Differential contribution of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis

Frontiers in Plant Science

Volumn 4, Issue FEB, 2013, Pages

  Schweizer, Fabian ^a   Bodenhausen, Natacha ^a,b   Lassueur, Steve ^a   Masclaux, Frédéric G ^a   Reymond, Philippe ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b ETH ZURICH   (Switzerland)

Author keywords

Arabidopsis thaliana; Defense; MYC2; MYC3; MYC4; Spodoptera littoralis; Transcription factors

Indexed keywords

EID: 84885867488     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00013     Document Type: Article

References (64)

1. Baldwin, I. T. (1998). Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc. Natl. Acad. Sci. U.S.A. 95, 8113-8118.
2. Beekwilder, J., van Leeuwen, W., van Dam, N. M., Bertossi, M., Grandi, V., Mizzi, L., et al. (2008). The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS ONE 3:e2068. doi:10.1371/journal.pone.0002068
3. Bodenhausen, N., and Reymond, P. (2007). Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol. Plant Microbe Interact. 20, 1406-1420.
4. Boter, M., Ruíz-Rivero, O., Abdeen, A., and Prat, S. (2004). Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes Dev. 18, 1577-1591.
5. Bu, Q., Jiang, H., Li, C.-B., Zhai, Q., Zhang, J., and Wu, X. (2008). Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res. 18, 756-767.
6. Chini, A., Fonseca, S., Fernández, G., Adie, B. A. T., Chico, J. M., Lorenzo, O., et al. (2007). The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671.
7. de Vos, M., Denekamp, M., Dicke, M., Vuylsteke, M., Van Loon, L. C., Smeekens, S. C., et al. (2006). The Arabidopsis thaliana transcription factor AtMYB102 functions in defense against the insect herbivore Pieris rapae. Plant Signal. Behav. 1, 305-311.
8. de Vos, M., Van Oosten, V. R., Van Poecke, R. M. P., Van Pelt, J. A., Pozo, M. J., Mueller, M. J., et al. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18, 923-937.
9. Devoto, A., Ellis, C., Magusin, A., Chang, H.-S., Chilcott, C., Zhu, T., et al. (2005). Expression profiling reveals COI1 to be a key regulator of genes involved in wound-and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol. Biol. 58, 497-513.
10. 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.
11. Fernández-Calvo, P., Chini, A., Fernández-Barbero, G., Chico, J. M., Gimenez-Ibanez, S., Geerinck, J., et al. (2011). The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23, 701-715.
12. Feys, B. J., Benedetti, C. E., Penfold, C. N., and Turner, J. G. (1994). Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6, 751-759.
13. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., et al. (2009). (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344-350.
14. Gigolashvili, T., Berger, B., Mock, H.-P., Müller, C., Weisshaar, B., and Flügge, U.-I. (2007). The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J. 50, 886-901.
15. Gigolashvili, T., Engqvist, M., Yatusevich, R., Müller, C., and Flügge, U.-I. (2008). HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis inArabidopsis thaliana. New Phytol. 177, 627-642.
16. Glauser, G., Schweizer, F., Turlings, T. C. J., and Reymond, P. (2012). Rapid profiling of intact glucosinolates inArabidopsis leaves by UHPLC-QTOFMS using a charged surface hybrid column. Phytochem. Anal. 23, 520-528.
17. Godoy, M., Franco-Zorrilla, J. M., Pérez-Pérez, J., Oliveros, J. C., Lorenzo, O., and Solano, R. (2011). Improved protein-binding microarrays for the identification of DNA-binding specificities of transcription factors. Plant J. 66, 700-711.
18. Grubb, C., and Abel, S. (2006). Glucosinolate metabolism and its control. Trends Plant Sci. 11, 89-100.
19. Halitschke, R., Schittko, U., Pohnert, G., Boland, W., and Baldwin, I. T. (2001). Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid-amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol. 125, 711-717.
20. Halkier, B. A., and Gershenzon, J. (2006). Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57, 303-333.
21. Hirai, M. Y., Sugiyama, K., Sawada, Y., Tohge, T., Obayashi, T., Suzuki, A., et al. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 6478-6483.
22. Howe, G. A., and Jander, G. (2007). Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59, 41-66.
23. Howe, G. A., Lightner, J., Browse, J., and Ryan, C. A. (1996). An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8, 2067-2077.
24. Johnson, E. T., and Dowd, P. F. (2004). Differentially enhanced insect resistance, at a cost, in Arabidopsis thalianaconstitutively expressing a transcription factor of defensive metabolites. J. Agric. Food Chem. 52, 5135-5138.
25. Kerchev, P. I., Fenton, B., Foyer, C. H., and Hancock, R. D. (2012). Plant responses to insect herbivory: interactions between photosynthesis, reactive oxygen species and hormonal signalling pathways. Plant Cell Environ. 35, 441-453.
26. Li, L., Zhao, Y., McCaig, B. C., Wingerd, B. A., Wang, J., Whalon, M. E., et al. (2004). The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16, 126-143.
27. Liechti, R., Csárdi, G., Bergmann, S., Schütz, F., Sengstag, T., Boj, S. F., et al. (2010). EuroDia: a beta-cell gene expression resource. Database (Oxford) 2010, baq024.
28. Liu, Y., Ahn, J.-E., Datta, S., Salzman, R. A., Moon, J., Huyghues-Despointes, B., et al. (2005). Arabidopsisvegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 139, 1545-1556.
29. 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 inArabidopsis. Plant Cell 16, 1938-1950.
30. Manners, J. M. J., Penninckx, I. A. I., Vermaere, K. K., Kazan, K. K., Brown, R. L. R., Morgan, A. A., et al. (1998). The promoter of the plant defensin gene PDF1.2 from Arabidopsis is systemically activated by fungal pathogens and responds to methyl jasmonate but not to salicylic acid. Plant Mol. Biol. 38, 1071-1080.
31. McConn, M., Creelman, R. A., Bell, E., Mullet, J. E., and Browse, J. (1997). Jasmonate is essential for insect defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 94, 5473-5477.
32. 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.
33. Misra, P., Pandey, A., Tiwari, M., Chandrashekar, K., Sidhu, O. P., Asif, M. H., et al. (2010). Modulation of transcriptome and metabolome of tobacco by Arabidopsis transcription factor, AtMYB12, leads to insect resistance. Plant Physiol. 152, 2258-2268.
34. Mittler, R., Kim, Y., Song, L., Coutu, J., Coutu, A., Ciftci-Yilmaz, S., et al. (2006). Gain-and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress. FEBS Lett. 580, 6537-6542.
35. Paschold, A., Halitschke, R., and Baldwin, I. T. (2007). Co(i)-ordinating defenses: NaCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J. 51, 79-91.
36. Pauwels, L., Barbero, G. F., Geerinck, J., Tilleman, S., Grunewald, W., Pérez, A. C., et al. (2010). NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464, 788-791.
37. Pauwels, L., and Goossens, A. (2011). The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23, 3089-3100.
38. Penninckx, I. A., Thomma, B. P. H. J., Buchala, A. J., Métraux, J. P., and Broekaert, W. F. (1998). Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene inArabidopsis. Plant Cell 10, 2103-2113.
39. Pieterse, C. M. J., der Does Van, D., Zamioudis, C., Leon-Reyes, A., and Van Wees, S. C. M. (2012). Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489-521.
40. Pré, M. M., Atallah, M. M., Champion, A. A., De Vos, M. M., Pieterse, C. M. J. C., and Memelink, J. J. (2008). The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 147, 1347-1357.
41. Reymond, P., Bodenhausen, N., Van Poecke, R. M. P., 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.
42. Reymond, P., Weber, H., Damond, M., and Farmer, E. E. (2000). Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12, 707-720.
43. Rizhsky, L., Davletova, S., Liang, H., and Mittler, R. (2004). The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J. Biol. Chem. 279, 11736-11743.
44. Rowe, H. C., Walley, J. W., Corwin, J., Chan, E. K.-F., Dehesh, K., and Kliebenstein, D. J. (2010). Deficiencies in jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog.6:e1000861. doi:10.1371/journal.ppat.1000861
45. Schoonhoven, L. M., van Loon, J. J. A., and Dicke, M. (2005). Insect-Plant Biology. Oxford: Oxford University Press.
46. Sclep, G., Allemeersch, J., Liechti, R., De Meyer, B., Beynon, J., Bhalerao, R., et al. (2007). CATMA, a comprehensive genome-scale resource for silencing and transcript profiling of Arabidopsis genes. BMC Bioinformatics 8:400. doi:10.1186/1471-2105-8-400
47. Shang, Y., Yan, L., Liu, Z.-Q., Cao, Z., Mei, C., Xin, Q., et al. (2010). The Mg-chelatase H subunit of Arabidopsisantagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22, 1909-1935.
48. Sheard, L. B., Tan, X., Mao, H., Withers, J., Ben-Nissan, G., Hinds, T. R., et al. (2010). Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468, 400-405.
49. Skibbe, M., Qu, N., Galis, I., and Baldwin, I. T. (2008). Induced plant defenses in the natural environment:Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20, 1984-2000.
50. Sønderby, I. E., Burow, M., Rowe, H. C., Kliebenstein, D. J., and Halkier, B. A. (2010). A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis. Plant Physiol.153, 348-363.
51. Stintzi, A., Weber, H., Reymond, P., Browse, J., and Farmer, E. E. (2001). Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl. Acad. Sci. U.S.A. 98, 12837-12842.
52. Thaler, J. S., Owen, B., and Higgins, V. J. (2004). The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol. 135, 530-538.
53. Thines, B., Katsir, L., Melotto, M., Niu, Y., Mandaokar, A., Liu, G., et al. (2007). JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448, 661-665.
54. Thomma, B. P. H. J., Eggermont, K., and Broekaert, W. F. (2000). Disease development of several fungi onArabidopsis can be reduced by treatment with methyl jasmonate. Plant Physiol. Biochem. 38, 421-427.
55. Tran, L.-S. P., Nakashima, K., Sakuma, Y., Simpson, S. D., Fujita, Y., Maruyama, K., et al. (2004). Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16, 2481-2498.
56. Verhage, A., Vlaardingerbroek, I., Raaijmakers, C., Van Dam, N., Dicke, M., Van Wees, S. C. M., et al. (2011). Rewiring of the jasmonate signaling pathway in Arabidopsis during insect gerbivory. Front. Plant Sci. 2:47. doi:10.3389/fpls.2011.00047
57. Vogt, T. (2010). Phenylpropanoid biosynthesis. Mol. Plant 3, 2-20.
58. Walling, L. L. (2000). The myriad plant responses to herbivores. J. Plant Growth Regul. 19, 195-216.
59. Wittstock, U., and Gershenzon, J. (2002). Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr. Opin. Plant Biol. 5, 300-307.
60. Xie, D., Feys, B. J., James, S., Nieto-Rostro, M., and Turner, J. G. (1998). COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094.
61. Xu, X., Chen, C., Fan, B., and Chen, Z. (2006). Physical and functional interactions between pathogen-inducedArabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18, 1310-1326.
62. Yan, Y., Stolz, S., Chételat, A., Reymond, P., Pagni, M., Dubugnon, L., et al. (2007). A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell 19, 2470-2483.
63. Zheng, X.-Y., Spivey, N. W., Zeng, W., Liu, P.-P., Fu, Z. Q., Klessig, D. F., et al. (2012). Coronatine promotesPseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587-596.
64. Zhu, Z., An, F., Feng, Y., Li, P., Xue, L. A. M., Jiang, Z., et al. (2011). Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 12539-12544