol Res 111:748-757 (2007). Parsa S, Ortiz V, Gómez-Jiménez MI, Kramer M and Vega FE, Root environment is a key determinant of fungal entomopathogen endophytism following seed treatment in the common bean, Phaseolus vulgaris. Biol Control 116:74-81 (2018). Rajab L, Ahmad M and Gazal I, Endophytic establishment of the fungal entomopathogen, Beauveria bassiana (Bals.) Vuil., in cucumber plants. Egypt J Biol Pest Control 30:143 (2020). Tefera T and Vidal S, Effect of inoculation method and plant growth medium on endophytic colonization of sorghum by the entomopathogenic fungus Beauveria bassiana. BioControl 54:663-669 (2009). Rasool S, Vidkjaer NH, Hooshmand K, Jensen B, Fomsgaard IS and Meyling NV, Seed inoculations with entomopathogenic fungi affect aphid populations coinciding with modulation of plant secondary metabolite profiles across plant families. New Phytol 229:1715-1727 (2021). Rondot Y and Reineke A, Endophytic Beauveria bassiana in grapevine Vitis vinifera (L.) reduces infestation with piercing-sucking insects. Biol Control 116:82-89 (2018). Gange AC, Brown VK and Aplin DM, Multitrophic links between arbuscular mycorrhizal fungi and insect parasitoids. Ecol Lett 6:1051-1055 (2003). Fontana A, Reichelt M, Hempel S, Gershenzon J and Unsicker SB, The effects of arbuscular mycorrhizal fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833-843 (2009). Jallow MFA, Dugassa-Gobena D and Vidal S, Influence of an endophytic fungus on host plant selection by a polyphagous moth via volatile spectrum changes. Arthropod-Plant Interact 2:53-62 (2008). D'Alessandro M, Erb M, Ton J, Brandenburg A, Karlen D, Zopfi J et al., Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell Environ 37:813-826 (2014). Miranda-Fuentes P, Yousef-Yousef M, Valverde-García P, Rodríguez-Gómez IM, Garrido-Jurado I and Quesada-Moraga E, Entomopathogenic fungal endophyte-mediated tritrophic interactions between Spodoptera littoralis and its parasitoid Hyposoter didymator. J Pest Sci 94:933-945 (2021). Preszler RW, Gaylord ES and Boecklen WJ, Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia 108:159-166 (1996). Rivas-Franco F, Hampton JG, Morán-Diez ME, Narciso J, Rostás M, Wessman P et al., Effect of coating maize seed with entomopathogenic fungi on plant growth and resistance against Fusarium graminearum and Costelytra giveni. Trends Plant Sci 29:877-900 (2019). Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ and Dicke M, Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507-514 (2010). Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, van Wees SCM and Bakker PAHM, Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347-375 (2014). Qin X, Zhao X, Huang S, Deng J, Li X, Luo Z et al., Pest management via endophytic colonization of tobacco seedlings by the insect fungal pathogen Beauveria bassiana. Pest Manag Sci 77:2007-2018 (2021). Takemoto H and Takabayashi J, Parasitic wasps Aphidius ervi are more attracted to a blend of host-induced plant volatiles than to the independent compounds. J Chem Ecol 41:801-807 (2015). Mumm R and Dicke M, Variation in natural plant products and the attraction of bodyguards involved in indirect plant defense. Can J Zool 88:628-667 (2010). Gols R, Bullock JM, Dicke M, Bukovinszky T and Harvey JA, Smelling the wood from the trees: non-linear parasitoid responses to volatile attractants produced by wild and cultivated cabbage. J Chem Ecol 37:795-807 (2011). James DG, Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481-495 (2005). Houshyani B, Assareh M, Busquets A, Ferrer A, Bouwmeester HJ and Kappers IF, Three-step pathway engineering results in more incidence rate and higher emission of nerolidol and improved attraction of Diadegma semiclausum. Metab Eng 15:88-97 (2013). Yang JN, Wei JN and Kang L, Feeding of pea leafminer larvae simultaneously activates jasmonic and salicylic acid pathways in plants to release a terpenoid for indirect defense. Insect Sci 28:811-824 (2021). D'Alessandro M, Held M, Triponez Y and Turlings TCJ, The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32:2733-2748 (2006). Ye M, Veyrat N, Xu H, Hu L, Turlings TCJ and Erb M, An herbivore-induced plant volatile reduces parasitoid attraction by changing the smell of caterpillars. Sci Adv 4:1-9 (2018). Heuskin S, Lorge S, Godin B, Leroy P, Frère I, Verheggen FJ et al., Optimisation of a semiochemical slow-release alginate formulation attractive towards Aphidius ervi Haliday parasitoids. Pest Manag Sci 68:127-136 (2012). Sasso R, Iodice L, Cristina Digilio M, Carretta A, Ariati L and Guerrieri E, Host-locating response by the aphid parasitoid Aphidius ervi to tomato plant volatiles. J Plant Interact 2:175-183 (2007). Sasso R, Iodice L, Woodcock CM, Pickett JA and Guerrieri E, Electrophysiological and behavioural responses of Aphidius ervi (Hymenoptera: Braconidae) to tomato plant volatiles. Chem 19:195-201 (2009). Tasin M, Bäckman AC, Coracini M, Casado D, Ioriatti C and Witzgall P, Synergism and redundancy in a plant volatile blend attracting grapevine moth females. Phytochemistry 68:203-209 (2007). |
| معلومات مُعتمدة: | 1S79919N Fonds Wetenschappelijk Onderzoek; C24E/19/052 KU Leuven; BB/X010953/1 Growing Health Institute Strategic Programme funded by the Biotechnology and Biological Sciences Research Council (BBSRC); BBS/OS/CP/000001 Industrial Strategy Challenge Fund funded by the Biotechnology and Biological Sciences Research Council (BBSRC) |
| فهرسة مساهمة: | Keywords: Akanthomyces muscarius; Capsicum annuum; Lecanicillium muscarium; Myzus persicae var. nicotianae; biological control; endophyte |
| تواريخ الأحداث: | Date Created: 20230908 Date Completed: 20240112 Latest Revision: 20240112 |
| رمز التحديث: | 20240112 |
| DOI: | 10.1002/ps.7762 |
| PMID: | 37682693 |
| قاعدة البيانات: | MEDLINE |
Full Text Finder كن أول من يترك تعليقا!