More than trichomes and acylsugars: the role of jasmonic acid as mediator of aphid resistance in tomato

References

• Agrawal AA. 2014. Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol. 28(6):1404–1412. doi:10.1111/1365-2435.12271.
   Web of Science ®Google Scholar
• Alba JM, Montserrat M, Fernández-Muñoz R. 2009. Resistance to the two-spotted spider mite (Tetranychus urticae) by acylsucroses of wild tomato (Solanum pimpinellifolium) trichomes studied in a recombinant inbred line population. Experimental and Applied Acarology. 47. doi:10.1007/s10493-008-9192-4.
   PubMed Web of Science ®Google Scholar
• Alba JM, Schimmel BCJ, Glas JJ, Ataide LM, Pappas ML, Villarroel CA, … Kant MR. 2015. Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol. 205(2):828–840. doi:10.1111/nph.13075.
   PubMed Web of Science ®Google Scholar
• Ali JG, Agrawal AA. 2014. Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol. 28(6):1404–1412. doi:10.1111/1365-2435.12271.
   Web of Science ®Google Scholar
• Aslam H, Mushtaq S, Maalik S, Bano N, Eed EM, Bibi A, Tahir A, Ijaz I, Tanwir S, Khalifa AS. 2022. Exploring the effect of jasmonic acid for aphids control for improving the yield ofTriticum aestivum varieties. Peer J. doi:10.7717/peerj.14018.
   Web of Science ®Google Scholar
• Avila CA, Arévalo-Soliz LM, Jia L, Navarre DA, Chen Z, Howe GA, … Goggin FL. 2012. Loss of function of FATTY ACID DESATURASE7 in tomato enhances basal aphid resistance in a salicylate-dependent manner. Plant Physiol. 158(4):2028–2041. doi:10.1104/pp.111.191262.
   PubMed Web of Science ®Google Scholar
• Bhattarai KK, Xie QG, Pourshalimi D, Younglove T, Kaloshian I. 2007. Coi1-dependent signaling pathway Is Not required forMi-1—mediated potato aphid resistance. Molecular Plant-Microbe Interactions®. 20:276–282. doi:10.1094/MPMI-20-3-0276.
   PubMed Web of Science ®Google Scholar
• Blanco-Sánchez L, Planelló R, Llorente L, Díaz-Pendón JA, Ferrero V, Fernández-Muñoz R, … de la Peña E. 2021. Characterization of the detrimental effects of type IV glandular trichomes on the aphid Macrosiphum euphorbiaein tomato. Pest Management Science. 77. doi:10.1002/ps.6437.
   PubMed Web of Science ®Google Scholar
• Brading PA, Hammond-Kosack KE, Parr A, Jones JDG. 2000. Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J. 23:305–318. doi:10.1046/j.1365-313x.2000.00778.x.
   PubMed Web of Science ®Google Scholar
• Conrath U, Beckers GJM, Langenbach CJG, Jaskiewicz MR. 2015. Priming for enhanced defense. Annu Rev Phytopathol. 53. doi:10.1146/annurev-phyto-080614-120132.
   PubMed Web of Science ®Google Scholar
• Cooper WR, Goggin FL. 2005. Effects of jasmonate-induced defenses in tomato on the potato aphid Macrosiphum euphorbiae. Entomol Exp Appl. 115(1). doi:10.1111/j.1570-7458.2005.00289.x.
   Web of Science ®Google Scholar
• da Silva AA, Andrade MC, Carvalho R, de C, Neiva IP, Santos DC, Maluf WR. 2016. Resistência à Helicoverpa armigera em genótipos de tomateiro obtidos do cruzamento de Solanum lycopersicum com Solanum galapagense. Pesquisa Agropecuária Brasileira. 51. doi:10.1590/S0100-204X2016000700002.
   Google Scholar
• De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, … Pieterse CM. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Molecular Plant-Microbe Interactions®. 18(9):923–937. doi:10.1094/MPMI-18-0923.
   PubMed Web of Science ®Google Scholar
• Dugravot S, Brunissen L, Létocart E, Tjallingii WF, Vincent C, Giordanengo P, Cherqui A. 2007. Local and systemic responses induced by aphids in Solanum tuberosum plants. Entomol Exp Appl. 123(3):271–277. doi:10.1111/j.1570-7458.2007.00542.x.
   Web of Science ®Google Scholar
• Eisenring M, Glauser G, Meissle M, Romeis J. 2018. Differential impact of herbivores from three feeding guilds on systemic secondary metabolite induction, phytohormone levels and plant-mediated herbivore interactions. J Chem Ecol. 44:1178–1189. doi:10.1007/s10886-018-1015-4.
   PubMed Web of Science ®Google Scholar
• Ellis C, Karafyllidis I, Turner JG. 2002. Constitutive activation of jasmonate signaling in an Arabidopsis Mutant correlates with enhanced resistance to Erysiphe cichoracearum, Pseudomonas syringae, and Myzus persicae. Molecular Plant-Microbe Interactions®. 15. doi:10.1094/MPMI.2002.15.10.1025.
   PubMed Web of Science ®Google Scholar
• El-Wakeil NE, Volkmar C, Sallam AA. 2010. Jasmonic acid induces resistance to economically important insect pests in winter wheat. Pest Management Science: Formerly Pesticide Science. 66(5):549–554.
   PubMed Web of Science ®Google Scholar
• Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol. 70. doi:10.1146/annurev-Faarplant-050718-095910.
   PubMed Web of Science ®Google Scholar
• Escobar-Bravo R, Alba JM, Pons C, Granell A, Kant MR, Moriones E, Fernández-Muñoz R. 2016. A jasmonate-inducible defense trait transferred from wild into cultivated tomato establishes increased whitefly resistance and reduced viral disease incidence. Front Plant Sci. 7:1732.
   PubMed Web of Science ®Google Scholar
• Feng JL, Zhang J, Yang J, Zou LP, Fang TT, Xu HL, Cai QN. 2021. Exogenous salicylic acid improves resistance of aphid-susceptible wheat to the grain aphid, Sitobion avenae (F.) (Hemiptera: Aphididae). Bull Entomol Res. 111(5):544–552. doi:10.1017/S0007485321000237.
   PubMed Web of Science ®Google Scholar
• Ferrero V, Baeten L, Blanco-Sánchez L, Planelló R, Díaz-Pendón JA, Rodríguez-Echeverría S, Haegeman A, de la Peña E. 2020. Complex patterns in tolerance and resistance to pests and diseases underpin the domestication of tomato. New Phytologist. 226(1):254–266. doi:10.1111/nph.16353.
   PubMed Web of Science ®Google Scholar
• Fürstenberg-Hägg J, Zagrobelny M, Bak S. 2013. Plant defense against insect herbivores. Int J Mol Sci. 14(5). doi:10.3390/ijms140510242.
   PubMed Web of Science ®Google Scholar
• Gao J, Tao T, Arthurs SP, Ye F, An X, Hussain M, Mao R. 2023. Plant jasmonic acid mediated contrasting effects of two citrus aphid species on Diaphorina citri Kuwayama. Pest Management Science. 79(2):811–820. doi:10.1002/ps.7249.
   PubMed Web of Science ®Google Scholar
• Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR. 2012. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci. 13(12). doi:10.3390/ijms131217077.
   PubMed Web of Science ®Google Scholar
• Goffreda JC, Steffens JC, Mutschler MA. 1990. Association of epicuticular sugars with aphid resistance in hybrids with wild tomato. J Am Soc Hortic Sci. 115(1):161–165. doi:10.21273/JASHS.115.1.161.
   Web of Science ®Google Scholar
• Islam T, Moore BD, Johnson SN. 2022. Plant silicon defences reduce the performance of a chewing insect herbivore which benefits a contemporaneous sap-feeding insect. Ecol Entomol. 47(6):951–958. doi:10.1111/een.13183.
   Web of Science ®Google Scholar
• Javed K, Wang Y, Javed H, Wang C, Liu C, Huang Y. 2023. Tomato aphid (Aphis gossypii) secreted saliva can enhance aphid resistance by upregulating signaling molecules in tomato (Solanum lycopersicum). Int J Mol Sci. 24(16):12768. doi:10.3390/ijms241612768.
   PubMed Web of Science ®Google Scholar
• Johnson SN, Rowe RC, Hall CR. 2020. Aphid feeding induces phytohormonal cross-talk without affecting silicon defense against subsequent chewing herbivores. Plants. 9(8):1009. doi:10.3390/plants9081009.
   Google Scholar
• Juvik JA, Shapiro JA, Young TE, Mutschler MA. 1994. Acylglucoses from wild tomatoes alter behavior and reduce growth and survival of Helicoverpa zea and Spodoptera exigua (Lepidoptera: Noctuidae). J Econ Entomol. 87(2). doi:10.1093/jee/87.2.482.
   Web of Science ®Google Scholar
• Kortbeek RWJ, Galland MD, Muras A, van der Kloet FM, André B, Heilijgers M, van Hijum SAFT, Haring MA, Schuurink RC, Bleeker PM. 2021. Natural variation in wild tomato trichomes; selecting metabolites that contribute to insect resistance using a random forest approach. BMC Plant Biol. 21(1). doi:10.1186/s12870-021-03070-x.
   PubMed Web of Science ®Google Scholar
• Kroes A, Stam JM, David A, Boland W, van Loon JJA, Dicke M, Poelman EH. 2016. Plant-mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage. Plant Biology. 18:981–12991. doi:10.1111/plb.12490.
   PubMed Web of Science ®Google Scholar
• Kuśnierczyk A, Tran DHT, Winge P, Jørstad TS, Reese JC, Troczyńska J, Bones AM. 2011. Testing the importance of jasmonate signalling in induction of plant defences upon cabbage aphid (brevicoryne brassicae) attack. BMC Genomics. 12. doi:10.1186/1471-2164-12-423.
   PubMed Web of Science ®Google Scholar
• Leckie BM, D’Ambrosio DA, Chappell TM, Halitschke R, de Jong DM, Kessler A, Kennedy GG, Mutschler MA. 2016. Differential and synergistic functionality of acylsugars in suppressing oviposition by insect herbivores. PLoS ONE. 11(4). doi:10.1371/journal.pone.0153345.
   Web of Science ®Google Scholar
• Li C, Liu G, Xu C, Lee GI, Bauer P, Ling HQ, Ganal MW, Howe GA. 2003. The tomato suppressor of prosystemin-mediated responses 2 gene encodes a fatty acid desaturase required for the biosynthesis of jasmonic acid and the production of a systemic wound signal for defense gene expression. Plant Cell. 15:1646–1661. doi:10.1105/tpc.012237.
   PubMed Web of Science ®Google Scholar
• Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, … Howe GA. 2004. The tomato homolog of CORONATINE-INSENSITIVE1 Is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development[W]. Plant Cell. 16(1):126–143. doi:10.1105/tpc.017954.
   PubMed Web of Science ®Google Scholar
• Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I. 2006. Mi-1-mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Molecular Plant-Microbe Interactions®. 19(6):655–664. doi:10.1094/MPMI-19-0655.
   PubMed Web of Science ®Google Scholar
• Li Y, Cai L, Ding T, Tian E, Yan X, Wang X, Zhang J, Yu K, Chen Z. 2023. Comparative transcriptome analysis reveals the molecular basis of brassica napus in response to aphid stress. Plants. 12(15):2855. doi:10.3390/plants12152855.
   Google Scholar
• Li YH, Meijer D, Dicke M, Gols R. 2018. Oviposition preference of three lepidopteran species is not affected by previous aphid infestation in wild cabbage. Entomol Exp Appl. 166:402–411. doi:10.1111/eea.12663.
   Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 25(4):402–408. doi:10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar
• López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ. 2010. Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot. 61:2589–2601. doi:10.1093/jxb/erq089.
   PubMed Web of Science ®Google Scholar
• McDowell ET, Kapteyn J, Schmidt A, Li C, Kang JH, Descour A, … Gang DR. 2011. Comparative functional genomic analysis of Solanum glandular trichome types. Plant Physiol. 155(1):524–539. doi:10.1104/pp.110.167114.
   PubMed Web of Science ®Google Scholar
• Mewis I, Appel HM, Hom A, Raina R, Schultz JC. 2005. Major signaling pathways modulate arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol. 138(2). doi:10.1104/pp.104.053389.
   PubMed Web of Science ®Google Scholar
• Moran PJ, Thompson GA. 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125(2). doi:10.1104/pp.125.2.1074.
   Web of Science ®Google Scholar
• Moreira X, Abdala-Roberts L, Castagneyrol B. 2018. Interactions between plant defence signalling pathways: evidence from bioassays with insect herbivores and plant pathogens. J Ecol. 106(6). doi:10.1111/1365-2745.12987.
   Web of Science ®Google Scholar
• Morkunas I, Mai VC, Gabryś B. 2011. Phytohormonal signaling in plant responses to aphid feeding. Acta Physiol Plant. 33(6). doi:10.1007/s11738-011-0751-7.
   Web of Science ®Google Scholar
• Nguyen D, Rieu I, Mariani C, van Dam NM. 2016. How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol Biol. 91:727–740. doi:10.1007/s11103-016-0481-8.
   PubMed Web of Science ®Google Scholar
• Oldroyd GED, Staskawicz BJ. 1998. Genetically engineered broad-spectrum disease resistance in tomato. Proc Natl Acad Sci USA. 95:10300–10305. PMID: 9707642. doi:10.1073/pnas.95.17.10300.
   PubMed Web of Science ®Google Scholar
• Ontiveros I, López-Moya JJ, Díaz-Pendón JA. 2022. Coinfection of tomato plants with Tomato yellow leaf curl virus and Tomato chlorosis virus affects the interaction with host and whiteflies. Phytopathology®. 112:944–952. doi:10.1094/PHYTO-08-21-0341-R.
   PubMed Web of Science ®Google Scholar
• Pieterse CMJ, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SCM. 2012. Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 28. doi:10.1146/annurev-cellbio-092910-154055.
   PubMed Web of Science ®Google Scholar
• Planelló R, Llorente L, Herrero Ó, Novo M, Blanco-Sánchez L, Díaz-Pendón JA, … de la Peña E. 2022. Transcriptome analysis of aphids exposed to glandular trichomes in tomato reveals stress and starvation related responses. Sci Rep. 12(1):20154. doi:10.1038/s41598-022-24490-1.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/.
   Google Scholar
• Rodríguez-López MJ, Garzo E, Bonani JP, Fereres A, Fernández-Muñoz R, Moriones E. 2011. Whitefly resistance traits derived from the wild tomato Solanum pimpinellifolium affect the preference and feeding behavior of Bemisia tabaci and reduce the spread of Tomato yellow leaf curl virus. Phytopathology. 101(10). doi:10.1094/PHYTO-01-11-0028.
   PubMed Web of Science ®Google Scholar
• Rodríguez-López MJ, Moriones E, Fernández-Muñoz R. 2020. An acylsucrose-producing tomato line derived from the wild species Solanum pimpinellifolium decreases fitness of the whitefly trialeurodes vaporariorum. Insects. 11(9):616. doi:10.3390/insects11090616.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS. 2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol. 36:1043–21057. doi:10.1007/s10886-010-9854-7.
   PubMed Web of Science ®Google Scholar
• Ryan CA. 2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology. 1477(1-2):112–121. doi:10.1016/S0167-4838(99)00269-1.
   PubMedGoogle Scholar
• Sanmartín N, Sánchez-Bel P, Pastor V, Pastor-Fernández J, Mateu D, Pozo MJ, … Flors V. 2020. Root-to-shoot signalling in mycorrhizal tomato plants upon Botrytis cinerea infection. Plant Sci. 298:110595. doi:10.1016/j.plantsci.2020.110595.
   PubMed Web of Science ®Google Scholar
• Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, … Janssen A. 2011. A herbivore that manipulates plant defence. Ecol Lett. 14(3):229–110236. doi:10.1111/j.1461-0248.2010.01575.x.
   PubMed Web of Science ®Google Scholar
• Schuurink R, Tissier A. 2020. Glandular trichomes: micro-organs with model status? New Phytol. 225(6):2251–2266. doi:10.1111/nph.16283.
   PubMed Web of Science ®Google Scholar
• Schwartzberg EG, Tumlinson JH. 2014. Aphid honeydew alters plant defence responses. Funct Ecol. 28(2). DOI: 10.1111/1365-2435.12182
   Web of Science ®Google Scholar
• Schweiger R, Heise AM, Persicke M, Müller C. 2014. Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types. Plant Cell Environ. 37(7):1574–1585. doi:10.1111/pce.12257.
   PubMed Web of Science ®Google Scholar
• Simmons AT, Gurr GM. 2005. Trichomes of lycopersicon species and their hybrids: effects on pests and natural enemies. Agric For Entomol. 7(4). doi:10.1111/j.1461-9555.2005.00271.x.
   Web of Science ®Google Scholar
• Soler R, Badenes-Pérez FR, Broekgaarden C, Zheng SJ, David A, Boland W, Dicke M. 2012. Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription. Funct Ecol. 26:156–166. doi:10.1111/j.1365-2435.2011.01902.x.
   Web of Science ®Google Scholar
• Stam JM, Kroes A, Li Y, Gols R, van Loon JJA, Poelman EH, Dicke M. 2014. Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol. 65. doi:10.1146/annurev-arplant-050213-035937.
   PubMed Web of Science ®Google Scholar
• Steinbrenner AD, Muñoz-Amatriaín M, Chaparro AF, Aguilar-Venegas JM, Lo S, Okuda S, … Crubaugh D. 2020. A receptor-like protein mediates plant immune responses to herbivore-associated molecular patterns. Proc Natl Acad Sci USA. 117(49):31510–31518. doi:10.1073/pnas.2018415117.
   PubMed Web of Science ®Google Scholar
• Tian D, Tooker J, Peiffer M, Chung SH, Felton GW. 2012. Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta. 236(4). doi:10.1007/s00425-012-1651-9.
   Web of Science ®Google Scholar
• Uppalapati SR, Ayoubi P, Weng H, Palmer DA, Mitchell RE, Jones W, Bender CL. 2005. The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J. 42(2):201–217. doi:10.1111/j.1365-313X.2005.02366.x.
   PubMed Web of Science ®Google Scholar
• van Emden HF, Harrington R. 2007. Aphids as crop pests. Aphids as Crop Pests. doi:10.2135/cropsci2008.02.0001br.
   Google Scholar
• War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC. 2012. Mechanisms of plant defense against insect herbivores. Plant Signaling and Behavior. 7(10). doi:10.4161/psb.21663.
   PubMedGoogle Scholar
• Zhang Y, Li X. 2019. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol. 50:29–36. doi:10.1016/j.pbi.2019.02.004.
   PubMed Web of Science ®Google Scholar
• Zhu-Salzman K, Salzman RA, Ahn JE, Koiwa H. 2004. Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol. 134(1). doi:10.1104/pp.103.028324.
   PubMed Web of Science ®Google Scholar
• Züst T, Agrawal AA. 2016. Mechanisms and evolution of plant resistance to aphids. Nat Plants. 2. doi:10.1038/nplants.2015.206.
   PubMed Web of Science ®Google Scholar