CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa
Abstract
Summary Lignin is the major phenolic polymer in plant secondary cell walls and is polymerized from monomeric subunits, the monolignols. Eleven enzyme families are implicated in monolignol biosynthesis. Here, we studied the functions of members of the cinnamyl alcohol dehydrogenase ( CAD ) and cinnamoyl‐CoA reductase ( CCR ) families in wood formation in Populus trichocarpa , including the regulatory effects of their transcripts and protein activities on monolignol biosynthesis. Enzyme activity assays from stem‐differentiating xylem ( SDX ) proteins showed that RNA i suppression of Ptr CAD 1 in P. trichocarpa transgenics caused a reduction in SDX CCR activity. RNA i suppression of Ptr CCR 2 , the only CCR member highly expressed in SDX , caused a reciprocal reduction in SDX protein CAD activities. The enzyme assays of mixed and coexpressed recombinant proteins supported physical interactions between Ptr CAD 1 and Ptr CCR 2. Biomolecular fluorescence complementation and pull‐down/co‐immunoprecipitation experiments supported a hypothesis of Ptr CAD 1/Ptr CCR 2 heterodimer formation. These results provide evidence for the formation of Ptr CAD 1/Ptr CCR 2 protein complexes in monolignol biosynthesis in planta .
- Authors:
-
- Chinese Academy of Forestry, Beijing (China)
- North Carolina State Univ., Raleigh, NC (United States)
- Univ. of Wisconsin, Madison, WI (United States)
- Northeast Forestry Univ., Harbin (China); Beihua Univ., Jilin (China)
- Northeast Forestry Univ., Harbin (China); National Taiwan Univ., Taipei (Taiwan)
- North Carolina State Univ., Raleigh, NC (United States); Northeast Forestry Univ., Harbin (China)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1506674
- Alternate Identifier(s):
- OSTI ID: 1479510
- Grant/Contract Number:
- SC0018409; BER DE‐FC02‐07ER64494; DE‐SC0018409
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 222; Journal Issue: 1; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; co‐immunoprecipitation; enzyme activity; monolignol biosynthetic pathway; nuclear magnetic resonance (NMR); Populus trichocarpa; stem‐differentiating xylem protein
Citation Formats
Yan, Xiaojing, Liu, Jie, Kim, Hoon, Liu, Baoguang, Huang, Xiong, Yang, Zhichang, Lin, Ying‐Chung Jimmy, Chen, Hao, Yang, Chenmin, Wang, Jack P., Muddiman, David C., Ralph, John, Sederoff, Ronald R., Li, Quanzi, and Chiang, Vincent L. CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa. United States: N. p., 2018.
Web. doi:10.1111/nph.15505.
Yan, Xiaojing, Liu, Jie, Kim, Hoon, Liu, Baoguang, Huang, Xiong, Yang, Zhichang, Lin, Ying‐Chung Jimmy, Chen, Hao, Yang, Chenmin, Wang, Jack P., Muddiman, David C., Ralph, John, Sederoff, Ronald R., Li, Quanzi, & Chiang, Vincent L. CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa. United States. https://doi.org/10.1111/nph.15505
Yan, Xiaojing, Liu, Jie, Kim, Hoon, Liu, Baoguang, Huang, Xiong, Yang, Zhichang, Lin, Ying‐Chung Jimmy, Chen, Hao, Yang, Chenmin, Wang, Jack P., Muddiman, David C., Ralph, John, Sederoff, Ronald R., Li, Quanzi, and Chiang, Vincent L. Mon .
"CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa". United States. https://doi.org/10.1111/nph.15505. https://www.osti.gov/servlets/purl/1506674.
@article{osti_1506674,
title = {CAD 1 and CCR 2 protein complex formation in monolignol biosynthesis in Populus trichocarpa},
author = {Yan, Xiaojing and Liu, Jie and Kim, Hoon and Liu, Baoguang and Huang, Xiong and Yang, Zhichang and Lin, Ying‐Chung Jimmy and Chen, Hao and Yang, Chenmin and Wang, Jack P. and Muddiman, David C. and Ralph, John and Sederoff, Ronald R. and Li, Quanzi and Chiang, Vincent L.},
abstractNote = {Summary Lignin is the major phenolic polymer in plant secondary cell walls and is polymerized from monomeric subunits, the monolignols. Eleven enzyme families are implicated in monolignol biosynthesis. Here, we studied the functions of members of the cinnamyl alcohol dehydrogenase ( CAD ) and cinnamoyl‐CoA reductase ( CCR ) families in wood formation in Populus trichocarpa , including the regulatory effects of their transcripts and protein activities on monolignol biosynthesis. Enzyme activity assays from stem‐differentiating xylem ( SDX ) proteins showed that RNA i suppression of Ptr CAD 1 in P. trichocarpa transgenics caused a reduction in SDX CCR activity. RNA i suppression of Ptr CCR 2 , the only CCR member highly expressed in SDX , caused a reciprocal reduction in SDX protein CAD activities. The enzyme assays of mixed and coexpressed recombinant proteins supported physical interactions between Ptr CAD 1 and Ptr CCR 2. Biomolecular fluorescence complementation and pull‐down/co‐immunoprecipitation experiments supported a hypothesis of Ptr CAD 1/Ptr CCR 2 heterodimer formation. These results provide evidence for the formation of Ptr CAD 1/Ptr CCR 2 protein complexes in monolignol biosynthesis in planta .},
doi = {10.1111/nph.15505},
journal = {New Phytologist},
number = 1,
volume = 222,
place = {United States},
year = {Mon Oct 01 00:00:00 EDT 2018},
month = {Mon Oct 01 00:00:00 EDT 2018}
}
Web of Science
Works referenced in this record:
Lignin Biosynthesis
journal, June 2003
- Boerjan, Wout; Ralph, John; Baucher, Marie
- Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546
Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees
journal, August 1999
- Hu, Wen-Jing; Harding, Scott A.; Lung, Jrhau
- Nature Biotechnology, Vol. 17, Issue 8, p. 808-812
Plant biotechnology for lignocellulosic biofuel production
journal, October 2014
- Li, Quanzi; Song, Jian; Peng, Shaobing
- Plant Biotechnology Journal, Vol. 12, Issue 9
Genetic Transformation of Populus trichocarpa Genotype Nisqually-1: A Functional Genomic Tool for Woody Plants
journal, November 2006
- Song, Jingyuan; Lu, Shanfa; Chen, Zenn-Zong
- Plant and Cell Physiology, Vol. 47, Issue 11, p. 1582-1589
Phosphorylation is an on/off switch for 5-hydroxyconiferaldehyde O -methyltransferase activity in poplar monolignol biosynthesis
journal, June 2015
- Wang, Jack P.; Chuang, Ling; Loziuk, Philip L.
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 27
Different Routes for Conifer- and Sinapaldehyde and Higher Saccharification upon Deficiency in the Dehydrogenase CAD1
journal, September 2017
- Van Acker, Rebecca; Déjardin, Annabelle; Desmet, Sandrien
- Plant Physiology, Vol. 175, Issue 3
Red Xylem and Higher Lignin Extractability by Down-Regulating a Cinnamyl Alcohol Dehydrogenase in Poplar
journal, December 1996
- Baucher, M.; Chabbert, B.; Pilate, G.
- Plant Physiology, Vol. 112, Issue 4
Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007
- Chen, Fang; Dixon, Richard A.
- Nature Biotechnology, Vol. 25, Issue 7, p. 759-761
Down-regulation of glycosyltransferase 8D genes in Populus trichocarpa caused reduced mechanical strength and xylan content in wood
journal, February 2011
- Li, Q.; Min, D.; Wang, J. P. -Y.
- Tree Physiology, Vol. 31, Issue 2
The origin and evolution of lignin biosynthesis: Tansley review
journal, June 2010
- Weng, Jing-Ke; Chapple, Clint
- New Phytologist, Vol. 187, Issue 2
Membrane protein complexes catalyze both 4- and 3-hydroxylation of cinnamic acid derivatives in monolignol biosynthesis
journal, December 2011
- Chen, H. -C.; Li, Q.; Shuford, C. M.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
GOLD HULL AND INTERNODE2 Encodes a Primarily Multifunctional Cinnamyl-Alcohol Dehydrogenase in Rice
journal, January 2006
- Zhang, Kewei; Qian, Qian; Huang, Zejun
- Plant Physiology, Vol. 140, Issue 3
Phenylalanine ammonia lyase and cinnamic acid hydroxylases as assembled consecutive enzymes on microsomal membranes of cucumber cotyledons: Cooperation and subcellular distribution
journal, January 1977
- Czichi, Ursula; Kindl, H.
- Planta, Vol. 134, Issue 2
Disrupting the cinnamyl alcohol dehydrogenase 1 gene ( BdCAD1 ) leads to altered lignification and improved saccharification in Brachypodium distachyon
journal, December 2012
- Bouvier d'Yvoire, Madeleine; Bouchabke-Coussa, Oumaya; Voorend, Wannes
- The Plant Journal, Vol. 73, Issue 3
Caffeoyl Shikimate Esterase (CSE) Is an Enzyme in the Lignin Biosynthetic Pathway in Arabidopsis
journal, August 2013
- Vanholme, R.; Cesarino, I.; Rataj, K.
- Science, Vol. 341, Issue 6150
Evidence for enzyme complexes in the phenylpropanoid and flavonoid pathways
journal, September 1999
- Winkel-Shirley, Brenda
- Physiologia Plantarum, Vol. 107, Issue 1
MYB103 is required for FERULATE-5-HYDROXYLASE expression and syringyl lignin biosynthesis in Arabidopsis stems
journal, October 2012
- Öhman, David; Demedts, Brecht; Kumar, Manoj
- The Plant Journal, Vol. 73, Issue 1
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
The biosynthesis of monolignols: a “metabolic grid”, or independent pathways to guaiacyl and syringyl units?
journal, August 2001
- Dixon, Richard A.; Chen, Fang; Guo, Dianjing
- Phytochemistry, Vol. 57, Issue 7
Pathways for monolignol biosynthesis via metabolic grids: coniferyl aldehyde 5-hydroxylase, a possible key enzyme in angiosperm syringyl lignin biosynthesis
journal, January 2003
- Higuchi, Takayoshi
- Proceedings of the Japan Academy, Series B, Vol. 79B, Issue 8
Identification of Grass-specific Enzyme That Acylates Monolignols with p-Coumarate
journal, January 2012
- Withers, Saunia; Lu, Fachuang; Kim, Hoon
- Journal of Biological Chemistry, Vol. 287, Issue 11, p. 8347-8355
Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis
journal, November 2010
- Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
- Trends in Plant Science, Vol. 15, Issue 11, p. 625-632
A standard reaction condition and a single HPLC separation system are sufficient for estimation of monolignol biosynthetic pathway enzyme activities
journal, June 2012
- Liu, Jie; Shi, Rui; Li, Quanzi
- Planta, Vol. 236, Issue 3
Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency): Marker for ferulic acid incorporation into lignins
journal, October 2007
- Ralph, John; Kim, Hoon; Lu, Fachuang
- The Plant Journal, Vol. 53, Issue 2
A Genomics Approach to Deciphering Lignin Biosynthesis in Switchgrass
journal, November 2013
- Shen, H.; Mazarei, M.; Hisano, H.
- The Plant Cell, Vol. 25, Issue 11
Lignin Biosynthesis and Structure
journal, May 2010
- Vanholme, R.; Demedts, B.; Morreel, K.
- Plant Physiology, Vol. 153, Issue 3, p. 895-905
Cross-Coupling of Hydroxycinnamyl Aldehydes into Lignins
journal, July 2000
- Kim, Hoon; Ralph, John; Yahiaoui, Nabila
- Organic Letters, Vol. 2, Issue 15
Towards a Systems Approach for Lignin Biosynthesis in Populus trichocarpa: Transcript Abundance and Specificity of the Monolignol Biosynthetic Genes
journal, December 2009
- Shi, Rui; Sun, Ying-Hsuan; Li, Quanzi
- Plant and Cell Physiology, Vol. 51, Issue 1
Inheritance, gene expression, and lignin characterization in a mutant pine deficient in cinnamyl alcohol dehydrogenase
journal, July 1997
- MacKay, J. J.; O'Malley, D. M.; Presnell, T.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 15
Colocalization of l-Phenylalanine Ammonia-Lyase and Cinnamate 4-Hydroxylase for Metabolic Channeling in Phenylpropanoid Biosynthesis
journal, October 2004
- Achnine, Lahoucine; Blancaflor, Elison B.; Rasmussen, Susanne
- The Plant Cell, Vol. 16, Issue 11
The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
journal, September 2006
- Tuskan, G. A.; DiFazio, S.; Jansson, S.
- Science, Vol. 313, Issue 5793, p. 1596-1604
Stress-Induced Phenylpropanoid Metabolism
journal, July 1995
- Dixon, Richard A.; Paiva, Nancy L.
- The Plant Cell, Vol. 7, Issue 7
Systems Biology of Lignin Biosynthesis in Populus trichocarpa : Heteromeric 4-Coumaric Acid:Coenzyme A Ligase Protein Complex Formation, Regulation, and Numerical Modeling
journal, March 2014
- Chen, Hsi-Chuan; Song, Jina; Wang, Jack P.
- The Plant Cell, Vol. 26, Issue 3
Phenylpropanoid biosynthesis and its regulation
journal, June 1998
- Weisshaar, Bernd; Jenkins, Gareth I.
- Current Opinion in Plant Biology, Vol. 1, Issue 3
Metabolic pathways as enzyme complexes: Evidence for the synthesis of phenylpropanoids and flavonoids on membrane associated enzyme complexes
journal, February 1985
- Hrazdina, Geza; Wagner, George J.
- Archives of Biochemistry and Biophysics, Vol. 237, Issue 1
Disruption of LACCASE4 and 17 Results in Tissue-Specific Alterations to Lignification of Arabidopsis thaliana Stems
journal, March 2011
- Berthet, Serge; Demont-Caulet, Nathalie; Pollet, Brigitte
- The Plant Cell, Vol. 23, Issue 3
Monolignol ferulate conjugates are naturally incorporated into plant lignins
journal, October 2016
- Karlen, Steven D.; Zhang, Chengcheng; Peck, Matthew L.
- Science Advances, Vol. 2, Issue 10
Downregulation of Cinnamoyl-Coenzyme A Reductase in Poplar: Multiple-Level Phenotyping Reveals Effects on Cell Wall Polymer Metabolism and Structure
journal, November 2007
- Leplé, Jean-Charles; Dauwe, Rebecca; Morreel, Kris
- The Plant Cell, Vol. 19, Issue 11
The cinnamate/monolignol pathway
journal, November 2009
- Umezawa, Toshiaki
- Phytochemistry Reviews, Vol. 9, Issue 1
Brown-midrib maize (bm1) - a mutation affecting the cinnamyl alcohol dehydrogenase gene
journal, June 1998
- Halpin, Claire; Holt, Karen; Chojecki, Jan
- The Plant Journal, Vol. 14, Issue 5
Comprehensive Quantification of Monolignol-Pathway Enzymes in Populus trichocarpa by Protein Cleavage Isotope Dilution Mass Spectrometry
journal, May 2012
- Shuford, Christopher M.; Li, Quanzi; Sun, Ying-Hsuan
- Journal of Proteome Research, Vol. 11, Issue 6
Stress-Induced Phenylpropanoid Metabolism.
journal, July 1995
- Dixon, R. A.; Paiva, N. L.
- The Plant Cell
Protein–Protein and Protein–Membrane Associations in the Lignin Pathway
journal, November 2012
- Bassard, Jean-Etienne; Richert, Ludovic; Geerinck, Jan
- The Plant Cell, Vol. 24, Issue 11
Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa
journal, June 2013
- Lu, S.; Li, Q.; Wei, H.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 26
NMR analysis of lignins in CAD-deficient plants. Part 1. Incorporation of hydroxycinnamaldehydes and hydroxybenzaldehydes into lignins
journal, December 2002
- Kim, Hoon; Ralph, John; Lu, Fachuang
- Organic & Biomolecular Chemistry, Vol. 1, Issue 2
Constitutively Elevated Salicylic Acid Levels Alter Photosynthesis and Oxidative State but Not Growth in Transgenic Populus
journal, July 2013
- Xue, L. -J.; Guo, W.; Yuan, Y.
- The Plant Cell, Vol. 25, Issue 7
Lignin biosynthesis perturbations affect secondary cell wall composition and saccharification yield in Arabidopsis thaliana
journal, January 2013
- Van Acker, Rebecca; Vanholme, Ruben; Storme, Véronique
- Biotechnology for Biofuels, Vol. 6, Article No. 46
Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation
journal, July 2007
- Nakagawa, Tsuyoshi; Kurose, Takayuki; Hino, Takeshi
- Journal of Bioscience and Bioengineering, Vol. 104, Issue 1
Splice variant of the SND1 transcription factor is a dominant negative of SND1 members and their regulation in Populus trichocarpa
journal, August 2012
- Li, Q.; Lin, Y. -C.; Sun, Y. -H.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 36
A simple improved-throughput xylem protoplast system for studying wood formation
journal, August 2014
- Lin, Ying-Chung; Li, Wei; Chen, Hao
- Nature Protocols, Vol. 9, Issue 9
Molecular Phenotyping of the pal1 and pal2 Mutants of Arabidopsis thaliana Reveals Far-Reaching Consequences on Phenylpropanoid, Amino Acid, and Carbohydrate Metabolism
journal, September 2004
- Rohde, Antje; Morreel, Kris; Ralph, John
- The Plant Cell, Vol. 16, Issue 10
Hydroxycinnamates in lignification
journal, August 2009
- Ralph, John
- Phytochemistry Reviews, Vol. 9, Issue 1, p. 65-83
Lignin engineering
journal, June 2008
- Vanholme, R.; Morreel, K.; Ralph, J.
- Current Opinion in Plant Biology, Vol. 11, Issue 3, p. 278-285
Complete Proteomic-Based Enzyme Reaction and Inhibition Kinetics Reveal How Monolignol Biosynthetic Enzyme Families Affect Metabolic Flux and Lignin in Populus trichocarpa
journal, March 2014
- Wang, Jack P.; Naik, Punith P.; Chen, Hsi-Chuan
- The Plant Cell, Vol. 26, Issue 3
Structural Alterations of Lignins in Transgenic Poplars with Depressed Cinnamyl Alcohol Dehydrogenase or Caffeic Acid O -Methyltransferase Activity Have an Opposite Impact on the Efficiency of Industrial Kraft Pulping
journal, January 1999
- Lapierre, Catherine; Pollet, Brigitte; Petit-Conil, Michel
- Plant Physiology, Vol. 119, Issue 1
Clarification of Cinnamoyl Co-enzyme A Reductase Catalysis in Monolignol Biosynthesis of Aspen
journal, July 2005
- Li, Laigeng; Cheng, Xiaofei; Lu, Shanfa
- Plant and Cell Physiology, Vol. 46, Issue 7
Syringyl lignin biosynthesis is directly regulated by a secondary cell wall master switch
journal, July 2010
- Zhao, Q.; Wang, H.; Yin, Y.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 32, p. 14496-14501
MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis
journal, January 2009
- Zhou, Jianli; Lee, Chanhui; Zhong, Ruiqin
- The Plant Cell, Vol. 21, Issue 1
Works referencing / citing this record:
Transcriptomic analysis of early fruit development in Chinese white pear (Pyrus bretschneideri Rehd.) and functional identification of PbCCR1 in lignin biosynthesis
journal, October 2019
- Su, Xueqiang; Zhao, Yu; Wang, Han
- BMC Plant Biology, Vol. 19, Issue 1
Enzymatic basis for C‐lignin monomer biosynthesis in the seed coat of Cleome hassleriana
journal, May 2019
- Zhuo, Chunliu; Rao, Xiaolan; Azad, Rajeev
- The Plant Journal, Vol. 99, Issue 3
Enzyme-Enzyme Interactions in Monolignol Biosynthesis
journal, January 2019
- Wang, Jack P.; Liu, Baoguang; Sun, Yi
- Frontiers in Plant Science, Vol. 9
Passive membrane transport of lignin-related compounds
journal, October 2019
- Vermaas, Josh V.; Dixon, Richard A.; Chen, Fang
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 46
Lignin biosynthesis: old roads revisited and new roads explored
journal, December 2019
- Dixon, Richard A.; Barros, Jaime
- Open Biology, Vol. 9, Issue 12
An introduction to a Virtual Issue on Wood Biology
journal, January 2020
- Groover, Andrew; Mansfield, Shawn D.
- New Phytologist, Vol. 225, Issue 4
Lignin biosynthesis: old roads revisited and new roads explored
journal, December 2019
- Dixon, Richard A.; Barros, Jaime
- Open Biology, Vol. 9, Issue 12
Transcriptomic analysis of early fruit development in Chinese white pear (Pyrus bretschneideri Rehd.) and functional identification of PbCCR1 in lignin biosynthesis
journal, October 2019
- Su, Xueqiang; Zhao, Yu; Wang, Han
- BMC Plant Biology, Vol. 19, Issue 1
Enzyme-Enzyme Interactions in Monolignol Biosynthesis
journal, January 2019
- Wang, Jack P.; Liu, Baoguang; Sun, Yi
- Frontiers in Plant Science, Vol. 9
Functional Characteristics of Caffeoyl Shikimate Esterase in Larix Kaempferi and Monolignol Biosynthesis in Gymnosperms
journal, December 2019
- Wang, Xuechun; Chao, Nan; Zhang, Meng
- International Journal of Molecular Sciences, Vol. 20, Issue 23