Arabidopsis redox status in response to caterpillar herbivory

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  Paudel, Jamuna ^a   Copley, Tanya ^a   Amirizian, Alexandre ^a   Prado, Alberto ^a   Bede, Jacqueline C ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Arabidopsis thaliana; Caterpillar herbivory; Cross talk; Induced defenses; Signaling pathways; Spodoptera exigua

Indexed keywords

EID: 84893237406     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00113     Document Type: Article

References (84)

1. Arimura, G., Ozawa, R., and Maffei, M. E. (2011). Recent advances in plant early signaling in response to herbivory. Int. J. Mol. Sci. 12, 3723-3739.
2. Ball, L., Accotto, G. P., Bechtold, U., Creissen, G., Funck, D., Jimenez, A., et al. (2004). Evidence for a direct link between glutathione biosynthesis and stress defense gene expression in Arabidopsis. Plant Cell 16, 2448-2462.
3. Bede, J. C., Musser, R. O., Felton, G. W., and Korth, K. L. (2006). Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol. Biol. 60, 519-531.
4. 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.
5. Bodenhausen, N., and Reymond, P. (2007). Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol. Plant Microbe Interact. 20, 1406-1420.
6. Boyes, D. C., Zayed, A. M., Ascenzi, R., McCaskill, A. J., Hoffman, N. E., Davis, K. R., et al. (2001). Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13, 1499-1510.
7. Brunner, A. M., Yakovlev, I. A., and Strauss, S. H. (2004). Validating internal controls for quantitative plant gene expression studies. BMC Plant Biol. 4:14. doi: 10.1186/1471-2229-4-14
8. Conn, V. M., Walker, A. R., and Franco, C. M. M. (2008). Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol. Plant Microbe Interact. 21, 208-218.
9. Després, C., Chubak, C., Rochon, A., Clark, R., Bethune, T., Desveaux, D., et al. (2003). The Arabidopsis NPR1 disease resistance protein is a novel cofactor that confers redox regulation of DNA binding activity to the basic domain/leucine zipper transcription factor TGA1. Plant Cell 15, 2181-2191.
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, 1576-1587.
11. Doares, S. H., Narvaez-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. Dombrecht, B., Xue, G. P., Sprague, S. J., Kirkegaard, J. A., Ross, J. J., Reid, J. B., et al. (2007). MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19, 2225-2245.
13. Dubreuil-Mauriza, C., Vitecek, J., Marty, L., Branciard, L., Frettinger, P., Wendehenne, D., et al. (2011). Glutathione deficiency of the Arabidopsis mutant pad2-1 affects oxidative stress-related events, defense gene expression, and the hypersensitive response. Plant Physiol. 157, 2000-2012.
14. Dufresne, P. J., Ubalijoro, E., Fortin, M. G., and Laliberte, J.-F. (2008). Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus. J. Gen. Virol. 89, 2339-2348.
15. Eichenseer, H., Mathews, M. C., Powell, J. S., and Felton, G. W. (2010). Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J. Chem. Ecol. 36, 885-897.
16. Espunya, M. C., De Michele, R., Gómez-Cadenas, A., and Carmen Martínez, M. C. (2012). S-nitrosoglutathione is a component of wound-and salicylic acid-induced systemic responses in Arabidopsis thaliana. J. Exp. Bot. 63, 3219-3227.
17. Felton, G. W. (2008). "Caterpillar secretions and induced plant responses, " in Induced Plant Resistance to Herbivory, ed. A. Schaller (Berlin: Springer-Scientific), 369-387.
18. Felton, G. W., and Korth, K. L. (2000). Trade-offs between pathogen and herbivore resistance. Curr. Opin. Plant Biol. 3, 309-314.
19. Fobert, P. R., and Després, C. (2005). Redox control of systemic acquired resistance. Curr. Opin. Plant Biol 8, 378-382.
20. Fodor, J., Gullner, G., Adam, A. L., Barna, B., Komives, T., and Kiraly, Z. (1997). Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid to tobacco. Plant Physiol. 114, 1443-1451.
21. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Prozel, A., Kramell, R., et al. (2009). (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344-350.
22. Forman, H. J., Maiorino, M., and Ursini, F. (2010). Signaling functions of reactive oxygen species. Biochemistry 49, 835-842.
23. Gfeller, A., Baerenfaller, K., Loscos, J., Chételat, A., Baginsky, S., and Farmer, E. E. (2011). Jasmonate controls polypeptide patterning in undamaged tissue in wounded Arabidopsis leaves. Plant Physiol. 156, 1797-1807.
24. Glazebrook, J. (2005). Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
25. Griffith, O. W. (1980). Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 106, 207-212.
26. Hogenhout, S. A., and Bos, J. I. B. (2011). Effector proteins that modulate plant-insect interactions. Curr. Opin. Plant Biol. 14, 422-428.
27. Jirage, D., Zhou, N., Cooper, B., Clarke, J. D., Dong, X., and Glazebrook, J. (2001). Constitutive salicylic acid-dependent signaling in cpr1 and cpr6 mutants requires PAD4. Plant J. 26, 395-407.
28. Kazan, K., and Manners, J. M. (2008). Jasmonate signaling: toward an integrated view. Plant Physiol. 146, 1459-1468.
29. Koornneef, A., Leon-Reyes, A., Ritsema, T., Verhage, A., Den Otter, F. C., Van Loon, L. C., et al. (2008). Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358-1368.
30. Koornneef, A., and Pieterse, C. M. J. (2008). Cross talk in defense signaling. Plant Physiol. 146, 839-844.
31. Kusnierczyk, A., Winge, P., Midelfart, H., Armbruster, W. S., Rossiter, J. T., and Bones, A. M. (2007). Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J. Exp. Bot. 58, 2537-2552.
32. Leon-Reyes, A., Spoel, S. H., De Lange, E. S., Abe, H., Kobayashi, M., Tsuda, S., et al. (2009). Ethylene mediates the role of NONEXPRESSOR of PATHOGENESIS RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149, 1797-1809.
33. Leon-Reyes, A., Van der Does, D., De Lange, E. S., Delker, C., Wasternack, C., Van Wees, S. C. M., et al. (2010). Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta 232, 1423-1432.
34. Lindermayr, C., Sell, S., Müller, B., Leister, D., and Durner, J. (2010). Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22, 2894-2907.
35. Lorenzo, O., Chico, J. M., Sánchez-Serrano, J. J., and Solano, R. (2004). JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938-1950.
36. Lorenzo, O., Piqueras, R., Sánchez-Serrano, J. J., and Solano, R. (2003). ETHYLENE RESPONSE FACTOR1 integrates signaling from ethylene and jasmonate pathway in plant defense. Plant Cell 15, 165-178.
37. Lorenzo, O., and Solano, R. (2005). Molecular players regulating the jasmonate signalling network. Curr. Opin. Plant Biol. 8, 532-540.
38. Lou, Y., and Baldwin, I. T. (2006). Silencing of a germin-like gene in Nicotiana attenuata improves the performance of native herbivores. Plant Physiol. 140, 1126-1136.
39. Maffei, M. E., Mithöfer, A., Arimura, G., Uchtenhagen, H., Bossi, S., Bertea, C., et al. (2006). Effects of feeding Spodoptera littoralis on lima bean leaves. III Membrane depolarization and involvement of hydrogen peroxide. Plant Physiol. 140, 1022-1035.
40. Mateo, A., Funck, D., Mühlenbock, P., Kular, B., Mullineaux, P. M., and Karpinski, S. (2006). Controlled levels of salicylic acid are required for optimal photosynthesis and redox homeostasis. J. Exp. Bot. 57, 1795-1807.
41. Mewis, I., Tokuhisa, J. G., Schultz, J. C., Appel, H. M., Ulrichs, C., and Gershenzon, J. (2006). Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67, 2450-2462.
42. Mhamdi, A., Hager, J., Chaouch, S., Queval, G., Han, Y., Taconnat, L., et al. (2010). Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways. Plant Physiol. 153, 1144-1160.
43. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113, 935-944.
44. Mueller, S., Hilbert, B., Dueckershoff, K., Roitsch, T., Krischke, M., Muelle, M. J., et al. (2008). General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20, 768-785.
45. Mur, L. A. J., Kenton, P., Atzorn, R., Miersch, O., and 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.
46. Musser, R. O., Hum-Musser, S. M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J. B., et al. (2002). Caterpillar saliva beats plant defenses: a new weapon emerges in the coevolutionary race between plants and herbivores. Nature 416, 599-600.
47. Ndamukong, I., Abdallat, A. A., Thurow, C., Fode, B., Zander, M., Weigel, R., et al. (2007). SA-inducible Arabidopsis glutaredoxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50, 128-139.
48. Ng, C. F., Schafer, F. Q., Buettner, G. R., and Rodgers, V. G. J. (2007). The rate of cellular hydrogen peroxide removal shows dependency on GSH: mathematical insight into in vivo H2O2 and GPx concentrations. Free Radic. Res. 41, 1201-1211.
49. Noctor, G., Mhamdi, A., Chaouch, S., Han, Y., Neukermans, J., Marquez-Garcia, B., et al. (2012). Glutathione in plants: an integrated overview. Plant Cell Environ. 35, 454-484.
50. Onkokesung, N., Baldwin, I. T., and Gális, I. (2010). The role of jasmonic acid and ethylene crosstalk in direct defense of Nicotiana attenuata plants against chewing herbivores. Plant Signal. Behav. 5, 1305-1307.
51. Parisy, V., Poinssot, B., Owsianowski, L., Buchala, A., Glazebrook, J., and Mauch, F. (2007). Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J. 49, 159-172.
52. Penninckx, E. A. M. A., Thomma, B. P. H. J., Buchala, A., Metraux, J.-P., and Broekaert, W. F. (1998). Concomitant activation of jasmonate and ethylene response pathway is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10, 2103-2113.
53. Potter, S., Ukes, S., Lawton, K., Winter, A. M., Chandler, D., Di Maio, J., et al. (1993). Regulation of a hevein-like gene in Arabidopsis. Mol. Plant Microbe Interact. 6, 680-685.
54. Pré, M., Atallah, M., Champion, A., De Vos, M., Pieterse, C. M. J., and Memelink, J. (2008). The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347-1357.
55. Queval, G., Hager, J., Gakière, B., and Noctor, G. (2008). Why are literature data for H2O2 contents so variable? A discussion of potential difficulties in the quantitative assay of leaf extracts. J. Exp. Bot. 59, 135-146.
56. Queval, G., and Noctor, G. (2007). A plate reader method for the measurement of NAD, NADP, glutathione, and ascorbate in tissue extracts: application to redox profiling during Arabidopsis rosette development. Anal. Biochem. 363, 58-69.
57. Rahman, I., Kode, A., and Biswas, S. K. (2006). Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 1, 3159-3165.
58. Rao, M. V., Paliyath, G., Ormrod, D. P., Murr, D. P., and Watkins, C. B. (1997). Influence of salicylic acid on H2O2 production, oxidative stress and H2O2-metabolizing enzymes. Plant Physiol. 115, 137-149.
59. Rayapuram, C., and Baldwin, I. T. (2007). Increased SA in NPR1-silenced plants antagonizes JA and JA-dependent direct and indirect defenses in herbivore-attacked Nicotiana attenuata in nature. Plant J. 52, 700-715.
60. Reymond, P., Bodenhausen, N., Van Poecke, R. M., Krishnamurthy, V., Dicke, M., and Farmer, E. E. (2004). A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16, 3132-3147.
61. Rieu, I., and Powers, S. J. (2009). Real-time quantitative RT-PCR: design, calculations and statistics. Plant Cell 21, 1031-1033.
62. Robert-Seilaniantz, A., Grant, M., and Jones, J. D. G. (2011). Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu. Rev. Phytopathol. 49, 317-343.
63. Schlaeppi, K., Bodenhausen, N., Buchala, A., Mauch, F., and Reymond, P. (2008). The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J. 55, 774-786.
64. Schröder, E., and Eaton, P. (2008). Hydrogen peroxide as an endogenous mediator and exogenous tool in cardiovascular research: issues and considerations. Curr. Opin. Pharmacol. 8, 153-159.
65. Spoel, S. H., and Dong, X. (2008). Making sense of hormone crosstalk during plant immune response. Cell Host Microbe 3, 348-351.
66. Spoel, S. H., Koornneef, A., Claessens, S. M. C., Korzellus, J. P., Van Pelt, J. A., Mueller, J. A., et al. (2003). NPR1 modulates crosstalk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytoplasm. Plant Cell 15, 760-770.
67. Spoel, S. H., Mou, Z., Tada, Y., Spivey, N. W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcriptional activator NPR1 plays a dual role in regulating plant immunity. Cell 137, 860-872.
68. Stotz, H. U., Pittendrigh, B. R., Kroymann, J., Weniger, K., Fritsche, J., Bauke, A., et al. (2000). Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiol. 124, 1007-1018.
69. Ströher, E., Wang, X.-J., Roloff, N., Klein, P., Husemann, A., and Dietz, K.-J. (2009). Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Mol. Plant 2, 357-367.
70. Swarup, R., Perry, P., Hagenbeek, D., Van Der Straeten, D., Beemster, G. T. S., Sandberg, G., et al. (2007). Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 19, 2186-2196.
71. Szalai, G., Kellös, T, Galiba, G., and Kocsy, G. (2009). Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. J. Plant Growth Regul. 28, 66-80.
72. Tada, Y., Spoel, S. H., Pajerowska-Mukhtar, K., Mou, Z., Song, J., Wang, C., et al. (2008). Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952-956.
73. Thivierge, K., Prado, A., Driscoll, B. T., Bonneil, É., Thibault, P., and Bede, J. C. (2010). Caterpillar-and salivary-specific modification of plant proteins. J. Proteome Res. 9, 5887-5895.
74. Van der Does, D., Leon-Reyes, A., Koorneef, A., Van Verk, M. C., Rodenburg, N., Pauwels, L., et al. (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.
75. Verhage, A., Vlaardingerbroek, I., Raaymakers, C., Van Dam, N. M., Dicke, M., Van Wees, S. C. M., et al. (2011). Rewiring of the jasmonate signaling pathway in Arabidopsis during insect herbivory. Front. Plant Sci. 2:47. doi: 10.3389/ fpls.2011.00047
76. Walling, L. L. (2008). Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146, 859-866.
77. Weech, M.-H., Chapleau, M., Pan, L., Ide, C., and Bede, J. C. (2008). Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J. Exp. Bot. 59, 2437-2448.
78. Wünsche, H., Baldwin, I. T., and Wu, J. (2011). S-nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene is induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J. Exp. Bot. 62, 4605-4616.
79. Zander, M., Chen, S., Imkampe, J., Thurow, C., and Gatz, C. (2011). Repression of the Arabidopsis thaliana jasmonic acid/ethylene-induced defense pathway by TGA interacting glutaredoxins depends on their C-terminal ALWL. Mol. Plant 5, 831-840.
80. Zander, M., La Camera, S., Lamotte, O., Métraux, J. P., and Gatz, C. (2010) Arabidopsis thaliana class-II TGA transcription factors are essential activators of jasmonic acid/ethylene-induced defense responses. Plant J. 61, 200-210.
81. Zarei, A., Körbes, A. P., Younessi, P., Montiel, G., Champion, A., and Memelink, J. (2011). Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of PDF1.2 promoter in Arabidopsis. Plant Mol. Biol. 75, 321-331.
82. Zebelo, S. A., and Maffei, M. E. (2012). The ventral eversible gland (VEG) of Spodoptera littoralis triggers early responses to herbivory in Arabidopsis thaliana. Arthropod Plant Interact. 6, 543-551.
83. Zhang, Y., Fan, W., Kinkema, M., Li, X., and Dong, X. (1999). Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc. Natl. Acad. Sci. U.S.A. 96, 6523-6528.
84. Zhang, Y., Tessaro, M. J., Lassner, M., and Li, X. (2003). Knockout analysis of Arabidopsis transcription factors TGA2, TGA5 and TGA6 reveals their redundant and essential roles in Systemic Acquired Resistance. Plant Cell 15, 2647-2653.