Wang Lab

Lab Tabs

Our Research

Research Interests

Research in my lab focuses on the cellular signaling mechanisms that control plant growth and responses to the environment. Plant growth is highly modulated by environmental signals such as light and temperature, by endogenous hormones such as brassinosteroid (BR), auxin, gibberellic acid (GA), and abscisic acid (ABA), as well as by sugar. Our research is illustrating the complex molecular networks that integrate these environmental and endogenous signals with gene transcription, protein translation and modification, and cellular membrane organization, which drive cell division and expansion. We use a wide range of research approaches, including genetics, genomics, proteomics, and imaging in the model organisms of Arabidopsis and Chlamydomonas. Our long-term goal is to improve plant productivity and resilience by engineering the cellular control system.

The brassinosteroid (BR) signaling pathway - the best-studied receptor kinase pathway in plants.

BR is a major growth-promoting hormone that regulates a wide range of developmental and physiological processes, including seed germination, cell elongation, growth, flowering, light responses, photosynthesis, and stress tolerance. Application of BR or increasing BR biosynthesis can enhance plant growth and biomass production. Research on BR has great potential of increasing crop yield.
BR is perceived by the cell-surface receptor kinase BRI1 (Figure 1), which contains an extracellular leucine-rich repeat domain and a cytoplasmic serine/threonine kinase domain. BR binding to the extracellular domain of BRI1 activates its kinase and initiates a signaling cascade leading to regulation of gene expression in the nucleus. This signaling cascade includes the BR-signaling kinases (BSKs), the PP1-like phosphatase BSU1, the GSK3-like kinase BIN2, and protein phosphatase 2A (PP2A), the phosphopeptide-binding 14-3-3 proteins, and the homologous transcription factors BZR1 and BZR2 (also named BES1). When BR level is high, BRI1 phosphorylates BSKs/CDG1 kinases which in turn phosphorylate BSU1. BSU1 dephosphorylates BIN2 to inhibit its kinase activity and to increase its ubiquitination mediated by the KIB1 E3 ubiquitin ligase. As such, BR induces rapid accumulation of dephosphorylated BZR1 and BZR2/BES1 in the nucleus due to dephosphorylation by PP2A. BZR1 and BZR2 directly regulate the expression of thousands of target genes. Our works have established the BR signaling pathway as the best-understood receptor-kinase signaling pathway in plants.

Figure 1)

Signal crosstalk and Integration of multiple pathways into networks

We have further gained insight into the molecular mechanisms that integrate BR with other major growth-regulation signals, including gibberellin (GA), auxin, light, temperature, pathogen signals, and nutrient signals. Using modern genomic approaches of RNA-Seq and ChIP-Seq, we have identified thousands of genes directly regulated by BZR1, the light-regulated transcription factor PIF4, and the auxin response factor 6 (ARF6). These genome-wide targets not only identify diverse cellular and developmental functions controlled by these signaling pathways, but also revealed extensive overlaps among the target genes these distinct transcription factors. We further discovered that these TFs directly interact with each other and also interact with the gibberellin (GA) signaling DELLA proteins. Our research has thus revealed a central growth-regulation (CGR) network that integrates multiple hormonal and developmental pathways for growth regulation in plants (Figure 2). The CGR network also integrates additional signals such as temperature, sugar, the circadian clock.

Figure 2)

Proteomic Analysis of Signaling networks

Our current research focuses on proteomic studies of steroid and sugar signaling mechanisms. We are still the only lab in the world that has reported proteomic profiling of O-linked N-acetylglucosamine (O-GlcNAc) modifications in plants and we have identified 262 O-GlcNAcylated proteins in Arabidopsis. These are mostly nuclear proteins with regulatory functions including key components of hormonal pathways. These studies are expanding the posttranslational modification networks that integrate hormonal and sugar signaling pathways for growth regulation. Examples of ongoing research projects include: (1) Signaling mechanisms for BR regulation of translation, vesical trafficking, cytokinesis (cell division), and carbon metabolism, (2) cell integrity signaling by receptor kinases in stress adaptation, (3) proteomic and functional studies of glycosylation (O-GlcNAcylation and O-fucosylation) in metabolic signaling and growth regulation.

Figure 3)

Review papers

Chaiwanon J, Wang W, Zhu JY, Oh E, Wang ZY. (2016) Information Integration and Communication in Plant Growth Regulation. Cell 164(6):1257-68.
Wang W, Bai MY, Wang ZY. (2014). The brassinosteroid signaling network – a paradigm of signal integration. Curr. Opin. Plant Biol. 21:147–153 .
Wang W and Wang ZY. (2014). At the intersection of plant growth and immunity. Cell Host Microbe 15, 400–402.
Zhu JY, Sae-Seaw J, Wang ZY. (2013). Brassinosteroid signalling. Development. 140, 1615-1620.
Wang ZY, Bai MY, Oh E, Zhu JY (2012). Brassinosteroid signaling network and regulation of photomorphogenesis. Annu. Rev. Genet. 46:701-724.
Kim TW and Wang ZY. (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol.61, 681-704.

News

Lab PI

Zhiyong Wang

Acting Director & Senior Staff Scientist

Plant Biology

Carnegie Institution for Science

zwang@carnegiescience.edu
650-739-4205
Office:
260 Panama Street
Stanford, CA 94305, US

Profile

Bio

I am interested in how hormones regulate plant growth according to endogenous nutrient and energy status and environmental conditions. We use broad research approaches to dissect the molecular mechanisms by which plants perceive, transduce, and integrate internal and external signals into cellular decisions to divide, expand, differentiate, defend, or acclimate. Our goal is to understand the signaling and regulatory networks and to generate knowledge that enables engineering plants with enhanced yield and resilience.

Affiliation

Carnegie Affiliation:

DPB Employees

DPB Affiliation:

DPB Faculty

Operational Division:

DPB Administration

Labs:

Wang Lab

Teaching

Websites

Lab Members

Yang Bi (Postdoctoral Fellow)
Roberto Bogomolni (Visiting Investigator)
Efren Gonzalez (Research Assistant)
Yuchun Hsiao (Postdoctoral Fellow)
I am interested in receptor kinase function in salt signaling pathway and how the BR-auxin circuitry regulates root growth and development.
Chuan-Chih Hsu (Postdoctoral Fellow)
I am from Taichung City, Taiwan. I obtained a BS in Agricultural Chemistry from National Taiwan University in Taipei City, Taiwan in June 2007. I then decided to study analytical chemistry so I spent two years to complete a MS in Chemistry at National Taiwan University with Dr. Yu-Ju Chen as my advisor in June 2009. I then moved to West Lafayette in Auguest 2012, and I joined Dr. Andy Tao's lab and spent time designing novel (phospho)proteomic strategies toward comprehensive phosphoproteomic analysis. I recieved my PhD degree in Biochemistry from Purdue University in September 2017, and I joined Dr. Wang's lab as a postdoc in June 2018. I am interested in the development of novel mass spectrometry(MS)-based approaches that faciliate systematically analysis of plant signal transduction and proteome perturbation in response to extracellular stimuli. I believe that MS is a cutting-edge technique to identify all the proteins involved in various biological processes and to illustrate their functional mechanisms in plant cells. My current research project focuses on the study of phosphorylation events in plants under environmental stresses. In my spare time, I enjoy jogging, watching movie, and listening to classical music.
Marcia Margis (Visitor)
Frej Tulin (Postdoctoral Fellow)
I am interested in how plants coordinate cell growth and division. Brassinosteroid (BR) hormones are known for their growth-promoting activity, but also help regulate cell division in certain tissues. I am exploring mechanistic links between BR signaling and cell division, using Arabidopsis and the alga Chlamydomonas as models.

I received a M.S. from KTH in Stockholm, Sweden, and a Ph.D. from the Rockefeller University. I like running and ping pong.
Zhenzhen Zhang (Postdoctoral Fellow)
I am interested in mechanisms of plant growth regulated by sugar and brassinosteroid signaling.

Former Lab Members and Current Affiliation

Postdoc/Graduate Students:

Joshua Gendron, Assistant Professor, Yale University, USA
Ying Sun, Professor, Hebei Normal University, China
Soo-Hwan Kim, Professor, Yonsei University, Korea
Junxian He, Assistant Professor, the Chinese University of Hong Kong
Srinivas Gampala, Dow Agrosciences, USA
Wenqiang Tang, Professor, Hebei Normal University, China
Yu Sun, Professor, Hebei Normal University, China
Zhiping Deng, Group leader, Zhejiang Academy of Agricultural Sciences, China
Tae-Wuk Kim, Associate Professor, Hanyang U. Korea
Eunkyoo Oh, Korea University, Korea
Shouling Xu, Director of Proteomics at the Carnegie Institution for Science
Wenfei Wang, Professor, Fujian Agriculture and Forestry University
Xuelian Yang, Associate Professor, Fujian Agriculture and Forestry University
Sunita Patil, Stanford University
Juthamas Chaiwanon, Lecturer, Chulalongkorn U., Thailand
Mingyi Bai, Professor, Shandong University, China
Min Fan, Assistant Professor, Shandong University, China
Thomas Hartwig, Group Leader, Max Planck Institute for Plant Breeding Research, Cologne, Germany

Visiting Scholars/Students/Technishia:

Man Ao
Ruiju Wang, 2007-2009 Postdoc, Hebei Normal U. China
Yaqi Hao, 2008-2011 Research Associate, Shannxi Normal U. China
Jianxiu Shang 2009-2011 Research Associate, Hebei Normal U. China
Hongjuan Yang, 2009-2010 Graduate program director, IB, CAS
Rafael Augusto, 2010-2011 Univers. Federal do Rio Grande do Sul. Brazil
Hak-Soo Lee 2010-2011 Student, Yonsei U. Korea
Yang Bai, 2010-2012 Student, Northeast U. China
Shuolei Bu, 2011-2013 Student. China
Jiangshu Liu, 2007-2009 Postdoc, U. Toronto, Canada
Min Yuan, 2008-2010 Assistant Professor, Hebei Sci Tech U. China
Tian Li, 2007-2009 Lecturer, Lanzhou U. China
Peng Xu, 2009-2011, Postdoc, UCSF
Hui Yang, 2008-2010 Professor, Lanzhou Institute of Biology, China
Zhiguang Zhao, 2008-2009 Professor, Lanzhou University, China
Tonglin Mao, 2008-2009 Professor, China Agriculture U.
Shengwei Zhu, 2009-2010 Group Leader, Institute of Botany, CAS, China
Chuangqi Wei, 2012-2015. China
Lauro Bücker Neto, 2012-2014 Visiting graduate student from Brazil
Shengwei Zhang 2014-2015 Visiting scholar from China

Undergraduate or high school students (send Zhiyong your contact if your name is missing):
Catherine Qing Sun, UCSF Medical School; Joyce Xue, UC Berkeley; Jemma Taylor, University of Warwick, UK; Emily Luise Hulme, Stanford University; Andrew Ma, Cal Tech; Denial Li, Stanford Medical School.

Publications

Selected Publications

(see full publication list at: https://scholar.google.com/citations?user=DSbbGNIAAAAJ&hl=en&oi=ao)

Major Reviews:

Chaiwanon J, Wang W, Zhu JY, Oh E, Wang ZY. (2016) Information Integration and Communication in Plant Growth Regulation. Cell 164(6):1257-68.

Wang W, Bai MY, Wang ZY.(2014). The brassinosteroid signaling network – a paradigm of signal integration. Curr. Opin. Plant Biol. 21:147–153.

Zhu JY, Sae-Seaw J, Wang ZY (2013). Brassinosteroid signalling. Development 140, 1615-1620.

Wang ZY, Bai MY, Oh E, Zhu JY (2012). Brassinosteroid signaling network and regulation of photomorphogenesis. Annu. Rev. Genet. 46:701-724.

Kim TW and Wang ZY. (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61, 681-704.

Research articles

Yang Bi, Zhiping Deng, Weimin Ni, Dasha Savage, Thomas Hartwig, Sunita Patil, Juan A. Oses-Prieto, Kathy H. Li, Peter H Quail, Alma L Burlingame, Shou-Ling Xu, and Zhi-Yong Wang (2020). An O-GlcNAc-modified protein promotes seed germination and flowering through alternative RNA splicing and transcription of key regulators in Arabidopsis. Nature Communication, Revised.

Garcia VJ, Xu SL, Ravikumar R, Wang W, Elliott L, Fesenko M, Altmann M, Falter-Braun P, Moore I, Assaad F, Wang ZY. (2019) Proteomic studies of the Arabidopsis TRAPP complexes reveal conserved organization and a novel plant-specific component with a role in plant development. BioRxiv doi: http://dx.doi.org/10.1101/684258.

Park CH, Youn JH, Xu SL, Kim JG, Bi Y, Xu N, Mudgett MB, Kim SK, Kim TW, & Wang ZY. (2019) BSU1 family phosphatases mediate Flagellin-FLS2 signaling through a specific phosphocode. BioRxiv doi: http://dx.doi.org/10.1101/685610.

Kim TW, Park CH, Hsu CC, Zhu JY, Hsiao Y, Branon T, Xu SL, Ting AY, and Wang ZY. (2019) Application of TurboID-mediated proximity labeling for mapping a GSK3 kinase signaling network in Arabidopsis. BioRxiv, doi: http://dx.doi.org/10.1101/636324.

Kim EJ, Lee SH, Park CH, Kim SH, Hsu CC, Xu S, Wang ZY, Kim SK, Kim TW. (2019). Plant U-Box40 Mediates Degradation of the Brassinosteroid-Responsive Transcription Factor BZR1 in Arabidopsis Roots. Plant Cell 31(4):791-808. doi: 10.1105/tpc.18.00941

Song L, Chen W, Wang B, Yao QM, Valliyodan B, Bai MY, Zhao MZ, Ye H, Wang ZY, Nguyen HT. (2019) GmBZL3 acts as a major BR signaling regulator through crosstalk with multiple pathways in Glycine max. BMC Plant Biol 19:86. doi: 10.1186/s12870-019-1677-2.

Tian Y, Fan M, Qin Z, Lv H, Wang M, Zhang Z, Zhou W, Zhao N, Li X, Han C, Ding Z, Wang W, Wang ZY, Bai MY. (2018). Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat Communication14;9(1):1063.

Zhu J-Y, Li Y, Cao D, Yang H, Oh E, Bi Y, Zhu S, Wang Z-Y (2017) The F-box protein KIB1 mediates brassinosteroid-induced inactivation and degradation of GSK3-like kinases in Arabidopsis. Mol Cell 66(5):648-657.

Xu SL, Chalkley RJ, Maynard JC, Wang W, Ni W, Jiang X, Shin K,Cheng L, Savage D, Hühmer AFR, Burlingame AL, Wang Z-Y. (2017) Proteomic Analysis Reveals O-GlcNAc Modification on Proteins with Key Regulatory Functions in Arabidopsis. PNAS 114(8):E1536-E1543.

Zhu JY, Oh E, Wang T, Wang ZY. (2016) TOC1-PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis. Nat Communication 7:13692.

Zhang Z, Zhu JY, Roh J, Marchive C, Kim SK, Meyer C, Sun Y, Wang W, Wang ZY.(2016). TOR Signaling Promotes Accumulation of BZR1 to Balance Growth with Carbon Availability in Arabidopsis. Curr Biol. 26:1854-60.

Chaiwanon J and Wang ZY. (2015) Spatiotemporal brassinosteroid signaling and antagonism with auxin pattern stem cell dynamics in Arabidopsis roots. Current Biology 25(8):1031-42.

Ni WM, Xu SL, Tepperman JM, Stanley DJ, Maltby DA, Gross JD, Burlingame AL, Wang ZY and Quail PH(2014). A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344, 1160-1164.

Oh E, Zhu JY, Bai MY, and Wang ZY. (2014). A central transcription module regulates cell elongation and development by integrating major environmental and hormonal signals in Arabidopsis. eLife:e03031.

Oh E, Zhu JY, Ryu H, Hwang I, Wang ZY. (2014). TOPLESS mediates brassinosteroid-induced transcriptional repression through interaction with BZR1. Nature Communications18;5:4140.

Fan M, Bai MY, Kim JG, Wang T, Oh E, Chen L, Park CH, Son SH, Kim SK, Mudgett MB, Wang ZY. (2014). The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26, 828-841.

Gendron JM, Liu JS, Fan M, Bai MY, Wenkel S, Springer PS, Barton MK, Wang ZY (2012). Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc Natl Acad Sci USA 109, 21152-21157.

Bai MY, Fan M, Oh E, Wang ZY(2012) A triple-HLH/bHLH Cascade Controls Cell Elongation Downstream of Multiple Hormonal and Environmental Signaling Pathways in Arabidopsis. Plant Cell 24:4917-4929

Oh E, Zhu JY, Wang ZY. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nature Cell Biol.14, 802-809.

Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY. (2012). Brassinosteroid, gibberellin, and phytochrome impinge on a common transcription module in Arabidopsis. Nature Cell Biol.14, 810-819.

Kim TW, Michniewicz M, Bergmann DC, Wang ZY. (2012). Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482, 419-422.

Hao Y, Oh E, Choi G, Liang Z, Wang ZY. (2012). Interactions between HLH and bHLH Factors Modulate Light-Regulated Plant Development. Mol. Plant 5, 688-697.

Kim TW, Guan S, Burlingame AL, Wang ZY. (2011). The CDG1 Kinase Mediates Brassinosteroid Signal Transduction from BRI1 Receptor Kinase to BSU1 Phosphatase and GSK3-like Kinase BIN2. Mol. Cell 43, 561-571.PMCID: PMC3206214

Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, Gendron JM, Jonassen EM, Lillo C, DeLong A, Burlingame AL, Sun Y, Wang ZY. (2011). PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1. Nature Cell Biol.13:124-131. PMCID: PMC3077550

Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev. Cell 19, 756-777. PMCID: PMC3018842.

Luo XM, Lin WH, Zhu S, Zhu JY, Sun Y, Fan XY, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang ZY. (2010). Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19: 872-883.

Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang JX, Sun Y, Burlingame AL, Wang ZY. (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nature Cell Biol. 11, 1254-1262.

Tang W, Kim TW, Oses-PrietoJA,Sun Y, Deng Z, Zhu S, Wang R, Burlingame AL, Wang ZY (2008). BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321, 557-560.

Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM, Chen H, Shibagaki N, Ferl RJ, Ehrhardt D, Chong K, Burlingame AL, Wang ZY. (2007). An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis.Dev. Cell 13, 177-189.

Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY. (2007). Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc.Natl. Acad. Sci. USA 104, 13939-13844.

He JX, Gendron JM, Sun Y, Gampala SS, Gendron N, Sun CQ, Wang ZY (2005). BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses. Science 307(5715): 1634-1638.

Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, Chory J(2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2(4): 505-513.

Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J. (2001) BRI1 is a critical component of a plasma membrane receptor for plant steroids. Nature 410(6826): 380-382.

He Z, Wang ZY, Li J, Zhu Q, Lamb C, Ronald P, Chory J. (2000) Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 288(5475): 2360-2363.

Weigel D, Ahn JH, Blázquez MA, Borevitz JO, Christensen SK, Fankhauser C, Ferrándiz C, Kardailsky I, Malancharuvil EJ, Neff MM, Nguyen JT, Sato S, Wang ZY, Xia Y, Dixon RA, Harrison MJ, Lamb CJ, Yanofsky MF, Chory J. (2000). Activation tagging in Arabidopsis. Plant Physiology 122(4): 1003-1013.

Wang ZY, Tobin EM (1998) Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1(CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93(7): 1207-1217.

Websites

Join Us

If you are interested in joining us, please send email to zywang24@stanford.edu.

Potential research projects:

1. Proteomic and functional study of O-GlcNAc and O-fucose modififications.

2. Signaling and regulation of vesicle trafficking.

3. Signaling and regulation of cytokinesis.

4. Signaling and regulation of protein translaiton.

5. Modeling and engineering of signaling neworks - logics of information integration and decision making.