Environmental history modulates Arabidopsis pattern-triggered immunity in a histone acetyltransferase1-dependent manner

Plant Cell

Volumn 26, Issue 6, 2014, Pages 2676-2688

  Singh, Prashant ^a,b   Yekondi, Shweta ^a   Chen, Po Wen ^a   Tsai, Chia Hong ^a,c   Yu, Chun Wei ^a   Wu, Keqiang ^a   Zimmerli, Laurent ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b IOWA STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84904999739     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.123356     Document Type: Article

References (57)

1. Alvarez-Venegas, R., Pien, S., Sadder, M., Witmer, X., Grossniklaus, U., and Avramova, Z. (2003). ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr. Biol. 13: 627-637.
2. Ausubel, F. M. (2005). Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6: 973-979.
3. Bilichak, A., Ilnystkyy, Y., Hollunder, J., and Kovalchuk, I. (2012). The progeny ofArabidopsis thalianaplants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS ONE7: e30515.
4. Bodenhausen, N., and Reymond, P. (2007). Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol. Plant Microbe Interact. 20: 1406-1420.
5. Boller, T., and Felix, G. (2009). A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60: 379-406.
6. Bordoli, L., Netsch, M., Lüthi, U., Lutz, W., andEckner, R. (2001). Plant orthologs of p300/CBP: Conservation of a core domain in metazoan p300/CBP acetyltransferase-related proteins. Nucleic Acids Res. 29: 589-597.
7. 2+ sensor protein kinases. Nature 464: 418-422.
8. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., Hollunder, J., and Meins, F., Jr., and Kovalchuk, I. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS ONE5: e9514.
9. Brooks, D. M., Hernández-Guzmán, G., Kloek, A. P., Alarcón-Chaidez, F., Sreedharan, A., Rangaswamy, V., Peñaloza-Vázquez, A., Bender, C. L., and Kunkel, B. N. (2004). Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringaepv. tomatoDC3000. Mol. Plant Microbe Interact. 17: 162-174.
10. Cheng, C., Gao, X., Feng, B., Sheen, J., Shan, L., and He, P. (2013). Plant immune response to pathogens differs with changing temperatures. Nat. Commun. 4: 2530.
11. Cheong, Y. H., Chang, H. S., Gupta, R., Wang, X., Zhu, T., and Luan, S. (2002). Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 129: 661-677.
12. Deng, W. W., Liu, C., Pei, Y., Deng, X., Niu, L., and Cao, X. (2007). Involvement of the histone acetyltransferase AtHAC1 in the regulation of flowering time via repression of FLOWERING LOCUS C in Arabidopsis. Plant Physiol. 143: 1660-1668. Erratum. Plant Physiol. 144: 1233.
13. Desclos-Theveniau, M., Arnaud, D., Huang, T. Y., Lin, G. J. C., Chen, W. Y., Lin, Y. C., and Zimmerli, L. (2012). The Arabidopsis lectin receptor kinase LecRK-V. 5 represses stomatal immunity induced by Pseudomonas syringaepv. tomato DC3000. PLoS Pathog. 8: e1002513.
14. Ding, Y., Fromm, M., and Avramova, Z. (2012). Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat. Commun. 3: 740.
15. Felix, G., Duran, J. D., Volko, S., andBoller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterialflagellin. Plant J. 18: 265-276.
16. Fernández-Calvo, P., et al. (2011). TheArabidopsisbHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell23: 701-715.
17. Glazebrook, J. (2001). Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4: 301-308.
18. Guo, L., Yu, Y., Law, J. A., andZhang, X. (2010). SET DOMAIN GROUP2 is the major histone H3 lysine [corrected] 4 trimethyltransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 107: 18557-18562.
19. Han, S. K., Song, J. D., Noh, Y. S., and Noh, B. (2007). Role of plant CBP/p300-like genes in the regulation offlowering time. Plant J. 49: 103-114.
20. Ito, H., Gaubert, H., Bucher, E., Mirouze, M., Vaillant, I., and Paszkowski, J. (2011). An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature472: 115-119.
21. Jaskiewicz, M., Conrath, U., and Peterhänsel, C. (2011). Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep. 12: 50-55.
22. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature444: 323-329.
23. Kim, J. M., To, T. K., Ishida, J., Morosawa, T., Kawashima, M., Matsui, A., Toyoda, T., Kimura, H., Shinozaki, K., and Seki, M. (2008). Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions inArabidopsis thaliana. PlantCell Physiol. 49: 1580-1588.
24. Lang-Mladek, C., Popova, O., Kiok, K., Berlinger, M., Rakic, B., Aufsatz, W., Jonak, C., Hauser, M. T., and Luschnig, C. (2010). Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing inArabidopsis. Mol. Plant3: 594-602.
25. Larkindale, J., and Vierling, E. (2008). Core genome responses involved in acclimation to high temperature. Plant Physiol. 146: 748-761.
26. Li, J., Brader, G., and Palva, E. T. (2004). The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylatemediated signals in plant defense. Plant Cell16: 319-331.
27. 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.
28. Luna, E., Bruce, T. J. A., Roberts, M. R., Flors, V., andTon, J. (2012). Next-generation systemic acquired resistance. Plant Physiol. 158: 844-853.
29. Lusser, A. (2002). Acetylated, methylated, remodeled: Chromatin states for gene regulation. Curr. Opin. Plant Biol. 5: 437-443.
30. Návarová, H., Bernsdorff, F., Döring, A. C., and Zeier, J. (2012). Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell24: 5123-5141.
31. Pandey, R., Müller, A., Napoli, C. A., Selinger, D. A., Pikaard, C. S., Richards, E. J., Bender, J., Mount, D. W., and Jorgensen, R. A. (2002). Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thalianasuggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30: 5036-5055.
32. Pastori, G. M., and Foyer, C. H. (2002). Common components, networks, and pathways of cross-tolerance to stress: The central role of "redox" and abscisic acid-mediated controls. Plant Physiol. 129: 460-468.
33. Pecinka, A., and Mittelsten Scheid, O. (2012). Stress-induced chromatin changes: A critical view on their heritability. Plant Cell Physiol. 53: 801-808.
34. Penninckx, I. A., Thomma, B. P., Buchala, A., 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. PlantCell10: 2103-2113.
35. Po-Wen, C., Singh, P., and Zimmerli, L. (2013). Priming of the Arabidopsispattern-triggered immunity response upon infection by necrotrophic Pectobacterium carotovorum bacteria. Mol. Plant Pathol. 14: 58-70.
36. Raj, S., Bräutigam, K., Hamanishi, E. T., Wilkins, O., Thomas, B. R., Schroeder, W., Mansfield, S. D., Plant, A. L., and Campbell, M. M. (2011). Clone history shapes Populus drought responses. Proc. Natl. Acad. Sci. USA108: 12521-12526.
37. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., and Mittler, R. (2004). When defense pathways collide: The response of Arabidopsisto a combination of drought and heat stress. Plant Physiol. 134: 1683-1696.
38. Rojo, E., León, J., and Sánchez-Serrano, J. J. (1999). Cross-talk between wound signalling pathways determines local versus systemic gene expression inArabidopsis thaliana. PlantJ. 20: 135-142.
39. Roudier, F., Teixeira, F. K., and Colot, V. (2009). Chromatin indexing in Arabidopsis: An epigenomic tale of tails and more. Trends Genet. 25: 511-517.
40. Sani, E., Herzyk, P., Perrella, G., Colot, V., and Amtmann, A. (2013). Hyperosmotic priming ofArabidopsisseedlings establishes a longterm somatic memory accompanied by specific changes of the epigenome. Genome Biol. 14: R59.
41. Schweizer, F., Fernández-Calvo, P., Zander, M., Diez-Diaz, M., Fonseca, S., Glauser, G., Lewsey, M. G., Ecker, J. R., Solano, R., and Reymond, P. (2013). Arabidopsisbasic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell25: 3117-3132.
42. Singh, P., Kuo, Y. C., Mishra, S., Tsai, C. H., Chien, C. C., Chen, C. W., Desclos-Theveniau, M., Chu, P. W., Schulze, B., Chinchilla, D., Boller, T., and Zimmerli, L. (2012). The lectin receptor kinase-VI. 2 is required for priming and positively regulates Arabidopsispatterntriggered immunity. Plant Cell 24: 1256-1270.
43. Strahl, B. D., and Allis, C. D. (2000). The language of covalent histone modifications. Nature403: 41-45.
44. Sung, D. Y., Kaplan, F., Lee, K. J., and Guy, C. L. (2003). Acquired tolerance to temperature extremes. Trends Plant Sci. 8: 179-187.
45. Thomma, B. P. H. J., Eggermont, K., Penninckx, I. A. M. A., Mauch-Mani, B., Vogelsang, R., Cammue, B. P. A., and Broekaert, W. F. (1998). Separate jasmonate-dependent and salicylate-dependent defenseresponse pathways in Arabidopsisare essential for resistance to distinct microbial pathogens. Proc. Natl. Acad. Sci. USA95: 15107-15111.
46. Tsuda, K., and Katagiri, F. (2010). Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13: 459-465.
47. Tsuda, K., Sato, M., Glazebrook, J., Cohen, J. D., and Katagiri, F. (2008). Interplay between MAMP-triggered and SA-mediated defense responses. Plant J. 53: 763-775.
48. vanHulten, M., Pelser, M., vanLoon, L. C., Pieterse, C. M. J., and Ton, J. (2006). Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA103: 5602-5607.
49. Whittle, C. A., Otto, S. P., Johnston, M. O., and Krochko, J. E. (2009). Adaptive epigenetic memory of ancestral temperature regime in Arabidopsis thaliana. Botany87: 650-657.
50. Windram, O., et al. (2012). Arabidopsisdefense against Botrytis cinerea: Chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24: 3530-3557.
51. Wu, C. C., Singh, P., Chen, M. C., and Zimmerli, L. (2010). L-Glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming inArabidopsis. J. Exp. Bot. 61: 995-1002.
52. Xiao, F., He, P., Abramovitch, R. B., Dawson, J. E., Nicholson, L. K., Sheen, J., and Martin, G. B. (2007). The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant J. 52: 595-614.
53. Xiong, L., and Yang, Y. (2003). Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15: 745-759.
54. Yu, C. W., Liu, X., Luo, M., Chen, C., Lin, X., Tian, G., Lu, Q., Cui, Y., and Wu, K. (2011). HISTONE DEACETYLASE6 interacts with FLOWERING LOCUS D and regulatesflowering in Arabidopsis. Plant Physiol. 156: 173-184.
55. Zhu, J., Dong, C.-H., and Zhu, J.-K. (2007). Interplay between coldresponsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr. Opin. PlantBiol. 10: 290-295.
56. Zimmerli, L., Jakab, G., Metraux, J. P., and Mauch-Mani, B. (2000). Potentiation of pathogen-specific defense mechanisms inArabidopsis by beta-aminobutyric acid. Proc. Natl. Acad. Sci. USA97: 12920-12925.
57. Zimmerli, L., Métraux, J. P., and Mauch-Mani, B. (2001). b-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea. Plant Physiol. 126: 517-523.