Xylem vessel‐specific SND5 and its homologs regulate secondary wall biosynthesis through activating secondary wall NAC binding elements

Zhong, Ruiqin; Lee, Chanhui; Haghighat, Marziyeh; Ye, Zheng‐Hua

doi:10.1111/nph.17425

Title: Xylem vessel‐specific SND5 and its homologs regulate secondary wall biosynthesis through activating secondary wall NAC binding elements

Journal Article · Fri Jun 18 00:00:00 EDT 2021 · New Phytologist

DOI:https://doi.org/10.1111/nph.17425· OSTI ID:1797599

Zhong, Ruiqin ^[1]; Lee, Chanhui ^[2]; Haghighat, Marziyeh ^[1];

^[1]

Department of Plant Biology University of Georgia Athens GA 30602 USA
Department of Plant Biology University of Georgia Athens GA 30602 USA, Department of Plant &, Environmental New Resources College of Life Sciences Kyung Hee University Yongin 17104 Republic of Korea

Summary Secondary cell wall biosynthesis has been shown to be regulated by a suite of transcription factors. Here, we identified a new xylem vessel‐specific NAC domain transcription factor, secondary wall‐associated NAC domain protein5 (SND5), in Arabidopsis thaliana and studied its role in regulating secondary wall biosynthesis. We showed that the expression of SND5 and its close homolog, SND4/ANAC075 , was specifically associated with secondary wall‐containing cells and dominant repression of their functions severely reduced secondary wall thickening in these cells. Overexpression of SND4/5 as well as their homologs SND2/3 fused with the activation domain of the viral protein VP16 led to ectopic secondary wall deposition in cells that are normally parenchymatous. SND2/3/4/5 regulated the expression of the same downstream target genes as do the secondary wall NAC master switches (SWNs) by binding to and activating the secondary wall NAC binding elements (SNBEs). Furthermore, we demonstrated that the poplar ( Populus trichocarpa ) orthologs of SND2/3/4/5 also activated SNBEs and regulated secondary wall biosynthesis during wood formation. Together, these findings indicate that SND2/3/4/5 and their poplar orthologs regulate the expression of secondary wall‐associated genes through activating SNBEs and they are positioned at an upper level in the SWN‐mediated transcriptional network.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: DE‐FG02‐03ER15415

OSTI ID:: 1797599

Journal Information:: New Phytologist, Journal Name: New Phytologist Vol. 231 Journal Issue: 4; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (39)

Reconstitution of a Secondary Cell Wall in a Secondary Cell Wall-Deficient Arabidopsis Mutant Sakamoto, Shingo; Mitsuda, Nobutaka Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu208	journal	December 2014
The Use of an Optical Brightener in the Study of Plant Structure Hughes, J.; McCully, Margaret E. Stain Technology, Vol. 50, Issue 5 https://doi.org/10.3109/10520297509117082	journal	January 1975
Involvement of VNS NAC-domain transcription factors in tracheid formation in Pinus taeda Akiyoshi, Nobuhiro; Nakano, Yoshimi; Sano, Ryosuke Tree Physiology, Vol. 40, Issue 6 https://doi.org/10.1093/treephys/tpz106	journal	December 2019
MYB83 Is a Direct Target of SND1 and Acts Redundantly with MYB46 in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis McCarthy, R. L.; Zhong, R.; Ye, Z. -H. Plant and Cell Physiology, Vol. 50, Issue 11 https://doi.org/10.1093/pcp/pcp139	journal	October 2009
Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death-related processes Farage-Barhom, S.; Burd, S.; Sonego, L. Journal of Experimental Botany, Vol. 59, Issue 12 https://doi.org/10.1093/jxb/ern176	journal	July 2008
Complexity of the transcriptional network controlling secondary wall biosynthesis Zhong, Ruiqin; Ye, Zheng-Hua Plant Science, Vol. 229 https://doi.org/10.1016/j.plantsci.2014.09.009	journal	December 2014
Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis Ko, Jae-Heung; Kim, Won-Chan; Han, Kyung-Hwan The Plant Journal, Vol. 60, Issue 4, p. 649-665 https://doi.org/10.1111/j.1365-313X.2009.03989.x	journal	November 2009
Monoclonal Antibodies to Plant Cell Wall Xylans and Arabinoxylans McCartney, Lesley; Marcus, Susan E.; Knox, J. Paul Journal of Histochemistry & Cytochemistry, Vol. 53, Issue 4 https://doi.org/10.1369/jhc.4B6578.2005	journal	April 2005
Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis Yoo, Sang-Dong; Cho, Young-Hee; Sheen, Jen Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.199	journal	June 2007
Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis Kim, Won-Chan; Ko, Jae-Heung; Han, Kyung-Hwan Plant Molecular Biology, Vol. 78, Issue 4-5 https://doi.org/10.1007/s11103-012-9880-7	journal	January 2012
MYB46-Mediated Transcriptional Regulation of Secondary Wall Biosynthesis Ko, Jae-Heung; Kim, Won-Chan; Kim, Joo-Yeol Molecular Plant, Vol. 5, Issue 5, p. 961-963 https://doi.org/10.1093/mp/sss076	journal	September 2012
OsSND2, a NAC family transcription factor, is involved in secondary cell wall biosynthesis through regulating MYBs expression in rice Ye, Yafeng; Wu, Kun; Chen, Jianfeng Rice, Vol. 11, Issue 1 https://doi.org/10.1186/s12284-018-0228-z	journal	May 2018
MYB20, MYB42, MYB43, and MYB85 Regulate Phenylalanine and Lignin Biosynthesis during Secondary Cell Wall Formation Geng, Pan; Zhang, Su; Liu, Jinyue Plant Physiology, Vol. 182, Issue 3 https://doi.org/10.1104/pp.19.01070	journal	December 2019
Dissection of the Transcriptional Program Regulating Secondary Wall Biosynthesis during Wood Formation in Poplar Zhong, Ruiqin; McCarthy, Ryan L.; Lee, Chanhui Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.181354	journal	September 2011
Transcriptional Regulation of Secondary Growth and Wood Formation Du, Juan; Groover, Andrew Journal of Integrative Plant Biology, Vol. 52, Issue 1 https://doi.org/10.1111/j.1744-7909.2010.00901.x	journal	January 2010
The MYB46 Transcription Factor Is a Direct Target of SND1 and Regulates Secondary Wall Biosynthesis in Arabidopsis Zhong, R.; Richardson, E. A.; Ye, Z.-H. The Plant Cell Online, Vol. 19, Issue 9, p. 2776-2792 https://doi.org/10.1105/tpc.107.053678	journal	September 2007
Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis Zhong, Ruiqin; Richardson, Elizabeth A.; Ye, Zheng-Hua Planta, Vol. 225, Issue 6 https://doi.org/10.1007/s00425-007-0498-y	journal	March 2007
Multiple Classes of Transcription Factors Regulate the Expression of VASCULAR-RELATED NAC-DOMAIN7, a Master Switch of Xylem Vessel Differentiation Endo, Hitoshi; Yamaguchi, Masatoshi; Tamura, Taizo Plant and Cell Physiology, Vol. 56, Issue 2 https://doi.org/10.1093/pcp/pcu134	journal	September 2014
Regulation of secondary wall synthesis and cell death by NAC transcription factors in the monocot Brachypodium distachyon Valdivia, Elene R.; Herrera, María Teresa; Gianzo, Cristina Journal of Experimental Botany, Vol. 64, Issue 5 https://doi.org/10.1093/jxb/ers394	journal	February 2013
MYB46 and MYB83 Bind to the SMRE Sites and Directly Activate a Suite of Transcription Factors and Secondary Wall Biosynthetic Genes Zhong, Ruiqin; Ye, Zheng-Hua Plant and Cell Physiology, Vol. 53, Issue 2 https://doi.org/10.1093/pcp/pcr185	journal	December 2011
Arabidopsis NAC Domain Proteins, VND1 to VND5, Are Transcriptional Regulators of Secondary Wall Biosynthesis in Vessels Zhou, Jianli; Zhong, Ruiqin; Ye, Zheng-Hua PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105726	journal	August 2014
Transcriptional Activation of Secondary Wall Biosynthesis by Rice and Maize NAC and MYB Transcription Factors Zhong, R.; Lee, C.; McCarthy, R. L. Plant and Cell Physiology, Vol. 52, Issue 10 https://doi.org/10.1093/pcp/pcr123	journal	September 2011
The Arabidopsis Xylem Peptidase XCP1 Is a Tracheary Element Vacuolar Protein That May Be a Papain Ortholog Funk, Vanessa; Kositsup, Boonthida; Zhao, Chengsong Plant Physiology, Vol. 128, Issue 1 https://doi.org/10.1104/pp.010514	journal	January 2002
NAC Transcription Factors, NST1 and NST3, Are Key Regulators of the Formation of Secondary Walls in Woody Tissues of Arabidopsis Mitsuda, N.; Iwase, A.; Yamamoto, H. The Plant Cell, Vol. 19, Issue 1, p. 270-280 https://doi.org/10.1105/tpc.106.047043	journal	January 2007
Regulation of secondary cell wall biosynthesis by a NAC transcription factor from Miscanthus Golfier, Philippe; Volkert, Christopher; He, Feng Plant Direct, Vol. 1, Issue 5 https://doi.org/10.1002/pld3.24	journal	November 2017
A NAC domain protein family contributing to the regulation of wood formation in poplar: NAC domain protein family regulates wood formation Ohtani, Misato; Nishikubo, Nobuyuki; Xu, Bo The Plant Journal, Vol. 67, Issue 3 https://doi.org/10.1111/j.1365-313X.2011.04614.x	journal	June 2011
Chimeric repressor of PtSND2 severely affects wood formation in transgenic Populus Wang, H. H.; Tang, R. J.; Liu, H. Tree Physiology, Vol. 33, Issue 8 https://doi.org/10.1093/treephys/tpt058	journal	August 2013
Global Analysis of Direct Targets of Secondary Wall NAC Master Switches in Arabidopsis Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua Molecular Plant, Vol. 3, Issue 6 https://doi.org/10.1093/mp/ssq062	journal	November 2010
A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis Zhong, R.; Lee, C.; Zhou, J. The Plant Cell, Vol. 20, Issue 10, p. 2763-2782 https://doi.org/10.1105/tpc.108.061325	journal	October 2008
Functional Characterization of Poplar Wood-Associated NAC Domain Transcription Factors Zhong, Ruiqin; Lee, Chanhui; Ye, Zheng-Hua Plant Physiology, Vol. 152, Issue 2 https://doi.org/10.1104/pp.109.148270	journal	December 2009
ANAC075, a putative regulator of VASCULAR-RELATED NAC-DOMAIN7, is a repressor of flowering Fujiwara, Sumire; Mitsuda, Nobutaka Plant Biotechnology, Vol. 33, Issue 4 https://doi.org/10.5511/plantbiotechnology.16.0215b	journal	January 2016
The NAC Transcription Factors NST1 and NST2 of Arabidopsis Regulate Secondary Wall Thickenings and Are Required for Anther Dehiscence Mitsuda, Nobutaka; Seki, Motoaki; Shinozaki, Kazuo The Plant Cell, Vol. 17, Issue 11 https://doi.org/10.1105/tpc.105.036004	journal	October 2005
VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots Yamaguchi, Masatoshi; Kubo, Minoru; Fukuda, Hiroo The Plant Journal, Vol. 55, Issue 4 https://doi.org/10.1111/j.1365-313X.2008.03533.x	journal	August 2008
Functional Characterization of NAC and MYB Transcription Factors Involved in Regulation of Biomass Production in Switchgrass (Panicum virgatum) Zhong, Ruiqin; Yuan, Youxi; Spiekerman, John J. PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0134611	journal	August 2015
Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis Hiratsu, Keiichiro; Matsui, Kyoko; Koyama, Tomotsugu The Plant Journal, Vol. 34, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01759.x	journal	June 2003
Transgenic poplars: expression of chimeric genes using four different constructs Leple, Jean Charles; Brasileiro, Ana Cristina Miranda; Michel, Marie France Plant Cell Reports, Vol. 11, Issue 3, p. 137-141 https://doi.org/10.1007/BF00232166	journal	April 1992
SND1, a NAC Domain Transcription Factor, Is a Key Regulator of Secondary Wall Synthesis in Fibers of Arabidopsis Zhong, Ruiqin; Demura, Taku; Ye, Zheng-Hua The Plant Cell, Vol. 18, Issue 11 https://doi.org/10.1105/tpc.106.047399	journal	November 2006
Transcription switches for protoxylem and metaxylem vessel formation Kubo, M. Genes & Development, Vol. 19, Issue 16 https://doi.org/10.1101/gad.1331305	journal	August 2005
MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis Zhou, Jianli; Lee, Chanhui; Zhong, Ruiqin The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.063321	journal	January 2009

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