Epigenetic regulation of lignin biosynthesis in wood formation

IF 8.3 1区 生物学 Q1 PLANT SCIENCES
New Phytologist Pub Date : 2024-12-05 DOI:10.1111/nph.20328
Hongyan Ma, Liwei Su, Wen Zhang, Yi Sun, Danning Li, Shuang Li, Ying-Chung Jimmy Lin, Chenguang Zhou, Wei Li
{"title":"Epigenetic regulation of lignin biosynthesis in wood formation","authors":"Hongyan Ma, Liwei Su, Wen Zhang, Yi Sun, Danning Li, Shuang Li, Ying-Chung Jimmy Lin, Chenguang Zhou, Wei Li","doi":"10.1111/nph.20328","DOIUrl":null,"url":null,"abstract":"<h2> Introduction</h2>\n<p>Lignin is a phenolic polymer and a major component of wood, constituting <i>c</i>. 20–30% of the wood biomass. It is the key limiting factor for wood conversion efficiency because it must be removed to extract the other two wood components, cellulose (40–50% of wood) and hemicelluloses (20–30% of wood), for paper making (Sarkanen, <span>1976</span>; Chiang, <span>2002</span>; Ragauskas <i>et al</i>., <span>2006</span>). Wood cellulose and hemicelluloses are potentially commercial feedstock for biofuel production (Sarkanen, <span>1976</span>). Lignin is synthesized through the polymerization of three canonical monolignols, <i>p</i>-coumaryl, coniferyl, and sinapyl alcohols, known as the <i>p</i>-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units, respectively (Freudenberg, <span>1965</span>; Sarkanen &amp; Ludwig, <span>1971</span>; Higuchi, <span>1997</span>). Monolignols are biosynthesized from phenylalanine through a complex network pathway mediated by &gt; 20 pathway enzymes. The mediation requires combined catalysis functions of individual enzymes (Higuchi, <span>1997</span>; Sulis <i>et al</i>., <span>2023</span>; Li <i>et al</i>., <span>2024</span>), enzyme complexes (Chen <i>et al</i>., <span>2011</span>, <span>2014</span>; Lin <i>et al</i>., <span>2015</span>; Yan <i>et al</i>., <span>2018</span>; X. Zhao <i>et al</i>., <span>2023</span>), and protein phosphorylation (Wang <i>et al</i>., <span>2015</span>) to produce monolignols for lignin polymerization.</p>\n<p>At the genetic level, the expression of genes encoding pathway enzymes controls monolignol production, affecting lignin biosynthesis and thus the recalcitrance of wood to conversion. Transregulation of monolignol gene expression has been extensively studied. Approximately 50 transcription factors (TFs) belonging to MYB, NAC, WRKY, ERF, WBLH, TZF, HSF, MADS-box, and LBD families have been implicated in such regulation (Supporting Information Table S1; Li <i>et al</i>., <span>2024</span>). Only a few TFs, such as PtoMYB221, PtrMYB092, PtrMYB161, PtrMYB189, PdMYB221/LTF1, BpNAC012, PtrHSFB3-1, and PagERF81, have been demonstrated to directly regulate monolignol biosynthesis genes (including <i>COMT2</i>, <i>CAld5H1</i>, <i>CAld5H2</i>, <i>CCoAOMT2</i>, <i>CCoAOMT1</i>, <i>4CL</i>5, <i>C3H3</i>, <i>C4H1</i>, <i>PAL2</i>, <i>PAL4</i>, <i>PAL5</i>, <i>CSE1</i>, <i>4CL1</i>, <i>CCR2</i>, and <i>CCR1</i>) (Tang <i>et al</i>., <span>2015</span>; Gui <i>et al</i>., <span>2019</span>; H. Chen <i>et al</i>., <span>2019</span>; Hu <i>et al</i>., <span>2019</span>; Wang <i>et al</i>., <span>2020</span>; Liu <i>et al</i>., <span>2021</span>; X. W. Zhao <i>et al</i>., <span>2023</span>). These TFs bind to the promoters of monolignol genes and interact with other regulators to exert activating or repressive effects on lignin biosynthesis.</p>\n<p>Gene expression can be controlled by histone modifications, including acetylation and methylation (Grunstein, <span>1997</span>; Berger, <span>2002</span>; Reyes <i>et al</i>., <span>2002</span>; Kouzarides, <span>2007</span>). Histone acetylation plays a crucial role in regulating gene expression during various developmental processes in plants. The dynamic balance of histone acetylation and deacetylation is regulated by histone acetyltransferases (HATs) (Balasubramanian <i>et al</i>., <span>2002</span>; Berger, <span>2002</span>) and histone deacetylases (HDAs or HDACs) (Roth &amp; Allis, <span>1996</span>; Kadosh &amp; Struhl, <span>1997</span>; Strahl &amp; Allis, <span>2000</span>). Histone acetylation is catalyzed by HAT complexes (Shahbazian &amp; Grunstein, <span>2007</span>), often containing GENERAL CONTROL NON-DEREPRESSIBLE5 (GCN5) as the catalytic subunit (Brownell <i>et al</i>., <span>1996</span>) and ALTERATION/DEFICIENCY IN ACTIVATION2 (ADA2) as an adaptor protein (Grant <i>et al</i>., <span>1997</span>). ADA2 enhances the HAT activity of GCN5 (Balasubramanian <i>et al</i>., <span>2002</span>). Conversely, histone deacetylation is catalyzed not only by HDAC corepressor complexes (Rundlett <i>et al</i>., <span>1996</span>; Long <i>et al</i>., <span>2006</span>; Gonzalez <i>et al</i>., <span>2007</span>; Krogan <i>et al</i>., <span>2012</span>; Hung <i>et al</i>., <span>2018</span>) but also primarily through direct interactions with certain transregulators (Liu <i>et al</i>., <span>2014</span>; W. Q. Chen <i>et al</i>., <span>2019</span>; Kumar <i>et al</i>., <span>2021</span>).</p>\n<p>Histone deacetylases were confirmed to suppress the expression of target genes (<i>FLC</i>, <i>MAF4</i>, <i>AGL19</i>, <i>AG</i>, <i>AP3</i>, <i>SEP3</i>, or <i>HSL1</i>) to regulate flowering time or development, or seed germination by interacting with various TFs and binding to these genes' promoters (Yu <i>et al</i>., <span>2011</span>; Krogan <i>et al</i>., <span>2012</span>; Kim <i>et al</i>., <span>2013</span>; Zhou <i>et al</i>., <span>2013</span>; Zeng <i>et al</i>., <span>2019</span>). These HDACs also respond to abiotic stresses, exhibiting similar regulatory functions (Kim <i>et al</i>., <span>2008</span>; Luo <i>et al</i>., <span>2012</span>; Mehdi <i>et al</i>., <span>2015</span>; Yang <i>et al</i>., <span>2020</span>). HDA15, an essential HDAC, plays distinct roles in various plant developmental processes. It specifically interacts with PIF3, playing a role in photomorphogenesis in <i>Arabidopsis</i> (Liu <i>et al</i>., <span>2013</span>). HDA15 forms a complex with the MYB96 protein to negatively regulate ABA signaling genes (<i>ROP6</i>, <i>ROP10</i>, and <i>ROP11</i>) by deacetylation H3 and H4 histones at their binding sites (Lee &amp; Seo, <span>2019</span>). However, the function of HDACs in regulating lignin biosynthesis remains largely unknown.</p>\n<p>In this study, we report the discovery of epigenetic regulation that represses lignin biosynthesis during wood formation in <i>Populus trichocarpa</i>. The HDAC PtrHDA15 acts as an epigenetic inhibitor and is recruited by the key wood-forming TF PtrbZIP44-A1 to the promoter of the target monolignol genes, <i>PtrCCoAOMT2</i> and <i>PtrCCR2</i>. This recruitment leads to chromatin histone modifications that suppress these genes, consequently reducing lignin content in wood.</p>","PeriodicalId":214,"journal":{"name":"New Phytologist","volume":"66 1","pages":""},"PeriodicalIF":8.3000,"publicationDate":"2024-12-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"New Phytologist","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1111/nph.20328","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Introduction

Lignin is a phenolic polymer and a major component of wood, constituting c. 20–30% of the wood biomass. It is the key limiting factor for wood conversion efficiency because it must be removed to extract the other two wood components, cellulose (40–50% of wood) and hemicelluloses (20–30% of wood), for paper making (Sarkanen, 1976; Chiang, 2002; Ragauskas et al., 2006). Wood cellulose and hemicelluloses are potentially commercial feedstock for biofuel production (Sarkanen, 1976). Lignin is synthesized through the polymerization of three canonical monolignols, p-coumaryl, coniferyl, and sinapyl alcohols, known as the p-hydroxyphenyl (H), guaiacyl (G), and syringyl (S) units, respectively (Freudenberg, 1965; Sarkanen & Ludwig, 1971; Higuchi, 1997). Monolignols are biosynthesized from phenylalanine through a complex network pathway mediated by > 20 pathway enzymes. The mediation requires combined catalysis functions of individual enzymes (Higuchi, 1997; Sulis et al., 2023; Li et al., 2024), enzyme complexes (Chen et al., 2011, 2014; Lin et al., 2015; Yan et al., 2018; X. Zhao et al., 2023), and protein phosphorylation (Wang et al., 2015) to produce monolignols for lignin polymerization.

At the genetic level, the expression of genes encoding pathway enzymes controls monolignol production, affecting lignin biosynthesis and thus the recalcitrance of wood to conversion. Transregulation of monolignol gene expression has been extensively studied. Approximately 50 transcription factors (TFs) belonging to MYB, NAC, WRKY, ERF, WBLH, TZF, HSF, MADS-box, and LBD families have been implicated in such regulation (Supporting Information Table S1; Li et al., 2024). Only a few TFs, such as PtoMYB221, PtrMYB092, PtrMYB161, PtrMYB189, PdMYB221/LTF1, BpNAC012, PtrHSFB3-1, and PagERF81, have been demonstrated to directly regulate monolignol biosynthesis genes (including COMT2, CAld5H1, CAld5H2, CCoAOMT2, CCoAOMT1, 4CL5, C3H3, C4H1, PAL2, PAL4, PAL5, CSE1, 4CL1, CCR2, and CCR1) (Tang et al., 2015; Gui et al., 2019; H. Chen et al., 2019; Hu et al., 2019; Wang et al., 2020; Liu et al., 2021; X. W. Zhao et al., 2023). These TFs bind to the promoters of monolignol genes and interact with other regulators to exert activating or repressive effects on lignin biosynthesis.

Gene expression can be controlled by histone modifications, including acetylation and methylation (Grunstein, 1997; Berger, 2002; Reyes et al., 2002; Kouzarides, 2007). Histone acetylation plays a crucial role in regulating gene expression during various developmental processes in plants. The dynamic balance of histone acetylation and deacetylation is regulated by histone acetyltransferases (HATs) (Balasubramanian et al., 2002; Berger, 2002) and histone deacetylases (HDAs or HDACs) (Roth & Allis, 1996; Kadosh & Struhl, 1997; Strahl & Allis, 2000). Histone acetylation is catalyzed by HAT complexes (Shahbazian & Grunstein, 2007), often containing GENERAL CONTROL NON-DEREPRESSIBLE5 (GCN5) as the catalytic subunit (Brownell et al., 1996) and ALTERATION/DEFICIENCY IN ACTIVATION2 (ADA2) as an adaptor protein (Grant et al., 1997). ADA2 enhances the HAT activity of GCN5 (Balasubramanian et al., 2002). Conversely, histone deacetylation is catalyzed not only by HDAC corepressor complexes (Rundlett et al., 1996; Long et al., 2006; Gonzalez et al., 2007; Krogan et al., 2012; Hung et al., 2018) but also primarily through direct interactions with certain transregulators (Liu et al., 2014; W. Q. Chen et al., 2019; Kumar et al., 2021).

Histone deacetylases were confirmed to suppress the expression of target genes (FLC, MAF4, AGL19, AG, AP3, SEP3, or HSL1) to regulate flowering time or development, or seed germination by interacting with various TFs and binding to these genes' promoters (Yu et al., 2011; Krogan et al., 2012; Kim et al., 2013; Zhou et al., 2013; Zeng et al., 2019). These HDACs also respond to abiotic stresses, exhibiting similar regulatory functions (Kim et al., 2008; Luo et al., 2012; Mehdi et al., 2015; Yang et al., 2020). HDA15, an essential HDAC, plays distinct roles in various plant developmental processes. It specifically interacts with PIF3, playing a role in photomorphogenesis in Arabidopsis (Liu et al., 2013). HDA15 forms a complex with the MYB96 protein to negatively regulate ABA signaling genes (ROP6, ROP10, and ROP11) by deacetylation H3 and H4 histones at their binding sites (Lee & Seo, 2019). However, the function of HDACs in regulating lignin biosynthesis remains largely unknown.

In this study, we report the discovery of epigenetic regulation that represses lignin biosynthesis during wood formation in Populus trichocarpa. The HDAC PtrHDA15 acts as an epigenetic inhibitor and is recruited by the key wood-forming TF PtrbZIP44-A1 to the promoter of the target monolignol genes, PtrCCoAOMT2 and PtrCCR2. This recruitment leads to chromatin histone modifications that suppress these genes, consequently reducing lignin content in wood.

求助全文
约1分钟内获得全文 求助全文
来源期刊
New Phytologist
New Phytologist 生物-植物科学
自引率
5.30%
发文量
728
期刊介绍: New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信