Mitogen-activated protein kinase 6 negatively regulates secondary wall biosynthesis by modulating MYB46 protein stability in Arabidopsis thaliana
Abstract
The R2R3-MYB transcription factor MYB46 functions as a master switch for secondary cell wall biosynthesis, ensuring the exquisite expression of the secondary wall biosynthetic genes in the tissues where secondary walls are critical for growth and development. At the same time, suppression of its function is needed when/where formation of secondary walls is not desirable. Little is known about how this opposing control of secondary cell wall formation is achieved. We used both transient and transgenic expression of MYB46 and mitogen-activated protein kinase 6 (MPK6) to investigate the molecular mechanism of the post-translational regulation of MYB46. We show that MYB46 is phosphorylated by MPK6, leading to site specific phosphorylation-dependent degradation of MYB46 by the ubiquitin-mediated proteasome pathway. In addition, the MPK6-mediated MYB46 phosphorylation was found to regulate in planta secondary wall forming function of MYB46. Furthermore, we provide experimental evidences that MYB83, a paralog of MYB46, is not regulated by MPK6. The coupling of MPK signaling to MYB46 function provides insights into the tissue- and/or condition-specific activity of MYB46 for secondary wall biosynthesis.
- Authors:
-
[2];
[4];
[4]
- Michigan State Univ., East Lansing, MI (United States); National Academy of Agricultural Science, Jeonju (Korea)
- Kyung Hee Univ., Gyeonggi-do (Korea)
- Kyungpook National Univ., Daegu (Korea)
- Michigan State Univ., East Lansing, MI (United States)
- Publication Date:
- Research Org.:
- Great Lakes Bioenergy Research Center (GLBRC), Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1804441
- Grant/Contract Number:
- SC0018409
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PLoS Genetics
- Additional Journal Information:
- Journal Volume: 17; Journal Issue: 4; Journal ID: ISSN 1553-7404
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Im, Jong Hee, Ko, Jae-Heung, Kim, Won-Chan, Crain, Brent, Keathley, Daniel, and Han, Kyung-Hwan. Mitogen-activated protein kinase 6 negatively regulates secondary wall biosynthesis by modulating MYB46 protein stability in Arabidopsis thaliana. United States: N. p., 2021.
Web. doi:10.1371/journal.pgen.1009510.
Im, Jong Hee, Ko, Jae-Heung, Kim, Won-Chan, Crain, Brent, Keathley, Daniel, & Han, Kyung-Hwan. Mitogen-activated protein kinase 6 negatively regulates secondary wall biosynthesis by modulating MYB46 protein stability in Arabidopsis thaliana. United States. https://doi.org/10.1371/journal.pgen.1009510
Im, Jong Hee, Ko, Jae-Heung, Kim, Won-Chan, Crain, Brent, Keathley, Daniel, and Han, Kyung-Hwan. Wed .
"Mitogen-activated protein kinase 6 negatively regulates secondary wall biosynthesis by modulating MYB46 protein stability in Arabidopsis thaliana". United States. https://doi.org/10.1371/journal.pgen.1009510. https://www.osti.gov/servlets/purl/1804441.
@article{osti_1804441,
title = {Mitogen-activated protein kinase 6 negatively regulates secondary wall biosynthesis by modulating MYB46 protein stability in Arabidopsis thaliana},
author = {Im, Jong Hee and Ko, Jae-Heung and Kim, Won-Chan and Crain, Brent and Keathley, Daniel and Han, Kyung-Hwan},
abstractNote = {The R2R3-MYB transcription factor MYB46 functions as a master switch for secondary cell wall biosynthesis, ensuring the exquisite expression of the secondary wall biosynthetic genes in the tissues where secondary walls are critical for growth and development. At the same time, suppression of its function is needed when/where formation of secondary walls is not desirable. Little is known about how this opposing control of secondary cell wall formation is achieved. We used both transient and transgenic expression of MYB46 and mitogen-activated protein kinase 6 (MPK6) to investigate the molecular mechanism of the post-translational regulation of MYB46. We show that MYB46 is phosphorylated by MPK6, leading to site specific phosphorylation-dependent degradation of MYB46 by the ubiquitin-mediated proteasome pathway. In addition, the MPK6-mediated MYB46 phosphorylation was found to regulate in planta secondary wall forming function of MYB46. Furthermore, we provide experimental evidences that MYB83, a paralog of MYB46, is not regulated by MPK6. The coupling of MPK signaling to MYB46 function provides insights into the tissue- and/or condition-specific activity of MYB46 for secondary wall biosynthesis.},
doi = {10.1371/journal.pgen.1009510},
journal = {PLoS Genetics},
number = 4,
volume = 17,
place = {United States},
year = {Wed Apr 07 00:00:00 EDT 2021},
month = {Wed Apr 07 00:00:00 EDT 2021}
}
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Works referenced in this record:
Biosynthesis of plant cell wall polysaccharides — a complex process
journal, December 2006
- Lerouxel, Olivier; Cavalier, David M.; Liepman, Aaron H.
- Current Opinion in Plant Biology, Vol. 9, Issue 6
MYB46-Mediated Transcriptional Regulation of Secondary Wall Biosynthesis
journal, September 2012
- Ko, Jae-Heung; Kim, Won-Chan; Kim, Joo-Yeol
- Molecular Plant, Vol. 5, Issue 5, p. 961-963
Identification of direct targets of transcription factor MYB46 provides insights into the transcriptional regulation of secondary wall biosynthesis
journal, May 2014
- Kim, Won-Chan; Kim, Joo-Yeol; Ko, Jae-Heung
- Plant Molecular Biology, Vol. 85, Issue 6
The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis
journal, September 2007
- Zhong, R.; Richardson, E. A.; Ye, Z.-H.
- The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792
Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis
journal, November 2009
- Ko, Jae-Heung; Kim, Won-Chan; Han, Kyung-Hwan
- The Plant Journal, Vol. 60, Issue 4, p. 649-665
MYB46 directly regulates the gene expression of secondary wall-associated cellulose synthases in Arabidopsis
journal, November 2012
- Kim, Won-Chan; Ko, Jae-Heung; Kim, Joo-Yeol
- The Plant Journal, Vol. 73, Issue 1
Transcription factor MYB46 is an obligate component of the transcriptional regulatory complex for functional expression of secondary wall-associated cellulose synthases in Arabidopsis thaliana
journal, October 2013
- Kim, Won-Chan; Kim, Joo-Yeol; Ko, Jae-Heung
- Journal of Plant Physiology, Vol. 170, Issue 15
Transcription factors that directly regulate the expression of CSLA9 encoding mannan synthase in Arabidopsis thaliana
journal, November 2013
- Kim, Won-Chan; Reca, Ida-Barbara; Kim, YongSig
- Plant Molecular Biology, Vol. 84, Issue 4-5
An Arabidopsis gene regulatory network for secondary cell wall synthesis
journal, December 2014
- Taylor-Teeples, M.; Lin, L.; de Lucas, M.
- Nature, Vol. 517, Issue 7536
Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins
journal, September 2000
- Wu, Yajun; Cosgrove, Daniel J.
- Journal of Experimental Botany, Vol. 51, Issue 350
Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6
journal, December 2000
- Ichimura, Kazuya; Mizoguchi, Tsuyoshi; Yoshida, Riichiro
- The Plant Journal, Vol. 24, Issue 5
MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays
journal, December 2008
- Popescu, S. C.; Popescu, G. V.; Bachan, S.
- Genes & Development, Vol. 23, Issue 1
Docking domains and substrate-specificity determination for MAP kinases
journal, September 2000
- Sharrocks, Andrew D.; Yang, Shen-His; Galanis, Alex
- Trends in Biochemical Sciences, Vol. 25, Issue 9
Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana
journal, August 2010
- Yu, Lijuan; Nie, Jianing; Cao, Chunyan
- New Phytologist, Vol. 188, Issue 3
Salt Stress in Arabidopsis: Lipid Transfer Protein AZI1 and Its Control by Mitogen-Activated Protein Kinase MPK3
journal, April 2014
- Pitzschke, Andrea; Datta, Sneha; Persak, Helene
- Molecular Plant, Vol. 7, Issue 4
A Mitogen-Activated Protein Kinase Cascade Module, MKK3-MPK6 and MYC2, Is Involved in Blue Light-Mediated Seedling Development in Arabidopsis
journal, August 2014
- Sethi, Vishmita; Raghuram, Badmi; Sinha, Alok Krishna
- The Plant Cell, Vol. 26, Issue 8
Proteasome inhibitors: valuable new tools for cell biologists
journal, October 1998
- Lee, Do Hee; Goldberg, Alfred L
- Trends in Cell Biology, Vol. 8, Issue 10, p. 397-403
MYB83 Is a Direct Target of SND1 and Acts Redundantly with MYB46 in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis
journal, October 2009
- McCarthy, R. L.; Zhong, R.; Ye, Z. -H.
- Plant and Cell Physiology, Vol. 50, Issue 11
Identification of Sites Required for Down-regulation of Na+/H+ Exchanger NHE3 Activity by cAMP-dependent Protein Kinase
journal, November 1997
- Kurashima, Kazuyoshi; Yu, Frank H.; Cabado, Ana G.
- Journal of Biological Chemistry, Vol. 272, Issue 45
Two Mitogen-Activated Protein Kinases, MPK3 and MPK6, Are Required for Funicular Guidance of Pollen Tubes in Arabidopsis
journal, April 2014
- Guan, Yuefeng; Lu, Jianping; Xu, Juan
- Plant Physiology, Vol. 165, Issue 2
Stomatal Development and Patterning Are Regulated by Environmentally Responsive Mitogen-Activated Protein Kinases in Arabidopsis
journal, January 2007
- Wang, Huachun; Ngwenyama, Njabulo; Liu, Yidong
- The Plant Cell, Vol. 19, Issue 1
The MKK2 Pathway Mediates Cold and Salt Stress Signaling in Arabidopsis
journal, July 2004
- Teige, Markus; Scheikl, Elisabeth; Eulgem, Thomas
- Molecular Cell, Vol. 15, Issue 1
Constitutively Active Mitogen-Activated Protein Kinase Versions Reveal Functions of Arabidopsis MPK4 in Pathogen Defense Signaling
journal, October 2012
- Berriri, Souha; Garcia, Ana Victoria; dit Frey, Nicolas Frei
- The Plant Cell, Vol. 24, Issue 10
High Throughput Identification of Potential Arabidopsis Mitogen-activated Protein Kinases Substrates
journal, October 2005
- Feilner, Tanja; Hultschig, Claus; Lee, Justin
- Molecular & Cellular Proteomics, Vol. 4, Issue 10
Ubiquitin and Proteasomes in Transcription
journal, July 2012
- Geng, Fuqiang; Wenzel, Sabine; Tansey, William P.
- Annual Review of Biochemistry, Vol. 81, Issue 1
Phosphorylation-Dependent Degradation of p300 by Doxorubicin-Activated p38 Mitogen-Activated Protein Kinase in Cardiac Cells
journal, April 2005
- Poizat, Coralie; Puri, Pier Lorenzo; Bai, Yan
- Molecular and Cellular Biology, Vol. 25, Issue 7
AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis
journal, May 2015
- Jeong, Eun-Young; Seo, Pil Joon; Woo, Je Chang
- BMC Plant Biology, Vol. 15, Issue 1
Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation
journal, February 2015
- Kawamoto, Nozomi; Sasabe, Michiko; Endo, Motomu
- Scientific Reports, Vol. 5, Issue 1
Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis
journal, April 2011
- Mao, Guohong; Meng, Xiangzong; Liu, Yidong
- The Plant Cell, Vol. 23, Issue 4
Phosphorylation of an ERF Transcription Factor by Arabidopsis MPK3/MPK6 Regulates Plant Defense Gene Induction and Fungal Resistance
journal, March 2013
- Meng, Xiangzong; Xu, Juan; He, Yunxia
- The Plant Cell, Vol. 25, Issue 3
Post-translational modification of an R2R3-MYB transcription factor by a MAP Kinase during xylem development
journal, September 2009
- Morse, Alison M.; Whetten, Ross W.; Dubos, Christian
- New Phytologist, Vol. 183, Issue 4
Phosphorylation-Coupled Proteolysis of the Transcription Factor MYC2 Is Important for Jasmonate-Signaled Plant Immunity
journal, April 2013
- Zhai, Qingzhe; Yan, Liuhua; Tan, Dan
- PLoS Genetics, Vol. 9, Issue 4
NAN fusions: a synthetic sialidase reporter gene as a sensitive and versatile partner for GUS
journal, November 2002
- Kirby, J.; Kavanagh, T. A.
- The Plant Journal, Vol. 32, Issue 3