Organelle-targeted biosensors reveal distinct oxidative events during pattern-triggered immune responses

被引:28
作者
Arnaud, Dominique [1 ]
Deeks, Michael J. [1 ]
Smirnoff, Nicholas [1 ]
机构
[1] Univ Exeter, Coll Life & Environm Sci, Biosci, Exeter EX4 4QD, Devon, England
基金
英国生物技术与生命科学研究理事会;
关键词
NADPH OXIDASE RBOHD; KINASE BIK1; ARABIDOPSIS; PEROXIDASE; DEFENSE; SIGNAL; ACCUMULATION; ATRBOHF; COMPLEX; SYSTEM;
D O I
10.1093/plphys/kiac603
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Reactive oxygen species are produced in response to pathogens and pathogen-associated molecular patterns, as exemplified by the rapid extracellular oxidative burst dependent on the NADPH oxidase isoform RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) in Arabidopsis (Arabidopsis thaliana). We used the H2O2 biosensor roGFP2-Orp1 and the glutathione redox state biosensor GRX1-roGFP2 targeted to various organelles to reveal unsuspected oxidative events during the pattern-triggered immune response to flagellin (flg22) and after inoculation with Pseudomonas syringae. roGFP2-Orp1 was oxidized in a biphasic manner 1 and 6 h after treatment, with a more intense and faster response in the cytosol compared to chloroplasts, mitochondria, and peroxisomes. Peroxisomal and cytosolic GRX1-roGFP2 were also oxidized in a biphasic manner. Interestingly, our results suggested that bacterial effectors partially suppress the second phase of roGFP2-Orp1 oxidation in the cytosol. Pharmacological and genetic analyses indicated that the pathogen-associated molecular pattern-induced cytosolic oxidation required the BRI1-ASSOCIATED RECEPTOR KINASE (BAK1) and BOTRYTIS-INDUCED KINASE 1 (BIK1) signaling components involved in the immune response but was largely independent of NADPH oxidases RBOHD and RESPIRATORY BURST OXIDASE HOMOLOG F (RBOHF) and apoplastic peroxidases peroxidase 33 (PRX33) and peroxidase 34 (PRX34). The initial apoplastic oxidative burst measured with luminol was followed by a second oxidation burst, both of which preceded the two waves of cytosolic oxidation. In contrast to the cytosolic oxidation, these bursts were RBOHD-dependent. Our results reveal complex oxidative sources and dynamics during the pattern-triggered immune response, including that cytosolic oxidation is largely independent of the preceding extracellular oxidation events.
引用
收藏
页码:2551 / 2569
页数:19
相关论文
共 65 条
[11]   A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence [J].
Chinchilla, Delphine ;
Zipfel, Cyril ;
Robatzek, Silke ;
Kemmerling, Birgit ;
Nuernberger, Thorsten ;
Jones, Jonathan D. G. ;
Felix, Georg ;
Boller, Thomas .
NATURE, 2007, 448 (7152) :497-U12
[12]   iNID: An Analytical Framework for Identifying Network Models for Interplays among Developmental Signaling in Arabidopsis [J].
Choi, Daeseok ;
Choi, Jaemyung ;
Kang, Byeongsoo ;
Lee, Seungchul ;
Cho, Young-hyun ;
Hwang, Ildoo ;
Hwang, Daehee .
MOLECULAR PLANT, 2014, 7 (05) :792-813
[13]   Floral dip:: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana [J].
Clough, SJ ;
Bent, AF .
PLANT JOURNAL, 1998, 16 (06) :735-743
[14]   Antioxidant status, peroxidase activity, and PR protein transcript levels in ascorbate-deficient Arabidopsis thaliana vtc mutants [J].
Colville, Louise ;
Smirnoff, Nicholas .
JOURNAL OF EXPERIMENTAL BOTANY, 2008, 59 (14) :3857-3868
[15]   The Apoplastic Oxidative Burst Peroxidase in Arabidopsis Is a Major Component of Pattern-Triggered Immunity [J].
Daudi, Arsalan ;
Cheng, Zhenyu ;
O'Brien, Jose A. ;
Mammarella, Nicole ;
Khan, Safina ;
Ausubel, Frederick M. ;
Bolwell, G. Paul .
PLANT CELL, 2012, 24 (01) :275-287
[16]   Nitric oxide functions as a signal in plant disease resistance [J].
Delledonne, M ;
Xia, YJ ;
Dixon, RA ;
Lamb, C .
NATURE, 1998, 394 (6693) :585-588
[17]   Arabidopsis peroxidase-catalyzed copolymerization of coniferyl and sinapyl alcohols: Kinetics of an endwise process [J].
Demont-Caulet, Nathalie ;
Lapierre, Catherine ;
Jouanin, Lise ;
Baumberger, Stephanie ;
Mechin, Valerie .
PHYTOCHEMISTRY, 2010, 71 (14-15) :1673-1683
[18]   A Golden Gate Modular Cloning Toolbox for Plants [J].
Engler, Carola ;
Youles, Mark ;
Gruetzner, Ramona ;
Ehnert, Tim-Martin ;
Werner, Stefan ;
Jones, Jonathan D. G. ;
Patron, Nicola J. ;
Marillonnet, Sylvestre .
ACS SYNTHETIC BIOLOGY, 2014, 3 (11) :839-843
[19]   Photosynthesis-dependent H2O2 transfer from chloroplasts to nuclei provides a high-light signalling mechanism [J].
Exposito-Rodriguez, Marino ;
Laissue, Pierre Philippe ;
Yvon-Durocher, Gabriel ;
Smirnoff, Nicholas ;
Mullineaux, Philip M. .
NATURE COMMUNICATIONS, 2017, 8
[20]   Arabidopsis Proline Dehydrogenase Contributes to Flagellin-Mediated PAMP-Triggered Immunity by Affecting RBOHD [J].
Fabro, Georgina ;
Soledad Rizzi, Yanina ;
Elena Alvarez, Maria .
MOLECULAR PLANT-MICROBE INTERACTIONS, 2016, 29 (08) :620-628