Mutation of Mediator subunit $CDK$ counteracts the stunted growth and salicylic acid hyperaccumulation phenotypes of an Arabidopsis $MED$ mutant
Abstract
Summary The Mediator complex functions as a hub for transcriptional regulation. MED 5, an Arabidopsis Mediator tail subunit, is required for maintaining phenylpropanoid homeostasis. A semidominant mutation ( ref4‐3 ) that causes a single amino acid substitution in MED 5b functions as a strong suppressor of the pathway, leading to decreased soluble phenylpropanoid accumulation, reduced lignin content and dwarfism. By contrast, loss of MED 5 results in increased concentrations of phenylpropanoids. We used a reverse genetic approach to identify suppressors of ref4‐3 and found that ref4‐3 requires CDK 8, a kinase module subunit of Mediator, to repress plant growth. The genetic interaction between MED 5 and CDK 8 was further characterized using m RNA ‐sequencing ( RNA ‐seq) and metabolite analysis. Growth inhibition and suppression of phenylpropanoid metabolism can be genetically separated in ref4‐3 by elimination of CDK 8 kinase activity; however, the stunted growth of ref4‐3 is not dependent on the phosphorylation event introduced by the G383S mutation. In addition, rather than perturbation of lignin biosynthesis, misregulation of DJC 66 , a gene encoding a DNAJ protein, is involved in the dwarfism of the med5 mutants. Together, our study reveals genetic interactions between Mediator tail and kinase module subunitsmore »
- Authors:
-
[1];
[2];
[4];
[1]
- Purdue Univ., West Lafayette, IN (United States). Dept. of Biochemistry; Purdue Univ., West Lafayette, IN (United States). Purdue Center for Plant Biology
- Purdue Univ., West Lafayette, IN (United States). Dept. of Biochemistry
- Purdue Univ., West Lafayette, IN (United States). Dept. of Biochemistry; Northwest Missouri State Univ., Maryville, MO (United States)
- Purdue Univ., West Lafayette, IN (United States). Dept. of Biochemistry; Purdue Univ., West Lafayette, IN (United States). Purdue University Center for Cancer Research
- Publication Date:
- Research Org.:
- Purdue Univ., West Lafayette, IN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1597908
- Alternate Identifier(s):
- OSTI ID: 1501715
- Grant/Contract Number:
- FG02-07ER15905
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 223; Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Mao, Xiangying, Kim, Jeong Im, Wheeler, Mitchell T., Heintzelman, Anne K., Weake, Vikki M., and Chapple, Clint. Mutation of Mediator subunit $CDK$ counteracts the stunted growth and salicylic acid hyperaccumulation phenotypes of an Arabidopsis $MED$ mutant. United States: N. p., 2019.
Web. doi:10.1111/nph.15741.
Mao, Xiangying, Kim, Jeong Im, Wheeler, Mitchell T., Heintzelman, Anne K., Weake, Vikki M., & Chapple, Clint. Mutation of Mediator subunit $CDK$ counteracts the stunted growth and salicylic acid hyperaccumulation phenotypes of an Arabidopsis $MED$ mutant. United States. https://doi.org/10.1111/nph.15741
Mao, Xiangying, Kim, Jeong Im, Wheeler, Mitchell T., Heintzelman, Anne K., Weake, Vikki M., and Chapple, Clint. Mon .
"Mutation of Mediator subunit $CDK$ counteracts the stunted growth and salicylic acid hyperaccumulation phenotypes of an Arabidopsis $MED$ mutant". United States. https://doi.org/10.1111/nph.15741. https://www.osti.gov/servlets/purl/1597908.
@article{osti_1597908,
title = {Mutation of Mediator subunit $CDK$ counteracts the stunted growth and salicylic acid hyperaccumulation phenotypes of an Arabidopsis $MED$ mutant},
author = {Mao, Xiangying and Kim, Jeong Im and Wheeler, Mitchell T. and Heintzelman, Anne K. and Weake, Vikki M. and Chapple, Clint},
abstractNote = {Summary The Mediator complex functions as a hub for transcriptional regulation. MED 5, an Arabidopsis Mediator tail subunit, is required for maintaining phenylpropanoid homeostasis. A semidominant mutation ( ref4‐3 ) that causes a single amino acid substitution in MED 5b functions as a strong suppressor of the pathway, leading to decreased soluble phenylpropanoid accumulation, reduced lignin content and dwarfism. By contrast, loss of MED 5 results in increased concentrations of phenylpropanoids. We used a reverse genetic approach to identify suppressors of ref4‐3 and found that ref4‐3 requires CDK 8, a kinase module subunit of Mediator, to repress plant growth. The genetic interaction between MED 5 and CDK 8 was further characterized using m RNA ‐sequencing ( RNA ‐seq) and metabolite analysis. Growth inhibition and suppression of phenylpropanoid metabolism can be genetically separated in ref4‐3 by elimination of CDK 8 kinase activity; however, the stunted growth of ref4‐3 is not dependent on the phosphorylation event introduced by the G383S mutation. In addition, rather than perturbation of lignin biosynthesis, misregulation of DJC 66 , a gene encoding a DNAJ protein, is involved in the dwarfism of the med5 mutants. Together, our study reveals genetic interactions between Mediator tail and kinase module subunits and enhances our understanding of dwarfing in phenylpropanoid pathway mutants.},
doi = {10.1111/nph.15741},
journal = {New Phytologist},
number = 1,
volume = 223,
place = {United States},
year = {Mon Mar 18 00:00:00 EDT 2019},
month = {Mon Mar 18 00:00:00 EDT 2019}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 16 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Linking development to defense: auxin in plant–pathogen interactions
journal, July 2009
- Kazan, Kemal; Manners, John M.
- Trends in Plant Science, Vol. 14, Issue 7
Mediator structure and rearrangements required for holoenzyme formation
journal, March 2017
- Tsai, Kuang-Lei; Yu, Xiaodi; Gopalan, Sneha
- Nature, Vol. 544, Issue 7649
Site-specific Srb10-dependent phosphorylation of the yeast Mediator subunit Med2 regulates gene expression from the 2- m plasmid
journal, February 2004
- Hallberg, M.; Polozkov, G. V.; Hu, G. -Z.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 10
Identification of Mediator Kinase Substrates in Human Cells using Cortistatin A and Quantitative Phosphoproteomics
journal, April 2016
- Poss, Zachary C.; Ebmeier, Christopher C.; Odell, Aaron T.
- Cell Reports, Vol. 15, Issue 2
Cyclin C/CDK8 and cyclin H/CDK7/p36 are biochemically distinct CTD kinases
journal, January 1999
- Rickert, Paula; Corden, Jeffry L.; Lees, Emma
- Oncogene, Vol. 18, Issue 4
Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance.
journal, October 1991
- Ward, E. R.; Uknes, S. J.; Williams, S. C.
- The Plant Cell
Salicylic acid mediates the reduced growth of lignin down-regulated plants
journal, November 2011
- Gallego-Giraldo, L.; Escamilla-Trevino, L.; Jackson, L. A.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 51
CYCLIN-DEPENDENT KINASE8 Differentially Regulates Plant Immunity to Fungal Pathogens through Kinase-Dependent and -Independent Functions in Arabidopsis
journal, October 2014
- Zhu, Yingfang; Schluttenhoffer, Craig M.; Wang, Pengcheng
- The Plant Cell, Vol. 26, Issue 10
Salicylic Acid Biosynthesis and Metabolism
journal, January 2011
- Dempsey, D'Maris Amick; Vlot, A. Corina; Wildermuth, Mary C.
- The Arabidopsis Book, Vol. 9
Growth–Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness
journal, August 2014
- Huot, Bethany; Yao, Jian; Montgomery, Beronda L.
- Molecular Plant, Vol. 7, Issue 8
Quantification of free and total salicylic acid in plants by solid-phase extraction and isocratic high-performance anion-exchange chromatography
journal, July 2005
- Rozhon, Wilfried; Petutschnig, Elena; Wrzaczek, Michael
- Analytical and Bioanalytical Chemistry, Vol. 382, Issue 7
Selective lignin downregulation leads to constitutive defense response expression in alfalfa (Medicago sativa L.)
journal, January 2011
- Gallego-Giraldo, Lina; Jikumaru, Yusuke; Kamiya, Yuji
- New Phytologist, Vol. 190, Issue 3
The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation
journal, October 2010
- Malik, Sohail; Roeder, Robert G.
- Nature Reviews Genetics, Vol. 11, Issue 11
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
journal, January 2002
- Edgar, R.
- Nucleic Acids Research, Vol. 30, Issue 1
Cyclin-dependent protein kinase and cyclin homologs SSN3 and SSN8 contribute to transcriptional control in yeast.
journal, April 1995
- Kuchin, S.; Yeghiayan, P.; Carlson, M.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 9
Suppression of wheat TaCDK8/TaWIN1 interaction negatively affects germination of Blumeria graminis f.sp. tritici by interfering with very-long-chain aldehyde biosynthesis
journal, December 2017
- Kong, Lingyao; Chang, Cheng
- Plant Molecular Biology, Vol. 96, Issue 1-2
Core Mediator structure at 3.4 Å extends model of transcription initiation complex
journal, May 2017
- Nozawa, Kayo; Schneider, Thomas R.; Cramer, Patrick
- Nature, Vol. 545, Issue 7653
The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function
journal, February 2009
- Knuesel, M. T.; Meyer, K. D.; Bernecky, C.
- Genes & Development, Vol. 23, Issue 4
Subunit Architecture and Functional Modular Rearrangements of the Transcriptional Mediator Complex
journal, June 2014
- Tsai, Kuang-Lei; Tomomori-Sato, Chieri; Sato, Shigeo
- Cell, Vol. 157, Issue 6
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
journal, December 2008
- Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A.
- Nature Protocols, Vol. 4, Issue 1
CDK8 kinase—An emerging target in targeted cancer therapy
journal, October 2015
- Rzymski, Tomasz; Mikula, Michał; Wiklik, Katarzyna
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1854, Issue 10
Auxin in action: signalling, transport and the control of plant growth and development
journal, September 2006
- Teale, William D.; Paponov, Ivan A.; Palme, Klaus
- Nature Reviews Molecular Cell Biology, Vol. 7, Issue 11
Evidence for Network Evolution in an Arabidopsis Interactome Map
journal, July 2011
- Dreze, M.; Carvunis, A. -R.; Charloteaux, B.
- Science, Vol. 333, Issue 6042
Arabidopsis AtGSTF2 is regulated by ethylene and auxin, and encodes a glutathione S-transferase that interacts with flavonoids
journal, November 2003
- Smith, Aaron P.; Nourizadeh, Saeid D.; Peer, Wendy A.
- The Plant Journal, Vol. 36, Issue 4
The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats
journal, January 1997
- Cao, Hui; Glazebrook, Jane; Clarke, Joseph D.
- Cell, Vol. 88, Issue 1
Indole Glucosinolate Biosynthesis Limits Phenylpropanoid Accumulation in Arabidopsis thaliana
journal, May 2015
- Kim, Jeong Im; Dolan, Whitney L.; Anderson, Nickolas A.
- The Plant Cell, Vol. 27, Issue 5
Poly(ADP-Ribose)Polymerase Activity Controls Plant Growth by Promoting Leaf Cell Number
journal, February 2014
- Schulz, Philipp; Jansseune, Karel; Degenkolbe, Thomas
- PLoS ONE, Vol. 9, Issue 2
yucca6 , a Dominant Mutation in Arabidopsis, Affects Auxin Accumulation and Auxin-Related Phenotypes
journal, September 2007
- Kim, Jeong Im; Sharkhuu, Altanbadralt; Jin, Jing Bo
- Plant Physiology, Vol. 145, Issue 3
HTSeq--a Python framework to work with high-throughput sequencing data
journal, September 2014
- Anders, S.; Pyl, P. T.; Huber, W.
- Bioinformatics, Vol. 31, Issue 2
The Role of the Anaphase-Promoting Complex/Cyclosome in Plant Growth
journal, September 2015
- Eloy, Nubia B.; de Freitas Lima, Marcelo; Ferreira, Paulo C. G.
- Critical Reviews in Plant Sciences, Vol. 34, Issue 5
Plant Mediator complex and its critical functions in transcription regulation: Plant Mediator complex and its function
journal, September 2015
- Yang, Yan; Li, Ling; Qu, Li-Jia
- Journal of Integrative Plant Biology, Vol. 58, Issue 2
The TRAP100 component of the TRAP/Mediator complex is essential in broad transcriptional events and development
journal, July 2002
- Ito, M.
- The EMBO Journal, Vol. 21, Issue 13
HUA ENHANCER3 reveals a role for a cyclin-dependent protein kinase in the specification of floral organ identity in Arabidopsis
journal, July 2004
- Wang, W.
- Development, Vol. 131, Issue 13
Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation
journal, January 2012
- McCarthy, Davis J.; Chen, Yunshun; Smyth, Gordon K.
- Nucleic Acids Research, Vol. 40, Issue 10
Semidominant Mutations in Reduced Epidermal Fluorescence 4 Reduce Phenylpropanoid Content in Arabidopsis
journal, April 2008
- Stout, Jake; Romero-Severson, Ethan; Ruegger, Max O.
- Genetics, Vol. 178, Issue 4
A conserved Mediator–CDK8 kinase module association regulates Mediator–RNA polymerase II interaction
journal, April 2013
- Tsai, Kuang-Lei; Sato, Shigeo; Tomomori-Sato, Chieri
- Nature Structural & Molecular Biology, Vol. 20, Issue 5
The two faces of Cdk8, a positive/negative regulator of transcription
journal, February 2014
- Nemet, Josipa; Jelicic, Branka; Rubelj, Ivica
- Biochimie, Vol. 97
Suppression of Mediator is regulated by Cdk8-dependent Grr1 turnover of the Med3 coactivator
journal, February 2014
- Gonzalez, D.; Hamidi, N.; Del Sol, R.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 7
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana
journal, December 1998
- Clough, Steven J.; Bent, Andrew F.
- The Plant Journal, Vol. 16, Issue 6, p. 735-743
Subunit Architecture and Functional Modular Rearrangements of the Transcriptional Mediator Complex
journal, July 2014
- Tsai, Kuang-Lei; Tomomori-Sato, Chieri; Sato, Shigeo
- Cell, Vol. 158, Issue 2
Conserved Structures of Mediator and RNA Polymerase II Holoenzyme
journal, February 1999
- Asturias, F. J.; Jiang, Y. W.; Myers, L. C.
- Science, Vol. 283, Issue 5404
Auxin-dependent compositional change in Mediator in ARF7- and ARF19-mediated transcription
journal, May 2016
- Ito, Jun; Fukaki, Hidehiro; Onoda, Makoto
- Proceedings of the National Academy of Sciences, Vol. 113, Issue 23
Mediator Complex Subunits MED2, MED5, MED16, and MED23 Genetically Interact in the Regulation of Phenylpropanoid Biosynthesis
journal, December 2017
- Dolan, Whitney L.; Dilkes, Brian P.; Stout, Jake M.
- The Plant Cell, Vol. 29, Issue 12
Evolution of Chloroplast J Proteins
journal, July 2013
- Chiu, Chi-Chou; Chen, Lih-Jen; Su, Pai-Hsiang
- PLoS ONE, Vol. 8, Issue 7
Function and regulation of the Mediator complex
journal, April 2011
- Conaway, Ronald C.; Conaway, Joan Weliky
- Current Opinion in Genetics & Development, Vol. 21, Issue 2
Temporal Regulation of RNA Polymerase II by Srb10 and Kin28 Cyclin-Dependent Kinases
journal, July 1998
- Hengartner, Christoph J.; Myer, Vic E.; Liao, Sha-Mei
- Molecular Cell, Vol. 2, Issue 1
Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant
journal, March 2014
- Bonawitz, Nicholas D.; Kim, Jeong Im; Tobimatsu, Yuki
- Nature, Vol. 509, Issue 7500, p. 376-380
A Complex of the Srb8, -9, -10, and -11 Transcriptional Regulatory Proteins from Yeast
journal, August 2002
- Borggrefe, Tilman; Davis, Ralph; Erdjument-Bromage, Hediye
- Journal of Biological Chemistry, Vol. 277, Issue 46
REF4 and RFR1, Subunits of the Transcriptional Coregulatory Complex Mediator, Are Required for Phenylpropanoid Homeostasis in Arabidopsis
journal, December 2011
- Bonawitz, Nicholas D.; Soltau, Whitney L.; Blatchley, Michael R.
- Journal of Biological Chemistry, Vol. 287, Issue 8
Cyclin-dependent Kinase E1 (CDKE1) Provides a Cellular Switch in Plants between Growth and Stress Responses
journal, December 2012
- Ng, Sophia; Giraud, Estelle; Duncan, Owen
- Journal of Biological Chemistry, Vol. 288, Issue 5
Signal perception and transduction in plant defense responses.
journal, July 1997
- Yang, Y.; Shah, J.; Klessig, D. F.
- Genes & Development, Vol. 11, Issue 13
Mutations That Reduce Sinapoylmalate Accumulation in Arabidopsis thaliana Define Loci With Diverse Roles in Phenylpropanoid Metabolism
journal, December 2001
- Ruegger, Max; Chapple, Clint
- Genetics, Vol. 159, Issue 4
Persistence of adoptively transferred T cells with a kinetically engineered IL-2 receptor agonist
journal, January 2020
- Parisi, Giulia; Saco, Justin D.; Salazar, Felix B.
- Nature Communications, Vol. 11, Issue 1
Coordinate Gene Activity in Response to Agents That Induce Systemic Acquired Resistance
journal, October 1991
- Ward, Eric R.; Uknes, Scott J.; Williams, Shericca C.
- The Plant Cell, Vol. 3, Issue 10
Works referencing / citing this record:
Arabidopsis MYB4 plays dual roles in flavonoid biosynthesis
journal, November 2019
- Wang, Xiao‐Chen; Wu, Jie; Guan, Meng‐Ling
- The Plant Journal, Vol. 101, Issue 3