title: The Arabidopsis Mitochondrial Protease FtSH4 Is Involved in Leaf Senescence via Regulation of WRKY-Dependent Salicylic Acid Accumulation and Signaling.
abstract: Mitochondria and autophagy play important roles in the networks that regulate plant leaf senescence and cell death. However, the molecular mechanisms underlying the interactions between mitochondrial signaling and autophagy are currently not well understood. This study characterized the function of the Arabidopsis (Arabidopsis thaliana) mitochondrial AAA-protease geneFtSH4in regulating autophagy and senescence, finding that FtSH4 mediates WRKY-dependent salicylic acid (SA) accumulation and signaling. Knockout ofFtSH4in theftsh4-4mutant resulted in severe leaf senescence, cell death, and high autophagy levels. The level of SA increased dramatically in theftsh4-4mutant. Expression ofnahGin theftsh4-4mutant led to decreased SA levels and suppressed the leaf senescence and cell death phenotypes. The transcript levels of several SA synthesis and signaling genes, includingSALICYLIC ACIDINDUCTION DEFICIENT2(SID2),NON-RACE-SPECIFIC DISEASE RESISTANCE1(NDR1), andNONEXPRESSOR OF PATHOGENESIS-RELATED PROTEINS1(NPR1), increased significantly in theftsh4-4mutants compared with the wild type. Loss of function ofSID2,NDR1, orNPR1in theftsh4-4mutant reversed theftsh4-4senescence and autophagy phenotypes. Furthermore,ftsh4-4mutants had elevated levels of transcripts of severalWRKYgenes, includingWRKY40,WRKY46,WRKY51,WRKY60,WRKY63, andWRKY75; all of these WRKY proteins can bind to the promoter ofSID2Loss of function ofWRKY75in theftsh4-4mutants decreased the levels of SA and reversed the senescence phenotype. Taken together, these results suggest that the mitochondrial ATP-dependent protease FtSH4 may regulate the expression ofWRKYgenes by modifying the level of reactive oxygen species and the WRKY transcription factors that control SA synthesis and signaling in autophagy and senescence.
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Shengchun
authors.identifier: 0000-0001-5252-0524
authors.initials: S
authors.lastname: Zhang
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Cui
authors.initials: C
authors.lastname: Li
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Rui
authors.identifier: 0000-0003-1389-4763
authors.initials: R
authors.lastname: Wang
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Yaxue
authors.initials: Y
authors.lastname: Chen
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Si
authors.initials: S
authors.lastname: Shu
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Ruihua
authors.initials: R
authors.lastname: Huang
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Daowei
authors.initials: D
authors.lastname: Zhang
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Jian
authors.initials: J
authors.lastname: Li
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Shi
authors.identifier: 0000-0002-6632-8952
authors.initials: S
authors.lastname: Xiao
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.).
authors.forename: Nan
authors.identifier: 0000-0002-2045-5462
authors.initials: N
authors.lastname: Yao
authors.affiliation: Guangdong Key Laboratory of Biotechnology for Plant Development, College of Life Sciences, South China Normal University, Guangzhou 510631, China (S.Z., C.L., R.W., Y.C., S.S., R.H., D.Z. C.Y.); and yangchw@scnu.edu.cn.|State Key Laboratory of Biocontrol, Guangdong Provincial Key Laboratory of Plant Resources, Collaborative Innovation Center of Genetics and Development, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China (J.L., S.X., N.Y.) yangchw@scnu.edu.cn.
authors.forename: Chengwei
authors.identifier: 0000-0002-2648-3181
authors.initials: C
authors.lastname: Yang
mesh_terms: D017360:Arabidopsis / Q000166:cytology / Q000235:genetics / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001343:Autophagy / Q000235:genetics; D000071187:Autophagy-Related Protein 5; D000071190:Autophagy-Related Protein 8 Family; D016923:Cell Death / Q000235:genetics; D019751:Intramolecular Transferases / Q000235:genetics / Q000378:metabolism; D045726:Metalloproteases / Q000235:genetics / Q000378:metabolism*; D018613:Microscopy, Confocal; D024101:Mitochondrial Proteins / Q000235:genetics / Q000378:metabolism*; D006899:Mixed Function Oxygenases / Q000235:genetics / Q000378:metabolism; D009154:Mutation; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism* / Q000502:physiology; D011401:Promoter Regions, Genetic / Q000235:genetics; D011485:Protein Binding; D020133:Reverse Transcriptase Polymerase Chain Reaction; D020156:Salicylic Acid / Q000378:metabolism*; D015398:Signal Transduction; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*
chemical_list: C000597073:ATG8 protein, Arabidopsis; D029681:Arabidopsis Proteins; D000071187:Autophagy-Related Protein 5; D000071190:Autophagy-Related Protein 8 Family; D024101:Mitochondrial Proteins; C105496:NPR1 protein, Arabidopsis; D014157:Transcription Factors; C557639:WRKY51 protein, Arabidopsis; C544317:WRKY75 protein, Arabidopsis; D006899:Mixed Function Oxygenases; C022619:salicylate 1-monooxygenase; C518662:Atg5 protein, Arabidopsis; C506771:FtsH4 protein, Arabidopsis; D045726:Metalloproteases; D019751:Intramolecular Transferases; C058486:isochorismate synthase; D020156:Salicylic Acid