Spider mites suppress tomato defenses downstream of jasmonate and salicylate independently of hormonal crosstalk

New Phytologist

Volumn 205, Issue 2, 2015, Pages 828-840

  Alba, Juan M ^a   Schimmel, Bernardus C J ^a   Glas, Joris J ^a   Ataide, Livia M S ^b   Pappas, Maria L ^c   Villarroel, Carlos A ^d   Schuurink, Robert C ^d   Sabelis, Maurice W ^a   Kant, Merijn R ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b University of Vicosa   (Brazil)

^c DEMOCRITUS UNIVERSITY OF THRACE   (Greece)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Defense suppression; Herbivore communities; Hormonal crosstalk; Jasmonic acid (JA); Salicylic acid (SA); Solanum lycopersicum (tomato); Tetranychus spp. (spider mite)

Indexed keywords

ACARI; LYCOPERSICON ESCULENTUM; TETRANYCHIDAE; TETRANYCHUS; TETRANYCHUS EVANSI; TETRANYCHUS URTICAE;

CYCLOPENTANE DERIVATIVE; JASMONIC ACID; OXYLIPIN; SALICYLIC ACID;

ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HERBIVORY; METABOLISM; PHYSIOLOGY; PLANT LEAF; TETRANYCHIDAE; TOMATO;

ANIMALS; CYCLOPENTANES; FEMALE; GENE EXPRESSION REGULATION, PLANT; HERBIVORY; LYCOPERSICON ESCULENTUM; OXYLIPINS; PLANT LEAVES; SALICYLIC ACID; TETRANYCHIDAE;

EID: 84919868957     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13075     Document Type: Article

References (95)

1. Abramovitch RB, Anderson JC, Martin GB. 2006. Bacterial elicitation and evasion of plant innate immunity. Nature Reviews. Molecular Cell Biology 7: 601-611.
2. Adato A, Mandel T, Mintz-Oron S, Venger I, Levy D, Yativ M, Dominguez E, Wang ZH, De Vos RCH, Jetter R et al. 2009. Fruit-surface flavonoid accumulation in tomato is controlled by a SIMYB12-regulated transcriptional network. PLoS Genetics 5: e1000777.
3. Alba JM, Glas JJ, Schimmel BCJ, Kant MR. 2011. Avoidance and suppression of plant defenses by herbivores and pathogens. Journal of Plant Interactions 6: 1-7.
4. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC. 2004. Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiology 135: 2025-2037.
5. Ament K, Krasikov V, Allmann S, Rep M, Takken FLW, Schuurink RC. 2010. Methyl salicylate production in tomato affects biotic interactions. Plant Journal 62: 124-134.
6. Belliure B, Janssen A, Maris PC, Peters D, Sabelis MW. 2005. Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters 8: 70-79.
7. Bonaventure G, VanDoorn A, Baldwin IT. 2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends in Plant Science 16: 294-299.
8. Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA. 2010. A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (Green Peach Aphid). PLoS Genetics 6: e1001216.
9. Boubou A, Migeon A, Roderick GK, Auger P, Cornuet JM, Magalhaes S, Navajas M. 2012. Test of colonisation scenarios reveals complex invasion history of the red tomato spider mite Tetranychus evansi. PLoS ONE 7: e35601.
10. Burgyán J, Havelda Z. 2011. Viral suppressors of RNA silencing. Trends in Plant Science 16: 265-272.
11. Casteel CL, Hansen AK, Walling LL, Paine TD. 2012. Manipulation of plant defense responses by the tomato psyllid (Bactericerca cockerelli) and its associated endosymbiont Candidatus Liberibacter Psyllaurous. PLoS ONE 7: e35191.
12. Casteel CL, Yang C, Nanduri AC, De Jong HN, Whitham SA, Jander G. 2014. The Nia-Pro protein of Turnip mosaic virus improves growth and reproduction of the aphid vector, Myzus persicae (green peach aphid). Plant Journal 77: 653-663.
13. Chen H, Jones AD, Howe GA. 2006. Constitutive activation of the jasmonate signaling pathway enhances the production of secondary metabolites in tomato. FEBS Letters 580: 2540-2546.
14. Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA. 2005. Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proceedings of the National Academy of Sciences, USA 102: 19237-19242.
15. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671.
16. 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. Proceedings of the National Academy of Sciences, USA 110: 15728-15733.
17. Colquhoun TA, Kim JY, Wedde AE, Levin LA, Schmitt KC, Schuurink RC, Clark DG. 2011. PhMYB4 fine-tunes the floral volatile signature of Petunia × hybrida through PhC4H. Journal of Experimental Botany 62: 1133-1143.
18. Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, Bruessow F, Sobhy I, Reymond P. 2012. Insect oral secretions suppress wound-induced responses in Arabidopsis. Journal of Experimental Botany 63: 727-737.
19. Constabel CP, Barbehenn RV. 2008. Defensive roles of polyphenol oxidase in plants. In: Schaller A, ed. Induced plant resistance to herbivory. New York, NY, USA: Springer Verlag, 253-269.
20. Da Cunha L, Sreerekha M-V, Mackey D. 2007. Defense suppression by virulence effectors of bacterial phytopathogens. Current Opinion in Plant Biology 10: 349-357.
21. Dal Cin V, Tieman DM, Tohge T, McQuinn R, de Vos RCH, Osorio S, Schmelz EA, Taylor MG, Smits-Kroon MT, Schuurink RC et al. 2011. Identification of genes in the phenylalanine metabolic pathway by ectopic expression of a MYB transcription factor in tomato fruit. Plant Cell 23: 2738-2753.
22. De Jonge R, Bolton M, Thomma BPHJ. 2011. How filamentous pathogens co-opt plants: the ins and outs of fungal effectors. Current Opinion in Plant Biology 14: 400-406.
23. Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbic M, Clark RM, Feyereisen R, Van Leeuwen TAF. 2012. A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proceedings of the National Academy of Sciences, USA 110: E112-E113.
24. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiology 150: 1576-1586.
25. Dorey S, Baillieul F, Saindrenan P, Fritig B, Kauffmann S. 1998. Tobacco class I and II catalases are differentially expressed during elicitor-induced hypersensitive cell death and localized acquired resistance. Molecular Plant-Microbe Interactions: MPMI 11: 1102-1109.
26. Engelberth J, Contreras CF, Viswanathan S. 2012. Transcriptional analysis of distant signaling induced by insect elicitors and mechanical wounding in Zea mays. PLoS ONE 7: e34855.
27. Farmer EE, Johnson RR, Ryan CA. 1992. Regulation of expression of proteinase-inhibitor genes by methyl jasmonate and jasmonic acid. Plant Physiology 98: 995-1002.
28. Felton GW, Donato K, Del Vecchio RJ, Duffey SS. 1989. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. Journal of Chemical Ecology 15: 2667-2694.
29. Ferragut F, Garzon-Luque E, Pekas A. 2013. The invasive spider mite Tetranychus evansi (Acari: Tetranychidae) alters community composition and host-plant use of native relatives. Experimental and Applied Acarology 60: 321-341.
30. Gadea J, Mayda ME, Conejero V, Vera P. 1996. Characterization of defense-related genes ectopically expressed in viroid-infected tomato plants. Molecular Plant-Microbe Interactions: MPMI 9: 409-415.
31. Glazebrook J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43: 205-227.
32. Gomez S, Steinbrenner AD, Osorio S, Schueller M, Ferrieri RA, Fernie AR, Orians CM. 2012. From shoots to roots: transport and metabolic changes in tomato after simulated feeding by a specialist lepidopteran. Entomologia Experimentalis et Applicata 144: 101-111.
33. Gonzales-Vigil E, Bianchetti CM, Philips GN Jr, Howe GA. 2011. Adaptive evolution of threonine deaminase in plant defense against herbivores. Proceedings of the National Academy of Sciences, USA 108: 5897-5902.
34. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, Osborne EJ, Dermauw W, Ngoc PCT, Ortego F et al. 2011. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479: 487-492.
35. Gruner K, Griebel T, Navarova H, Attaran E, Zeier J. 2013. Reprogramming of plants during systemic acquired resistance. Frontiers in Plant Science 4: 252.
36. Haegeman A, Mantelin S, Jones JT, Gheysen G. 2012. Functional roles of effectors of plant-parasitic nematodes. Gene 492: 19-31.
37. Hogenhout SA, Bos JIB. 2011. Effector proteins that modulate plant-insect interactions. Current Opinion in Plant Biology 14: 1-7.
38. Howe GA, Jander G. 2008. Plant immunity to insect herbivores. Annual Review of Plant Biology 59: 41-66.
39. Howe GA, Lightner J, Browse J, Ryan CA. 1996. An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8: 2067-2077.
40. Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R et al. 2013. Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341: 175-179.
41. Itkin M, Rogachev I, Alkan N, Rosenberg T, Malitsky S, Masini L, Meir S, Iijima Y, Aoki K, de Vos R et al. 2011. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23: 4507-4525.
42. Jeppson LR, Keifer HH, Baker EW. 1975. Injurious Tetranychid mites. In: Jeppson LR, Keifer HH, Baker EW, eds. Mites injurious to economic plants. Berkeley, CA, USA: University of California Press, 127-252.
43. Kaloshian I, Walling LL. 2005. Hemipterans as plant pathogens. Annual Review of Phytopathology 43: 491-521.
44. Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44: 41-60.
45. Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW. 2007. Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proceedings of the National Academy of Sciences, USA 104: 12205-12210.
46. Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC. 2004. Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiology 135: 483-495.
47. Kant MR, Bleeker PM, Van Wijk M, Schuurink RC, Haring MA. 2009. Plant volatiles in defence. In: Van Loon LC, ed. Advances in botanical research (volume 51, plant innate immunity). Burlington, VT, USA: Academic Press, 613-666.
48. Kant MR, Sabelis MW, Haring MA, Schuurink RC. 2008. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proceedings. Biological Sciences/The Royal Society 275: 443-452.
49. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53: 299-328.
50. Klingler JP, Nair RM, Edwards OR, Singh KB. 2009. A single gene, AIN, in Medicago truncatula mediates a hypersensitive response to both bluegreen aphid and pea aphid, but confers resistance only to bluegreen aphid. Journal of Experimental Botany 60: 4115-4127.
51. 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 Physiology 147: 1358-1368.
52. Lemos F, Sarmento RA, Pallini A, Dias CR, Sabelis MW, Janssen A. 2010. Spider mite web mediates anti-predator behaviour. Experimental and Applied Acarology 52: 1-10.
53. Lers A, Sonego L, Green PJ, Burd S. 2006. Suppression of LX Ribonuclease in tomato results in a delay of leaf senescence and abscission. Plant Physiology 142: 710-721.
54. Li C, Williams MM, Loh YT, Lee GI, Howe GA. 2002. Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiology 130: 494-503.
55. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA. 2004. The tomato homolog of CORONATINE-INSENSITIVE 1 is required for maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143.
56. Lisón P, Rodrigo I, Conejero V. 2006. A novel function for the cathepsin D inhibitor in tomato. Plant Physiology 142: 1329-1339.
57. Matsushima R, Ozawa R, Uefune M, Gotoh T, Takabayashi J. 2006. Intraspecies variation in the Kanzawa spider mite differentially affects induced defensive response in lima bean plants. Journal of Chemical Ecology 32: 2501-2512.
58. Meier BM, Shaw N, Slusarenko AJ. 1993. Spatial and temporal accumulation of defense gene transcripts in bean (Phaseolus vulgaris) leaves in relation to bacteria-induced hypersensitive cell-death. Molecular Plant-Microbe Interactions: MPMI 6: 453-466.
59. Miles PW. 1972. The saliva of Hemiptera. Advances in Insect Physiology 9: 183-255.
60. Milner SE, Brunton NP, Jones PW, O'Brien NM, Collins SG, Maguire AR. 2011. Bioactivities of glycoalkaloids and their aglycones from Solanum species. Journal of Agricultural and Food Chemistry 59: 3454-3484.
61. Mintz-Oron S, Mandel T, Rogachev I, Feldberg L, Lotan O, Yativ M, Wang Z, Jetter R, Venger I, Adato A et al. 2008. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiology 147: 823-851.
62. Mithöfer A, Wanner G, Boland W. 2005. Effect of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiology 137: 1160-1168.
63. 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 Physiology 140: 249-262.
64. Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW. 2005. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Archives of Insect Biochemistry and Physiology 58: 128-137.
65. Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW. 2002. Caterpillar saliva beats plant defences. Nature 416: 599-600.
66. Navajas M, de Moraes GJ, Auger P, Migeon A. 2013. Review of the invasion of Tetranychus evansi: biology, colonization pathways, potential expansion and prospects for biological control. Experimental and Applied Acarology 59: 43-65.
67. Newman SM, Eannetta NT, Yu HF, Prince JP, Devicente MC, Tanksley SD, Steffens JC. 1993. Organization of the tomato polyphenol oxidase gene family. Plant Molecular Biology 21: 1035-1051.
68. Ozawa R, Matsushima R, Maffei M, Takabayashi J. 2011. Interaction between Phaseolus plants and two strains of Kanzawa spider mites. Journal of Plant Interactions 6: 125-128.
69. Paschold A, Halitschke R, Baldwin IT. 2007. Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant Journal 51: 79-91.
70. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5: 308-316.
71. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28: 489-521.
72. Rodriguez PA, Bos JIB. 2013. Toward understanding the role of aphid effectors in plant infestation. Molecular Plant-Microbe Interactions: MPMI 26: 25-30.
73. Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima E, Kant M, Sabelis MW, Janssen A. 2011a. A herbivore that manipulates plant defence. Ecology Letters 14: 229-236.
74. Sarmento RA, Lemos F, Dias CR, Kikuchi WT, Rodrigues JCP, Pallini A, Sabelis MW, Janssen A. 2011b. A herbivorous mite down-regulates plant defence and produces web to exclude competitors. PLoS ONE 6: e23757.
75. Schittko U, Preston CA, Baldwin IT. 2000. Eating the evidence? Manduca sexta larvae can not disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption. Planta 210: 343-346.
76. Serrano A, Wang B, Aryal B, Garcion C, Abou-Monsour E, Heck S, Geisler M, Mauch F, Nawrath C, Metraux J-P. 2013. Export of salicylic acid from the chloroplast requires the MATE-like transporter EDS5. Plant Physiology 162: 1815-1821.
77. Stuart JJ, Chen M-S, Shukle R, Harris MO. 2012. Gall midges (Hessian flies) as plant pathogens. Annual Review of Phytopathology 50: 339-357.
78. Sugio A, Kingdom HN, MacLean AM, Grieve VM, Hogenhout SA. 2011. Phytoplasma protein effector SAP11 enhances insect vector reproduction by manipulating plant development and defense hormone biosynthesis. Proceedings of the National Academy of Sciences, USA 108: E1254-E1263.
79. Thipyapong P, Melkonian J, Wolfe DW, Steffens JC. 2004. Suppression of polyphenol oxidases increases stress tolerance in tomato. Plant Science 167: 693-703.
80. Tornero P, Gadea J, Conejero J, Vera P. 1997. Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Molecular Plant-Microbe Interactions: MPMI 10: 624-634.
81. Van Kan JAL, Joosten MHAJ, Wagemakers CAM, Van den Berg-Velthuis GCM, de Wit PJGM. 1992. Differential accumulation of messenger-RNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium-fulvum. Plant Molecular Biology 20: 513-527.
82. Van Loon LC, Van Strien EA. 1999. The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiological and Molecular Plant Pathology 55: 85-97.
83. Verdonk JC, de Vos CHR, Verhoeven HA, Haring MA, Van Tunen AJ, Schuurink RC. 2003. Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 62: 997-1008.
84. Vlot AC, Dempsey DA, Klessig DF. 2009. Salicylic acid, a multifaceted hormone to combat disease. Annual Review of Phytopathology 47: 177-206.
85. Walling LL. 2000. The myriad plant responses to herbivores. Journal of Plant Growth Regulation 19: 195-216.
86. 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. Journal of Experimental Botany 59: 2437-2448.
87. Weygoldt P. 1998. Evolution and systematics of the Chelicerata. Experimental and Applied Acarology 22: 63-79.
88. Will T, Tjallingii WF, Thonnessen A, Van Bel AJE. 2007. Molecular sabotage of plant defense by aphid saliva. Proceedings of the National Academy of Sciences, USA 104: 10536-10541.
89. Wu J, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annual Review of Genetics 44: 1-24.
90. Wu J, Hettenhausen C, Meldau S, Baldwin IT. 2007. Herbivory rapidly activates MAPK signalling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19: 1096-1122.
91. Wu S, Peiffer M, Luthe DS, Felton GW. 2012. ATP hydrolyzing salivary enzymes of caterpillars suppress plant defenses. PLoS ONE 7: e41947.
92. Zarate SI, Kempema LA, Walling LL. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiology 143: 866-875.
93. Zhang P, Zhu X, Huang F, Liu Y, Zhang J, Lu Y, Ruan Y. 2011. Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis. PLoS ONE 6: e22378.
94. Zhang PJ, Zheng SJ, Van Loon JJA, Boland W, David A, Mumm R, Dicke M. 2009. Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proceedings of the National Academy of Sciences, USA 106: 21202-21207.
95. Zhang T, Luan JB, Qi JF, Huang CJ, Li M, Zhou XP, Liu SS. 2012. Begomovirus-whitefly mutualism is achieved through repression of plant defences by a virus pathogenicity factor. Molecular Ecology 21: 1294-1304.