Feeding by Whiteflies Suppresses Downstream Jasmonic Acid Signaling by Eliciting Salicylic Acid Signaling

Journal of Chemical Ecology

Volumn 39, Issue 5, 2013, Pages 612-619

  Zhang, Peng Jun ^a   Li, Wei Di ^a   Huang, Fang ^a   Zhang, Jin Ming ^a   Xu, Fang Cheng ^b   Lu, Yao Bin ^a  

^a INSTITUTE OF PLANT PROTECTION AND MICROBIOLOGY   (China)

^b Wenzhou Vocational Technical College   (China)

Author keywords

Bemisia tabaci; Cross talk; Jasmonic acid; Salicylic acid; Vegetative storage protein1 (VSP1)

Indexed keywords

ARABIDOPSIS PROTEIN; CYCLOPENTANE DERIVATIVE; DNA BINDING PROTEIN; EDS1 PROTEIN, ARABIDOPSIS; JASMONIC ACID; OPR3 PROTEIN, ARABIDOPSIS; OXIDOREDUCTASE; OXYLIPIN; PR 1 PROTEIN, ARABIDOPSIS; PR-1 PROTEIN, ARABIDOPSIS; PROTEINASE; SALICYLIC ACID; VSP1 PROTEIN, ARABIDOPSIS;

BIOASSAY; CROP DAMAGE; DEFENSE BEHAVIOR; FEEDING BEHAVIOR; GENE EXPRESSION; HERB; HOST PLANT; INTEGRATED PEST MANAGEMENT; ORGANIC ACID; PROTEIN; SIGNALING; WHITEFLY;

ANIMAL; ARABIDOPSIS; ARTICLE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HEMIPTERA; HERBIVORY; MALE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYCLOPENTANES; DNA-BINDING PROTEINS; ENDOPEPTIDASES; FEMALE; GENE EXPRESSION REGULATION, PLANT; HEMIPTERA; HERBIVORY; MALE; OXIDOREDUCTASES; OXYLIPINS; SALICYLIC ACID; SIGNAL TRANSDUCTION;

ALEYRODIDAE; ARABIDOPSIS; ARABIDOPSIS THALIANA; BEMISIA TABACI;

EID: 84877156003     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-013-0283-2     Document Type: Article

References (42)

1. Arimura, G. I., Ozawa, R., Nishioka, T., Boland, W., Koch, T., Kühnemann, F., and Takabayashi, J. 2002. Herbivore-induced volatiles induce the emission of ethylene in neighboring lima bean plants. Plant J. 29: 87-98.
2. Beckers, G. J. M. and Spoel, S. H. 2006. Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol. 8: 1-10.
3. Bell, E., Creelman, R. A., and Mullet, J. E. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 92: 8675-8679.
4. Bruessow, F., Gouhier-Darimont, C., Buchala, A., Metraux, J. P., and Reymond, P. 2010. Insect eggs suppress plant defense against chewing herbivores. Plant J. 62: 876-885.
5. Cao, H., Glazebrook, J., Clarke, J. D., Volko, S., and Dong, X. N. 1997. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Plant Cell 88: 57-63.
6. Cipollini, D., Enright, S., Traw, M. B., and Bergelson, J. 2004. Salicylic acid inhibits jasmonic acid-induced resistance of Arabidopsis thaliana to Spodoptera exigua. Mol. Ecol. 13: 1643-1653.
7. Clarke, J. D., Liu, Y., Klessig, D. F., and Dong, X. N. 1998. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant. Plant Cell 10: 557-569.
8. Delaney, T. P., Uknes, S., Vernooij, B., Friedrich, L., Weymann, K., Negrotto, D., Gaffney, T., Gut-Rella, M., Kessmann, H., Waed, E., and Ryals, J. 1994. A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250.
9. Dicke, M., van Loon, J. J. A., and Soler, R. 2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5: 317-324.
10. Diezel, C., von Dahl, C. C., Gaquerel, E., and Baldwin, I. T. 2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150: 1576-1586.
11. Doares, S. H., Narvaes-Vasquez, J., Conconi, A., and Ryan, C. A. 1995. Salicylic acid inhibits synthesis of proteinase inhibitors in tomato leaves induced by systemin and jasmonic acid. Plant Physiol. 108: 1741-1746.
12. Engelberth, J., Koch, T., Schüler, G., Bachmann, N., Rechtenbach, J., and Boland, W. 2001. Ion channel-forming alamethicin is a potent elicitor of volatile biosynthesis and tendril coiling. Cross talk between jasmonate and salicylate signaling in lima bean. Plant Physiol. 125: 369-377.
13. Erb, M., Meldau, S., and Howe, G. A. 2012. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17: 250-259.
14. Funk, C. J. 2001. Alkaline phosphatase activity in whitefly salivary glands and saliva. Arch. Insect Biochem. Physiol. 46: 165-174.
15. Guzman, P. and Ecker, J. R. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-523.
16. Jirage, D., Zhou, N., Cooper, B., Clarke, J. D., Dong, X. N., and Glazebrook, J. 2001. Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. Plant J. 26: 395-407.
17. Kachroo, P., Shanklin, J., Shah, J., Whittle, E. J., and Klessig, D. F. 2001. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc. Natl. Acad. Sci. U. S. A. 98: 9448-9453.
18. Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago University Press, Chicago.
19. Kempema, L. A., Cui, X. P., Holzer, F. M., and Walling, L. L. 2007. Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol. 143: 849-865.
20. Koornneef, A. and Pieterse, C. M. J. 2008. Cross talk in defense signaling. Plant Physiol. 146: 839-844.
21. Koornneef, A., Leon-Reyes, A., Ritsema, T., Verhage, A., den Otter, F. C., van Loon, L. C., and Pieterse, C. M. J. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147: 1358-1368.
22. Kunkel, B. N. and Brooks, D. M. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5: 325-331.
23. Leon-reyes, A., Du, Y., Koornneef, A., Proietti, S., Körbes, A. P., Memelink, J., Pieterse, C. M., and Ritsema, T. 2010. Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol. Plant Microbe Interact. 23: 187-197.
24. Li, J., Brader, G., and Palva, E. T. 2004. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16: 319-331.
25. Liu, T. X. 2000. Population dynamics of Bemisia argentifolii (Homoptera: Aleyrodidae) on spring collard and relationship to yield in the lower Rio Grande valley of Texas. J. Econ. Entomol. 93: 750-756.
26. Liu, Y. L., Ahn, J. E., Datta, S., Salzman, R. A., Moon, J., Huyghues-Despointes, B., Pittendrigh, B., Murdock, L. L., Koiwa, H., and Zhu-Salzman, K. 2005. Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 139: 1545-1556.
27. Mohase, L. and van der Westhuizen, A. J. 2002. Salicylic acid is involved in resistance responses in the Russian wheat aphid-wheat interaction. J. Plant Physiol. 159: 585-590.
28. Ndamukong, I., Al Abdallat, A., Thurow, C., Fode, B., Zander, M., Weigel, R., and Gatz, C. 2007. SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1. 2 transcription. Plant J. 50: 128-139.
29. Ochsenbein, C., Przybyla, D., Danon, A., Landgraf, F., Göbel, C., Imboden, A., Feussner, I., and Apel, K. 2006. The role of EDS1 (enhanced disease susceptibility) during singlet oxygen-mediated stress responses of Arabidopsis. Plant J. 47: 445-456.
30. Sarmento, R. A., Lemos, F., Bleeker, P. M., Schuurink, R. C., Pallini, A., Oliveira, M. G. A., Lima, E. R., Kant, M., Sabelis, M. W., and Jassen, A. 2011. A herbivore that manipulate plant defense. Ecol. Lett. 14: 229-236.
31. Schaller, F., Biesgen, C., Müssig, C., Altmann, T., and Weiler, E. W. 2000. 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210: 979-984.
32. Spoel, S. H., Koornneef, A., Claessens, S. M., Korzelius, J. P., van Pelt, J. A., Mueller, M. J., Buchala, A. J., Métraux, J. P., Brown, R., Kazan, K., van Loon, L. C., Dong, X. N., and Pieterse, C. M. J. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15: 760-770.
33. Thaler, J. S., Humphrey, P. T., and Whiteman, N. K. 2012. Evolution of jasmonate and salycilate signal crosstalk. Trends Plant Sci. 17: 260-270.
34. van de Ven, W. T. G., Levesque, C. S., Perring, T. M., and Walling, L. L. 2000. Local and systemic changes in squash gene expression in response to silverleaf whitefly feeding. Plant Cell 12: 1409-1423.
35. von Malek, B., van der Graaff, E., Schneitz, K., and Keller, B. 2002. The Arabidopsis male-sterile mutant dde2-2 is defective in the ALLENE OXIDE SYNTHASE gene encoding one of the key enzymes of the jasmonic acid biosynthesis pathway. Planta 216: 187-192.
36. Walling, L. L. 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19: 195-216.
37. Walling, L. L. 2008. Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146: 859-866.
38. Wu, J. Q. and Baldwin, I. T. 2009. Herbivory-induced signalling in plants: perception and action. Plant Cell Environ. 32: 1161-1174.
39. Zarate, S. I., Kempema, L. A., and Walling, L. L. 2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143: 866-875.
40. Zhang, P. J., Zheng, S. J., van Loon, J. J. A., Boland, W., David, A., Mumm, R., and Dicke, M. 2009. Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc. Natl. Acad. Sci. U. S. A. 106: 21202-21207.
41. Zhang, P. J., Zhu, X. Y., Huang, F., Liu, Y., Zhang, J. M., Lu, Y. B., and Ruan, Y. M. 2011. Suppression of jasmonic acid-dependent defense in cotton plant by the mealybug Phenacoccus solenopsis. PLoS One 6: e22378.
42. Zhang, P. J., Broekgaarden, C., Zheng, S. J., Snoeren, T. A. L., van Loon, J. J. A., Gols, R., and Dicke, M. 2013. Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol. 197: 1291-1299.