Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence

Leaf senescence is a developmentally programmed cell death process that is influenced by a variety of endogenous signals and environmental factors. Here, we report that MPK3 and MPK6, two Arabidopsis mitogen-activated protein kinases (MAPKs or MPKs), and their two upstream MAPK kinases (MAPKKs or MK...

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Main Authors: Hongjiao Wu, Qi Si, Jianmin Liu, Liuyi Yang, Shuqun Zhang, Juan Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.864986/full
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author Hongjiao Wu
Qi Si
Jianmin Liu
Liuyi Yang
Shuqun Zhang
Juan Xu
author_facet Hongjiao Wu
Qi Si
Jianmin Liu
Liuyi Yang
Shuqun Zhang
Juan Xu
author_sort Hongjiao Wu
collection DOAJ
description Leaf senescence is a developmentally programmed cell death process that is influenced by a variety of endogenous signals and environmental factors. Here, we report that MPK3 and MPK6, two Arabidopsis mitogen-activated protein kinases (MAPKs or MPKs), and their two upstream MAPK kinases (MAPKKs or MKKs), MKK4 and MKK5, are key regulators of leaf senescence. Weak induction of constitutively active MAPKKs driven by steroid-inducible promoter, which activates endogenous MPK3 and MPK6, induces leaf senescence. This gain-of-function phenotype requires functional endogenous MPK3 and MPK6. Furthermore, loss of function of both MKK4 and MKK5 delays leaf senescence. Expression profiling leads to the identification of matrix metalloproteinases (MMPs), a family of zinc- and calcium-dependent endopeptidases, as the downstream target genes of MPK3/MPK6 cascade. MPK3/MPK6 activation-triggered leaf senescence is associated with rapid and strong induction of At3-MMP and At2-MMP. Expression of Arabidopsis MMP genes is strongly induced during leaf senescence, qualifying them as senescence-associated genes (SAGs). In addition, either constitutive or inducible overexpression of At3-MMP is sufficient to trigger leaf senescence. Based on these findings, we conclude that MPK3/MPK6 MAPK cascade and MMP target genes further downstream are involved in regulating leaf senescence in Arabidopsis.
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spelling doaj.art-d42b70e18064419a92fc3f0489adaa2d2022-12-21T23:14:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-04-011310.3389/fpls.2022.864986864986Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf SenescenceHongjiao Wu0Qi Si1Jianmin Liu2Liuyi Yang3Shuqun Zhang4Juan Xu5State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaInterdisciplinary Plant Group, Division of Biochemistry, University of Missouri, Columbia, MO, United StatesState Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaLeaf senescence is a developmentally programmed cell death process that is influenced by a variety of endogenous signals and environmental factors. Here, we report that MPK3 and MPK6, two Arabidopsis mitogen-activated protein kinases (MAPKs or MPKs), and their two upstream MAPK kinases (MAPKKs or MKKs), MKK4 and MKK5, are key regulators of leaf senescence. Weak induction of constitutively active MAPKKs driven by steroid-inducible promoter, which activates endogenous MPK3 and MPK6, induces leaf senescence. This gain-of-function phenotype requires functional endogenous MPK3 and MPK6. Furthermore, loss of function of both MKK4 and MKK5 delays leaf senescence. Expression profiling leads to the identification of matrix metalloproteinases (MMPs), a family of zinc- and calcium-dependent endopeptidases, as the downstream target genes of MPK3/MPK6 cascade. MPK3/MPK6 activation-triggered leaf senescence is associated with rapid and strong induction of At3-MMP and At2-MMP. Expression of Arabidopsis MMP genes is strongly induced during leaf senescence, qualifying them as senescence-associated genes (SAGs). In addition, either constitutive or inducible overexpression of At3-MMP is sufficient to trigger leaf senescence. Based on these findings, we conclude that MPK3/MPK6 MAPK cascade and MMP target genes further downstream are involved in regulating leaf senescence in Arabidopsis.https://www.frontiersin.org/articles/10.3389/fpls.2022.864986/fullMAPK cascadematrix metalloproteinaseleaf senescenceArabidopsistranscription regulation
spellingShingle Hongjiao Wu
Qi Si
Jianmin Liu
Liuyi Yang
Shuqun Zhang
Juan Xu
Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
Frontiers in Plant Science
MAPK cascade
matrix metalloproteinase
leaf senescence
Arabidopsis
transcription regulation
title Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
title_full Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
title_fullStr Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
title_full_unstemmed Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
title_short Regulation of Arabidopsis Matrix Metalloproteinases by Mitogen-Activated Protein Kinases and Their Function in Leaf Senescence
title_sort regulation of arabidopsis matrix metalloproteinases by mitogen activated protein kinases and their function in leaf senescence
topic MAPK cascade
matrix metalloproteinase
leaf senescence
Arabidopsis
transcription regulation
url https://www.frontiersin.org/articles/10.3389/fpls.2022.864986/full
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AT jianminliu regulationofarabidopsismatrixmetalloproteinasesbymitogenactivatedproteinkinasesandtheirfunctioninleafsenescence
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