Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa
Abstract
Significance Wood is a widely used renewable feedstock for industrial production and energy generation. The secondary cell wall (SCW) is the major component of wood. Two key transcription factor families, Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND), are master gene regulators for SCW biosynthesis. However, plants exhibit stunted growth or abnormal SCW development under excess VND or SND gene expression. In this study, we show that two splice variants, PtrVND6-C1 IR and PtrSND1-A2 IR , each from VND and SND families, act as negative regulators. We propose that PtrVND6-C1 IR and PtrSND1-A2 IR function together for reciprocal cross-regulation of VND and SND families to maintain homeostasis for xylem differentiation and plant development.
- Authors:
-
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040 China,, Department of Life Sciences, College of Life Science, National Taiwan University, Taipei 10617, Taiwan,, Institute of Plant Biology, College of Life Science, National Taiwan University, Taipei 10617, Taiwan,, Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695,
- Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695,
- State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China,
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040 China,, Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695,
- Crop and Soil Sciences Department, North Carolina State University, Raleigh, NC 27695,
- Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC 27695,, College of Forestry, Fujian Agriculture and Forestry University, Fuzhou 350002, China,
- State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, 150040 China,
- Department of Forestry, National Chung Hsing University, Taichung 40227, Taiwan
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1402120
- Grant/Contract Number:
- SC000691
- Resource Type:
- Published Article
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Additional Journal Information:
- Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 114 Journal Issue: 45; Journal ID: ISSN 0027-8424
- Publisher:
- Proceedings of the National Academy of Sciences
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Lin, Ying-Chung Jimmy, Chen, Hao, Li, Quanzi, Li, Wei, Wang, Jack P., Shi, Rui, Tunlaya-Anukit, Sermsawat, Shuai, Peng, Wang, Zhifeng, Ma, Hongyan, Li, Huiyu, Sun, Ying-Hsuan, Sederoff, Ronald R., and Chiang, Vincent L. Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa. United States: N. p., 2017.
Web. doi:10.1073/pnas.1714422114.
Lin, Ying-Chung Jimmy, Chen, Hao, Li, Quanzi, Li, Wei, Wang, Jack P., Shi, Rui, Tunlaya-Anukit, Sermsawat, Shuai, Peng, Wang, Zhifeng, Ma, Hongyan, Li, Huiyu, Sun, Ying-Hsuan, Sederoff, Ronald R., & Chiang, Vincent L. Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa. United States. https://doi.org/10.1073/pnas.1714422114
Lin, Ying-Chung Jimmy, Chen, Hao, Li, Quanzi, Li, Wei, Wang, Jack P., Shi, Rui, Tunlaya-Anukit, Sermsawat, Shuai, Peng, Wang, Zhifeng, Ma, Hongyan, Li, Huiyu, Sun, Ying-Hsuan, Sederoff, Ronald R., and Chiang, Vincent L. Mon .
"Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa". United States. https://doi.org/10.1073/pnas.1714422114.
@article{osti_1402120,
title = {Reciprocal cross-regulation of VND and SND multigene TF families for wood formation in Populus trichocarpa},
author = {Lin, Ying-Chung Jimmy and Chen, Hao and Li, Quanzi and Li, Wei and Wang, Jack P. and Shi, Rui and Tunlaya-Anukit, Sermsawat and Shuai, Peng and Wang, Zhifeng and Ma, Hongyan and Li, Huiyu and Sun, Ying-Hsuan and Sederoff, Ronald R. and Chiang, Vincent L.},
abstractNote = {Significance Wood is a widely used renewable feedstock for industrial production and energy generation. The secondary cell wall (SCW) is the major component of wood. Two key transcription factor families, Vascular-Related NAC-Domain (VND) and Secondary Wall-Associated NAC Domain (SND), are master gene regulators for SCW biosynthesis. However, plants exhibit stunted growth or abnormal SCW development under excess VND or SND gene expression. In this study, we show that two splice variants, PtrVND6-C1 IR and PtrSND1-A2 IR , each from VND and SND families, act as negative regulators. We propose that PtrVND6-C1 IR and PtrSND1-A2 IR function together for reciprocal cross-regulation of VND and SND families to maintain homeostasis for xylem differentiation and plant development.},
doi = {10.1073/pnas.1714422114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 45,
volume = 114,
place = {United States},
year = {Mon Oct 23 00:00:00 EDT 2017},
month = {Mon Oct 23 00:00:00 EDT 2017}
}
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https://doi.org/10.1073/pnas.1714422114
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Works referenced in this record:
Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation
journal, October 2010
- Ohashi-Ito, Kyoko; Oda, Yoshihisa; Fukuda, Hiroo
- The Plant Cell, Vol. 22, Issue 10
Coordinated Activation of Cellulose and Repression of Lignin Biosynthesis Pathways in Rice
journal, December 2010
- Ambavaram, Madana M. R.; Krishnan, Arjun; Trijatmiko, Kurniawan R.
- Plant Physiology, Vol. 155, Issue 2
Tissue and cell-type co-expression networks of transcription factors and wood component genes in Populus trichocarpa
journal, January 2017
- Shi, Rui; Wang, Jack P.; Lin, Ying-Chung
- Planta, Vol. 245, Issue 5
A NAC transcription factor, EjNAC1 , affects lignification of loquat fruit by regulating lignin
journal, April 2015
- Xu, Qian; Wang, Wenqiu; Zeng, Jiaoke
- Postharvest Biology and Technology, Vol. 102
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
Emerging roles of long non-coding RNA in root developmental plasticity and regulation of phosphate homeostasis
journal, June 2015
- Bazin, Jeremie; Bailey-Serres, Julia
- Frontiers in Plant Science, Vol. 6
TopHat: discovering splice junctions with RNA-Seq
journal, March 2009
- Trapnell, Cole; Pachter, Lior; Salzberg, Steven L.
- Bioinformatics, Vol. 25, Issue 9
The Basic Helix-Loop-Helix Protein Family: Comparative Genomics and Phylogenetic Analysis
journal, May 2001
- Ledent, V.; Vervoort, M.
- Genome Research, Vol. 11, Issue 5
VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation: Direct target genes of VND7
journal, March 2011
- Yamaguchi, Masatoshi; Mitsuda, Nobutaka; Ohtani, Misato
- The Plant Journal, Vol. 66, Issue 4
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants
journal, May 2015
- Nakano, Yoshimi; Yamaguchi, Masatoshi; Endo, Hitoshi
- Frontiers in Plant Science, Vol. 6
Choose your partners: dimerization in eukaryotic transcription factors
journal, May 2008
- Amoutzias, Grigoris D.; Robertson, David L.; Van de Peer, Yves
- Trends in Biochemical Sciences, Vol. 33, Issue 5
A Self-Regulatory Circuit of CIRCADIAN CLOCK-ASSOCIATED1 Underlies the Circadian Clock Regulation of Temperature Responses in Arabidopsis
journal, June 2012
- Seo, Pil Joon; Park, Mi-Jeong; Lim, Mi-Hye
- The Plant Cell, Vol. 24, Issue 6
A NAC domain protein family contributing to the regulation of wood formation in poplar: NAC domain protein family regulates wood formation
journal, June 2011
- Ohtani, Misato; Nishikubo, Nobuyuki; Xu, Bo
- The Plant Journal, Vol. 67, Issue 3
Intron retention is a major phenomenon in alternative splicing in Arabidopsis
journal, September 2004
- Ner-Gaon, Hadas; Halachmi, Ronit; Savaldi-Goldstein, Sigal
- The Plant Journal, Vol. 39, Issue 6
SND1 Transcription Factor-Directed Quantitative Functional Hierarchical Genetic Regulatory Network in Wood Formation in Populus trichocarpa
journal, November 2013
- Lin, Y. -C.; Li, W.; Sun, Y. -H.
- The Plant Cell, Vol. 25, Issue 11
Competitive inhibition of transcription factors by small interfering peptides
journal, October 2011
- Seo, Pil Joon; Hong, Shin-Young; Kim, Sang-Gyu
- Trends in Plant Science, Vol. 16, Issue 10
Genomewide identification, classification and analysis of NAC type gene family in maize
journal, September 2015
- Peng, Xiaojian; Zhao, Yang; Li, Xiaoming
- Journal of Genetics, Vol. 94, Issue 3
In vitro xylem vessel elements formation from banana embryogenic cells and expression analysis of vessel development-related genes
journal, February 2015
- Negi, Sanjana; Tak, Himanshu; Ganapathi, T. R.
- Plant Biotechnology Reports, Vol. 9, Issue 2
The Role of Alternative Splicing in the Control of Immune Homeostasis and Cellular Differentiation
journal, December 2015
- Yabas, Mehmet; Elliott, Hannah; Hoyne, Gerard
- International Journal of Molecular Sciences, Vol. 17, Issue 1
SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis
journal, November 2006
- Zhong, Ruiqin; Demura, Taku; Ye, Zheng-Hua
- The Plant Cell, Vol. 18, Issue 11
A scaling normalization method for differential expression analysis of RNA-seq data
journal, March 2010
- Robinson, Mark D.; Oshlack, Alicia
- Genome Biology, Vol. 11, Issue 3, Article No. R25
Transcription switches for protoxylem and metaxylem vessel formation
journal, August 2005
- Kubo, M.
- Genes & Development, Vol. 19, Issue 16
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
Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta
journal, November 2008
- Waadt, Rainer; Schmidt, Lena K.; Lohse, Marc
- The Plant Journal, Vol. 56, Issue 3
Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration
journal, April 2012
- Thorvaldsdottir, H.; Robinson, J. T.; Mesirov, J. P.
- Briefings in Bioinformatics, Vol. 14, Issue 2, p. 178-192
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
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis
journal, June 2007
- Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen
- Nature Protocols, Vol. 2, Issue 7
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
Transcriptional repression in eukaryotes: repressors and repression mechanisms
journal, April 2003
- Gaston, K.; Jayaraman, P. -S.
- Cellular and Molecular Life Sciences (CMLS), Vol. 60, Issue 4
PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors
journal, October 2013
- Jin, Jinpu; Zhang, He; Kong, Lei
- Nucleic Acids Research, Vol. 42, Issue D1
ANAC012, a member of the plant-specific NAC transcription factor family, negatively regulates xylary fiber development in Arabidopsis thaliana: ANAC012 suppresses xylary fiber formation
journal, June 2007
- Ko, Jae-Heung; Yang, Seung Hwan; Park, Andrew H.
- The Plant Journal, Vol. 50, Issue 6
MicroProteins: small size – big impact
journal, August 2015
- Eguen, Tenai; Straub, Daniel; Graeff, Moritz
- Trends in Plant Science, Vol. 20, Issue 8
VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 Effectively Induce Transdifferentiation into Xylem Vessel Elements under Control of an Induction System
journal, May 2010
- Yamaguchi, Masatoshi; Goué, Nadia; Igarashi, Hisako
- Plant Physiology, Vol. 153, Issue 3
NAC domain function and transcriptional control of a secondary cell wall master switch: NST1 function and regulation
journal, October 2011
- Wang, Huanzhong; Zhao, Qiao; Chen, Fang
- The Plant Journal, Vol. 68, Issue 6
Function of alternative splicing
journal, February 2013
- Kelemen, Olga; Convertini, Paolo; Zhang, Zhaiyi
- Gene, Vol. 514, Issue 1
Renewable Resources for the Production of Fuels and Chemicals
journal, February 1976
- Sarkanen, K. V.
- Science, Vol. 191, Issue 4228
Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis
journal, November 2010
- Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua
- Molecular Plant, Vol. 3, Issue 6
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
Intron-Mediated Alternative Splicing of WOOD-ASSOCIATED NAC TRANSCRIPTION FACTOR1B Regulates Cell Wall Thickening during Fiber Development in Populus Species
journal, January 2014
- Zhao, Yunjun; Sun, Jiayan; Xu, Peng
- Plant Physiology, Vol. 164, Issue 2
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
A robust chromatin immunoprecipitation protocol for studying transcription factor–DNA interactions and histone modifications in wood-forming tissue
journal, August 2014
- Li, Wei; Lin, Ying-Chung; Li, Quanzi
- Nature Protocols, Vol. 9, Issue 9
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
Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors
journal, February 2004
- Ernst, Heidi A.; Nina Olsen, Addie; Skriver, Karen
- EMBO reports, Vol. 5, Issue 3
Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism
journal, May 2011
- Seo, Pil Joon; Kim, Mi Jung; Ryu, Jae-Yong
- Nature Communications, Vol. 2, Issue 1
Alternative splicing in plants – coming of age
journal, October 2012
- Syed, Naeem H.; Kalyna, Maria; Marquez, Yamile
- Trends in Plant Science, Vol. 17, Issue 10
Regulation of protein function by ‘microProteins’
journal, December 2010
- Staudt, Annica-Carolin; Wenkel, Stephan
- EMBO reports, Vol. 12, Issue 1
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Alternative splicing of transcription factors in plant responses to low temperature stress: mechanisms and functions
journal, April 2013
- Seo, Pil Joon; Park, Mi-Jeong; Park, Chung-Mo
- Planta, Vol. 237, Issue 6
Alternative splicing in plants: directing traffic at the crossroads of adaptation and environmental stress
journal, April 2015
- Filichkin, Sergei; Priest, Henry D.; Megraw, Molly
- Current Opinion in Plant Biology, Vol. 24
The WRKY superfamily of plant transcription factors
journal, May 2000
- Eulgem, Thomas; Rushton, Paul J.; Robatzek, Silke
- Trends in Plant Science, Vol. 5, Issue 5, p. 199-206