Abstract
The study of defense mechanisms of plants against herbivorous insects can clarify the evolutionary mechanisms of these interactions and has significant implications for agriculture. The herbivore Eurydema oleracea is an invasive crop pest; however, knowledge on how it affects plant immune responses is lacking. In the present study, we demonstrate that insect feeding causes the induction of both salicylic acid (SA) and jasmonic acid (JA)-mediated signaling pathways in infested Arabidopsis plants. Using transgenic SA-deficient NahG, we show that the two phytohormones crosstalk antagonistically. In particular, the rapid and strong induction of SA-related gene expression partially suppresses the JA-dependent signaling pathway. This results in increased plant susceptibility to the herbivore, evidenced by an increase of leaf damage inflicted by the adult insects and increased development of the nymphs. Our findings suggest that E. oleracea manipulates hormone signaling components of Arabidopsis as a strategy of attack to suppress plant defense traits. Our work contributes to knowledge on the adaptation of insect pests to plant responses, and is useful for developing management strategies to combat harmful herbivores in agriculture.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alba JM, Schimmel BCJ, Glas JJ, Ataide LM, Pappas ML, Villarroel CA, Schuurink RC, Sabelis MW, Kant MR (2015) Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytol 205:828–840. https://doi.org/10.1111/nph.13075
Arimura GI, Ozawa R, Maffei ME (2011) Recent advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739. https://doi.org/10.3390/ijms12063723
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488. https://doi.org/10.1007/s11103-008-9435-0
Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant Microbe Interact 20:1406–1420. https://doi.org/10.1094/MPMI-20-11-1406
Bohinc T, Trdan S (2012) Trap crops for reducing damage caused by cabbage stink bugs (Eurydema spp.) and flea beetles (Phyllotreta spp.) on white cabbage: fact or fantasy? J Food Agric Environ 10:1365–1370. https://doi.org/10.1234/4.2012.3273
Bruessow F, Gouhier-Darimont C, Buchala A, Metraux JP, Reymond P (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62:876–885. https://doi.org/10.1111/j.1365-313X.2010.04200.x
Caarls L, CornPieterse CMJ, Van Wees SCM (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170. https://doi.org/10.3389/fpls.2015.00170
Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110:15728–15733. https://doi.org/10.1073/pnas.1308867110
Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gutrella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant-disease resistance. Science 266:1247–1250. https://doi.org/10.1126/science.266.5188.1247
Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586. https://doi.org/10.1104/pp.109.139550
Ederli L, Brunetti C, Centritto M, Colazza S, Frati F, Loreto F, Marino G, Salerno G, Pasqualini S (2017) Infestation of broad bean (Vicia faba) by the green stink bug (Nezara viridula) decreases shoot abscisic acid contents under well-watered and drought conditions. Front Plant Sci 8:959. https://doi.org/10.3389/fpls.2017.00959
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259. https://doi.org/10.1016/j.tplants.2012.01.003
Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R (2009) (+)-7-iso-Jasmonoyl-l-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol 5:344–350. https://doi.org/10.1038/nchembio.161
Friedrich L, Lawton K, Ruess W, Masner P, Specker N, Rella MG, Meier B, Dincher S, Staub T, Uknes S, Metraux JP, Kessmann H, Ryals J (1996) A benzothiadiazole derivative induces systemic acquired resistance in tobacco. Plant J 10:61–70. https://doi.org/10.1046/j.1365-313X.1996.10010061.x
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863. https://doi.org/10.1146/annurev-arplant-042811-105606
Inbar M, Doostdar H, Sonoda M, Leibee GL, Mayer RT (1998) Elicitors of plant defensive systems reduce insect densities and disease incidence. J Chem Ecol 24:135–149. https://doi.org/10.1023/A:1022397130895
Jaouannet M, Rodriguez PA, Thorpe P, Lenoir CJG, MacLeod R, Escudero-Martinez C, Bos JIB (2014) Plant immunity in plant-aphid interactions. Front Plant Sci 5:663. https://doi.org/10.3389/fpls.2014.00663
Kästner J, von Knorre D, Himanshu H, Erb M, Baldwin IT, Meldau S (2014) Salicylic acid, a plant defense hormone, is specifically secreted by a molluscan herbivore. PLoS ONE 9:e86500. https://doi.org/10.1371/journal.pone.0086500
Kerchev PI, Fenton B, Foyer CH, Hancock RD (2012) Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ 35:441–453. https://doi.org/10.1111/j.1365-3040.2011.02399.x
Kiep V, Vadassery J, Lattke J, Maaß JP, Boland W, Peiter E, Mithöfer A (2015) Systemic cytosolic Ca2+ elevation is activated upon wounding and herbivory in Arabidopsis. New Phytol 207:996–1004. https://doi.org/10.1111/nph.13493
Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844. https://doi.org/10.1104/pp.107.112029
Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368. https://doi.org/10.1104/pp.108.121392
Lazebnik J, Frago E, Dicke M, van Loon JJA (2014) Phytohormone mediation of interactions between herbivores and plant pathogens. J Chem Ecol 40:730–741. https://doi.org/10.1007/s10886-014-0480-7
Leon-Reyes A, Van der Does D, De Lange ES, Delker C, Wasternack C, Van Wees SCM, Ritsema T, Pieterse CMJ (2010) Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232:1423–1432. https://doi.org/10.1007/s00425-010-1265-z
Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800. https://doi.org/10.1104/pp.106.090837
Liu L, Sonbol FM, Huot B, Gu Y, Withers J, Mwimba M, Yao J, He SY, Dong X (2016) Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat Commun 7:13099. https://doi.org/10.1038/ncomms13099
Martel C, Zhurov V, Navarro M, Martinez M, Cazaux M, Auger P (2015) Tomato whole genome transcriptional response to Tetranychus urticae identifies divergence of spider mite-induced responses between tomato and Arabidopsis. Mol Plant Microbe Interact 28:343–361. https://doi.org/10.1094/MPMI-09-14-0291-FI
Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262. https://doi.org/10.1104/pp.105.072348
Pieterse CMJ, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569. https://doi.org/10.1016/j.tplants.2007.09.004
Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316. https://doi.org/10.1038/nchembio.164
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 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055
Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379. https://doi.org/10.1016/j.pbi.2007.06.003
Santamaría ME, Arnaiz A, Velasco-Arroyo B, Grbic V, Diaz I, Martinez M (2018) Arabidopsis response to the spider mite Tetranychus urticae depends on the regulation of reactive oxygen species homeostasis. Sci Rep-UK 8:1–13. https://doi.org/10.1038/s41598-018-27904-1
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P (2013) Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25:3117–3132. https://doi.org/10.1105/tpc.113.115139
Spoel SH, Johnson JS, Dong X (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci USA 104:18842–18847. https://doi.org/10.1073/pnas.0708139104
Su Q, Chen G, Mescher MC, Peng Z, Xie W, Wang S, Wu Q, Liu J, Li C, Wang W, Zhang Y (2018) Whitefly aggregation on tomato is mediated by feeding-induced changes in plant metabolites that influence the behaviour and performance of conspecifics. Funct Ecol 32:1180–1193. https://doi.org/10.1111/1365-2435.13055
Sweat TA, Wolpert TJ (2007) Thioredoxin h5 Is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19:673–687. https://doi.org/10.1105/tpc.106.047563
Tally A, Oostendorp M, Lawton K, Staub T, Bassi B (1999) Commercial development of elicitors of induced resistance to pathogens. In: Agrawal AA, Tuzun S, Bent E (eds) Induced plant defences against pathogens and herbivores: biochemistry, ecology, and agriculture. APS Press, St Paul, pp 357–369
Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270. https://doi.org/10.1016/j.tplants.2012.02.010
Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164. https://doi.org/10.1105/tpc.000679
Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T, Van Wees SCM, Pieterse CMJ (2013) Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 25:744–761. https://doi.org/10.1105/tpc.112.108548
Verrillo F, Occhipinti A, Kanchiswamy CN, Maffei ME (2014) Quantitative analysis of herbivore-induced cytosolic calcium by using a Cameleon (YC 3.6) calcium sensor in Arabidopsis thaliana. J Plant Physiol 171:136–139. https://doi.org/10.1016/j.jplph.2013.09.020
Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866. https://doi.org/10.1104/pp.107.113142
War AR, Taggar GK, Hussain B, Taggar MS, Nair RM, Sharma HC (2018) Special issue: using non-model systems to explore plant-pollinator and plant-herbivore interactions: plant defence against herbivory and insect adaptations. AoB Plants 10:1–19. https://doi.org/10.1093/aobpla/ply037
Weech MH, Chapleau M, Pan L, Ide C, Bede JC (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot 59:2437–2448. https://doi.org/10.1093/jxb/ern108
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–565. https://doi.org/10.1038/35107108
Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122. https://doi.org/10.1105/tpc.106.049353
Zebelo SA, Maffei ME (2015) Role of early signalling events in plant-insect interactions. J Exp Bot 66:435–448. https://doi.org/10.1093/jxb/eru480
Zhang PJ, Huang F, Zhang JM, Wei JN, Lu YB (2015) The mealybug Phenacoccus solenopsis suppresses plant defense responses by manipulating JA-SA crosstalk. Sci Rep-UK 5:9354. https://doi.org/10.1038/srep09354
Zhang PJ, He YC, Zhao C, Ye ZH, Yu XP (2018) Jasmonic acid-dependent defenses play a key role in defending tomato against Bemisia tabaci nymphs, but not adults. Front Plant Sci 9:1065. https://doi.org/10.3389/fpls.2018.01065
Zheng XY, Spivey NW, Zeng W, Liu PP, Fu ZQ, Klessig DF, He SY, Dong X (2012) Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11:587–596. https://doi.org/10.1016/j.chom.2012.04.014
Zhurov V, Navarro M, Bruinsma KA, Arbona V, Santamaria ME, Cazaux M, Wybouw N, Osborne EJ, Ens C, Rioja C, Vermeirssen V, Rubio-Somoza I, Krishna P, Diaz I, Schmid M, Gómez-Cadenas A, Van de Peer Y, Grbic M, Clark RM, Van Leeuwen T, Grbic V (2014) Reciprocal responses in the interaction between arabidopsis and the cell-content-feeding chelicerate herbivore spider mite. Plant Physiol 164:384–399. https://doi.org/10.1104/pp.113.231555
Funding
This work was supported by the “Fondo di Ateneo per la Ricerca di Base 2017” financed by University of Perugia.
Author information
Authors and Affiliations
Contributions
LE, GS and SP conceived and designed the experiments; LE, GS, CB performed the experiments and analyzed the data; all of the authors interpreted the results, drafted and revised the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All applicable international, national and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.
Additional information
Communicated by Ritu Chaudhary.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Heikki Hokkanen.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ederli, L., Salerno, G., Bianchet, C. et al. Eurydema oleracea negatively affects defenses in Arabidopsis by inducing salicylic acid-mediated signaling pathway. Arthropod-Plant Interactions 14, 139–148 (2020). https://doi.org/10.1007/s11829-019-09728-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-019-09728-6