The BLADE-ON-PETIOLE genes of Arabidopsis are essential for resistance induced by methyl jasmonate

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Canet, Juan Vicente ^a   Dobón, Albor ^a   Fajmonová, Jana ^b   Tornero, Pablo ^c  

^a JOHN INNES CENTRE   (United Kingdom)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^c CSIC   (Spain)

Author keywords

Arabidopsis; BOPs; Defense; Methyl jasmonate; NPR1; Salicylic acid

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ACETIC ACID DERIVATIVE; ARABIDOPSIS PROTEIN; BOP1 PROTEIN, ARABIDOPSIS; BOP2 PROTEIN, ARABIDOPSIS; CYCLOPENTANE DERIVATIVE; JASMONIC ACID METHYL ESTER; NPR1 PROTEIN, ARABIDOPSIS; OXYLIPIN;

ALLELE; ARABIDOPSIS; ARTICLE; DISEASE RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHENOTYPE; PHYSIOLOGY; TRANSGENIC PLANT;

ACETATES; ALLELES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYCLOPENTANES; DISEASE RESISTANCE; GENE EXPRESSION REGULATION, PLANT; OXYLIPINS; PHENOTYPE; PLANTS, GENETICALLY MODIFIED;

MLCS; MLOWN;

EID: 84868258889     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-199     Document Type: Article

References (60)

1. Vlot AC, Dempsey DMA, Klessig DF. Salicylic Acid, a Multifaceted Hormone to Combat Disease. Ann Rev Phytopathology 2009, 47(1):177-206.
2. Katagiri F, Thilmony S, He SY. The Arabidopsis thaliana-Pseudomonas syringae Interaction. The Arabidopsis Book 2002, Rockville: American Society of Plant Biologists, http://www.aspb.org/publications/arabidopsis/..
3. Ross AF. Systemic acquired resistance induced by localized virus infections in plants. Virology 1961, 14:340-358. 10.1016/0042-6822(61)90319-1, 13743578.
4. Lopez MA, Bannenberg G, Castresana C. Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr Opin Plant Biol 2008, 11(4):420-427. 10.1016/j.pbi.2008.05.002, 18585953.
5. Browse J. Jasmonate Passes Muster: A Receptor and Targets for the Defense Hormone. Annu Rev Plant Biol 2009, 60(1):183-205. 10.1146/annurev.arplant.043008.092007, 19025383.
6. Dong X. NPR1, all things considered. Curr Opin Plant Biol 2004, 7(5):547-552. 10.1016/j.pbi.2004.07.005, 15337097.
7. Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X. Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 2006, 48(5):647-656. 10.1111/j.1365-313X.2006.02903.x, 17076807.
8. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG. The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 2003, 130(1):161-172. 10.1242/dev.00196, 12441300.
9. Liu G, Holub EB, Alonso JM, Ecker JR, Fobert PR. An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant J 2005, 41(2):304-318.
10. Fu ZQ, Yan S, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 2012, 486(7402):228-232. 3376392, 22699612.
11. Canet JV, Dobón A, Roig A, Tornero P. Structure-Function Analysis of npr1 Alleles in Arabidopsis Reveals a Role for its Paralogs in the Perception of Salicylic Acid. Plant Cell Environ 2010, 33:1911-1922. 10.1111/j.1365-3040.2010.02194.x, 20561252.
12. Zhang Y, Fan W, Kinkema M, Li X, Dong X. 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 1999, 96(11):6523-6528. 10.1073/pnas.96.11.6523, 26915, 10339621.
13. Pieterse CM, van Wees SC, van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, van Loon LC. A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 1998, 10(9):1571-1580. 144073, 9724702.
14. Ton J, De Vos M, Robben C, Buchala A, Metraux JP, Van Loon LC, Pieterse CM. Characterization of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 2002, 29(1):11-21. 10.1046/j.1365-313x.2002.01190.x, 12060223.
15. Kinkema M, Fan W, Dong X. Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 2000, 12(12):2339-2350. 102222, 11148282.
16. Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, et al. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 2003, 15(3):760-770. 10.1105/tpc.009159, 150028, 12615947.
17. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 2003, 34(2):217-228. 10.1046/j.1365-313X.2003.01717.x, 12694596.
18. Johansson A, Staal J, Dixelius C. Early responses in the Arabidopsis-Verticillium longisporum pathosystem are dependent on NDR1, JA- and ET-associated signals via cytosolic NPR1 and RFO1. Mol Plant Microbe Interact 2006, 19(9):958-969. 10.1094/MPMI-19-0958, 16941900.
19. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RA, Ritsema T, Pieterse CM. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 2009, 149(4):1797-1809. 10.1104/pp.108.133926, 2663751, 19176718.
20. Ramirez V, Van der Ent S, Garcia-Andrade J, Coego A, Pieterse CM, Vera P. OCP3 is an important modulator of NPR1-mediated jasmonic acid-dependent induced defenses in Arabidopsis. BMC Plant Biol 2010, 10:199. 10.1186/1471-2229-10-199, 2956548, 20836879.
21. Hepworth SR, Zhang Y, McKim S, Li X, Haughn GW. BLADE-ON-PETIOLE-dependent signaling controls leaf and floral patterning in Arabidopsis. Plant Cell 2005, 17(5):1434-1448. 10.1105/tpc.104.030536, 1091766, 15805484.
22. Ha CM, Jun JH, Nam HG, Fletcher JC. BLADE-ON-PETIOLE1 encodes a BTB/POZ domain protein required for leaf morphogenesis in Arabidopsis thaliana. Plant Cell Physiol 2004, 45(10):1361-1370. 10.1093/pcp/pch201, 15564519.
23. Canet JV, Dobón A, Ibáñez F, Perales L, Tornero P. Resistance and biomass in Arabidopsis: a new model for Salicylic Acid perception. Plant Biotech J 2010, 8:126-141.
24. Cao H, Bowling SA, Gordon AS, Dong X. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 1994, 6(11):1583-1592. 160545, 12244227.
25. Dobón A, Canet JV, Perales L, Tornero P. Quantitative genetic analysis of salicylic acid perception in Arabidopsis. Planta 2011, 234:671-684. 10.1007/s00425-011-1436-6, 21614499.
26. Zhang X, Chen S, Mou Z. Nuclear localization of NPR1 is required for regulation of salicylate tolerance, isochorismate synthase 1 expression and salicylate accumulation in Arabidopsis. J Plant Physiol 2010, 167(2):144-148. 10.1016/j.jplph.2009.08.002, 19716624.
27. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 1997, 88(1):57-63. 10.1016/S0092-8674(00)81858-9, 9019406.
28. Lawton K, Weymann K, Friedrich L, Vernooij B, Uknes S, Ryals J. Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Mol Plant Microbe Interact 1995, 8(6):863-870. 10.1094/MPMI-8-0863, 8664495.
29. Nawrath C, Heck S, Parinthawong N, Metraux JP. EDS5, an essential component of salicylic acid-dependent signaling for disease resistance in Arabidopsis, is a member of the MATE transporter family. Plant Cell 2002, 14(1):275-286. 10.1105/tpc.010376, 150564, 11826312.
30. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 2001, 414(6863):562-565. 10.1038/35107108, 11734859.
31. Khan M, Xu M, Murmu J, Tabb P, Liu Y, Storey K, McKim SM, Douglas CJ, Hepworth SR. Antagonistic interaction of BLADE-ON-PETIOLE1 and 2 with BREVIPEDICELLUS and PENNYWISE regulates Arabidopsis inflorescence architecture. Plant Physiol 2011, 158(2):946-960. 3271780, 22114095.
32. Schwab R, Ossowski S, Riester M, Warthmann N, Weigel D. Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 2006, 18(5):1121-1133. 10.1105/tpc.105.039834, 1456875, 16531494.
33. Norberg M, Holmlund M, Nilsson O. The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 2005, 132(9):2203-2213. 10.1242/dev.01815, 15800002.
34. Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG. COI1: An Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 1998, 280:1091-1094. 10.1126/science.280.5366.1091, 9582125.
35. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, et al. MYC2 Differentially Modulates Diverse Jasmonate-Dependent Functions in Arabidopsis. Plant Cell 2007, 19(7):2225-2245. 10.1105/tpc.106.048017, 1955694, 17616737.
36. He Y, Fukushige H, Hildebrand DF, Gan S. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 2002, 128(3):876-884. 10.1104/pp.010843, 152201, 11891244.
37. Mittal S, Davis KR. Role of the phytotoxin Coronatine in the infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Mol Plant Microbe Interact 1995, 8(1):165-171. 10.1094/MPMI-8-0165, 7539639.
38. Ton J, Mauch-Mani B. Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose. Plant J 2004, 38(1):119-130. 10.1111/j.1365-313X.2004.02028.x, 15053765.
39. Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. Arabidopsis ethylene-response gene ETR1: Similarity of product to two-component regulators. Science 1993, 262:539-544. 10.1126/science.8211181, 8211181.
40. Jun JH, Ha CM, Fletcher JC. BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 2010, 22(1):62-76. 10.1105/tpc.109.070763, 2828709, 20118228.
41. Zhang Y, Tessaro MJ, Lassner M, Li X. Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 2003, 15(11):2647-2653. 10.1105/tpc.014894, 280568, 14576289.
42. Delaney TP, Friedrich L, Ryals JA. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance. Proc Natl Acad Sci U S A 1995, 92(14):6602-6606. 10.1073/pnas.92.14.6602, 41566, 11607555.
43. Ha CM, Jun JH, Nam HG, Fletcher JC. BLADE-ON-PETIOLE 1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 2007, 19(6):1809-1825. 10.1105/tpc.107.051938, 1955725, 17601823.
44. Xu M, Hu T, McKim SM, Murmu J, Haughn GW, Hepworth SR. Arabidopsis BLADE-ON-PETIOLE1 and 2 promote floral meristem fate and determinacy in a previously undefined pathway targeting APETALA1 and AGAMOUS-LIKE24. Plant J 2010, 63(6):974-989. 10.1111/j.1365-313X.2010.04299.x, 20626659.
45. McKim SM, Stenvik GE, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW. The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 2008, 135(8):1537-1546. 10.1242/dev.012807, 18339677.
46. Ha CM, Jun JH, Fletcher JC. Control of Arabidopsis leaf morphogenesis through regulation of the YABBY and KNOX families of transcription factors. Genetics 2010, 186(1):197-206. 10.1534/genetics.110.118703, 2940287, 20610407.
47. Stein E, Molitor A, Kogel KH, Waller F. Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant Cell Physiol 2008, 49(11):1747-1751. 10.1093/pcp/pcn147, 18842596.
48. Spoel SH, Mou Z, Tada Y, Spivey NW, Genschik P, Dong X. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 2009, 137(5):860-872. 10.1016/j.cell.2009.03.038, 2704463, 19490895.
49. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F. bZIP transcription factors in Arabidopsis. Trends Plant Sci 2002, 7(3):106-111. 10.1016/S1360-1385(01)02223-3, 11906833.
50. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301(5633):653-657. 10.1126/science.1086391, 12893945.
51. Tornero P, Dangl JL. A high throughput method for quantifying growth of phytopathogenic bacteria in Arabidopsis thaliana. Plant J 2001, 28(4):475-481.
52. Curtis MD, Grossniklaus U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 2003, 133(2):462-469. 10.1104/pp.103.027979, 523872, 14555774.
53. Ciannamea S, Kaufmann K, Frau M, Tonaco IA, Petersen K, Nielsen KK, Angenent GC, Immink RG. Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne. J Exp Bot 2006, 57(13):3419-3431. 10.1093/jxb/erl144, 17005923.
54. Vidal M, Legrain P. Yeast forward and reverse 'n'-hybrid systems. Nucleic Acids Res 1999, 27(4):919-929. 10.1093/nar/27.4.919, 148269, 9927722.
55. Miller JH. Experiments in Molecular Genetics 1972, Cold Spring Harbor, New York: Cold Spring Harbor Laboratory.
56. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 2007, 104(1):34-41. 10.1263/jbb.104.34, 17697981.
57. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 1998, 16(6):735-743. 10.1046/j.1365-313x.1998.00343.x, 10069079.
58. Johnson CM, Stout PR, Broyer TC, Carlton AB. Comparative chlorine requirements of different plant species. Plant Soil 1957, 8:337-353.
59. Abramoff MD, Magalhaes PJ, Ram SJ. Image Processing with ImageJ. Biophotonics International 2004, 11(7):36-42.
60. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3(7). RESEARCH0034.