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Molecular mechanisms of Evening Complex activity in Arabidopsis

The Evening Complex (EC), composed of the DNA binding protein LUX ARRHYTHMO (LUX) and two additional proteins EARLY FLOWERING 3 (ELF3) and ELF4, is a transcriptional repressor complex and a core component of the plant circadian clock. In addition to maintaining oscillations in clock gene expression, the EC also participates in temperature and light entrainment, acting as an important environmental sensor and conveying this information to growth and developmental pathways.

Catarina S. Silva, Aditya Nayak, Xuelei Lai, Stephanie Hutin, Véronique Hugouvieux, Jae-Hoon Jung, Irene López-Vidriero, Jose M. Franco-Zorrilla, Kishore C. S. Panigrahi, Max H. Nanao, Philip A. Wigge, and Chloe Zubieta

PNAS March 24, 2020 117 (12) 6901-6909

Significance

Circadian gene expression oscillates over a 24-h period and regulates many genes critical for growth and development in plants. A key component of the circadian clock is the Evening Complex (EC), a transcriptional repressor complex that contains the proteins LUX ARRHYTHMO, EARLY FLOWERING 3, and EARLY FLOWERING 4 (ELF4). By repressing the expression of genes such as PHYTOCHROME INTERACTING FACTOR4 (PIF4), the EC reduces elongation growth. At warmer temperatures, EC activity is lost, promoting thermomorphogenesis via PIF4 expression. The molecular mechanisms underlying EC activity are not well understood. Here, we combined structural studies with extensive in vitro assays to determine the molecular mechanisms of the temperature-dependent EC binding to DNA and demonstrate the critical role of ELF4 in this activity.

Abstract

The Evening Complex (EC), composed of the DNA binding protein LUX ARRHYTHMO (LUX) and two additional proteins EARLY FLOWERING 3 (ELF3) and ELF4, is a transcriptional repressor complex and a core component of the plant circadian clock. In addition to maintaining oscillations in clock gene expression, the EC also participates in temperature and light entrainment, acting as an important environmental sensor and conveying this information to growth and developmental pathways. However, the molecular basis for EC DNA binding specificity and temperature-dependent activity were not known. Here, we solved the structure of the DNA binding domain of LUX in complex with DNA. Residues critical for high-affinity binding and direct base readout were determined and tested via site-directed mutagenesis in vitro and in vivo. Using extensive in vitro DNA binding assays of LUX alone and in complex with ELF3 and ELF4, we demonstrate that, while LUX alone binds DNA with high affinity, the LUX–ELF3 complex is a relatively poor binder of DNA. ELF4 restores binding to the complex. In vitro, the full EC is able to act as a direct thermosensor, with stronger DNA binding at 4 °C and weaker binding at 27 °C. In addition, an excess of ELF4 is able to restore EC binding even at 27 °C. Taken together, these data suggest that ELF4 is a key modulator of thermosensitive EC activity.

 

See https://www.pnas.org/content/117/12/6901

Figure 1: LUX–DNA interactions. (A) High-scoring PBM-derived logos for LUX. Three logos are presented, including the LBS consensus (Left), the PRR9 promoter LBS sequence (Center), and a high-scoring PBM sequence (Right). (B) Representative gel EMSAs for LUXMYB. DNA concentration was constant with protein concentration increasing from 0 to 1,000 nM. The DNA sequences used correspond to the above motifs in A. Free DNA is indicated by an arrow, and protein–DNA complexes are indicated with stars. One star corresponds to one molecule of protein bound; two stars indicates multiple nonspecifically bound protein molecules at high protein concentrations. (C) Representative EMSA for LUXFL labeled as per B.

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