Zhang, Yong; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Fu, Yu ; Université de Liège - ULiège > TERRA Research Centre ; PHIM Plant Health Institute, Univ Montpellier, INRAE, CIRAD, Institut Agro, IRD, Montpellier, France
Liu, Xiaobei ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Form. doct. sc. agro. & ingé. biol. (paysage) ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Francis, Frédéric ; Université de Liège - ULiège > TERRA Research Centre > Gestion durable des bio-agresseurs
Fan, Jia; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Liu, Huan; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Wang, Qiang ; Université de Liège - ULiège ; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China
Sun, Yu; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Yumeng; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China ; College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
Chen, Julian; State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Language :
English
Title :
SmCSP4 from aphid saliva stimulates salicylic acid-mediated defence responses in wheat by interacting with transcription factor TaWKRY76
Publication date :
04 August 2023
Journal title :
Plant Biotechnology Journal
ISSN :
1467-7644
eISSN :
1467-7652
Publisher :
John Wiley and Sons Inc
Volume :
21
Issue :
11
Pages :
2389 - 2407
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
NSCF - National Natural Science Foundation of China
Acevedo, F.E., Rivera-Vega, L.J., Chung, S.H., Ray, S. and Felton, G.W. (2015) Cues from chewing insects-the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr. Opin. Plant Biol. 26, 80–86.
Alborn, H.T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H. and Tumlinson, J.H. (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science, 276, 945–949.
Alborn, H.T., Hansen, T.V., Jones, T.H., Bennett, D.C., Tumlinson, J.H., Schmelz, E.A. and Teal, P.E.A. (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc. Natl. Acad. Sci. USA, 104, 12976–12781.
Atamian, H.S., Chaudhary, R., Cin, V.D., Bao, E., Girke, T. and Kaloshian, I. (2013) In planta expression or delivery of potato aphid Macrosiphum euphorbiae effectors Me10 and Me23 enhances aphid fecundity. Mol. Plant Microbe Interact. 26, 67–74.
Avila, C.A., Arévalo-Soliz, L.M., Jia, L., Navarre, D.A., Chen, Z., Howe, G.A., Meng, Q.W. et al. (2012) Loss of function of FATTY ACID DESATURASE 7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol. 158, 2028–2041.
Bai, X.X., Zhan, G.M., Tian, S.X., Peng, H., Cui, X.Y., Islam, M.A. et al. (2021) Transcription factor BZR2 activates chitinase Cht20.2 transcription to confer resistance to wheat stripe rust. Plant Physiol. 187, 2749–2762.
Berens, M.L., Berry, H.M., Mine, A., Argueso, C.T. and Tsuda, K. (2017) Evolution of hormone signaling networks in plant defense. Annu. Rev. Phytopathol. 55, 401–425.
Blackman, R.L. and Eastop, V.F. (2000) Aphids on the world's crops: an identification and information guide. New York: John Wiley & Sons Ltd.
Bos, J.I., Prince, D., Pitino, M., Maffei, M.E., Win, J. and Hogenhout, S.A. (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet. 6, e1001216.
Boughton, A.J., Hoover, K. and Felton, G.W. (2006) Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomol. Exp. Appl. 120, 175–188.
Chaudhary, R., Atamian, H.S., Shen, Z., Briggs, S.P. and Kaloshian, I. (2014) GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc. Natl. Acad. Sci. USA, 111, 8919–8924.
Chaudhary, R., Peng, H.C., He, J., MacWilliams, J., Teixeira, M., Tsuchiya, T., Chesnais, Q. et al. (2019) Aphid effector Me10 interacts with tomato TFT7, a 14-3-3 isoform involved in aphid resistance. New Phytol. 221, 1518–1528.
Cheng, Y.L., Wu, K., Yao, J.N., Li, S.M., Wang, X.J., Huang, L.L. et al. (2017) PSTha5a23, a candidate effector from the obligate biotrophic pathogen Puccinia striiformis f. sp. tritici, is involved in plant defense suppression and rust pathogenicity. Environ. Microbiol. 19, 1717–1729.
Cherqui, A. and Tjallingii, W.F. (2000) Salivary proteins of aphids, a pilot study on identification, separation and immunolocalisation. J. Insect Physiol. 46, 1177–1186.
Cooper, W.C., Jia, L. and Goggin, F.L. (2004) Acquired and R-gene-mediated resistance against the potato aphid in tomato. J. Chem. Ecol. 30, 2527–2542.
Cui, N., Lu, H., Wang, T., Zhang, W., Kang, L. and Cui, F. (2019) Armet, an aphid effector protein, induces pathogen resistance in plants by promoting the accumulation of salicylic acid. Philos. Trans. R. Soc. Lond. B Biol. Sci. 4, 20180314.
De Vos, M. and Jander, G. (2009) Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 32, 1548–1560.
Elzinga, D.A. and Jander, G. (2013) The role of protein effectors in plant-aphid interactions. Curr. Opin. Plant Biol. 16, 451–456.
Elzinga, D.A., De Vos, M. and Jander, G. (2014) Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein. Mol. Plant Microbe Interact. 27, 747–756.
Escudero-Martinez, C., Rodriguez, P.A., Liu, S., Santos, P.A., Stephens, J. and Bos, J.I.B. (2020) An aphid effector promotes barley susceptibility through suppression of defence gene expression. J. Exp. Bot. 71, 2796–2807.
Guo, H., Zhang, Y., Tong, J., Ge, P., Wang, Q., Zhao, Z., Zhu-Salzman, K. et al. (2020) An aphid-secreted salivary protease activates plant defense in phloem. Curr. Biol. 30, 4826–4836.
Henningsen, E.C., Omidvar, V., Della Coletta, R., Michno, J.M., Gilbert, E., Li, F. et al. (2021) Identification of candidate susceptibility genes to Puccinia graminis f. sp. tritici in wheat. Front. Plant Sci. 12, 657796.
Hood, M. and Shew, H. (1996) Applications of KOH-aniline blue fluorescence in the study of plant-fungal interactions. Phytopathology, 86, 704–708.
Huang, X., Liu, D., Zhang, R. and Shi, X. (2019) Transcriptional responses in defense-related genes of Sitobion avenae (Hemiptera: Aphididae) feeding on wheat and barley. J. Econ. Entomol. 112, 382–395.
Ingham, V.A., Anthousi, A., Douris, V., Harding, N.J., Lycett, G., Morris, M. et al. (2020) A sensory appendage protein protects malaria vectors from pyrethroids. Nature, 577, 376–380.
Jefferson, R.A., Kavanagh, T.A. and Bevan, M.W. (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901–3907.
Ji, R., Yu, H., Fu, Q., Chen, H., Ye, W., Li, S. and Lou, Y. (2013) Comparative transcriptome analysis of salivary glands of two populations of rice brown planthopper, Nilaparvata lugens, that differ in virulence. PloS One, 8, e79612.
Ji, R., Fu, J., Shi, Y., Li, J., Jing, M., Wang, L., Yang, S. et al. (2021) Vitellogenin from planthopper oral secretion acts as a novel effector to impair plant defenses. New Phytol. 232, 802–817.
Jiang, X., Zhang, Q., Qin, Y., Yin, H., Zhang, S., Li, Q., Zhang, Y. et al. (2019) A chromosome-level draft genome of the grain aphid Sitobion miscanthi. GigaScience, 8, giz101.
Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323–329.
Kettles, G.J. and Kaloshian, I. (2016) The potato aphid salivary effector Me47 is a glutathione-S-transferase involved in modifying plant responses to aphid infestation. Front. Plant Sci. 7, e1142.
Li, F., Venthur, H., Wang, S., Homem, R.A. and Zhou, J.J. (2021) Evidence for the involvement of the chemosensory protein AgosCSP5 in resistance to insecticides in the cotton aphid, Aphis gossypii. Insects, 12, 335.
Li, Q., Xie, Q.G., Smith-Becker, J., Navarre, D.A. and Kaloshian, I. (2006) Mi-1-Mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol. Plant Microbe Interact. 19, 655–664.
Li, J., Qian, J., Xu, Y., Yan, S., Shen, J. and Yin, M. (2019) A facile-synthesized star polycation constructed as a highly efficient gene vector in pest management. ACS Sustainable Chem. Eng. 7, 6316–6322.
Li, Q., Fu, Y., Liu, X., Sun, J., Hou, M., Zhang, Y. and Chen, J. (2022) Activation of wheat defense response by Buchnera aphidicola-derived small chaperone protein GroES in wheat aphid saliva. J. Agric. Food Chem. 70, 1058–1067.
Liu, B., Chen, J., Ni, H. and Sun, J. (2002) Isolation, purification and structural identification of DIMBOA and its resistance to English grain aphid, Sitiobion avenae (F.). Chin. J. Appl. Environ. Biol. 8, 71–74.
Liu, G., Ma, H., Xie, H., Xuan, N., Guo, X., Fan, Z., Rajashekar, B. et al. (2016) Biotype characterization, developmental profiling, insecticide response and binding property of Bemisia tabaci chemosensory proteins: role of CSP in insect defense. PloS One, 11, e0154706.
Mutti, N.S., Park, Y., Reese, J.C. and Reeck, G.R. (2006) RNAi knockdown of a salivary transcript leading to lethality in the pea aphid, Acyrthosiphon pisum. J. Insect Sci. 6, 1–7.
Mutti, N.S., Louis, J., Pappan, L.K., Begum, K., Chen, M.S. and Park, Y. (2008) A protein from the salivary glands of the pea aphid, Acyrthosiphon pisum, is essential in feeding on a host plant. Proc. Natl. Acad. Sci. USA, 105, 9965–9969.
Niu, D., Hamby, R., Sanchez, J.N., Cai, Q., Yan, Q. and Jin, H. (2021) RNAs-A new frontier in crop protection. Curr. Opin. Biotechnol. 70, 204–212.
Pelosi, P., Iovinella, I., Zhu, J., Wang, G. and Dani, F.R. (2018) Beyond chemoreception: diverse tasks of soluble olfactory proteins in insects. Biol. Rev. Camb. Philos. Soc. 93, 184–200.
Peng, X., Qu, M.J., Wang, S.J., Huang, Y.X., Chen, C. and Chen, M.H. (2021) Chemosensory proteins participate in insecticide susceptibility in Rhopalosiphum padi, a serious pest on wheat crops. Insect Mol. Biol. 30, 138–151.
Prado, E. and Tjallingii, W.F. (1994) Aphid activities during sieve element punctures. Entomol. Exp. Appl. 72, 157–165.
Rodriguez, P.A., Stam, R., Warbroek, T. and Bos, J.I.B. (2014) Mp10 and Mp42 from the aphid species Myzus persicae trigger plant defenses in Nicotiana benthamiana through different activities. Mol. Plant Microbe Interact. 27, 30–39.
Schmelz, E.A., Carroll, M.J., LeClere, S., Phipps, S.M., Meredith, J., Chourey, P.S., Alborn, H.T. et al. (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc. Natl. Acad. Sci. USA, 103, 8894–8899.
Shan, D., Wang, C., Zheng, X., Hu, Z., Zhu, Y., Zhao, Y., Jiang, A. et al. (2021) MKK4-MPK3-WRKY17-mediated salicylic acid degradation increases susceptibility to Glomerella leaf spot in apple. Plant Physiol. 186, 1202–1219.
Silva-Sanzana, C., Estevez, J.M. and Blanco-Herrera, F. (2020) Influence of cell wall polymers and their modifying enzymes during plant–aphid interactions. J. Exp. Bot. 71, 3854–3864.
Stathopoulos, A., Van Drenth, M., Erives, A., Markstein, M. and Levine, M. (2002) Whole-genome analysis of dorsal-ventral patterning in the Drosophila embryo. Cell, 111, 687–701.
Thomazella, D.P.T., Seong, K., Mackelprang, R., Dahlbeck, D., Geng, Y., Gill, U.S. et al. (2021) Loss of function of a DMR6 ortholog in tomato confers broad-spectrum disease resistance. Proc. Natl. Acad. Sci. USA, 118, e2026152118.
Thorpe, P., Cock, P.J. and Bos, J.I.B. (2016) Comparative transcriptomics and proteomics of three different aphid species identifies core and diverse effector sets. BMC Genomics, 17, 172.
Tjallingii, W.F. and Esch, T.H. (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18, 317–328.
Upadhyaya, N.M., Mago, R., Staskawicz, B.J., Ayliffe, M.A., Ellis, J.G. and Dodds, P.N. (2014) A bacterial type III secretion assay for delivery of fungal effector proteins into wheat. Mol. Plant Microbe Interact. 27, 255–264.
Van Damme, M., Huibers, R.P., Elberse, J. and Van den Ackerveken, G. (2008) Arabidopsis DMR6 encodes a putative 2OG-Fe (II) oxygenase that is defense-associated but required for susceptibility to downy mildew. Plant J. 54, 785–793.
Wang, N., Zhao, P., Ma, Y., Yao, X., Sun, Y. and Huang, X. (2019) A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philos. Trans. R. S. Lond B. Biol. Sci. 374, 20180313.
Wang, N., Tang, C., Fan, X., He, M., Gan, P., Zhang, S., Hu, Z. et al. (2022) Inactivation of a wheat protein kinase gene confers broad-spectrum resistance to rust fungi. Cell, 185, 2961–2974.
Xiang, Y., Song, M., Wei, Z., Tong, J., Zhang, L., Xiao, L., Ma, Z. et al. (2011) A jacalin-related lectin-like gene in wheat is a component of the plant defence system. J. Exp. Bot. 62, 5471–5483.
Xu, Z., Chen, J., Cheng, D., Sun, J., Liu, Y. and Francis, F. (2011) Discovery of English grain aphid (Hemiptera: Aphididae) biotypes in China. J. Econ. Entomol. 104, 1080–1086.
Xu, H., Qian, L., Wang, X., Shao, R., Hong, Y., Liu, S.S. et al. (2019a) A salivary effector enables whitefly to feed on host plants by eliciting salicylic acid-signaling pathway. Proc. Natl. Acad. Sci. USA, 116, 490–495.
Xu, Q., Tang, C., Wang, X.D., Sun, S.T., Zhao, J.R., Kang, Z. et al. (2019b) An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function. Nat. Commun., 10, 5571.
Yan, S., Qian, J., Cai, C., Ma, Z., Li, J., Yin, M., Ren, B. et al. (2020) Spray method application of transdermal dsRNA delivery system for efficient gene silencing and pest control on soybean aphid Aphis glycines. J. Pest Sci. 93, 449–459.
Yates, A.D. and Michel, A. (2018) Mechanisms of aphid adaptation to host plant resistance. Curr. Opin. Insect Sci. 26, 41–49.
Zeilmaker, T., Ludwig, N.R., Elberse, J., Seidl, M.F., Berke, L., Van Doorn, A. et al. (2015) DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis. Plant J. 81, 210–222.
Zhang, G. (1999) Aphids in Agriculture and Forestry of Northwest China, 1st edn, pp. 432–433. Beijing: China Environmental Science Press.
Zhang, Y., Li, Z.X., Yu, X.D., Fan, J., Pickett, J.A., Jones, H.D., Zhou, J.J. et al. (2015) Molecular characterization of two isoforms of a farnesyl pyrophosphate synthase gene in wheat and their roles in sesquiterpene synthesis and inducible defence against aphid infestation. New Phytol. 206, 1101–1115.
Zhang, Y., Zhao, L., Zhao, J., Li, Y., Wang, J., Guo, R., Gan, S. et al. (2017) S5H/DMR6 encodes a salicylic acid 5-hydroxylase that fine-tunes salicylic acid homeostasis. Plant Physiol. 175, 1082–1093.
Zhang, Y., Fan, J., Francis, F. and Chen, J. (2017a) Watery saliva secreted by the grain aphid Sitobion avenae stimulates aphid resistance in wheat. J. Agric. Food Chem. 65, 8798–8805.
Zhang, Y., Fan, J., Sun, J., Francis, F. and Chen, J. (2017b) Transcriptome analysis of the salivary glands of the grain aphid, Sitobion avenae. Sci. Rep. 7, 15911.
Zhang, Y., Liu, X., Fu, Y., Crespo-Herrera, L., Liu, H., Wang, Q., Zhang, Y. et al. (2022) Salivary effector Sm9723 of grain aphid Sitobion miscanthi suppresses plant defense and is essential for aphid survival on wheat. Int. J. Mol. Sci. 23, 6909.
Zhao, M., Wang, J., Ji, S., Chen, Z., Xu, J., Tang, C. et al. (2018) Candidate effector Pst_8713 impairs the plant immunity and contributes to virulence of Puccinia striiformis f. sp. tritici. Front. Plant Sci. 9, 1294.
Züst, T. and Agrawal, A.A. (2016) Mechanisms and evolution of plant resistance to aphids. Nat. Plants, 2, 15206.
