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Journal of Integrative Agriculture  2025, Vol. 24 Issue (4): 1342-1358    DOI: 10.1016/j.jia.2024.05.018
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Oral secretions: A key molecular interface of plant–insect herbivore interactions

Bin Li1, 2, 3, Wangpeng Shi2, Shaoqun Zhou1#, Guirong Wang1, 3#

1 Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, China

2 Key Laboratory of Pest Monitoring and Green Management, Ministry of Agriculture and Rural Affairs/Department of Entomology, China Agricultural University, Beijing 100091, China

3 State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China

 Highlights 
Oral secretions of insect herbivores are complex mixture of biological molecules, living microbes, and inorganic solvents.
Specific components of insect oral secretions have been demonstrated to confer important functions in plant–insect interactions including elicitation and manipulation of plant defense mechanisms.
Future studies could benefit from an evolutionary perspective, investigating the evolutionary origins of functional components of insect oral secretions.

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摘要  
植食性昆虫的口腔分泌物是昆虫取食时沉积在植物组织上的有机和无机溶质以及酶等复杂的混合物。昆虫口腔分泌物中特定成分已被证明在分子水平上具有调控植物-昆虫相互作用的重要功能。在这篇综述中,我们搜集了关于昆虫口腔分泌物的生物化学研究,并对目前已知的组分进行总结。其次,我们不仅概括了昆虫口腔分泌物已知组分的功能研究,还重点关注了这些组分在植物中特定的分子靶标。最后,我们强调了在昆虫生理学背景下研究昆虫口腔分泌物组分的重要性,这可能有助于揭示一些多功能分子化合物的潜在进化轨迹。


Abstract  
The oral secretions of insect herbivores are complex mixtures of organic and inorganic solutes and enzymes that are deposited onto plant tissues during the feeding process.  Some specific components of insect oral secretions have been shown to confer important functions in mediating plant–insect interactions at the molecular level.  In this review, we examined the biochemical studies of insect oral secretions to summarize the current knowledge of their compositions.  We then moved beyond the functional studies of components of oral secretions, and focused on the literature that pinpointed specific molecular targets of these compounds.  Finally, we highlighted the investigations of oral secretion components in the context of insect physiology, which shed light on the potential evolutionary trajectory of these multi-functional molecules.


Keywords:  plant-insect interactions       insect herbivores        oral secretions        plant defense  
Received: 29 February 2024   Accepted: 07 April 2024
Fund: This research has received financial support from the Shenzhen Science and Technology Program, China (KQTD20180411143628272) and the special funds for Science Technology Innovation and Industrial Development of Shenzhen Dapeng New District, China (PT202101-02).
About author:  Bin Li, E-mail: libincaas@qq.com; #Correspondence Shaoqun Zhou, E-mail: zhoushaoqun@caas.cn; Guirong Wang, E-mail: wangguirong@caas.cn

Cite this article: 

Bin Li, Wangpeng Shi, Shaoqun Zhou, Guirong Wang. 2025. Oral secretions: A key molecular interface of plant–insect herbivore interactions. Journal of Integrative Agriculture, 24(4): 1342-1358.

Acevedo F E, Peiffer M, Ray S, Meagher R, Luthe D S, Felton G W. 2018. Intraspecific differences in plant defense induction by fall armyworm strains. New Phytologist218, 310–321.

Acevedo F E, Peiffer M, Tan C W, Stanley B A, Stanley A, Wang J, Jones A G, Hoover K, Rosa C, Luthe D, Felton G. 2017. Fall armyworm-associated gut bacteria modulate plant defense responses. Molecular Plant-Microbe Interactions30, 127–137.

Acevedo F E, Smith P, Peiffer M, Helms A, Tooker J, Felton G W. 2019. Phytohormones in fall armyworm saliva modulate defense responses in plants. Journal of Chemical Ecology45, 598–609.

Alborn H T, Turlings T C J, Jones T H, Stenhagen G, Loughrin J H, Tumlinson J H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science276, 945–949.

Allmann S, Baldwin I T. 2010. Insects betray themselves in nature to predators by rapid isomerization of green leaf volatiles. Science329, 1075–1078.

Allmann S, Spathe A, Bisch-Knaden S, Kallenbach M, Reinecke A, Sachse S, Baldwin I T, Hansson B S. 2013. Feeding-induced rearrangement of green leaf volatiles reduces moth oviposition. Elife2, e00421.

Ammar E D, Shatters R G, Hall D G. 2011. Localization of Candidatus Liberibacter asiaticus, associated with Citrus Huanglongbing disease, in its psyllid vector using fluorescence in situ hybridization. Journal of Phytopathology159, 726–734.

Apostolou A, Shen Y, Liang Y, Luo J, Fang S. 2008. Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Experimental Cell Research314, 2454–2467.

Bauer J A, Zámocká M, Majtán J, Bauerová-Hlinková V. 2022. Glucose oxidase, an enzyme “Ferrari”: Its structure, function, production and properties in the light of various industrial and biotechnological applications. Biomolecules12, 472.

Bos J I, Prince D, Pitino M, Maffei M E, Win J, Hogenhout S A. 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genetics6, e1001216.

Chaudhary R, Atamian H S, Shen Z, Briggs S P, Kaloshian I. 2014. GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proceedings of the National Academy of Sciences of the United States of America111, 8919–8924.

Chaudhary R, Peng H C, He J, Macwilliams J, Teixeira M, Tsuchiya T, Chesnais Q, Mudgett M B, Kaloshian I. 2019. Aphid effector Me10 interacts with tomato TFT7, a 14-3-3 isoform involved in aphid resistance. New Phytologist221, 1518–1528.

Chen C Y, Liu Y Q, Song W M, Chen D Y, Chen F Y, Chen X Y, Chen Z W, Ge S X, Wang C Z, Zhan S, Chen X Y, Mao Y B. 2019. An effector from cotton bollworm oral secretion impairs host plant defense signaling. Proceedings of the National Academy of Sciences of the United States of America116, 14331–14338.

Chen C Y, Mao Y B. 2020. Research advances in plant–insect molecular interaction. F1000Research9, doi: 10.12688/f1000research.21502.1.

Chen X, Liu Y Q, Wu M N, Yan L, Chen C Y, Mu Y P, Liu Y J, Wang M Y, Chen X Y, Mao Y B. 2022. A highly accumulated secretory protein from cotton bollworm interacts with basic helix-loop-helix transcription factors to dampen plant defense. New Phytologist237, 265–278.

Chen X, Peiffer M, Tan C W, Felton G W. 2020. Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plant–insect interactions. Arthropod-Plant Interactions14, 423–432.

Chung S H, Rosa C, Scully E D, Peiffer M, Tooker J F, Hoover K, Luthe D S, Felton G W. 2013. Herbivore exploits orally secreted bacteria to suppress plant defenses. Proceedings of the National Academy of Sciences of the United States of America110, 15728–15733.

Collatz K G, Mommsen T. 1974. The structure of the emulsifying substances in several invertebrates. Journal of Comparative Physiology94, 339–352.

Cui J R, Bing X L, Tang Y J, Liu F, Ren L, Zhou J Y, Liu H H, Wang M K, Hoffmann A A, Hong X Y. 2023. A conserved protein disulfide isomerase enhances plant resistance against herbivores. Plant Physiology191, 660–678.

Cui N, Lu H, Wang T, Zhang W, Kang L, Cui F. 2019. Armet, an aphid effector protein, induces pathogen resistance in plants by promoting the accumulation of salicylic acid. Philosophical Transactions of the Royal Society (B: Biological Sciences), 374, 20180314.

Dames P, Zimmermann B, Schmidt R, Rein J, Voss M, Schewe B, Walz B, Baumann O. 2006. cAMP regulates plasma membrane vacuolar-type H+-ATPase assembly and activity in blowfly salivary glands. Proceedings of the National Academy of Sciences of the United States of America103, 3926–3931.

Domazakis E, Wouters D, Lochman J, Visser R G, Joosten M H, Vleeshouwers V G. 2020. ELR is a true pattern recognition receptor that associates with elicitins from diverse Phytophthora species. BioRxiv, doi: org/10.1101/2020.09.21.305813.

Dong Y, Huang X, Yang Y, Li J, Zhang M, Shen H, Ren Y, Li X, Tian J, Shen D, Dou D, Xia A. 2022a. Characterization of salivary secreted proteins that induce cell death from Riptortus pedestris (Fabricius) and their roles in insect–plant interactions. Frontiers in Plant Science13, 912603.

Dong Y, Zhou J, Yang Y, Lu W, Jin Y, Huang X, Zhang W, Li J, Ai G, Yin Z, Shen D, Jing M, Dou D, Xia A. 2022b. Cyclophilin effector Al106 of mirid bug Apolygus lucorum inhibits plant immunity and promotes insect feeding by targeting PUB33. New Phytologist237, 2308–2403.

Du H, Xu H X, Wang F, Qian L X, Liu S S, Wang X W. 2022. Armet from whitefly saliva acts as an effector to suppress plant defenses by targeting tobacco cystatin. New Phytologist234, 1848–1862.

Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annual Review of Plant Biology70, 527–557.

Felix G, Duran J D, Volko S, Boller T. 1999. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant Journal18, 265–276.

Felton G W. 1995. Antioxidant systems in insects. Archives of Insect Biochemistry and Physiology29, 187–197.

Fu J, Shi Y, Wang L, Tian T, Li J, Gong L, Zheng Z, Jing M, Fang J, Ji R. 2022. Planthopper-secreted salivary calmodulin acts as an effector for defense responses in rice. Frontiers in Plant Science13, 841378.

Fu J, Shi Y, Wang L, Zhang H, Li J, Fang J, Ji R. 2020. Planthopper-secreted salivary disulfide isomerase activates immune responses in plants. Frontiers in Plant Science11, 622513.

Fürstenberg-Hägg J, Zagrobelny M, Bak S. 2013. Plant defense against insect herbivores. International Journal of Molecular Sciences14, 10242–10297.

Gao H, Zou J, Lin X, Zhang H, Yu N, Liu Z. 2022. Nilaparvata lugens salivary protein NlG14 triggered defense response in plants. Journal of Experimental Botany73, 7477–7487.

Gatehouse J A. 2002. Plant resistance towards insect herbivores: A dynamic interaction. New Phytologist156, 145–169.

Gaulin E, Bottin A, Dumas B. 2010. Sterol biosynthesis in oomycete pathogens. Plant Signaling and Behavior5, 258–260.

Gong G, Yuan L Y, Li Y F, Xiao H X, Li Y F, Zhang Y, Wu W J, Zhang Z F. 2022. Salivary protein 7 of the brown planthopper functions as an effector for mediating tricin metabolism in rice plants. Scientific Reports12, 3205.

Guo H, Wielsch N, Hafke J B, Svatoš A, Mithöfer A, Boland W. 2013. A porin-like protein from oral secretions of Spodoptera littoralis larvae induces defense-related early events in plant leaves. Insect Biochemistry and Molecular Biology43, 849–858.

Guo H, Zhang Y, Tong J, Ge P, Wang Q, Zhao Z, Zhu-Salzman K, Hogenhout S A, Ge F, Sun Y. 2020. An aphid-secreted salivary protease activates plant defense in phloem. Current Biology30, 4826–4836.

Guo J, Wang H, Guan W, Guo Q, Wang J, Yang J, Peng Y, Shan J, Gao M, Shi S, Shangguan X, Liu B, Jing S, Zhang J, Xu C, Huang J, Rao W, Zheng X, Wu D, Zhou C. 2023. A tripartite rheostat controls self-regulated host plant resistance to insects. Nature618, 799–807.

Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin I T. 2001. Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiology125, 711–717.

Hannula S E, Zhu F, Heinen R, Bezemer T M. 2019. Foliar-feeding insects acquire microbiomes from the soil rather than the host plant. Nature Communications10, 1–9.

Hind S R, Strickler S R, Boyle P C, Dunham D M, Bao Z, O’doherty I M, Baccile J A, Hoki J S, Viox E G, Clarke C R, Vinatzer B A, Schroeder F C, Martin G B. 2016. Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nature Plants2, 16128.

Hogenhout S A, Bos J I. 2011. Effector proteins that modulate plant--insect interactions. Current Opinion in Plant Biology14, 422–428.

Huang H J, Cui J R, Xia X, Chen J, Ye Y X, Zhang C X, Hong X Y. 2019. Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defence. New Phytologist224, 860–874.

Huang H J, Li L L, Ye Z X, Lu J B, Lou Y H, Wei Z Y, Sun Z T, Chen J P, Li J M, Zhang C X. 2024. Salivary proteins potentially derived from horizontal gene transfer are critical for salivary sheath formation and other feeding processes. Communication Biology7, 257.

Huang H J, Wang Y Z, Li L L, Lu H B, Lu J B, Wang X, Ye Z X, Zhang Z L, He Y J, Lu G, Zhuo J C, Mao Q Z, Sun Z T, Chen J P, Li J M, Zhang C X. 2023. Planthopper salivary sheath protein LsSP1 contributes to manipulation of rice plant defenses. Nature Communications14, 737.

Huffaker A, Dafoe N J, Schmelz E A. 2011. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiology155, 1325–1338.

Iida J, Desaki Y, Hata K, Uemura T, Yasuno A, Islam M, Maffei M E, Ozawa R, Nakajima T, Galis I, Arimura G I. 2019. Tetranins: New putative spider mite elicitors of host plant defense. New Phytologist224, 875–885.

Ji R, Fu J, Shi Y, Li J, Jing M, Wang L, Yang S, Tian T, Wang L, Ju J, Guo H, Liu B, Dou D, Hoffmann A A, Zhu-Salzman K, Fang J. 2021. Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses. New Phytologist232, 802–817.

Kallure G S, Kumari A, Shinde B A, Giri A P. 2022. Characterized constituents of insect herbivore oral secretions and their influence on the regulation of plant defenses. Phytochemistry193, 113008.

Kaloshian I, Walling L L. 2016. Hemipteran and dipteran pests: Effectors and plant host immune regulators. Journal of Integrative Plant Biology58, 350–361.

Kuhns E H, Seidl-Adams I, Tumlinson J H. 2012. A lepidopteran aminoacylase (L-ACY-1) in Heliothis virescens (Lepidoptera: Noctuidae) gut lumen hydrolyzes fatty acid-amino acid conjugates, elicitors of plant defense. Insect Biochemistry and Molecular Biology42, 32–40.

Labandeira C C. 2013. A paleobiologic perspective on plant–insect interactions. Current Opinion in Plant Biology16, 414–421.

Li P, Liu C, Deng W H, Yao D M, Pan L L, Li Y Q, Liu Y Q, Liang Y, Zhou X P, Wang X W. 2019. Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors. PLoS Pathogens15, e1007607.

Li R, Weldegergis B T, Li J, Jung C, Qu J, Sun Y, Qian H, Tee C, Van Loon J J, Dicke M, Chua N H, Liu S S, Ye J. 2014. Virulence factors of geminivirus interact with MYC2 to subvert plant resistance and promote vector performance. Plant Cell26, 4991–5008.

Liang X, Zhou J M. 2018. Receptor-like cytoplasmic kinases: Central players in plant receptor kinase-mediated signaling. Annual Review of Plant Biology69, 267–299.

Lin P A, Chen Y, Chaverra-Rodriguez D, Heu C C, Zainuddin N B, Sidhu J S, Peiffer M, Tan C W, Helms A, Kim D, Ali J, Rasgon J L, Lynch J, Anderson C T, Felton G W. 2021. Silencing the alarm: An insect salivary enzyme closes plant stomata and inhibits volatile release. New Phytologist230, 793–803.

Lin Y H, Silven J J M, Wybouw N, Fandino R A, Dekker H L, Vogel H, Wu Y L, De Koster C, Grosse-Wilde E, Haring M A, Schuurink R C, Allmann S. 2023. A salivary GMC oxidoreductase of Manduca sexta re-arranges the green leaf volatile profile of its host plant. Nature Communications14, 3666.

Lindner H A, Lunin V V, Alary A, Hecker R, Cygler M, Ménard R. 2003. Essential roles of zinc ligation and enzyme dimerization for catalysis in the Aminoacylase-1/M20 family. Journal of Biological Chemistry278, 44496–44504.

Liu H, Wang C, Qiu C L, Shi J H, Sun Z, Hu X J, Liu L, Wang M Q. 2021. A salivary odorant-binding protein mediates Nilaparvata lugens feeding and host plant phytohormone suppression. International Journal of Molecular Sciences22, 4988.

Liu S, Jaouannet M, Dempsey D A, Imani J, Coustau C, Kogel K H. 2020. RNA-based technologies for insect control in plant production. Biotechnology Advances39, 107463.

Louis J, Peiffer M, Ray S, Luthe D S, Felton G W. 2013. Host-specific salivary elicitor(s) of European corn borer induce defenses in tomato and maize. New Phytologist199, 66–73.

Luo M, Li B, Jander G, Zhou S. 2023. Non-volatile metabolites mediate plant interactions with insect herbivores. Plant Journal114, 1164–1177.

Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu Y G. 2015. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in Monocot and Dicot Plants. Molecular Plant8, 1274–1284.

Maclean A M, Orlovskis Z, Kowitwanich K, Zdziarska A M, Angenent G C, Immink R G, Hogenhout S A. 2014. Phytoplasma effector SAP54 hijacks plant reproduction by degrading MADS-box proteins and promotes insect colonization in a RAD23-dependent manner. PLoS Biology12, e1001835.

Maffei M E, Mithofer A, Boland W. 2007. Before gene expression: Early events in plant–insect interaction. Trends in Plant Science12, 310–316.

Marzorati M, Alma A, Sacchi L, Pajoro M, Palermo S, Brusetti L, Raddadi N, Balloi A, Tedeschi R, Clementi E, Corona S, Quaglino F, Bianco P A, Beninati T, Bandi C, Daffonchio D. 2006. A novel bacteroidetes symbiont is localized in Scaphoideus titanus, the insect vector of flavescence doree in vitis vinifera. Applied and Environmental Microbiology72, 1467–1475.

Mattiacci L, Dicke M, Posthumus M A. 1995. beta-Glucosidase: An elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America92, 2036–2040.

Mikes V, Milat M L, Ponchet M, Panabières F, Ricci P, Blein J P. 1998. Elicitins, proteinaceous elicitors of plant defense, are a new class of sterol carrier proteins. Biochemical and Biophysical Research Communications245, 133–139.

Misas-Villamil J C, Van Der Hoorn R A, Doehlemann G. 2016. Papain-like cysteine proteases as hubs in plant immunity. New Phytologist212, 902–907.

Mondal H A. 2017. Shaping the understanding of saliva-derived effectors towards aphid colony proliferation in host plant. Journal of Plant Biology60, 103–115.

Musser R O, Hum-Musser S M, Eichenseer H, Peiffer M, Ervin G, Murphy J B, Felton G W. 2002. Herbivory: Caterpillar saliva beats plant defences. Nature416, 599–600.

Mutti N S, Louis J, Pappan L K, Pappan K, Begum K, Chen M S, Park Y, Dittmer N, Marshall J, Reese J C, Reeck G R. 2008. A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proceedings of the National Academy of Sciences of the United States of America105, 9965–9969.

Naessens E, Dubreuil G, Giordanengo P, Baron O L, Minet-Kebdani N, Keller H, Coustau C. 2015. A secreted MIF cytokine enables aphid feeding and represses plant immune responses. Current Biology25, 1898–1903.

Newman M A, Sundelin T, Nielsen J T, Erbs G. 2013. MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers in Plant Science4, 139.

Orozco-Cardenas M, Mcgurl B, Ryan C A. 1993. Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proceedings of the National Academy of Sciences of the United States of America90, 8273–8276.

Palgi M, Greco D, Lindström R, Auvinen P, Heino T I. 2012. Gene expression analysis of Drosophilaa Manf mutants reveals perturbations in membrane traffic and major metabolic changes. BMC Genomics13, 1–20.

Palgi M, Lindström R, Peränen J, Piepponen T P, Saarma M, Heino T I. 2009. Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons. Proceedings of the National Academy of Sciences of the United States of America106, 2429–2434.

Pearce G, Strydom D, Johnson S, Ryan C A. 1991. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science253, 895–897.

Pitino M, Hoffman M T, Zhou L, Hall D G, Stocks I C, Duan Y. 2014. The phloem-sap feeding mealybug (Ferrisia virgata) carries ‘Candidatus Liberibacter asiaticus’ populations that do not cause disease in host plants. PLoS ONE9, e85503.

Poretsky E, Ruiz M, Ahmadian N, Steinbrenner A D, Dressano K, Schmelz E A, Huffaker A. 2021. Comparative analyses of responses to exogenous and endogenous antiherbivore elicitors enable a forward genetics approach to identify maize gene candidates mediating sensitivity to herbivore-associated molecular patterns. Plant Journal108, 1295–1316.

Quintana-Rodriguez E, Duran D, Heil M, Camacho Coronel X. 2018. Damage-associated molecular patterns (DAMPs) as future plant vaccines that protect crops from pests. Scientia Horticulturae237, 207–220.

Rao W, Zheng X, Liu B, Guo Q, Guo J, Wu Y, Shangguan X, Wang H, Wu D, Wang Z, Hu L, Xu C, Jiang W, Huang J, Shi S, He G. 2019. Secretome analysis and in planta expression of salivary proteins identify candidate effectors from the brown planthopper Nilaparvata lugensMolecular Plant-Microbe Interactions32, 227–239.

Rodriguez P A, Escudero-Martinez C, Bos J I. 2017. An aphid effector targets trafficking protein VPS52 in a host-specific manner to promote virulence. Plant Physiology173, 1892–1903.

Rodriguez P A, Stam R, Warbroek T, Bos J I. 2014. Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities. Molecular Plant-Microbe Interactions27, 30–39.

Rushton P J, Somssich I E, Ringler P, Shen Q J. 2010. WRKY transcription factors. Trends in Plant Science15, 247–258.

Schäfer M, Fischer C, Meldau S, Seebald E, Oelmüller R, Baldwin I T. 2011. Lipase activity in insect oral secretions mediates defense responses in Arabidopsis. Plant Physiology156, 1520–1534.

Schmelz E A. 2015. Impacts of insect oral secretions on defoliation-induced plant defense. Current Opinion in Insect Science9, 7–15.

Schmelz E A, Carroll M J, Leclere S, Phipps S M, Meredith J, Chourey P S, Alborn H T, Teal P E. 2006. Fragments of ATP synthase mediate plant perception of insect attack. Proceedings of the National Academy of Sciences of the United States of America103, 8894–8899.

Schmelz E A, Leclere S, Carroll M J, Alborn H T, Teal P E. 2007. Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiology144, 793–805.

Schuman M C, Baldwin I T. 2016. The layers of plant responses to insect herbivores. Annual Review of Entomology61, 373–394.

Shangguan X, Zhang J, Liu B, Zhao Y, Wang H, Wang Z, Guo J, Rao W, Jing S, Guan W, Ma Y, Wu Y, Hu L, Chen R, Du B, Zhu L, Yu D, He G. 2018. A mucin-like protein of planthopper is required for feeding and induces immunity response in plants. Plant Physiology176, 552–565.

Shinya T, Yasuda S, Hyodo K, Tani R, Hojo Y, Fujiwara Y, Hiruma K, Ishizaki T, Fujita Y, Saijo Y, Galis I. 2018. Integration of danger peptide signals with herbivore-associated molecular pattern signaling amplifies anti-herbivore defense responses in rice. Plant Journal94, 626–637.

Snoeck S, Guayazan-Palacios N, Steinbrenner A D. 2022. Molecular Tug-of-War: Plant immune recognition of herbivory. Plant Cell34, 1497–1513

Steinbrenner A D, Munoz-Amatriain M, Chaparro A F, Aguilar-Venegas J M, Lo S, Okuda S, Glauser G, Dongiovanni J, Shi D, Hall M, Crubaugh D, Holton N, Zipfel C, Abagyan R, Turlings T C J, Close T J, Huffaker A, Schmelz E A. 2020. A receptor-like protein mediates plant immune responses to herbivore-associated molecular patterns. Proceedings of the National Academy of Sciences of the United States of America117, 31510–31518.

Stringlis I A, Pieterse C M J. 2021. Evolutionary “hide and seek” between bacterial flagellin and the plant immune system. Cell Host & Microbe29, 548–550.

Su Q, Peng Z, Tong H, Xie W, Wang S, Wu Q, Zhang J, Li C, Zhang Y. 2019. A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation. Journal of Experimental Botany70, 3343–3355.

Sugio A, Maclean A M, Hogenhout S A. 2014. The small phytoplasma virulence effector SAP11 contains distinct domains required for nuclear targeting and CIN-TCP binding and destabilization. New Phytologist202, 838–848.

Takai H, Ozawa R, Takabayashi J, Fujii S, Arai K, Ichiki R T, Koeduka T, Dohra H, Ohnishi T, Taketazu S, Kobayashi J, Kainoh Y, Nakamura S, Fujii T, Ishikawa Y, Kiuchi T, Katsuma S, Uefune M, Shimada T, Matsui K. 2018. Silkworms suppress the release of green leaf volatiles by mulberry leaves with an enzyme from their spinnerets. Scientific Reports8, 11942.

Tatchell R. 1969. The ionic regulatory role of the salivary secretion of the cattle tick, Boophilus microplus. Journal of Insect Physiology15, 1421–1430.

Tian D, Peiffer M, Shoemaker E, Tooker J, Haubruge E, Francis F, Luthe D S, Felton G W. 2012. Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PLoS ONE7, e36168.

Tian T, Ji R, Fu J, Li J, Wang L, Zhang H, Yang S, Ye W, Fang J, Zhu-Salzman K. 2021. A salivary calcium-binding protein from Laodelphax striatellus acts as an effector that suppresses defense in rice. Pest Management Science77, 2272–2281.

Upson J L, Zess E K, Białas A, Wu C H, Kamoun S. 2018. The coming of age of EvoMPMI: Evolutionary molecular plant-microbe interactions across multiple timescales. Current Opinion in Plant Biology44, 108–116.

Wang H, Shi S, Hua W. 2023. Advances of herbivore-secreted elicitors and effectors in plant–insect interactions. Frontiers in Plant Science14, 1176048.

Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegmann J, Mithofer A, Kalbacher H, Felix G. 2018. The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nature Plants4, 152–156.

Wang N, Zhao P, Ma Y, Yao X, Sun Y, Huang X, Jin J, Zhang Y, Zhu C, Fang R, Ye J. 2019. A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philosophical Transactions of the Royal Society (B: Biological Sciences), 374, 20180313.

Wang Q, Yuan E, Ling X, Zhu-Salzman K, Guo H, Ge F, Sun Y. 2020. An aphid facultative symbiont suppresses plant defence by manipulating aphid gene expression in salivary glands. PlantCell and Environment43, 2311–2322.

Wang W, Dai H, Zhang Y, Chandrasekar R, Luo L, Hiromasa Y, Sheng C, Peng G, Chen S, Tomich J M, Reese J, Edwards O, Kang L, Reeck G, Cui F. 2015. Armet is an effector protein mediating aphid-plant interactions. FASEB Journal29, 2032–2045.

Wang Y, Tang M, Hao P, Yang Z, Zhu L, He G. 2008. Penetration into rice tissues by brown planthopper and fine structure of the salivary sheaths. Entomologia Experimentalis et Applicata129, 295–307.

Wang Y M, He Y Z, Ye X T, Guo T, Pan L L, Liu S S, Ng J C, Wang X W. 2022. A balance between vector survival and virus transmission is achieved through JAK/STAT signaling inhibition by a plant virus. Proceedings of the National Academy of Sciences of the United States of America119, e2122099119.

Wang Y Z, Ye Y X, Lu J B, Wang X, Lu H B, Zhang Z L, Ye Z X, Lu Y W, Sun Z T, Chen J P, Li J M, Zhang C X, Huang H J. 2023. Horizontally transferred salivary protein promotes insect feeding by suppressing ferredoxin-mediated plant defenses. Molecular Biology and Evolution40, msad221.

Wu D, Lei K, Wang D, Fu Z Q. 2024. Effector-triggered and self-regulated plant resistance to insects. Trends in Plant Science29, 1–3.

Wu D, Qi T, Li W X, Tian H, Gao H, Wang J, Ge J, Yao R, Ren C, Wang X B, Liu Y, Kang L, Ding S W, Xie D. 2017. Viral effector protein manipulates host hormone signaling to attract insect vectors. Cell Research27, 402–415.

Wu J, Baldwin I T. 2010. New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics44, 1–24.

Xu H X, Qian L X, Wang X W, Shao R X, Hong Y, Liu S S, Wang X W. 2019. A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proceedings of the National Academy of Sciences of the United States of America116, 490–495.

Yamasaki Y, Sumioka H, Takiguchi M, Uemura T, Kihara Y, Shinya T, Galis I, Arimura G I. 2021. Phytohormone-dependent plant defense signaling orchestrated by oral bacteria of the herbivore Spodoptera lituraNew Phytologist231, 2029–2038.

Yan Z W, Chen F Y, Zhang X, Cai W J, Chen C Y, Liu J, Wu M N, Liu N J, Ma B, Wang M Y, Chao D Y, Gao C J, Mao Y B. 2023. Endocytosis-mediated entry of a caterpillar effector into plants is countered by Jasmonate. Nature Communications14, 6551.

Ye W, Yu H, Jian Y, Zeng J, Ji R, Chen H, Lou Y. 2017. A salivary EF-hand calcium-binding protein of the brown planthopper Nilaparvata lugens functions as an effector for defense responses in rice. Scientific Reports7, 40498.

Yoshinaga N, Aboshi T, Abe H, Nishida R, Alborn H T, Tumlinson J H, Mori N. 2008. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proceedings of the National Academy of Sciences of the United States of America105, 18058–18063.

Yoshinaga N, Alborn H T, Nakanishi T, Suckling D M, Nishida R, Tumlinson J H, Mori N. 2010. Fatty acid-amino acid conjugates diversification in lepidopteran caterpillars. Journal of Chemical Ecology36, 319–325.

Zeng J, Ye W, Hu W, Jin X, Kuai P, Xiao W, Jian Y, Turlings T C J, Lou Y. 2023. The N-terminal subunit of vitellogenin in planthopper eggs and saliva acts as a reliable elicitor that induces defenses in rice. New Phytologist238, 1230–1244

Zhang Y, Fu Y, Liu X, Francis F, Fan J, Liu H, Wang Q, Sun Y, Zhang Y, Chen J. 2023. SmCSP4 from aphid saliva stimulates salicylic acid-mediated defence responses in wheat by interacting with transcription factor TaWKRY76. Plant Biotechnology Journal21, 2389–2407.

Zhang Y, Liu X, Francis F, Xie H, Fan J, Wang Q, Liu H, Sun Y, Chen J. 2022a. The salivary effector protein Sg2204 in the greenbug Schizaphis graminum suppresses wheat defence and is essential for enabling aphid feeding on host plants. Plant Biotechnology Journal20, 2187–2201.

Zhang Y, Liu X, Fu Y, Crespo-Herrera L, Liu H, Wang Q, Zhang Y, Chen J. 2022b. Salivary effector Sm9723 of grain aphid Sitobion miscanthi suppresses plant defense and is essential for aphid survival on wheat. International Journal of Molecular Sciences23, 6909.

Zhang Y, Song G, Lal N K, Nagalakshmi U, Li Y, Zheng W, Huang P J, Branon T C, Ting A Y, Walley J W, Dinesh-Kumar S P. 2019. TurboID-based proximity labeling reveals that UBR7 is a regulator of N NLR immune receptor-mediated immunity. Nature Communications10, 3252.

Zhao C, Escalante L N, Chen H, Benatti T R, Qu J, Chellapilla S, Waterhouse R M, Wheeler D, Andersson M N, Bao R, Batterton M, Behura S K, Blankenburg K P, Caragea D, Carolan J C, Coyle M, El-Bouhssini M, Francisco L, Friedrich M, Gill N. 2015. A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructorCurrent Biology25, 613–620.

Zhao J, Liu Y, Xu S, Wang J, Zhang Z, Wang M Q, Turlings T C, Zhang P, Zhou A. 2023. Mealybug salivary microbes inhibit induced plant defenses. Pest Management Science79, 4034–4047.

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