Advertisement

Eurydema oleracea negatively affects defenses in Arabidopsis by inducing salicylic acid-mediated signaling pathway

  • Luisa EderliEmail author
  • Gianandrea Salerno
  • Chantal Bianchet
  • Manuela Rebora
  • Silvana Piersanti
  • Stefania Pasqualini
Original Paper
  • 9 Downloads

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.

Keywords

Arabidopsis Eurydema oleracea Feeding behavior Salicylic and jasmonic-signaling pathways 

Notes

Author contribution

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.

Funding

This work was supported by the “Fondo di Ateneo per la Ricerca di Base 2017” financed by University of Perugia.

Compliance with ethical standards

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.

Supplementary material

11829_2019_9728_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 14 kb)

References

  1. 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 CrossRefPubMedGoogle Scholar
  2. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 CrossRefPubMedGoogle Scholar
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefPubMedGoogle Scholar
  7. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 CrossRefPubMedGoogle Scholar
  9. 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 CrossRefPubMedGoogle Scholar
  10. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 CrossRefPubMedGoogle Scholar
  14. 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 CrossRefGoogle Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. 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 CrossRefPubMedGoogle Scholar
  21. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844.  https://doi.org/10.1104/pp.107.112029 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 CrossRefPubMedGoogle Scholar
  24. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 CrossRefPubMedGoogle Scholar
  28. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 CrossRefPubMedGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefPubMedGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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 CrossRefPubMedGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 357–369Google Scholar
  40. 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 CrossRefPubMedGoogle Scholar
  41. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14(Suppl):S153–S164.  https://doi.org/10.1105/tpc.000679 CrossRefPubMedPubMedCentralGoogle Scholar
  42. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 CrossRefPubMedGoogle Scholar
  44. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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 CrossRefGoogle Scholar
  46. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 CrossRefPubMedGoogle Scholar
  48. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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 CrossRefPubMedGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Chemistry, Biology and BiotechnologyUniversity of PerugiaPerugiaItaly
  2. 2.Department of Agricultural, Food and Environmental SciencesUniversity of PerugiaPerugiaItaly

Personalised recommendations