{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,29]],"date-time":"2026-05-29T09:04:46Z","timestamp":1780045486004,"version":"3.53.1"},"reference-count":84,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2022,10,11]],"date-time":"2022-10-11T00:00:00Z","timestamp":1665446400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Service public de Wallonie economie emploi recherche, Beware program, project AphidVirBeet"},{"name":"Wallonia\u2014Brussels International"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Agriculture"],"abstract":"<jats:p>Neonicotinoid-based real control of aphids in sugar beet permitted the effective management of associated phytoviruses. However, the prohibition on their usage has prompted an urgent search for viable replacements. The development of sugar beet varieties with aphid and\/or virus resistance and\/or tolerance has a huge potential to reduce aphids and the harm caused by transmitted viruses. Semiochemicals also play a significant part in determining intra- and inter-specific interactions, which directly affect aphid fitness, feeding activity, and ultimately their capacity to spread viruses. Another method of aphid management involves the use of plant volatile organic compounds (VOCs) in conjunction with an attract and kill strategy. Entomopathogenic fungi could also be used to manage aphids without endangering helpful entomofauna. Finally, soil bacteria are particularly effective biocontrol agents because they induce systemic resistance (ISR) as plant growth promoting rhizobacteria (PGPR). The sugar beet-aphid virus model would be a perfect place to test these microbial players. The adoption of complementing eco-compatible techniques in the sugar beet crop will be ensured by the application of a variety of biocontrol opportunities connected to creative aphid control strategies. This should make it possible to create technical itineraries for a comprehensive approach to controlling aphids and related viruses depending on the situation.<\/jats:p>","DOI":"10.3390\/agriculture12101663","type":"journal-article","created":{"date-parts":[[2022,10,11]],"date-time":"2022-10-11T06:13:27Z","timestamp":1665468807000},"page":"1663","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Complementary Strategies for Biological Control of Aphids and Related Virus Transmission in Sugar Beet to Replace Neonicotinoids"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7731-0849","authenticated-orcid":false,"given":"Fr\u00e9d\u00e9ric","family":"Francis","sequence":"first","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christiane","family":"Then","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrien","family":"Francis","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yao Aime Constant","family":"Gbangbo","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Iannello","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4773-6686","authenticated-orcid":false,"given":"Ibtissem","family":"Ben Fekih","sequence":"additional","affiliation":[{"name":"Functional and Evolutionary Entomology, Terra, Gembloux Agro-Bio Tech, University of Liege, Passage des Deportes-2, B-5030 Gembloux, Belgium"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,10,11]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Bradshaw, J.E. (2010). Sugar Beet. Root and Tuber Crops, Springer.","DOI":"10.1007\/978-0-387-92765-7"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1111\/j.1365-3059.2005.01155.x","article-title":"Distribution and Properties of Geographically Distinct Isolates of Sugar Beet Yellowing Viruses","volume":"54","author":"Stevens","year":"2005","journal-title":"Plant Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1111\/ppa.13306","article-title":"New Insights into Virus Yellows Distribution in Europe and Effects of Beet Yellows Virus, Beet Mild Yellowing Virus, and Beet Chlorosis Virus on Sugar Beet Yield Following Field Inoculation","volume":"70","author":"Hossain","year":"2021","journal-title":"Plant Pathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/j.1744-7348.2004.tb00323.x","article-title":"The Effects of Beet Mild Yellowing Virus and Beet Chlorosis Virus on the Yield of UK Field-Grown Sugar Beet in 1997, 1999 and 2000","volume":"144","author":"Stevens","year":"2004","journal-title":"Ann. Appl. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1002\/ps.1616","article-title":"Applied Aspects of Neonicotinoid Uses in Crop Protection","volume":"64","author":"Elbert","year":"2008","journal-title":"Pest Manag. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1126\/science.abe1148","article-title":"Applied Pesticide Toxicity Shifts toward Plants and Invertebrates, Even in GM Crops","volume":"372","author":"Schulz","year":"2021","journal-title":"Science"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.cropro.2016.11.034","article-title":"Neonicotinoids in Sugar Beet Cultivation in Central and Northern Europe: Efficacy and Environmental Impact of Neonicotinoid Seed Treatments and Alternative Measures","volume":"93","author":"Hauer","year":"2017","journal-title":"Crop Prot."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1111\/1365-2664.12111","article-title":"Review: An Overview of the Environmental Risks Posed by Neonicotinoid Insecticides","volume":"50","author":"Goulson","year":"2013","journal-title":"J. Appl. Ecol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e2109909118","DOI":"10.1073\/pnas.2109909118","article-title":"Past Insecticide Exposure Reduces Bee Reproduction and Population Growth Rate","volume":"118","author":"Stuligross","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"431","DOI":"10.14411\/eje.2005.061","article-title":"Role of (E)-Farnesene in Systematic Aphid Prey Location by Episyrphus Balteatus Larvae (Diptera: Syrphidae)","volume":"102","author":"Francis","year":"2005","journal-title":"Eur. J. Entomol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1023\/B:JOEC.0000028429.13413.a2","article-title":"Olfactory Responses to Aphid and Host Plant Volatile Releases: (E)-Beta-Farnesene an Effective Kairomone for the Predator Adalia Bipunctata","volume":"30","author":"Francis","year":"2004","journal-title":"J. Chem. Ecol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"10963","DOI":"10.1038\/srep10963","article-title":"Infection of Host Plants by Cucumber Mosaic Virus Increases the Susceptibility of Myzus Persicae Aphids to the Parasitoid Aphidius Colemani","volume":"5","author":"Mauck","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1111\/1744-7917.12470","article-title":"Insect Transmission of Plant Viruses: Multilayered Interactions Optimize Viral Propagation","volume":"24","author":"Dader","year":"2017","journal-title":"Insect Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1111\/aab.12300","article-title":"Cucurbit Aphid-Borne Yellows Virus (CABYV) Modifies the Alighting, Settling and Probing Behaviour of Its Vector Aphis Gossypii Favouring Its Own Spread","volume":"169","author":"Moreno","year":"2016","journal-title":"Ann. Appl. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/bs.aivir.2018.02.007","article-title":"Evolutionary Determinants of Host and Vector Manipulation by Plant Viruses","volume":"101","author":"Mauck","year":"2018","journal-title":"Advances in Virus Research"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Ziegler-Graff, V. (2020). Molecular Insights into Host and Vector Manipulation by Plant Viruses. Viruses, 12.","DOI":"10.3390\/v12030263"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Wu, X., and Ye, J. (2020). Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors. Viruses, 12.","DOI":"10.3390\/v12020148"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1104\/pp.15.00332","article-title":"Disruption of Ethylene Responses by Turnip Mosaic Virus Mediates Suppression of Plant Defense against the Green Peach Aphid Vector","volume":"169","author":"Casteel","year":"2015","journal-title":"Plant Physiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1007\/s00442-019-04405-0","article-title":"Ethylene Signaling Mediates Potyvirus Spread by Aphid Vectors","volume":"190","author":"Bak","year":"2019","journal-title":"Oecologia"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/S0065-3527(10)76006-1","article-title":"Cross-Protection: A Century of Mystery","volume":"76","author":"Ziebell","year":"2010","journal-title":"Adv. Virus Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1094\/PHYTO.2000.90.5.467","article-title":"A Point Mutation in the FRNK Motif of the Potyvirus Helper Component-Protease Gene Alters Symptom Expression in Cucurbits and Elicits Protection Against the Severe Homologous Virus","volume":"90","year":"2000","journal-title":"Phytopathology"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1007\/s10327-005-0248-6","article-title":"Comparison of the Nucleotide and Amino Acid Sequences of Parental and Attenuated Isolates of Zucchini Yellow Mosaic Virus","volume":"72","author":"Wang","year":"2006","journal-title":"J. Gen. Plant Pathol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"2862","DOI":"10.1099\/vir.0.83138-0","article-title":"A Cucumber Mosaic Virus Mutant Lacking the 2b Counter-Defence Protein Gene Provides Protection against Wild-Type Strains","volume":"88","author":"Ziebell","year":"2007","journal-title":"J. Gen. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3389\/fmicb.2013.00076","article-title":"Developing an Understanding of Cross-Protection by Citrus Tristeza Virus","volume":"4","author":"Folimonova","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_25","unstructured":"Schlaefli, H., Marmonier, A., Chesnais, Q., Villeroy, C., and Brault, V. (2022, January 17\u201318). La Multi-Infection Virale de La Betterave \u00e0 Sucre: Effets Sur l\u2019Accumulation Des Virus et Leur Transmission Par Pucerons. Proceedings of the Journ\u00e9es BAPOA, Nice, France."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1002\/ps.569","article-title":"Identification and Exploitation of Novel Disease Resistance Genes in Sugar Beet","volume":"59","author":"Francis","year":"2003","journal-title":"Pest Manag. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1111\/j.1439-0523.2008.01515.x","article-title":"The Action of Three Beet Yellows Virus Resistance QTLs Depends on Alleles at a Novel Genetic Locus That Controls Symptom Development","volume":"127","author":"Grimmer","year":"2008","journal-title":"Plant Breed."},{"key":"ref_28","first-page":"164","article-title":"Varieties of the Future: Identification of \u201cbroad Spectrum\u201d Genetic Resistance in Sugar Beet","volume":"114","author":"James","year":"2012","journal-title":"Int. Sugar J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1111\/j.1744-7348.2008.00228.x","article-title":"Genetic Approaches to Sustainable Pest Management in Sugar Beet (Beta Vulgaris)","volume":"152","author":"Zhang","year":"2008","journal-title":"Ann. Appl. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/S0065-3527(09)07504-6","article-title":"Recessive Resistance to Plant Viruses","volume":"75","author":"Truniger","year":"2009","journal-title":"Adv. Virus Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1111\/j.1364-3703.2004.00258.x","article-title":"Beet Poleroviruses: Close Friends or Distant Relatives?","volume":"6","author":"Stevens","year":"2005","journal-title":"Mol. Plant Pathol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/j.coviro.2011.09.010","article-title":"The Genome-Linked Protein VPg of Plant Viruses\u2014A Protein with Many Partners","volume":"1","author":"Jiang","year":"2011","journal-title":"Curr. Opin. Virol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1094\/MPMI-07-12-0174-R","article-title":"Closely Related Poleroviruses Depend on Distinct Translation Initiation Factors to Infect Arabidopsis Thaliana","volume":"26","author":"Reinbold","year":"2013","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_34","unstructured":"Rollwage, L., Hossain, R., and Varrelmann, M. (2022, January 21\u201322). Zuckerr\u00fcbe Infizierende Poleroviren Interagieren Mit Multiplen Translationsintiationsfaktoren Ihres Wirtes. Proceedings of the 54. Jahrestagung des DPG ArbeitskreisesViruskrankheit der Pflanzen, Dossenheim, Germany."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1111\/j.1744-7348.1990.tb06633.x","article-title":"The Effects of Yellowing Viruses on Yield of Sugar Beet in Field Trials, 1985 and 1987","volume":"116","author":"Smith","year":"1990","journal-title":"Ann. Appl. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1046\/j.1364-3703.2003.00154.x","article-title":"Beet Yellows Virus: The Importance of Being Different","volume":"4","author":"Dolja","year":"2003","journal-title":"Mol. Plant Pathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1146\/annurev.phyto.41.012203.105815","article-title":"Luteovirus-Aphid Interactions","volume":"41","author":"Gray","year":"2003","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1017\/S0007485300035963","article-title":"Aphids Caught on Sticky Traps in Eastern England in Relation to the Spread of Yellowing Viruses of Sugar-Beet","volume":"64","author":"Heathcote","year":"1974","journal-title":"Bull. Entomol. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1017\/S0007485300056534","article-title":"The Time of Flight and the Relative Importance of Myzus Persicae (Sulz.) and Aphis Fabae Scop. in Relation to the Incidence of Beet Yellows as Shown by Trap Catches at Rothamsted and Broom\u2019s Barn","volume":"56","author":"Heathcote","year":"1966","journal-title":"Bull. Entomol. Res."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Boissinot, S., Pichon, E., Sorin, C., Piccini, C., Scheidecker, D., Ziegler-Graff, V., and Brault, V. (2017). Systemic Propagation of a Fluorescent Infectious Clone of a Polerovirus Following Inoculation by Agrobacteria and Aphids. Viruses, 9.","DOI":"10.3390\/v9070166"},{"key":"ref_41","first-page":"161","article-title":"Welche Bedeutung Haben Die Zur \u201cAphis Fabae-Gruppe\u201d Geh\u00f6renden Blattlausst\u00e4mme f\u00fcr die \u00dcbertragung des Schwachen Vergilbungsvirus Auf Beta-R\u00fcben?","volume":"86","author":"Thielemann","year":"1979","journal-title":"Z. Pflanz. Pflanzenschutz"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/s13059-016-1145-3","article-title":"Rapid Transcriptional Plasticity of Duplicated Gene Clusters Enables a Clonally Reproducing Aphid to Colonise Diverse Plant Species","volume":"18","author":"Mathers","year":"2017","journal-title":"Genome Biol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"19460","DOI":"10.1073\/pnas.1314122110","article-title":"Gene Amplification and Microsatellite Polymorphism Underlie a Recent Insect Host Shift","volume":"110","author":"Bass","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1007\/s10886-009-9737-y","article-title":"Sex Pheromones and Their Impact on Pest Management","volume":"36","author":"Witzgall","year":"2010","journal-title":"J. Chem. Ecol."},{"key":"ref_45","unstructured":"Abrol, D.P. (2014). Chapter 6\u2014Role of Semiochemicals in Integrated Pest Management. Integrated Pest Management: Current Concepts and Ecological Perspective, Academic Press."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Sharma, A., Sandhi, R.K., and Reddy, G.V.P. (2019). A Review of Interactions between Insect Biological Control Agents and Semiochemicals. Insects, 10.","DOI":"10.3390\/insects10120439"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1146\/annurev-ento-031616-035040","article-title":"Advances in Attract-and-Kill for Agricultural Pests: Beyond Pheromones","volume":"63","author":"Gregg","year":"2018","journal-title":"Annu. Rev. Entomol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/S2095-3119(13)60247-6","article-title":"Influence of Garlic Intercropping or Active Emitted Volatiles in Releasers on Aphid and Related Beneficial in Wheat Fields in China","volume":"12","author":"Zhou","year":"2013","journal-title":"J. Integr. Agric."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1007\/s10340-017-0888-2","article-title":"A Push\u2013Pull Strategy to Control Aphids Combines Intercropping with Semiochemical Releases","volume":"91","author":"Xu","year":"2018","journal-title":"J. Pest Sci."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"31552","DOI":"10.1038\/srep31552","article-title":"Use of Slow-Release Plant Infochemicals to Control Aphids: A First Investigation in a Belgian Wheat Field","volume":"6","author":"Zhou","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1080\/09583157.2018.1504885","article-title":"Combining E-\u03b2-Farnesene and Methyl Salicylate Release with Wheat-Pea Intercropping Enhances Biological Control of Aphids in North China","volume":"28","author":"Xu","year":"2018","journal-title":"Biocontrol. Sci. Technol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2847","DOI":"10.1007\/BF02098393","article-title":"Methyl Salicylate and (\u2212)-(1R,5S)-Myrtenal Are Plant-Derived Repellents for Black Bean Aphid, Aphis Fabae Scop. (Homoptera: Aphididae)","volume":"20","author":"Hardie","year":"1994","journal-title":"J. Chem. Ecol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2565","DOI":"10.1007\/BF02036192","article-title":"Winter Host Component Reduces Colonization by Bird-Cherry Oat Aphid, Rhopalosiphum Padi (L.) (Homoptera, Aphididae), and Other Aphids in Cereal Fields","volume":"20","author":"Pettersson","year":"1994","journal-title":"J. Chem. Ecol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"9329","DOI":"10.1073\/pnas.160241697","article-title":"New Roles for Cis-Jasmone as an Insect Semiochemical and in Plant Defense","volume":"97","author":"Birkett","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1046\/j.1461-9563.2003.00159.x","article-title":"Effects of Two Types of Semiochemical on Population Development of the Bird Cherry Oat Aphid Rhopalosiphum Padi in a Barley Crop","volume":"5","author":"Ninkovic","year":"2003","journal-title":"Agric. Entomol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1111\/j.1744-7348.1987.tb01477.x","article-title":"Effect of Dodecanoic Acid on the Colonisation of Sugar Beet by Aphids and the Secondary Spread of Virus Yellows","volume":"111","author":"Herrbach","year":"1987","journal-title":"Ann. Appl. Biol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1146\/annurev-ento-011613-162054","article-title":"Evolutionary Interaction Networks of Insect Pathogenic Fungi","volume":"59","author":"Boomsma","year":"2014","journal-title":"Annu. Rev. Entomol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jip.2015.07.009","article-title":"Insect Pathogens as Biological Control Agents: Back to the Future","volume":"132","author":"Lacey","year":"2015","journal-title":"J. Invertebr. Pathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1080\/09583150701593963","article-title":"Review on Safety of the Entomopathogenic Fungus Metarhizium Anisopliae","volume":"17","author":"Zimmermann","year":"2007","journal-title":"Biocontrol. Sci. Technol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1006\/pmpp.2001.0355","article-title":"The Phylogeny of Plant and Animal Pathogens in the Ascomycota","volume":"59","author":"Berbee","year":"2001","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Vega, F., and Kaya, H. (2012). Fungal Entomopathogens. Insect Pathology, Academic Press.","DOI":"10.1016\/B978-0-12-384984-7.00006-3"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"2002","DOI":"10.1111\/nph.15859","article-title":"Meta-Analysis of the Role of Entomopathogenic and Unspecialized Fungal Endophytes as Plant Bodyguards","volume":"223","author":"Gange","year":"2019","journal-title":"New Phytol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1002\/ps.4015","article-title":"Dual Effects of Metarhizium Spp. and Clonostachys Rosea against an Insect and a Seed-Borne Pathogen in Wheat","volume":"72","author":"Keyser","year":"2016","journal-title":"Pest Manag. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Mantzoukas, S., and Eliopoulos, P.A. (2020). Endophytic Entomopathogenic Fungi: A Valuable Biological Control Tool against Plant Pests. Appl. Sci., 10.","DOI":"10.3390\/app10010360"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1715","DOI":"10.1111\/nph.16979","article-title":"Seed Inoculations with Entomopathogenic Fungi Affect Aphid Populations Coinciding with Modulation of Plant Secondary Metabolite Profiles across Plant Families","volume":"229","author":"Rasool","year":"2021","journal-title":"New Phytol."},{"key":"ref_66","first-page":"138","article-title":"Efficacy of Different Entomopathogenic Fungi against Cowpea Aphid, Aphis Craccivora (Koch)","volume":"3","author":"Saranya","year":"2010","journal-title":"J. Biopestic."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1002\/ps.1928","article-title":"Evaluation of the Biocontrol Potential of Various Metarhizium Isolates against Green Peach Aphid Myzus Persicae (Homoptera: Aphididae)","volume":"66","author":"Shan","year":"2010","journal-title":"Pest Manag. Sci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1587","DOI":"10.1093\/jee\/toy135","article-title":"Evaluation of the Entomopathogenic Fungi Metarhizium Anisopliae, Beauveria Bassiana and Isaria Sp. for the Management of Aphis Craccivora (Hemiptera: Aphididdae)","volume":"111","author":"Mweke","year":"2018","journal-title":"J. Econ. Entomol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"2557","DOI":"10.1002\/ps.6294","article-title":"Intraspecies Variation of Metarhizium Brunneum against the Green Peach Aphid, Myzus Persicae, Provides Insight into the Complexity of Disease Progression","volume":"77","author":"Reingold","year":"2021","journal-title":"Pest Manag. Sci."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Branine, M., Bazzicalupo, A., and Branco, S. (2019). Biology and Applications of Endophytic Insect-Pathogenic Fungi. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1007831"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1007\/s00294-014-0447-9","article-title":"Stress Is the Rule Rather than the Exception for Metarhizium","volume":"61","author":"Lovett","year":"2015","journal-title":"Curr. Genet."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.pbi.2017.04.018","article-title":"Understanding and Exploiting Plant Beneficial Microbes","volume":"38","author":"Finkel","year":"2017","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"1062","DOI":"10.1094\/MPMI-19-1062","article-title":"Priming: Getting Ready for Battle","volume":"19","author":"Conrath","year":"2006","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"361","DOI":"10.1016\/S0065-2296(09)51009-9","article-title":"Chapter 9 Priming of Induced Plant Defense Responses","volume":"Volume 51","author":"Conrath","year":"2009","journal-title":"Advances in Botanical Research"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1094\/MPMI-06-11-0179","article-title":"Modulation of Host Immunity by Beneficial Microbes","volume":"25","author":"Zamioudis","year":"2012","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1146\/annurev-phyto-082712-102340","article-title":"Induced Systemic Resistance by Beneficial Microbes","volume":"52","author":"Pieterse","year":"2014","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Disi, J., Simmons, J., and Zebelo, S. (2019). Plant Growth-Promoting Rhizobacteria-Induced Defense Against Insect Herbivores. Field Crops: Sustainable Management by PGPR, Springer.","DOI":"10.1007\/978-3-030-30926-8_14"},{"key":"ref_78","first-page":"447","article-title":"Resistance Induced in Plants by Non-Pathogenic Microorganisms: Elicitation and Defense Responses","volume":"3","author":"Ongena","year":"2006","journal-title":"Floric. Ornam. Plant Biotechnol."},{"key":"ref_79","first-page":"437","article-title":"Caract\u00e9ristiques Mol\u00e9culaires de l\u2019immunit\u00e9 Des Plantes Induite Par Les Rhizobact\u00e9ries Non Pathog\u00e8nes","volume":"12","author":"Jourdan","year":"2008","journal-title":"Biotechnol. Agron. Soc. Environ."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2","DOI":"10.3390\/plants11030386","article-title":"Induced Systemic Resistance for Improving Plant Immunity by Beneficial Microbes","volume":"11","author":"Yu","year":"2022","journal-title":"Plants"},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Rabbee, M.F., Sarafat Ali, M., Choi, J., Hwang, B.S., Jeong, S.C., and Baek, K. (2019). Bacillus Velezensis: A Valuable Member of Bioactive Molecules within Plant Microbiomes. Molecules, 24.","DOI":"10.3390\/molecules24061046"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1002\/ps.1907","article-title":"PGPR and Entomopathogenic Fungus Bioformulation for the Synchronous Management of Leaffolder Pest and Sheath Blight Disease of Rice","volume":"66","author":"Karthiba","year":"2010","journal-title":"Pest Manag. Sci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1094\/MPMI-09-13-0262-R","article-title":"Plant Defense Stimulation by Natural Isolates of Bacillus Depends on Efficient Surfactin Production","volume":"27","author":"Cawoy","year":"2014","journal-title":"Mol. Plant-Microbe Interact."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"570","DOI":"10.1111\/1758-2229.12286","article-title":"Plant Polysaccharides Initiate Underground Crosstalk with Bacilli by Inducing Synthesis of the Immunogenic Lipopeptide Surfactin","volume":"7","author":"Debois","year":"2015","journal-title":"Environ. Microbiol. Rep."}],"container-title":["Agriculture"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0472\/12\/10\/1663\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:49:40Z","timestamp":1760143780000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0472\/12\/10\/1663"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,10,11]]},"references-count":84,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["agriculture12101663"],"URL":"https:\/\/doi.org\/10.3390\/agriculture12101663","relation":{},"ISSN":["2077-0472"],"issn-type":[{"value":"2077-0472","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,10,11]]}}}