Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis

Wang, Xiaoyu; Wang, Xianling; Hu, Qingnan; Dai, Xuemei; Tian, Hainan; Zheng, Kaijie; Wang, Xiaoping; Mao, Tonglin; Chen, Jin -Gui; Wang, Shucai

doi:10.1111/tpj.12887

Title: Characterization of an activation-tagged mutant uncovers a role of GLABRA2 in anthocyanin biosynthesis in Arabidopsis

Journal Article · Wed Jun 17 00:00:00 EDT 2015 · The Plant Journal

DOI:https://doi.org/10.1111/tpj.12887· OSTI ID:1286888

Wang, Xiaoyu ^[1]; Wang, Xianling ^[1]; Hu, Qingnan ^[1]; Dai, Xuemei ^[1]; Tian, Hainan ^[1]; Zheng, Kaijie ^[1]; Wang, Xiaoping ^[1]; Mao, Tonglin ^[2]; Chen, Jin -Gui ^[3]; Wang, Shucai ^[1]

Northeast Normal Univ., Jilin (China)
China Agricultural Univ., Beijing (China)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

In Arabidopsis, anthocyanin biosynthesis is controlled by a MYB-bHLH-WD40 (MBW) transcriptional activator complex. The MBW complex activates the transcription of late biosynthesis genes in the flavonoid pathway, leading to the production of anthocyanins. A similar MBW complex regulates epidermal cell fate by activating the transcription of GLABRA2 (GL2), a homeodomain transcription factor required for trichome formation in shoots and non-hair cell formation in roots. Here we provide experimental evidence to show that GL2 also plays a role in regulating anthocyanin biosynthesis in Arabidopsis. From an activation-tagged mutagenized population of Arabidopsis plants, we isolated a dominant, gain-of-function mutant with reduced anthocyanins. Molecular cloning revealed that this phenotype is caused by an elevated expression of GL2, thus the mutant was named gl2-1D. Consistent with the view that GL2 acts as a negative regulator of anthocyanin biosynthesis, gl2-1D seedlings accumulated less whereas gl2-3 seedlings accumulated more anthocyanins in response to sucrose. Gene expression analysis indicated that expression of late, but not early, biosynthesis genes in the flavonoid pathway was dramatically reduced in gl2-1D but elevated in gl2-3 mutants. Further analysis showed that expression of some MBW component genes involved in the regulation of late biosynthesis genes was reduced in gl2-1D but elevated in gl2-3 mutants, and chromatin immunoprecipitation results indicated that some MBW component genes are targets of GL2. We also showed that GL2 functions as a transcriptional repressor. Altogether, these results indicate that GL2 negatively regulates anthocyanin biosynthesis in Arabidopsis by directly repressing the expression of some MBW component genes.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Laboratory Directed Research and Development (LDRD) Program

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1286888

Journal Information:: The Plant Journal, Vol. 83, Issue 2; ISSN 0960-7412

Publisher:: Society for Experimental BiologyCopyright Statement

Country of Publication:: United States

Language:: English

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References (91)

Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins: Systematic analysis of MYB/BHLH-interactions Zimmermann, Ilona M.; Heim, Marc A.; Weisshaar, Bernd The Plant Journal, Vol. 40, Issue 1 https://doi.org/10.1111/j.1365-313X.2004.02183.x	journal	August 2004
Photoregulation of Anthocyanin Synthesis: VIII. Effect of Light Pretreatments Mancinelli, Alberto L. Plant Physiology, Vol. 75, Issue 2 https://doi.org/10.1104/pp.75.2.447	journal	June 1984
A Common Position-Dependent Mechanism Controls Cell-Type Patterning and GLABRA2 Regulation in the Root and Hypocotyl Epidermis of Arabidopsis Hung, Chen-Yi; Lin, Yan; Zhang, Meng Plant Physiology, Vol. 117, Issue 1 https://doi.org/10.1104/pp.117.1.73	journal	May 1998
Arabidopsis Transient Expression Analysis Reveals that Activation of GLABRA2 May Require Concurrent Binding of GLABRA1 and GLABRA3 to the Promoter of GLABRA2 Wang, S.; Chen, J. -G. Plant and Cell Physiology, Vol. 49, Issue 12 https://doi.org/10.1093/pcp/pcn159	journal	October 2008
Characterization of Flavonol Synthase and Leucoanthocyanidin Dioxygenase Genes in Arabidopsis (Further Evidence for Differential Regulation of "Early" and "Late" Genes) Pelletier, M. K.; Murrell, J. R.; Shirley, B. W. Plant Physiology, Vol. 113, Issue 4 https://doi.org/10.1104/pp.113.4.1437	journal	April 1997
TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis Schellmann, S.; Schnittger, A.; Kirik, V. The EMBO Journal, Vol. 21, Issue 19 https://doi.org/10.1093/emboj/cdf524	journal	October 2002
Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene Feinbaum, R. L.; Ausubel, F. M. Molecular and Cellular Biology, Vol. 8, Issue 5 https://doi.org/10.1128/mcb.8.5.1985-1992.1988	journal	May 1988
The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Rerie, W. G.; Feldmann, K. A.; Marks, M. D. Genes & Development, Vol. 8, Issue 12 https://doi.org/10.1101/gad.8.12.1388	journal	June 1994
Functional Properties of a Phenylalanine Ammonia-Lyase Promoter from Arabidopsis Ohl, Stephan; Hedrick, Susan A.; Chory, Joanne The Plant Cell, Vol. 2, Issue 9 https://doi.org/10.2307/3869320	journal	September 1990
A Genetic Regulatory Network in the Development of Trichomes and Root Hairs Ishida, Tetsuya; Kurata, Tetsuya; Okada, Kiyotaka Annual Review of Plant Biology, Vol. 59, Issue 1 https://doi.org/10.1146/annurev.arplant.59.032607.092949	journal	June 2008
Participation of the Arabidopsis bHLH Factor GL3 in Trichome Initiation Regulatory Events Morohashi, Kengo; Zhao, Mingzhe; Yang, Manli Plant Physiology, Vol. 145, Issue 3 https://doi.org/10.1104/pp.107.104521	journal	September 2007
Repression Domains of Class II ERF Transcriptional Repressors Share an Essential Motif for Active Repression Ohta, M. THE PLANT CELL ONLINE, Vol. 13, Issue 8 https://doi.org/10.1105/tpc.13.8.1959	journal	August 2001
Transcriptional control of flavonoid biosynthesis: Fine-tuning of the MYB-bHLH-WD40 (MBW) complex Li, Shutian Plant Signaling & Behavior, Vol. 9, Issue 1 https://doi.org/10.4161/psb.27522	journal	January 2014
AUX/IAA Proteins Are Active Repressors, and Their Stability and Activity Are Modulated by Auxin Tiwari, S. B. THE PLANT CELL ONLINE, Vol. 13, Issue 12 https://doi.org/10.1105/tpc.13.12.2809	journal	December 2001
An ankyrin repeat protein is involved in anthocyanin biosynthesis in Arabidopsis Yoo, Jihye; Shin, Dong Ho; Cho, Man-Ho Physiologia Plantarum, Vol. 142, Issue 4 https://doi.org/10.1111/j.1399-3054.2011.01468.x	journal	April 2011
CPC, a Single-Repeat R3 MYB, Is a Negative Regulator of Anthocyanin Biosynthesis in Arabidopsis Zhu, Hui-Fen; Fitzsimmons, Karen; Khandelwal, Abha Molecular Plant, Vol. 2, Issue 4 https://doi.org/10.1093/mp/ssp030	journal	July 2009
Pathways for Epidermal Cell Differentiation via the Homeobox Gene GLABRA2 : Update on the Roles of the Classic Regulator ^F Qing, Lin; Aoyama, Takashi Journal of Integrative Plant Biology, Vol. 54, Issue 10 https://doi.org/10.1111/j.1744-7909.2012.01159.x	journal	October 2012
Genetic dissection of trichome cell development in Arabidopsis Hülskamp, Martin; Miséra, Simon; Jürgens, Gerd Cell, Vol. 76, Issue 3 https://doi.org/10.1016/0092-8674(94)90118-X	journal	February 1994
cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis Won, Su-Kyung; Lee, Yong-Ju; Lee, Ha-Yeon Plant Physiology, Vol. 150, Issue 3 https://doi.org/10.1104/pp.109.140905	journal	May 2009
Structure and Mechanism of Anthocyanidin Synthase from Arabidopsis thaliana Wilmouth, Rupert C.; Turnbull, Jonathan J.; Welford, Richard W. D. Structure, Vol. 10, Issue 1 https://doi.org/10.1016/S0969-2126(01)00695-5	journal	January 2002
The bHLH genes GLABRA3 (GL3) andENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root Bernhardt, C. Development, Vol. 130, Issue 26 https://doi.org/10.1242/dev.00880	journal	December 2003
An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants Saleh, Abdelaty; Alvarez-Venegas, Raúl; Avramova, Zoya Nature Protocols, Vol. 3, Issue 6 https://doi.org/10.1038/nprot.2008.66	journal	May 2008
Regulation of epidermal cell fate in Arabidopsis roots: the importance of multiple feedback loops Schiefelbein, John; Huang, Ling; Zheng, Xiaohua Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00047	journal	January 2014
The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response Laby, Ron J.; Kincaid, M. Sean; Kim, Donggiun The Plant Journal, Vol. 23, Issue 5 https://doi.org/10.1046/j.1365-313x.2000.00833.x	journal	September 2000
Trichome Development in Arabidopsis thaliana. II. Isolation and Complementation of the GLABROUS1 Gene. Herman, P. L.; Marks, M. D. The Plant Cell https://doi.org/10.1105/tpc.1.11.1051	journal	November 1989
Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis Wang, Shucai; Hubbard, Leah; Chang, Ying BioMed Central https://doi.org/10.14288/1.0167730	text	January 2008
One, two, three…models for trichome patterning in Arabidopsis? Pesch, Marina; Hülskamp, Martin Current Opinion in Plant Biology, Vol. 12, Issue 5 https://doi.org/10.1016/j.pbi.2009.07.015	journal	October 2009
A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis Esch, J. J. Development, Vol. 130, Issue 24 https://doi.org/10.1242/dev.00812	journal	October 2003
The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci Zhao, M.; Morohashi, K.; Hatlestad, G. Development, Vol. 135, Issue 11 https://doi.org/10.1242/dev.016873	journal	April 2008
The Arabidopsis TT2 Gene Encodes an R2R3 MYB Domain Protein That Acts as a Key Determinant for Proanthocyanidin Accumulation in Developing Seed Nesi, Nathalie; Jond, Clarisse; Debeaujon, Isabelle The Plant Cell, Vol. 13, Issue 9 https://doi.org/10.1105/TPC.010098	journal	September 2001
Modulation of Phospholipid Signaling by GLABRA2 in Root-Hair Pattern Formation Ohashi, Y. Science, Vol. 300, Issue 5624 https://doi.org/10.1126/science.1083695	journal	May 2003
Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR Liu, Yao-Guang; Mitsukawa, Norihiro; Oosumi, Teruko The Plant Journal, Vol. 8, Issue 3 https://doi.org/10.1046/j.1365-313X.1995.08030457.x	journal	September 1995
Brassinosteroid Enhances Jasmonate-Induced Anthocyanin Accumulation in Arabidopsis Seedlings Peng, Zhihong; Han, Chengyun; Yuan, Libing Journal of Integrative Plant Biology, Vol. 53, Issue 8 https://doi.org/10.1111/j.1744-7909.2011.01042.x	journal	June 2011
Activation Tagging in Arabidopsis Weigel, Detlef; Ahn, Ji Hoon; Blázquez, Miguel A. Plant Physiology, Vol. 122, Issue 4 https://doi.org/10.1104/pp.122.4.1003	journal	April 2000
Cinnamate-4-Hydroxylase Expression in Arabidopsis (Regulation in Response to Development and the Environment) Bell-Lelong, D. A.; Cusumano, J. C.; Meyer, K. Plant Physiology, Vol. 113, Issue 3 https://doi.org/10.1104/pp.113.3.729	journal	March 1997
Trichome Development in Arabidopsis thaliana. II. Isolation and Complementation of the GLABROUS1 Gene Herman, Patricia L.; Marks, M. David The Plant Cell, Vol. 1, Issue 11 https://doi.org/10.2307/3869022	journal	November 1989
Regulation of cell fate determination by single-repeat R3 MYB transcription factors in Arabidopsis Wang, Shucai; Chen, Jin-Gui Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00133	journal	April 2014
Effects of Ionizing Radiation on a Plant Genome: Analysis of Two Arabidopsis transparent testa Mutations Shirley, Brenda W.; Hanley, Susan; Goodman, Howard M. The Plant Cell, Vol. 4, Issue 3 https://doi.org/10.2307/3869544	journal	March 1992
WEREWOLF, a MYB-Related Protein in Arabidopsis, Is a Position-Dependent Regulator of Epidermal Cell Patterning Lee, Myeong Min; Schiefelbein, John Cell, Vol. 99, Issue 5 https://doi.org/10.1016/S0092-8674(00)81536-6	journal	November 1999
Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings Gonzalez, Antonio; Zhao, Mingzhe; Leavitt, John M. The Plant Journal, Vol. 53, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03373.x	journal	March 2008
Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis Wang, Shucai; Li, Eryang; Porth, Ilga Scientific Reports, Vol. 4, Issue 1 https://doi.org/10.1038/srep05054	journal	May 2014
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana Clough, Steven J.; Bent, Andrew F. The Plant Journal, Vol. 16, Issue 6, p. 735-743 https://doi.org/10.1046/j.1365-313x.1998.00343.x	journal	December 1998
Activation Tagging Identifies a Conserved MYB Regulator of Phenylpropanoid Biosynthesis Borevitz, Justin O.; Xia, Yiji; Blount, Jack The Plant Cell, Vol. 12, Issue 12 https://doi.org/10.2307/3871236	journal	December 2000
The TT8 Gene Encodes a Basic Helix-Loop-Helix Domain Protein Required for Expression of DFR and BAN Genes in Arabidopsis Siliques Nesi, Nathalie; Debeaujon, Isabelle; Jond, Clarisse The Plant Cell, Vol. 12, Issue 10 https://doi.org/10.1105/tpc.12.10.1863	journal	October 2000
Control of trichome formation in Arabidopsis by poplar single-repeat R3 MYB transcription factors Zhou, Limei; Zheng, Kaijie; Wang, Xiaoyu Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00262	journal	June 2014
TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana Baudry, Antoine; Caboche, Michel; Lepiniec, Loïc The Plant Journal, Vol. 46, Issue 5 https://doi.org/10.1111/j.1365-313X.2006.02733.x	journal	June 2006
The TRANSPARENT TESTA GLABRA1 Locus, Which Regulates Trichome Differentiation and Anthocyanin Biosynthesis in Arabidopsis, Encodes a WD40 Repeat Protein Walker, Amanda R.; Davison, Paul A.; Bolognesi-Winfield, Agnese C. The Plant Cell, Vol. 11, Issue 7 https://doi.org/10.1105/tpc.11.7.1337	journal	July 1999
Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling: TFs of A. thaliana R2R3-MYB subgroup 7 Stracke, Ralf; Ishihara, Hirofumi; Huep, Gunnar The Plant Journal, Vol. 50, Issue 4 https://doi.org/10.1111/j.1365-313X.2007.03078.x	journal	April 2007
The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots Tominaga-Wada, Rumi; Iwata, Mineko; Sugiyama, Junji The Plant Journal, Vol. 60, Issue 3 https://doi.org/10.1111/j.1365-313X.2009.03976.x	journal	November 2009
The TT8 Gene Encodes a Basic Helix-Loop-Helix Domain Protein Required for Expression of DFR and BAN Genes in Arabidopsis Siliques Nesi, Nathalie; Debeaujon, Isabelle; Jond, Clarisse The Plant Cell, Vol. 12, Issue 10 https://doi.org/10.2307/3871198	journal	October 2000
REF4 and RFR1, Subunits of the Transcriptional Coregulatory Complex Mediator, Are Required for Phenylpropanoid Homeostasis in Arabidopsis Bonawitz, Nicholas D.; Soltau, Whitney L.; Blatchley, Michael R. Journal of Biological Chemistry, Vol. 287, Issue 8 https://doi.org/10.1074/jbc.M111.312298	journal	December 2011
TTG1 complex MYBs, MYB5 and TT2, control outer seed coat differentiation Gonzalez, Antonio; Mendenhall, John; Huo, Yujia Developmental Biology, Vol. 325, Issue 2 https://doi.org/10.1016/j.ydbio.2008.10.005	journal	January 2009
Recent advances on the regulation of anthocyanin synthesis in reproductive organs Petroni, Katia; Tonelli, Chiara Plant Science, Vol. 181, Issue 3 https://doi.org/10.1016/j.plantsci.2011.05.009	journal	September 2011
Distinct relationships between GLABRA2 and single-repeat R3 MYB transcription factors in the regulation of trichome and root hair patterning in Arabidopsis Wang, Shucai; Barron, Christa; Schiefelbein, John New Phytologist, Vol. 185, Issue 2 https://doi.org/10.1111/j.1469-8137.2009.03067.x	journal	October 2009
The TRANSPARENT TESTA GLABRA1 Locus, Which Regulates Trichome Differentiation and Anthocyanin Biosynthesis in Arabidopsis, Encodes a WD40 Repeat Protein Walker, Amanda R.; Davison, Paul A.; Bolognesi-Winfield, Agnese C. The Plant Cell, Vol. 11, Issue 7 https://doi.org/10.2307/3870753	journal	July 1999
Functional properties of a phenylalanine ammonia-lyase promoter from Arabidopsis. Ohl, S.; Hedrick, S. A.; Chory, J. The Plant Cell, Vol. 2, Issue 9 https://doi.org/10.1105/tpc.2.9.837	journal	September 1990
The Arabidopsis TDS4 gene encodes leucoanthocyanidin dioxygenase (LDOX) and is essential for proanthocyanidin synthesis and vacuole development Abrahams, Sharon; Lee, Elizabeth; Walker, Amanda R. The Plant Journal, Vol. 35, Issue 5 https://doi.org/10.1046/j.1365-313X.2003.01834.x	journal	September 2003
Transcriptional regulation of secondary metabolite biosynthesis in plants Patra, Barunava; Schluttenhofer, Craig; Wu, Yongmei Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1829, Issue 11 https://doi.org/10.1016/j.bbagrm.2013.09.006	journal	November 2013
A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis Bruex, Angela; Kainkaryam, Raghunandan M.; Wieckowski, Yana PLoS Genetics, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pgen.1002446	journal	January 2012
The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana Qi, Tiancong; Song, Susheng; Ren, Qingcuo The Plant Cell, Vol. 23, Issue 5 https://doi.org/10.1105/tpc.111.083261	journal	May 2011
The Arabidopsis thaliana 4-coumarate:CoA ligase (4CL) gene: stress and developmentally regulated expression and nucleotide sequence of its cDNA Lee, Diana; Ellard, Mary; Wanner, Leslie A. Plant Molecular Biology, Vol. 28, Issue 5 https://doi.org/10.1007/BF00042072	journal	August 1995
The Arabidopsis MYB5 Transcription Factor Regulates Mucilage Synthesis, Seed Coat Development, and Trichome Morphogenesis Li, Song Feng; Milliken, Olga Nicolaou; Pham, Hanh The Plant Cell, Vol. 21, Issue 1 https://doi.org/10.1105/tpc.108.063503	journal	January 2009
The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development Cristina, Manlio; Sessa, Giovanna; Dolan, Liam The Plant Journal, Vol. 10, Issue 3 https://doi.org/10.1046/j.1365-313X.1996.10030393.x	journal	September 1996
Complexity and robustness of the flavonoid transcriptional regulatory network revealed by comprehensive analyses of MYB-bHLH-WDR complexes and their targets in Arabidopsis seed Xu, Wenjia; Grain, Damaris; Bobet, Sophie New Phytologist, Vol. 202, Issue 1 https://doi.org/10.1111/nph.12620	journal	December 2013
Modulation of Cell Proliferation by Heterotrimeric G Protein in Arabidopsis Ullah, H. Science, Vol. 292, Issue 5524 https://doi.org/10.1126/science.1059040	journal	June 2001
A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis Zhang, F. Development, Vol. 130, Issue 20 https://doi.org/10.1242/dev.00681	journal	October 2003
Arabidopsis Ovate Family Protein 1 is a transcriptional repressor that suppresses cell elongation: AtOFP1 suppresses cell elongation Wang, Shucai; Chang, Ying; Guo, Jianjun The Plant Journal, Vol. 50, Issue 5 https://doi.org/10.1111/j.1365-313X.2007.03096.x	journal	April 2007
Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis Wang, Shucai; Hubbard, Leah; Chang, Ying BMC Plant Biology, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2229-8-81	journal	January 2008
Role of Anthocyanidin Reductase, Encoded by BANYULS in Plant Flavonoid Biosynthesis Xie, D. -Y. Science, Vol. 299, Issue 5605 https://doi.org/10.1126/science.1078540	journal	January 2003
Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. Shirley, B. W.; Hanley, S.; Goodman, H. M. The Plant Cell, Vol. 4, Issue 3 https://doi.org/10.1105/tpc.4.3.333	journal	March 1992
The Arabidopsis Transcription Factor MYB12 Is a Flavonol-Specific Regulator of Phenylpropanoid Biosynthesis Mehrtens, Frank; Kranz, Harald; Bednarek, Pawel Plant Physiology, Vol. 138, Issue 2 https://doi.org/10.1104/pp.104.058032	journal	May 2005
Ethylene Suppression of Sugar-Induced Anthocyanin Pigmentation in Arabidopsis Jeong, Seok-Won; Das, Prasanta Kumar; Jeoung, Sae Chae Plant Physiology, Vol. 154, Issue 3 https://doi.org/10.1104/pp.110.161869	journal	September 2010
Sugar-Dependent Expression of the CHS-A Gene for Chalcone Synthase from Petunia in Transgenic Arabidopsis Tsukaya, Hirokazu; Ohshima, Toshiyuki; Naito, Satoshi Plant Physiology, Vol. 97, Issue 4 https://doi.org/10.1104/pp.97.4.1414	journal	December 1991
Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Feinbaum, R. L.; Ausubel, F. M. Molecular and Cellular Biology, Vol. 8, Issue 5 https://doi.org/10.1128/MCB.8.5.1985	journal	May 1988
Analysis of Flavanone 3-Hydroxylase in Arabidopsis Seedlings (Coordinate Regulation with Chalcone Synthase and Chalcone Isomerase) Pelletier, M. K.; Shirley, B. W. Plant Physiology, Vol. 111, Issue 1 https://doi.org/10.1104/pp.111.1.339	journal	May 1996
Arabidopsis glabra2 mutant seeds deficient in mucilage biosynthesis produce more oil: Mucilage-deficient gl2 seeds produce more oil Shi, Lin; Katavic, Vesna; Yu, Yuanyuan The Plant Journal, Vol. 69, Issue 1 https://doi.org/10.1111/j.1365-313X.2011.04768.x	journal	October 2011
Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot Schiefelbein, John Current Opinion in Plant Biology, Vol. 6, Issue 1 https://doi.org/10.1016/S136952660200002X	journal	February 2003
Isolation and Characterization of Mutants Defective in Seed Coat Mucilage Secretory Cell Development in Arabidopsis Western, Tamara L.; Burn, Joanne; Tan, Wei Ling Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010410	journal	November 2001
Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation Pesch, Martina; Hülskamp, Martin Current Opinion in Genetics & Development, Vol. 14, Issue 4 https://doi.org/10.1016/j.gde.2004.06.007	journal	August 2004
The Homeobox Gene GLABRA2 Affects Seed Oil Content in Arabidopsis Shen, Bo; Sinkevicius, Kerstin W.; Selinger, David A. Plant Molecular Biology, Vol. 60, Issue 3 https://doi.org/10.1007/s11103-005-4110-1	journal	February 2006
Functional characterization of TRICHOMELESS2, a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis Gan, Lijun; Xia, Kai; Chen, Jin-Gui BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-176	journal	January 2011
HD-Zip Proteins GL2 and HDG11 Have Redundant Functions in Arabidopsis Trichomes, and GL2 Activates a Positive Feedback Loop via MYB23 Khosla, Aashima; Paper, Janet M.; Boehler, Allison P. The Plant Cell, Vol. 26, Issue 5 https://doi.org/10.1105/tpc.113.120360	journal	May 2014
Activation Tagging Identifies a Conserved MYB Regulator of Phenylpropanoid Biosynthesis Borevitz, Justin O.; Xia, Yiji; Blount, Jack The Plant Cell, Vol. 12, Issue 12 https://doi.org/10.1105/tpc.12.12.2383	journal	December 2000
Nitrogen depletion and small R3-MYB transcription factors affecting anthocyanin accumulation in Arabidopsis leaves Nemie-Feyissa, Dugassa; Olafsdottir, Solveig Margret; Heidari, Behzad Phytochemistry, Vol. 98 https://doi.org/10.1016/j.phytochem.2013.12.006	journal	February 2014
Sucrose-Specific Induction of Anthocyanin Biosynthesis in Arabidopsis Requires the MYB75/PAP1 Gene Teng, Sheng; Keurentjes, Joost; Bentsink, Leónie Plant Physiology, Vol. 139, Issue 4 https://doi.org/10.1104/pp.105.066688	journal	November 2005
Aux/IAA Proteins Contain a Potent Transcriptional Repression Domain Tiwari, Shiv B.; Hagen, Gretchen; Guilfoyle, Tom J. The Plant Cell, Vol. 16, Issue 2 https://doi.org/10.1105/tpc.017384	journal	January 2004
AUXIN RESPONSE FACTOR7 Restores the Expression of Auxin-Responsive Genes in Mutant Arabidopsis Leaf Mesophyll Protoplasts Wang, Shucai; Tiwari, Shiv B.; Hagen, Gretchen The Plant Cell, Vol. 17, Issue 7 https://doi.org/10.1105/tpc.105.031096	journal	May 2005
Negative Regulation of Anthocyanin Biosynthesis in Arabidopsis by a miR156-Targeted SPL Transcription Factor Gou, Jin-Ying; Felippes, Felipe F.; Liu, Chang-Jun The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.111.084525	journal	April 2011
The R2R3-MYB transcription factor MtMYB134 orchestrates flavonol biosynthesis in Medicago truncatula Naik, Jogindra; Rajput, Ruchika; Pucker, Boas Plant Molecular Biology, Vol. 106, Issue 1-2 https://doi.org/10.1007/s11103-021-01135-x	journal	March 2021
The Arabidopsis TT2 Gene Encodes and R2R3 MYB Domain Protein That Acts as a Key Determinant for Proanthocyanidin Accumulation in Developing Seed Nesi, Nathalie; Jond, Clarisse; Debeaujon, Isabelle The Plant Cell, Vol. 13, Issue 9 https://doi.org/10.2307/3871430	journal	September 2001
GL3 Encodes a bHLH Protein That Regulates Trichome Development in Arabidopsis Through Interaction With GL1 and TTG1 Payne, C. Thomas; Zhang, Fan; Lloyd, Alan M. Genetics, Vol. 156, Issue 3 https://doi.org/10.1093/genetics/156.3.1349	journal	November 2000

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COP9 signalosome subunit 5A affects phenylpropanoid metabolism, trichome formation and transcription of key genes of a regulatory tri-protein complex in Arabidopsis Wei, Shu; Li, Xiang; Gruber, Margaret Y. BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1347-9	journal	June 2018
RNA sequencing provides insights into the evolution of lettuce and the regulation of flavonoid biosynthesis Zhang, Lei; Su, Wenqing; Tao, Rong Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-02445-9	journal	December 2017
Ectopic expression of R3 MYB transcription factor gene OsTCL1 in Arabidopsis, but not rice, affects trichome and root hair formation Zheng, Kaijie; Tian, Hainan; Hu, Qingnan Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19254	journal	January 2016
An ABA down-regulated bHLH transcription repressor gene, bHLH129 regulates root elongation and ABA response when overexpressed in Arabidopsis Tian, Hainan; Guo, Hongyan; Dai, Xuemei Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17587	journal	December 2015
Constitutive Expression of OsIAA9 Affects Starch Granules Accumulation and Root Gravitropic Response in Arabidopsis Luo, Sha; Li, Qianqian; Liu, Shanda Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01156	journal	December 2015
Regulation of anthocyanin accumulation via MYB75/HAT1/TPL-mediated transcriptional repression Zheng, Ting; Tan, Wenrong; Yang, Huan PLOS Genetics, Vol. 15, Issue 3 https://doi.org/10.1371/journal.pgen.1007993	journal	March 2019
Class III OFPs function in the ER signaling pathway to regulate plant growth and development in Arabidopsis Wang, Xutong; Wang, Wei; Wang, Jie Journal of Plant Interactions, Vol. 14, Issue 1 https://doi.org/10.1080/17429145.2018.1550219	journal	December 2018
Critical analysis of protein signaling networks involved in the regulation of plant secondary metabolism: focus on anthocyanins Bulgakov, Victor P.; Avramenko, Tatiana V.; Tsitsiashvili, Gurami Sh. Critical Reviews in Biotechnology, Vol. 37, Issue 6 https://doi.org/10.3109/07388551.2016.1141391	journal	February 2016
Genetic evidence suggests that GIS functions downstream of TCL1 to regulate trichome formation in Arabidopsis Zhang, Na; Yang, Li; Luo, Sha BMC Plant Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12870-018-1271-z	journal	April 2018
T-6b allocates more assimilation product for oil synthesis and less for polysaccharide synthesis during the seed development of Arabidopsis thaliana Jin, Yunkai; Hu, Jia; Liu, Xun Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0706-3	journal	January 2017
Efficient isolation of protoplasts from freesia callus and its application in transient expression assays Shan, Xiaotong; Li, Yueqing; Zhou, Liudi Plant Cell, Tissue and Organ Culture (PCTOC), Vol. 138, Issue 3 https://doi.org/10.1007/s11240-019-01649-9	journal	July 2019
Overexpression of ERF96, a small ethylene response factor gene, enhances salt tolerance in Arabidopsis Wang, X.; Hou, C.; Zheng, K. Biologia plantarum, Vol. 61, Issue 4 https://doi.org/10.1007/s10535-017-0734-7	journal	December 2017
The Small Ethylene Response Factor ERF96 is Involved in the Regulation of the Abscisic Acid Response in Arabidopsis Wang, Xiaoping; Liu, Shanda; Tian, Hainan Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.01064	journal	November 2015
Two IIIf Clade-bHLHs from Freesia hybrida Play Divergent Roles in Flavonoid Biosynthesis and Trichome Formation when Ectopically Expressed in Arabidopsis Li, Yueqing; Shan, Xiaotong; Gao, Ruifang Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep30514	journal	July 2016
Arabidopsis ACYL-COA-BINDING PROTEIN1 interacts with STEROL C4-METHYL OXIDASE1-2 to modulate gene expression of homeodomain-leucine zipper IV transcription factors Lung, Shiu-Cheung; Liao, Pan; Yeung, Edward C. New Phytologist, Vol. 218, Issue 1 https://doi.org/10.1111/nph.14965	journal	December 2017
A novel family of transcription factors conserved in angiosperms is required for ABA signalling Tian, Hainan; Chen, Siyu; Yang, Wenting Plant, Cell & Environment, Vol. 40, Issue 12 https://doi.org/10.1111/pce.13058	journal	September 2017
Critical analysis of protein signaling networks involved in the regulation of plant secondary metabolism: focus on anthocyanins Bulgakov, Victor P.; Avramenko, Tatiana V.; Tsitsiashvili, Gurami Sh. Taylor & Francis https://doi.org/10.6084/m9.figshare.2798092	text	January 2016
Involvement of PACLOBUTRAZOL RESISTANCE6/KIDARI, an Atypical bHLH Transcription Factor, in Auxin Responses in Arabidopsis Zheng, Kaijie; Wang, Yating; Zhang, Na Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01813	journal	October 2017
Anthocyanins: From plant pigments to health benefits at mitochondrial level Bendokas, Vidmantas; Skemiene, Kristina; Trumbeckaite, Sonata Critical Reviews in Food Science and Nutrition, Vol. 60, Issue 19 https://doi.org/10.1080/10408398.2019.1687421	journal	November 2019
The R 2 R 3 MYB transcription factor P av MYB 10.1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry ( P runus avium L .) Jin, Wanmei; Wang, Hua; Li, Maofu Plant Biotechnology Journal, Vol. 14, Issue 11 https://doi.org/10.1111/pbi.12568	journal	May 2016

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