Light signals from the environment are perceived by distinct classes of photoreceptors and transduced to nuclear regulators to control developmental programs, in cooperation with developmental and other environmental cues. The long-term goal of my NIH funded research (now in year 22, R37-GM047850) is to fully understand the cellular and biochemical basis of light control network in plant development. Our ongoing NIH sponsored investigation has so far revealed an overall framework of three evolutionarily conserved multisubunit protein complexes (COP1-SPA complex or COP1 complex, COP10-DET1-DDB1 or CDD complex, and COP9 signalosome or CSN), whose key subunits were initially identified by our genetic analysis of the COP/DET/FUS loci in Arabidopsis. We have revealed the subunit composition and established that those three complexes largely act to modulate the stability and/or activity of specific transcription factors (including HY5 and HYH) that promote photomorphogenesis. While the COP1 complex and the CDD complex can collaborate with CUL4 to form large E3 complexes, CSN is a modulator of all Cullin-RING family of E3s. A number of major advances have been made about how light signals modulate changes in protein interaction landscape of these complexes and transcription factors, achieving signal-dependent regulation of gene expression. Here I propose four main aims to continue this NIH-sponsored research, which will address a number of general mechanistic issues that governs the light-regulated developmental switch, taking advantage of the knowledge and reagents developed from our previous and ongoing studies. Specifically, the proposed four main aims will cover three complementary aspects of further research. The first aspect, Aim 1, intends to identify novel modulators of COP1, which is expected to reveal new mechanistic insight on how COP1 is regulated with regard to its abundance, subcellular localization, and activity. The second aspect, including Aims 2 and 3, is to characterize the fundamental structural and biochemical basis of how COP1 and CDD complexes work and be regulated by distinct light stimuli. The third aspect, Aim 4, is to reveal the transcriptional network and the molecular action that govern a typical light-regulated developmental switch: photomorphogenesis vs skotomorphogenesis. The accomplishment of these proposed aims shall provide a comprehensive view of the regulatory network and fundamental mechanism essential for light control of development. Parts of our research findings on Arabidopsis may provide clues or even serve as guidance for investigating the roles of respective human counterparts of these protein complexes in human diseases.

Public Health Relevance

Our ongoing NIH sponsored investigation has so far revealed an overall framework of three evolutionarily conserved multisubunit protein complexes (COP1-SPA complex or COP1 complex, COP10-DET1-DDB1 or CDD complex, and COP9 signalosome or CSN), whose key subunits were initially identified by our genetic analysis of the COP/DET/FUS loci. These three complexes largely act to modulate the stability and/or activity of specific transcription factors in light and hormonal signaling pathways. The three complexes also have counterparts in humans, and the related biomedical studies have revealed their roles in tumorigenesis, lipid metabolism, cardiovascular functions and immune responses, which underscore the impact of our plant research toward better understanding of human health. Our future studies on the structures, regulatory mechanisms, and discovery of new regulatory components of those complexes will continue to provide guiding principles for parallel human health research.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Research Project (R01)
Project #
5R01GM047850-26
Application #
9417010
Study Section
Development - 1 Study Section (DEV1)
Program Officer
Maas, Stefan
Project Start
1992-08-01
Project End
2019-01-31
Budget Start
2018-02-01
Budget End
2019-01-31
Support Year
26
Fiscal Year
2018
Total Cost
Indirect Cost
Name
Yale University
Department
Biochemistry
Type
Schools of Arts and Sciences
DUNS #
043207562
City
New Haven
State
CT
Country
United States
Zip Code
06520
Lin, Fang; Xu, Dongqing; Jiang, Yan et al. (2017) Phosphorylation and negative regulation of CONSTITUTIVELY PHOTOMORPHOGENIC 1 by PINOID in Arabidopsis. Proc Natl Acad Sci U S A 114:6617-6622
Ling, Jun-Jie; Li, Jian; Zhu, Danmeng et al. (2017) Noncanonical role of Arabidopsis COP1/SPA complex in repressing BIN2-mediated PIF3 phosphorylation and degradation in darkness. Proc Natl Acad Sci U S A 114:3539-3544
Dong, Jie; Ni, Weimin; Yu, Renbo et al. (2017) Light-Dependent Degradation of PIF3 by SCFEBF1/2 Promotes a Photomorphogenic Response in Arabidopsis. Curr Biol 27:2420-2430.e6
Shi, Hui; Shen, Xing; Liu, Renlu et al. (2016) The Red Light Receptor Phytochrome B Directly Enhances Substrate-E3 Ligase Interactions to Attenuate Ethylene Responses. Dev Cell 39:597-610
Li, Kunlun; Yu, Renbo; Fan, Liu-Min et al. (2016) DELLA-mediated PIF degradation contributes to coordination of light and gibberellin signalling in Arabidopsis. Nat Commun 7:11868
Xu, Dongqing; Jiang, Yan; Li, Jigang et al. (2016) BBX21, an Arabidopsis B-box protein, directly activates HY5 and is targeted by COP1 for 26S proteasome-mediated degradation. Proc Natl Acad Sci U S A 113:7655-60
Shi, Hui; Liu, Renlu; Xue, Chang et al. (2016) Seedlings Transduce the Depth and Mechanical Pressure of Covering Soil Using COP1 and Ethylene to Regulate EBF1/EBF2 for Soil Emergence. Curr Biol 26:139-49
Sun, Ning; Wang, Jiajun; Gao, Zhaoxu et al. (2016) Arabidopsis SAURs are critical for differential light regulation of the development of various organs. Proc Natl Acad Sci U S A 113:6071-6
Shi, Hui; Wang, Xin; Mo, Xiaorong et al. (2015) Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination. Proc Natl Acad Sci U S A 112:3817-22
Huang, Hao; Yang, Mei; Su, Yan'e et al. (2015) Arabidopsis Atypical Kinases ABC1K1 and ABC1K3 Act Oppositely to Cope with Photodamage Under Red Light. Mol Plant 8:1122-4

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