{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,12]],"date-time":"2026-07-12T08:08:59Z","timestamp":1783843739835,"version":"3.55.0"},"reference-count":94,"publisher":"Wiley","issue":"8","license":[{"start":{"date-parts":[[2026,5,10]],"date-time":"2026-05-10T00:00:00Z","timestamp":1778371200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,5,10]],"date-time":"2026-05-10T00:00:00Z","timestamp":1778371200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"content-domain":{"domain":["scijournals.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Pest Management Science"],"published-print":{"date-parts":[[2026,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Microbial symbionts associated with herbivorous insects can modulate plant hormone networks and reconfigure induced defenses during feeding. This review synthesizes current knowledge on how symbiont effectors converge on conserved jasmonic acid (JA)\/salicylic acid (SA)\/ethylene (ET) signaling hubs to suppress or reprogram plant immunity. These microbial partners secrete a diverse arsenal of bioactive molecules, including effector proteins (e.g., the histidine\u2010rich Ca\n                    <jats:sup>2+<\/jats:sup>\n                    \u2010binding protein ApHRC from\n                    <jats:italic>Serratia symbiotica<\/jats:italic>\n                    in pea aphids), enzymes (e.g., gut microbiome\u2010derived proteases in\n                    <jats:italic>Anticarsia gemmatalis<\/jats:italic>\n                    larvae), and host metabolite mimics (e.g., cytokinin production induced by\n                    <jats:italic>Wolbachia<\/jats:italic>\n                    in the apple leaf\u2010mining moth). Through these mechanisms, symbionts selectively manipulate plant hormonal pathways, a form of molecular interference that often enhances herbivore performance by increasing feeding efficiency, fecundity, and host plant range, thereby increasing plant susceptibility to biotic stress. These physiological alterations trigger cascading ecological effects, reshaping multitrophic interactions: symbiont\u2010mediated changes in herbivore\u2010induced plant volatiles (HIPVs) and secondary metabolites influence the behavior of natural enemies, alter competitive outcomes among herbivores, and disrupt plant\u2013insect communication. Consequently, microbial symbionts act as hidden ecological engineers, driving community dynamics and evolutionary trajectories. By integrating molecular, ecological, and evolutionary perspectives, we propose a unified framework that explicitly links symbiont effector function to plant immune modulation and its ecosystem\u2010level consequences. Ultimately, this synthesis underscores the potential of targeting insect\u2013microbe partnerships through approaches such as effector blocking, microbiome augmentation, or symbiont disruption, for developing sustainable pest management strategies and advancing the field of plant defense ecology. \u00a9 2026 Society of Chemical Industry.\n                  <\/jats:p>","DOI":"10.1002\/ps.70885","type":"journal-article","created":{"date-parts":[[2026,5,11]],"date-time":"2026-05-11T05:02:53Z","timestamp":1778475773000},"page":"7249-7257","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Cross\u2010kingdom signaling manipulation by insect\u2010associated microbial symbionts: Linking molecular mechanisms to pest management strategies"],"prefix":"10.1002","volume":"82","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5011-6261","authenticated-orcid":false,"given":"Marzieh","family":"Kashkouli","sequence":"first","affiliation":[{"name":"Research Institute for Biotechnology and Bioengineering, Isfahan University of Technology  Isfahan Iran"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7963-5409","authenticated-orcid":false,"given":"Yaghoub","family":"Fathipour","sequence":"additional","affiliation":[{"name":"Department of Entomology, Faculty of Agriculture Tarbiat Modares University  Tehran Iran"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,5,10]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1590\/S1677-04202002000200001"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1042\/EBC20210090"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.952301"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1176048"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2012.08.013"},{"key":"e_1_2_9_7_1","first-page":"225","volume-title":"Insect\u2010Plant Interactions in a Crop Protection Perspective","author":"Giron D","year":"2017"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2023.0122"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2023.1146390"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41522-023-00435-y"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-981-16-3595-3_5"},{"key":"e_1_2_9_12_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10886-020-01209-y"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.1111\/ele.70183"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms13010189"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms252312951"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1093\/jxb\/eru435"},{"key":"e_1_2_9_17_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2435.12100"},{"key":"e_1_2_9_18_1","doi-asserted-by":"publisher","DOI":"10.1111\/1574-6976.12025"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2007.1211"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.genet.41.110306.130119"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tim.2017.02.014"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.2010.0226"},{"key":"e_1_2_9_23_1","first-page":"137","article-title":"The crucial role of the endosymbiont pantoea sp. in morphology and mating of the pistachio green stink bug, brachynema germari (hemiptera: Pentatomidae)","volume":"23","author":"Kashkouli M","year":"2021","journal-title":"J Agric Sci Technol"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2435.2008.01442.x"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.3390\/applmicrobiol5030090"},{"key":"e_1_2_9_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/mec.12421"},{"key":"e_1_2_9_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1570-7458.2009.00886.x"},{"key":"e_1_2_9_28_1","first-page":"2024","article-title":"The conserved aphid saliva chemosensory protein effector Mp10 targets plant AMSH deubiquitinases at cellular membranes to suppress pattern\u2010triggered immunity","volume":"17","author":"Gravino M","year":"2024","journal-title":"bioRxiv"},{"key":"e_1_2_9_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.pbi.2015.05.029"},{"key":"e_1_2_9_30_1","first-page":"2025","article-title":"Herbivorous insects independently evolved salivary effectors to regulate plant immunity by destabilizing the malectin\u2010LRR RLP","author":"Wang X","year":"2025","journal-title":"bioRxiv"},{"key":"e_1_2_9_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2008.10.017"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00360-013-0744-5"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10886-013-0313-0"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00068-13"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10886-018-0970-0"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jinsphys.2024.104746"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-ento-011019-024939"},{"key":"e_1_2_9_38_1","doi-asserted-by":"publisher","DOI":"10.1111\/brv.12098"},{"key":"e_1_2_9_39_1","doi-asserted-by":"publisher","DOI":"10.1111\/pce.13836"},{"key":"e_1_2_9_40_1","doi-asserted-by":"publisher","DOI":"10.1098\/rsbl.2010.0699"},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1288997"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1301886110"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1002\/ece3.331"},{"key":"e_1_2_9_44_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.funeco.2019.07.008"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms8618"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cois.2014.08.001"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.02419"},{"key":"e_1_2_9_48_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1308867110"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2019.0211"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.3389\/fphys.2022.1003746"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-017-01935-0"},{"key":"e_1_2_9_52_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2656.12705"},{"key":"e_1_2_9_53_1","doi-asserted-by":"publisher","DOI":"10.1128\/mBio.00890-18"},{"key":"e_1_2_9_54_1","doi-asserted-by":"publisher","DOI":"10.1111\/1365-2656.12942"},{"key":"e_1_2_9_55_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1195463"},{"key":"e_1_2_9_56_1","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.03049-13"},{"key":"e_1_2_9_57_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13104-021-05766-7"},{"key":"e_1_2_9_58_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.243593"},{"key":"e_1_2_9_59_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.crvi.2011.06.008"},{"key":"e_1_2_9_60_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.0335320100"},{"key":"e_1_2_9_61_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0965-1748(01)00115-1"},{"key":"e_1_2_9_62_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.222481399"},{"key":"e_1_2_9_63_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2013.06.027"},{"key":"e_1_2_9_64_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0140826"},{"key":"e_1_2_9_65_1","first-page":"277","volume-title":"Advances in Insect Physiology","author":"Oliver KM","year":"2020"},{"key":"e_1_2_9_66_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.aspen.2018.12.021"},{"key":"e_1_2_9_67_1","doi-asserted-by":"publisher","DOI":"10.1093\/aesa\/sav032"},{"key":"e_1_2_9_68_1","doi-asserted-by":"publisher","DOI":"10.1016\/B978-0-12-803265-7.00011-7"},{"key":"e_1_2_9_69_1","doi-asserted-by":"publisher","DOI":"10.1007\/s11829-017-9576-7"},{"key":"e_1_2_9_70_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cropro.2019.105076"},{"key":"e_1_2_9_71_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-phyto-080614-120132"},{"key":"e_1_2_9_72_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-981-16-3591-5_3"},{"key":"e_1_2_9_73_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.biocontrol.2017.05.008"},{"key":"e_1_2_9_74_1","doi-asserted-by":"publisher","DOI":"10.1111\/1744-7917.12603"},{"key":"e_1_2_9_75_1","doi-asserted-by":"publisher","DOI":"10.1038\/35051070"},{"key":"e_1_2_9_76_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cois.2023.101027"},{"key":"e_1_2_9_77_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1407687111"},{"key":"e_1_2_9_78_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00248-021-01768-x"},{"key":"e_1_2_9_79_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0011339"},{"key":"e_1_2_9_80_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10886-013-0264-5"},{"key":"e_1_2_9_81_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2018.01107"},{"key":"e_1_2_9_82_1","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy13030868"},{"key":"e_1_2_9_83_1","doi-asserted-by":"publisher","DOI":"10.1111\/1462-2920.15169"},{"key":"e_1_2_9_84_1","doi-asserted-by":"publisher","DOI":"10.1017\/S0007485319000245"},{"key":"e_1_2_9_85_1","doi-asserted-by":"publisher","DOI":"10.1093\/jee\/toy324"},{"key":"e_1_2_9_86_1","doi-asserted-by":"publisher","DOI":"10.1093\/ee\/nvz089"},{"key":"e_1_2_9_87_1","doi-asserted-by":"publisher","DOI":"10.1002\/ps.8844"},{"key":"e_1_2_9_88_1","doi-asserted-by":"publisher","DOI":"10.1093\/jee\/toaf136"},{"key":"e_1_2_9_89_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.aspen.2025.102496"},{"key":"e_1_2_9_90_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-981-16-3595-3_4"},{"key":"e_1_2_9_91_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00442-015-3277-7"},{"key":"e_1_2_9_92_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cois.2020.02.007"},{"key":"e_1_2_9_93_1","doi-asserted-by":"publisher","DOI":"10.4161\/cib.23804"},{"key":"e_1_2_9_94_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-017-1030-z"},{"key":"e_1_2_9_95_1","first-page":"25","volume-title":"Insect\u2010Plant Interactions in a Crop Protection Perspective","author":"Kergoat GJ","year":"2017"}],"container-title":["Pest Management Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/scijournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ps.70885","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/scijournals.onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/ps.70885","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/scijournals.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ps.70885","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,12]],"date-time":"2026-07-12T07:43:50Z","timestamp":1783842230000},"score":1,"resource":{"primary":{"URL":"https:\/\/scijournals.onlinelibrary.wiley.com\/doi\/10.1002\/ps.70885"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,5,10]]},"references-count":94,"journal-issue":{"issue":"8","published-print":{"date-parts":[[2026,8]]}},"alternative-id":["10.1002\/ps.70885"],"URL":"https:\/\/doi.org\/10.1002\/ps.70885","archive":["Portico"],"relation":{},"ISSN":["1526-498X","1526-4998"],"issn-type":[{"value":"1526-498X","type":"print"},{"value":"1526-4998","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,5,10]]},"assertion":[{"value":"2025-12-25","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-04-20","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-05-10","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}