Involvement of Nt ERF 3 in the cell death signalling pathway mediated by SIPK / WIPK and WRKY 1 in tobacco plants

Abstract We previously reported that one of the ethylene response factors ( ERF s), Nt ERF 3, and other members of the subgroup VIII ‐a ERF s of the AP 2/ ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of Nt ERF 3 in a cell death signal...

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Published inPlant biology (Stuttgart, Germany) Vol. 17; no. 5; pp. 962 - 972
Main Authors Ogata, T., Okada, H., Kawaide, H., Takahashi, H., Seo, S., Mitsuhara, I., Matsushita, Y.
Format Journal Article
LanguageEnglish
Published 01.09.2015
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Abstract Abstract We previously reported that one of the ethylene response factors ( ERF s), Nt ERF 3, and other members of the subgroup VIII ‐a ERF s of the AP 2/ ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of Nt ERF 3 in a cell death signalling pathway in tobacco plants, particularly downstream of Nt SIPK /Nt WIPK and Nt WRKY 1, which are mitogen‐activated protein kinases and a phosphorylation substrate of Nt SIPK , respectively. An ERF ‐associated amphiphilic repression ( EAR ) motif‐deficient Nt ERF 3b mutant ( Nt ERF 3bΔ EAR ) that lacked cell death‐inducing ability suppressed the induction of cell death caused by Nt ERF 3a . The transient co‐expression of Nt ERF 3bΔ EAR suppressed the hypersensitive reaction ( HR )‐like cell death induced by Nt SIPK and Nt WRKY 1 . The induction of cell death by Nt SIPK and Nt WRKY 1 was also inhibited in transgenic plants expressing Nt ERF 3bΔ EAR . Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK / WIPK and WRKY 1. Overall, these results suggest that Nt ERF 3 functions downstream of Nt SIPK / Nt WIPK and Nt WRKY 1 in a cell death signalling pathway, with some feedback regulation.
AbstractList Abstract We previously reported that one of the ethylene response factors ( ERF s), Nt ERF 3, and other members of the subgroup VIII ‐a ERF s of the AP 2/ ERF family exhibit cell death‐inducing ability in tobacco leaves. In this study, we focused on the involvement of Nt ERF 3 in a cell death signalling pathway in tobacco plants, particularly downstream of Nt SIPK /Nt WIPK and Nt WRKY 1, which are mitogen‐activated protein kinases and a phosphorylation substrate of Nt SIPK , respectively. An ERF ‐associated amphiphilic repression ( EAR ) motif‐deficient Nt ERF 3b mutant ( Nt ERF 3bΔ EAR ) that lacked cell death‐inducing ability suppressed the induction of cell death caused by Nt ERF 3a . The transient co‐expression of Nt ERF 3bΔ EAR suppressed the hypersensitive reaction ( HR )‐like cell death induced by Nt SIPK and Nt WRKY 1 . The induction of cell death by Nt SIPK and Nt WRKY 1 was also inhibited in transgenic plants expressing Nt ERF 3bΔ EAR . Analysis of gene expression, ethylene production and cell death symptoms in salicylic acid‐deficient tobacco plants suggested the existence of some feedback regulation in the HR cell death signalling pathway mediated by SIPK / WIPK and WRKY 1. Overall, these results suggest that Nt ERF 3 functions downstream of Nt SIPK / Nt WIPK and Nt WRKY 1 in a cell death signalling pathway, with some feedback regulation.
Author Seo, S.
Matsushita, Y.
Okada, H.
Ogata, T.
Kawaide, H.
Takahashi, H.
Mitsuhara, I.
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Cites_doi 10.2174/2211550111201010023
10.1105/tpc.104.026609
10.1093/pcp/pcq196
10.1046/j.1365-313x.2000.00709.x
10.1046/j.1365-313X.2003.01664.x
10.1104/pp.010862
10.4161/epi.6.2.13627
10.1111/j.1365-313X.2008.03565.x
10.1038/nrg2812
10.1126/science.261.5122.754
10.1093/pcp/pcp075
10.1093/pcp/pcm021
10.1111/j.1462-5822.2007.00944.x
10.1105/tpc.006940
10.1094/MPMI.1997.10.7.922
10.1074/jbc.M409674200
10.1073/pnas.98.2.741
10.1007/978-1-61779-154-3_5
10.1073/pnas.95.4.1933
10.1111/j.1365-313X.2006.03003.x
10.1111/j.1365-313X.2005.02618.x
10.1007/BF00028910
10.1111/tpj.12305
10.4161/psb.5.6.11576
10.1016/j.plantsci.2013.04.003
10.1038/nature05286
10.1094/MPMI-23-8-1032
10.1104/pp.109.151704
10.1073/pnas.96.14.7956
10.1046/j.1365-313x.2002.01191.x
10.1073/pnas.0810206106
10.1105/TPC.010127
10.1016/j.tplants.2010.02.006
10.1104/pp.106.086637
10.1023/A:1015553232309
10.1007/s10327-011-0355-5
10.1094/MPMI.2004.17.10.1162
10.1186/1471-2148-9-126
10.1186/1471-2229-11-89
10.1007/s00438-010-0580-1
10.1046/j.1365-313x.1998.00243.x
10.1371/journal.ppat.1000844
10.1016/S1360-1385(03)00135-3
10.1016/j.tplants.2006.01.004
10.2307/3870231
10.1111/j.1365-313X.2004.02180.x
10.1038/ncomms1926
10.1104/pp.105.073783
10.1093/oxfordjournals.pcp.a029609
10.1105/tpc.005348
10.1046/j.1365-313X.1999.00426.x
10.5511/plantbiotechnology.20.129
10.1105/tpc.13.8.1877
10.1094/MPMI-18-1027
10.1104/pp.108.117887
10.1105/tpc.000794
10.1111/j.1365-313X.2004.02085.x
10.1093/pcp/pcp048
10.1046/j.1365-313X.2003.01759.x
10.1038/nrmicro1239
10.1016/j.bbagrm.2011.08.004
10.1104/pp.109.135830
10.1093/jxb/erm239
10.1073/pnas.95.13.7433
10.1016/0092-8674(94)90283-6
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References e_1_2_6_51_1
e_1_2_6_53_1
e_1_2_6_32_1
e_1_2_6_30_1
Park J.M. (e_1_2_6_50_1) 2001; 13
e_1_2_6_19_1
e_1_2_6_13_1
e_1_2_6_36_1
e_1_2_6_59_1
e_1_2_6_11_1
e_1_2_6_34_1
e_1_2_6_17_1
e_1_2_6_55_1
e_1_2_6_15_1
e_1_2_6_38_1
e_1_2_6_57_1
e_1_2_6_62_1
e_1_2_6_64_1
e_1_2_6_43_1
e_1_2_6_20_1
e_1_2_6_41_1
Ohme‐Takagi M. (e_1_2_6_42_1) 1995; 7
e_1_2_6_60_1
e_1_2_6_9_1
e_1_2_6_5_1
e_1_2_6_7_1
e_1_2_6_24_1
e_1_2_6_49_1
e_1_2_6_3_1
e_1_2_6_22_1
e_1_2_6_66_1
e_1_2_6_28_1
e_1_2_6_45_1
e_1_2_6_26_1
e_1_2_6_47_1
e_1_2_6_68_1
e_1_2_6_52_1
e_1_2_6_54_1
e_1_2_6_10_1
e_1_2_6_31_1
e_1_2_6_14_1
e_1_2_6_35_1
e_1_2_6_12_1
e_1_2_6_33_1
e_1_2_6_18_1
e_1_2_6_39_1
e_1_2_6_56_1
e_1_2_6_16_1
e_1_2_6_37_1
e_1_2_6_58_1
e_1_2_6_63_1
e_1_2_6_65_1
e_1_2_6_21_1
e_1_2_6_40_1
e_1_2_6_61_1
e_1_2_6_8_1
e_1_2_6_4_1
e_1_2_6_6_1
e_1_2_6_25_1
e_1_2_6_48_1
e_1_2_6_23_1
e_1_2_6_2_1
e_1_2_6_29_1
e_1_2_6_44_1
e_1_2_6_67_1
e_1_2_6_27_1
e_1_2_6_46_1
References_xml – ident: e_1_2_6_25_1
  doi: 10.2174/2211550111201010023
– ident: e_1_2_6_27_1
  doi: 10.1105/tpc.104.026609
– ident: e_1_2_6_55_1
  doi: 10.1093/pcp/pcq196
– ident: e_1_2_6_43_1
  doi: 10.1046/j.1365-313x.2000.00709.x
– ident: e_1_2_6_17_1
  doi: 10.1046/j.1365-313X.2003.01664.x
– ident: e_1_2_6_46_1
  doi: 10.1104/pp.010862
– ident: e_1_2_6_20_1
  doi: 10.4161/epi.6.2.13627
– ident: e_1_2_6_30_1
  doi: 10.1111/j.1365-313X.2008.03565.x
– ident: e_1_2_6_6_1
  doi: 10.1038/nrg2812
– ident: e_1_2_6_10_1
  doi: 10.1126/science.261.5122.754
– ident: e_1_2_6_32_1
  doi: 10.1093/pcp/pcp075
– ident: e_1_2_6_59_1
  doi: 10.1093/pcp/pcm021
– ident: e_1_2_6_13_1
  doi: 10.1111/j.1462-5822.2007.00944.x
– ident: e_1_2_6_62_1
  doi: 10.1105/tpc.006940
– ident: e_1_2_6_7_1
  doi: 10.1094/MPMI.1997.10.7.922
– ident: e_1_2_6_38_1
  doi: 10.1074/jbc.M409674200
– ident: e_1_2_6_63_1
  doi: 10.1073/pnas.98.2.741
– ident: e_1_2_6_33_1
  doi: 10.1007/978-1-61779-154-3_5
– ident: e_1_2_6_23_1
  doi: 10.1073/pnas.95.4.1933
– ident: e_1_2_6_53_1
  doi: 10.1111/j.1365-313X.2006.03003.x
– ident: e_1_2_6_5_1
  doi: 10.1111/j.1365-313X.2005.02618.x
– ident: e_1_2_6_11_1
  doi: 10.1007/BF00028910
– ident: e_1_2_6_29_1
  doi: 10.1111/tpj.12305
– ident: e_1_2_6_19_1
  doi: 10.4161/psb.5.6.11576
– volume: 13
  start-page: 1035
  year: 2001
  ident: e_1_2_6_50_1
  article-title: Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2‐type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco
  publication-title: The Plant Cell
  contributor:
    fullname: Park J.M.
– ident: e_1_2_6_41_1
  doi: 10.1016/j.plantsci.2013.04.003
– ident: e_1_2_6_18_1
  doi: 10.1038/nature05286
– ident: e_1_2_6_24_1
  doi: 10.1094/MPMI-23-8-1032
– ident: e_1_2_6_21_1
  doi: 10.1104/pp.109.151704
– ident: e_1_2_6_26_1
  doi: 10.1073/pnas.96.14.7956
– ident: e_1_2_6_2_1
  doi: 10.1046/j.1365-313x.2002.01191.x
– ident: e_1_2_6_3_1
  doi: 10.1073/pnas.0810206106
– ident: e_1_2_6_44_1
  doi: 10.1105/TPC.010127
– ident: e_1_2_6_51_1
  doi: 10.1016/j.tplants.2010.02.006
– ident: e_1_2_6_47_1
  doi: 10.1104/pp.106.086637
– ident: e_1_2_6_37_1
  doi: 10.1023/A:1015553232309
– volume: 7
  start-page: 173
  year: 1995
  ident: e_1_2_6_42_1
  article-title: Ethylene‐inducible DNA binding proteins that interact with an ethylene‐responsive element
  publication-title: The Plant Cell
  contributor:
    fullname: Ohme‐Takagi M.
– ident: e_1_2_6_40_1
  doi: 10.1007/s10327-011-0355-5
– ident: e_1_2_6_9_1
  doi: 10.1094/MPMI.2004.17.10.1162
– ident: e_1_2_6_49_1
  doi: 10.1186/1471-2148-9-126
– ident: e_1_2_6_60_1
  doi: 10.1186/1471-2229-11-89
– ident: e_1_2_6_54_1
  doi: 10.1007/s00438-010-0580-1
– ident: e_1_2_6_58_1
  doi: 10.1046/j.1365-313x.1998.00243.x
– ident: e_1_2_6_68_1
  doi: 10.1371/journal.ppat.1000844
– ident: e_1_2_6_48_1
  doi: 10.1016/S1360-1385(03)00135-3
– ident: e_1_2_6_22_1
  doi: 10.1016/j.tplants.2006.01.004
– ident: e_1_2_6_52_1
  doi: 10.2307/3870231
– ident: e_1_2_6_67_1
  doi: 10.1111/j.1365-313X.2004.02180.x
– ident: e_1_2_6_39_1
  doi: 10.1038/ncomms1926
– ident: e_1_2_6_36_1
  doi: 10.1104/pp.105.073783
– ident: e_1_2_6_45_1
  doi: 10.1093/oxfordjournals.pcp.a029609
– ident: e_1_2_6_56_1
  doi: 10.1105/tpc.005348
– ident: e_1_2_6_8_1
  doi: 10.1046/j.1365-313X.1999.00426.x
– ident: e_1_2_6_15_1
  doi: 10.5511/plantbiotechnology.20.129
– ident: e_1_2_6_65_1
  doi: 10.1105/tpc.13.8.1877
– ident: e_1_2_6_31_1
  doi: 10.1094/MPMI-18-1027
– ident: e_1_2_6_4_1
  doi: 10.1104/pp.108.117887
– ident: e_1_2_6_12_1
  doi: 10.1105/tpc.000794
– ident: e_1_2_6_28_1
  doi: 10.1111/j.1365-313X.2004.02085.x
– ident: e_1_2_6_16_1
  doi: 10.1093/pcp/pcp048
– ident: e_1_2_6_14_1
  doi: 10.1046/j.1365-313X.2003.01759.x
– ident: e_1_2_6_57_1
  doi: 10.1038/nrmicro1239
– ident: e_1_2_6_34_1
  doi: 10.1016/j.bbagrm.2011.08.004
– ident: e_1_2_6_66_1
  doi: 10.1104/pp.109.135830
– ident: e_1_2_6_35_1
  doi: 10.1093/jxb/erm239
– ident: e_1_2_6_64_1
  doi: 10.1073/pnas.95.13.7433
– ident: e_1_2_6_61_1
  doi: 10.1016/0092-8674(94)90283-6
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Snippet Abstract We previously reported that one of the ethylene response factors ( ERF s), Nt ERF 3, and other members of the subgroup VIII ‐a ERF s of the AP 2/ ERF...
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