Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Advances in the role of auxin for transcriptional regulation of lignin biosynthesis

Gaoyi Qu A , Dan Peng A B D , Ziqin Yu A , Xinling Chen A , Xinrui Cheng A , Youzhen Yang A , Tao Ye A , Qiang Lv A , Wenjun Ji A , Xiangwen Deng C and Bo Zhou https://orcid.org/0000-0002-7876-6888 A B C D E F
+ Author Affiliations
- Author Affiliations

A Faculty of Life Science and Biotechnology of Central South University of Forestry and Technology; 410004, Changsha, China.

B Huitong National Field Station for Scientific Observation and Research of Chinese Fir Plantation Ecosystem in Hunan Province, Huitong 438107, China.

C National Engineering Laboratory of Applied Technology for Forestry and Ecology in Southern China, Changsha 410004, Hunan, China.

D Forestry Biotechnology Hunan Key Laboratories, Hunan Changsha, 410004, China.

E Key Laboratory of Cultivation and Protection for Non-Wood Forest Trees, Ministry of Education, Central South University of Forestry and Technology, 410018, Changsha, China.

F Corresponding author. Email: zhoubo8888899999@163.com

Functional Plant Biology 48(8) 743-754 https://doi.org/10.1071/FP20381
Submitted: 11 December 2020  Accepted: 13 February 2021   Published: 5 March 2021

Abstract

Lignin is a natural polymer interlaced with cellulose and hemicellulose in secondary cell walls (SCWs). Auxin acts via its signalling transduction to regulate most of plant physiological processes. Lignification responds to auxin signals likewise and affects the development of anther and secondary xylem in plants. In this review, the research advances of AUXIN RESPONSE FACTOR (ARF)-dependent signalling pathways regulating lignin formation are discussed in detail. In an effort to facilitate the understanding of several key regulators in this process, we present a regulatory framework that comprises protein–protein interactions at the top and protein–gene regulation divided into five tiers. This characterises the regulatory roles of auxin in lignin biosynthesis and links auxin signalling transduction to transcriptional cascade of lignin biosynthesis. Our works further point to several of significant problems that need to be resolved in the future to gain a better understanding of the underlying mechanisms through which auxin regulates lignin biosynthesis.

Keywords: auxin, anther endothecium, lignin biosynthesis, vessels, protein–protein interactions, secondary xylem, secondary cell walls.


References

Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annual Review of Plant Biology 54, 519–546.
Lignin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 14503002PubMed |

Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annual Review of Genetics 44, 337–363.
The genetics of lignin biosynthesis: connecting genotype to phenotype.Crossref | GoogleScholarGoogle Scholar | 20809799PubMed |

Bonner LJ, Dickinson HG (1989) Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects. New Phytologist 113, 97–115.
Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects.Crossref | GoogleScholarGoogle Scholar |

Cecchetti V, Pomponi M, Altamura MM, Pezzotti M, Marsilio S, D’Angeli S, Tornielli GB, Costantino P, Cardarelli M (2004) Expression of rolB in tobacco flowers affects the coordinated processes of anther dehiscence and style elongation. The Plant Journal 38, 512–525.
Expression of rolB in tobacco flowers affects the coordinated processes of anther dehiscence and style elongation.Crossref | GoogleScholarGoogle Scholar | 15086797PubMed |

Cecchetti V, Altamura MM, Falasca G, Costantino P, Cardarelli M (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. The Plant Cell 20, 1760–1774.
Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation.Crossref | GoogleScholarGoogle Scholar | 18628351PubMed |

Cecchetti V, Altamura MM, Brunetti P, Petrocelli V, Falasca G, Ljung K, Costantino P, Cardarelli M (2013) Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. The Plant Journal 74, 411–422.
Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 23410518PubMed |

Didi V, Jackson P, Hejatko J (2015) Hormonal regulation of secondary cell wall formation. Journal of Experimental Botany 66, 5015–5027.
Hormonal regulation of secondary cell wall formation.Crossref | GoogleScholarGoogle Scholar | 26002972PubMed |

Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N, Yoneda A, Kato K, Kubo M, Kajita S, Katayama Y, et al (2015) Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant & Cell Physiology 56, 242–254.
Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation.Crossref | GoogleScholarGoogle Scholar |

Fu Y, Win P, Zhang H, Li C, Luo K (2019) PtrARF2.1 is involved in regulation of leaf development and lignin biosynthesis in poplar trees. International Journal of Molecular Sciences 20, 4141
PtrARF2.1 is involved in regulation of leaf development and lignin biosynthesis in poplar trees.Crossref | GoogleScholarGoogle Scholar |

Fukuda H (2010) Plant tracheary elements. In: Encyclopedia of life sciences (ELS). pp. 1–5. (John Wiley & Sons, Ltd: Chichester)

Fukuda H, Ohashi-Ito K (2019) Vascular tissue development in plants. Current Topics in Developmental Biology 131, 141–160.
Vascular tissue development in plants.Crossref | GoogleScholarGoogle Scholar | 30612615PubMed |

Ghelli R, Brunetti P, Napoli N, De Paolis A, Cecchetti V, Tsuge T, Serino G, Matsui M, Mele G, Rinaldi G (2018) A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis. The Plant Cell 30, 620–637.
A newly identified flower-specific splice variant of AUXIN RESPONSE FACTOR8 regulates stamen elongation and endothecium lignification in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29514943PubMed |

Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414, 271–276.
Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins.Crossref | GoogleScholarGoogle Scholar | 11713520PubMed |

Guilfoyle TJ, Hagen G (2007) Auxin response factors. Current Opinion in Plant Biology 10, 453–460.
Auxin response factors.Crossref | GoogleScholarGoogle Scholar | 17900969PubMed |

Huang H, Gao H, Liu B, Qi T, Tong J, Xiao L, Xie D, Song S (2017) Arabidopsis MYB24 regulates jasmonate-mediated stamen development. Frontiers in Plant Science 8, 1525
Arabidopsis MYB24 regulates jasmonate-mediated stamen development.Crossref | GoogleScholarGoogle Scholar | 28928760PubMed |

Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, Jones J, Tonelli C, Weisshaar B, Martin C (2000) Transcriptional repression by AtMYB4 controls production of UV‐protecting sunscreens in Arabidopsis. The EMBO Journal 19, 6150–6161.
Transcriptional repression by AtMYB4 controls production of UV‐protecting sunscreens in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11080161PubMed |

Keijzer CJ (1987) The processes of anther dehiscence and pollen dispersal. New Phytologist 105, 499–507.
The processes of anther dehiscence and pollen dispersal.Crossref | GoogleScholarGoogle Scholar |

Kim W-C, Ko J-H, Han K-H (2012) Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis. Plant Molecular Biology 78, 489–501.
Identification of a cis-acting regulatory motif recognized by MYB46, a master transcriptional regulator of secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 22271306PubMed |

Kim W-C, Kim J-Y, Ko J-H, Kang H, Han K-H (2014) Identification of direct targets of transcription factor MYB46 provides insights into the transcriptional regulation of secondary wall biosynthesis. Plant Molecular Biology 85, 589–599.
Identification of direct targets of transcription factor MYB46 provides insights into the transcriptional regulation of secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 24879533PubMed |

Ko J-H, Kim W-C, Han K-H (2009) Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis. The Plant Journal 60, 649–665.
Ectopic expression of MYB46 identifies transcriptional regulatory genes involved in secondary wall biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19674407PubMed |

Ko J-H, Kim W-C, Kim J-Y, Ahn S-J, Han K-H (2012) MYB46-mediated transcriptional regulation of secondary wall biosynthesis. Molecular Plant 5, 961–963.
MYB46-mediated transcriptional regulation of secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 22914575PubMed |

Ko J-H, Jeon H-W, Kim W-C, Kim J-Y, Han K-H (2014) The MYB46/MYB83-mediated transcriptional regulatory programme is a gatekeeper of secondary wall biosynthesis. Annals of Botany 114, 1099–1107.
The MYB46/MYB83-mediated transcriptional regulatory programme is a gatekeeper of secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 24984711PubMed |

Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes & Development 19, 1855–1860.
Transcription switches for protoxylem and metaxylem vessel formation.Crossref | GoogleScholarGoogle Scholar |

Lavy M, Estelle M (2016) Mechanisms of auxin signaling. Development 143, 3226–3229.
Mechanisms of auxin signaling.Crossref | GoogleScholarGoogle Scholar | 27624827PubMed |

Mandaokar A, Browse J (2009) MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis. Plant Physiology 149, 851–862.
MYB108 acts together with MYB24 to regulate jasmonate-mediated stamen maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19091873PubMed |

Mandaokar A, Thines B, Shin B, Markus Lange B, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. The Plant Journal 46, 984–1008.
Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling.Crossref | GoogleScholarGoogle Scholar | 16805732PubMed |

McCarthy RL, Zhong R, Ye Z-H (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant & Cell Physiology 50, 1950–1964.
MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

McCarthy RL, Zhong R, Ye Z-H (2011) Secondary wall NAC binding element (SNBE), a key cis-acting element required for target gene activation by secondary wall NAC master switches. Plant Signaling & Behavior 6, 1282–1285.
Secondary wall NAC binding element (SNBE), a key cis-acting element required for target gene activation by secondary wall NAC master switches.Crossref | GoogleScholarGoogle Scholar |

Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. The Plant Cell 17, 2993–3006.
The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence.Crossref | GoogleScholarGoogle Scholar | 16214898PubMed |

Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. The Plant Cell 19, 270–280.
NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17237351PubMed |

Mizuno S, Osakabe Y, Maruyama K, Ito T, Osakabe K, Sato T, Shinozaki K, Yamaguchi-Shinozaki K (2007) Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. The Plant Journal 50, 751–766.
Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 17419837PubMed |

Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Frontiers in Plant Science 6, 288
NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants.Crossref | GoogleScholarGoogle Scholar | 25999964PubMed |

Ohashi-Ito K, Iwamoto K, Fukuda H (2018) LOB DOMAIN-CONTAINING PROTEIN 15 positively regulates expression of VND7, a master regulator of tracheary elements. Plant & Cell Physiology 59, 989–996.
LOB DOMAIN-CONTAINING PROTEIN 15 positively regulates expression of VND7, a master regulator of tracheary elements.Crossref | GoogleScholarGoogle Scholar |

Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, et al (2005) Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. The Plant Cell 17, 444–463.
Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19.Crossref | GoogleScholarGoogle Scholar | 15659631PubMed |

Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of lbd/asl genes in Arabidopsis. The Plant Cell 19, 118
ARF7 and ARF19 regulate lateral root formation via direct activation of lbd/asl genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17259263PubMed |

Parish R (1969) Effects of indoleacetic acid on lignification in wheat internodes and in vitro. Australian Journal of Biological Sciences 22, 343–350.
Effects of indoleacetic acid on lignification in wheat internodes and in vitro.Crossref | GoogleScholarGoogle Scholar |

Piya S, Shrestha SK, Binder B, Stewart CN, Hewezi T (2014) Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science 5, 744
Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25566309PubMed |

Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. The Plant Journal 40, 979–995.
AtMYB32 is required for normal pollen development in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 15584962PubMed |

Raes J, Rohde A, Christensen JH, Van de Peer Y, Boerjan W (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiology 133, 1051–1071.
Genome-wide characterization of the lignification toolbox in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 14612585PubMed |

Salehin M, Bagchi R, Estelle M (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. The Plant Cell 27, 9–19.
SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development.Crossref | GoogleScholarGoogle Scholar | 25604443PubMed |

Sanchez P, Nehlin L, Greb T (2012) From thin to thick: major transitions during stem development. Trends in Plant Science 17, 113–121.
From thin to thick: major transitions during stem development.Crossref | GoogleScholarGoogle Scholar | 22189413PubMed |

Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction 11, 297–322.
Anther developmental defects in Arabidopsis thaliana male-sterile mutants.Crossref | GoogleScholarGoogle Scholar |

Scarpella E, Francis P, Berleth T (2004) Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation. Development 131, 3445–3455.
Stage-specific markers define early steps of procambium development in Arabidopsis leaves and correlate termination of vein formation with mesophyll differentiation.Crossref | GoogleScholarGoogle Scholar | 15226260PubMed |

Schaller F, Biesgen C, Müssig C, Altmann T, Weiler EW (2000) 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210, 979–984.
12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis.Crossref | GoogleScholarGoogle Scholar | 10872231PubMed |

Soyano T, Thitamadee S, Machida Y, Chua N-H (2008) Asymmetric leaves2-like19/lateral organ boundaries domain30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. The Plant Cell 20, 3359–3373.
Asymmetric leaves2-like19/lateral organ boundaries domain30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19088331PubMed |

Stafford HA (1965) Factors controlling the synthesis of natural and induced lignins in Phleum and Elodea. Plant Physiology 40, 844–851.
Factors controlling the synthesis of natural and induced lignins in Phleum and Elodea.Crossref | GoogleScholarGoogle Scholar | 16656164PubMed |

Takahama U, Oniki T (1994) The association of ascorbate and ascorbate oxidase in the apoplast with iaa-enhanced elongation of epicotyls from Vigna angularis. Plant & Cell Physiology 35, 257–266.

Tashiro S, Tian CE, Watahiki MK, Yamamoto KT (2009) Changes in growth kinetics of stamen filaments cause inefficient pollination in massugu2, an auxin insensitive, dominant mutant of Arabidopsis thaliana. Physiologia Plantarum 137, 175–187.
Changes in growth kinetics of stamen filaments cause inefficient pollination in massugu2, an auxin insensitive, dominant mutant of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 19719484PubMed |

Uggla C, Moritz T, Sandberg G, Sundberg B (1996) Auxin as a positional signal in pattern formation in plants. Proceedings of the National Academy of Sciences of the United States of America 93, 9282–9286.
Auxin as a positional signal in pattern formation in plants.Crossref | GoogleScholarGoogle Scholar | 11607701PubMed |

Ursache R, Nieminen K, Helariutta Y (2013) Genetic and hormonal regulation of cambial development. Physiologia Plantarum 147, 36–45.
Genetic and hormonal regulation of cambial development.Crossref | GoogleScholarGoogle Scholar | 22551327PubMed |

Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiology 153, 895–905.
Lignin biosynthesis and structure.Crossref | GoogleScholarGoogle Scholar | 20472751PubMed |

Vanholme R, De Meester B, Ralph J, Boerjan W (2019) Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology 56, 230–239.
Lignin biosynthesis and its integration into metabolism.Crossref | GoogleScholarGoogle Scholar | 30913460PubMed |

Wang H-Z, Dixon RA (2012) On–off switches for secondary cell wall biosynthesis. Molecular Plant 5, 297–303.
On–off switches for secondary cell wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 22138968PubMed |

Wang R, Estelle M (2014) Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway. Current Opinion in Plant Biology 21, 51–58.
Diversity and specificity: auxin perception and signaling through the TIR1/AFB pathway.Crossref | GoogleScholarGoogle Scholar | 25032902PubMed |

Wang H, Zhao Q, Chen F, Wang M, Dixon RA (2011) NAC domain function and transcriptional control of a secondary cell wall master switch. The Plant Journal 68, 1104–1114.
NAC domain function and transcriptional control of a secondary cell wall master switch.Crossref | GoogleScholarGoogle Scholar | 21883551PubMed |

Weijers D, Wagner D (2016) Transcriptional responses to the auxin hormone. Annual Review of Plant Biology 67, 539–574.
Transcriptional responses to the auxin hormone.Crossref | GoogleScholarGoogle Scholar | 26905654PubMed |

Wilson ZA, Song J, Taylor B, Yang C (2011) The final split: the regulation of anther dehiscence. Journal of Experimental Botany 62, 1633–1649.
The final split: the regulation of anther dehiscence.Crossref | GoogleScholarGoogle Scholar | 21325605PubMed |

Xie M, Zhang J, Tschaplinski TJ, Tuskan GA, Chen JG, Muchero W (2018) Regulation of lignin biosynthesis and its role in growth-defense tradeoffs. Frontiers in Plant Science 9, 1427
Regulation of lignin biosynthesis and its role in growth-defense tradeoffs.Crossref | GoogleScholarGoogle Scholar | 30323825PubMed |

Xu C, Shen Y, He F, Fu X, Yu H, Lu W, Li Y, Li C, Fan D, Wang HC (2019a) Auxin‐mediated Aux/IAA‐ARF‐HB signaling cascade regulates secondary xylem development in Populus. New Phytologist 222, 752–767.
Auxin‐mediated Aux/IAA‐ARF‐HB signaling cascade regulates secondary xylem development in Populus.Crossref | GoogleScholarGoogle Scholar |

Xu XF, Wang B, Feng YF, Xue JS, Qian XX, Liu SQ, Zhou J, Yu YH, Yang NY, Xu P, et al (2019b) AUXIN RESPONSE FACTOR17 directly regulates MYB108 for anther dehiscence. Plant Physiology 181, 645–655.
AUXIN RESPONSE FACTOR17 directly regulates MYB108 for anther dehiscence.Crossref | GoogleScholarGoogle Scholar | 31345954PubMed |

Yamaguchi M, Demura T (2010) Transcriptional regulation of secondary wall formation controlled by NAC domain proteins. Plant Biotechnology (Sheffield, England) 27, 237–242.
Transcriptional regulation of secondary wall formation controlled by NAC domain proteins.Crossref | GoogleScholarGoogle Scholar |

Yamaguchi M, Kubo M, Fukuda H, Demura T (2008a) VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. The Plant Journal 55, 652–664.
VASCULAR-RELATED NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots.Crossref | GoogleScholarGoogle Scholar | 18445131PubMed |

Yamaguchi M, Kubo M, Fukuda H, Demura T (2008b) Vascular‐related NAC‐DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. The Plant Journal 55, 652–664.
Vascular‐related NAC‐DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots.Crossref | GoogleScholarGoogle Scholar | 18445131PubMed |

Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. The Plant Journal 66, 579–590.
VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation.Crossref | GoogleScholarGoogle Scholar | 21284754PubMed |

Yang JH, Wang H (2016) Molecular mechanisms for vascular development and secondary cell wall formation. Frontiers in Plant Science 7, 356
Molecular mechanisms for vascular development and secondary cell wall formation.Crossref | GoogleScholarGoogle Scholar | 27047525PubMed |

Yang C, Xu Z, Song J, Conner K, Vizcay Barrena G, Wilson ZA (2007) Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence. The Plant Cell 19, 534–548.
Arabidopsis MYB26/MALE STERILE35 regulates secondary thickening in the endothecium and is essential for anther dehiscence.Crossref | GoogleScholarGoogle Scholar | 17329564PubMed |

Yang J, Tian L, Sun MX, Huang XY, Zhu J, Guan YF, Jia QS, Yang ZN (2013) AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiology 162, 720–731.
AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 23580594PubMed |

Yang C, Song J, Ferguson AC, Klisch D, Simpson K, Mo R, Taylor B, Mitsuda N, Wilson ZA (2017) Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation. Plant Physiology 175, 333–350.
Transcription factor MYB26 is key to spatial specificity in anther secondary thickening formation.Crossref | GoogleScholarGoogle Scholar | 28724622PubMed |

Yao W, Zhang D, Zhou B, Wang J, Li R, Jiang T (2020) Over-expression of poplar NAC15 gene enhances wood formation in transgenic tobacco. BMC Plant Biology 20, 12
Over-expression of poplar NAC15 gene enhances wood formation in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 31914923PubMed |

Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annual Review of Plant Biology 61, 49–64.
Auxin biosynthesis and its role in plant development.Crossref | GoogleScholarGoogle Scholar | 20192736PubMed |

Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends in Plant Science 16, 227–233.
Transcriptional networks for lignin biosynthesis: more complex than we thought?Crossref | GoogleScholarGoogle Scholar | 21227733PubMed |

Zhao J, Zhang W, Zhao Y, Gong X, Guo L, Zhu G, Wang X, Gong Z, Schumaker KS, Guo Y (2007) SAD2, an importin β-like protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking. The Plant Cell 19, 3805–3818.
SAD2, an importin β-like protein, is required for UV-B response in Arabidopsis by mediating MYB4 nuclear trafficking.Crossref | GoogleScholarGoogle Scholar | 17993626PubMed |

Zhong R, Ye ZH (2009) Transcriptional regulation of lignin biosynthesis. Plant Signaling & Behavior 4, 1028–1034.
Transcriptional regulation of lignin biosynthesis.Crossref | GoogleScholarGoogle Scholar |

Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant & Cell Physiology 53, 368–380.
MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes.Crossref | GoogleScholarGoogle Scholar |

Zhong R, Ye ZH (2014) Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Science 229, 193–207.
Complexity of the transcriptional network controlling secondary wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 25443846PubMed |

Zhong R, Ye ZH (2015a) The Arabidopsis NAC transcription factor NST2 functions together with SND1 and NST1 to regulate secondary wall biosynthesis in fibers of inflorescence stems. Plant Signaling & Behavior 10, e989746
The Arabidopsis NAC transcription factor NST2 functions together with SND1 and NST1 to regulate secondary wall biosynthesis in fibers of inflorescence stems.Crossref | GoogleScholarGoogle Scholar |

Zhong R, Ye ZH (2015b) Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation. Plant & Cell Physiology 56, 195–214.
Secondary cell walls: biosynthesis, patterned deposition and transcriptional regulation.Crossref | GoogleScholarGoogle Scholar |

Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. The Plant Cell 18, 3158–3170.
SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17114348PubMed |

Zhong R, Richardson EA, Ye ZH (2007a) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. The Plant Cell 19, 2776–2792.
The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17890373PubMed |

Zhong R, Richardson EA, Ye ZH (2007b) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225, 1603–1611.
Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17333250PubMed |

Zhong R, Lee C, Zhou J, McCarthy RL, Ye ZH (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. The Plant Cell 20, 2763–2782.
A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18952777PubMed |

Zhong R, Lee C, Ye ZH (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Molecular Plant 3, 1087–1103.
Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 20935069PubMed |

Zhong R, McCarthy RL, Lee C, Ye ZH (2011) Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar. Plant Physiology 157, 1452–1468.
Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar.Crossref | GoogleScholarGoogle Scholar | 21908685PubMed |

Zhong R, Cui D, Ye ZH (2019) Secondary cell wall biosynthesis. New Phytologist 221, 1703–1723.
Secondary cell wall biosynthesis.Crossref | GoogleScholarGoogle Scholar |

Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. The Plant Cell 21, 248–266.
MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 19122102PubMed |