The ELF3-PIF7 Interaction Mediates the Circadian Gating of the Shade Response in Arabidopsis

Abstract

SummaryLight filtered through dense planting initiates the shade avoidance syndrome (SAS) in plants, which helps them compete against their neighbors. Quantitative trait loci (QTL)-based analysis identified the nighttime-expressed clock component ELF3 as a new player in the SAS, but its detailed mechanism is unclear. Here, we show that the circadian clock gates shade-induced gene expression and hypocotyl elongation at night. ELF3 is involved in nighttime suppression via interaction with and inactivation of PHYTOCHROME-INTERACTING FACTOR 7 (PIF7). Loss of function of ELF3 restores the shade induction, which is largely reduced in the absence of PIF7, indicating that ELF3 acts upstream of PIF7. Finally, we found that the repressive activity of ELF3 on the shade response is stronger under short days than under long days. Our results reveal that the interaction between ELF3 and PIF7 mediates the circadian gating of the SAS, which coordinates the daily control of physiological outputs.

Molecular pathways regulating elongation of aerial plant organs: a focus on light, the circadian clock, and temperature

“…One study has shown that in even photoperiods (12 h light/12 h dark), TOC1 and PRR5 prevent PIF4‐mediated induction of YUC8 in response to warm temperatures specifically during the later portion of the day and early night (Zhu et al ., 2016). A different study demonstrated that ELF3 acts early during SD nights to attenuate hypocotyl growth in response to low R:FR by sequestering PIF7 and reducing its binding to the promoters of IAA29 and PIL1 , thereby dampening their activation (Jiang et al ., 2019). However, beyond these two studies, little is known about how the circadian clock affects responses to temperature and low R:FR at the molecular level.…”

“…This hypothesis is supported by Y2H data indicating that the N‐terminal portion of ELF3 is primarily responsible for interactions with both COP1 and phyB (Liu et al ., 2001; Yu et al ., 2008a). It has been found that ELF3 inhibits hypocotyl growth by reducing PIF activity via two different mechanisms (Nusinow et al ., 2011; Nieto et al ., 2015; Jiang et al ., 2019). First, as a component of the evening complex (EC), a protein complex that functions as part of the circadian clock, ELF3 can directly repress the transcription of PIF4 and PIF5 (Nusinow et al ., 2011; Box et al ., 2015; Ezer et al ., 2017).…”

“…First, as a component of the evening complex (EC), a protein complex that functions as part of the circadian clock, ELF3 can directly repress the transcription of PIF4 and PIF5 (Nusinow et al ., 2011; Box et al ., 2015; Ezer et al ., 2017). Secondly, ELF3 also interacts with PIFs and inhibits their ability to associate with target promoters (Nieto et al ., 2015; Jiang et al ., 2019). Specifically, it has been demonstrated that both PIF4 and PIF7 interact with ELF3, and that ELF3 overexpression reduces the binding of constitutively expressed PIF4 or PIF7 to the promoters of genes such as PIL1 without affecting the accumulation of either protein (Nieto et al ., 2015; Huang et al ., 2016; Jiang et al ., 2019).…”

“…Secondly, ELF3 also interacts with PIFs and inhibits their ability to associate with target promoters (Nieto et al ., 2015; Jiang et al ., 2019). Specifically, it has been demonstrated that both PIF4 and PIF7 interact with ELF3, and that ELF3 overexpression reduces the binding of constitutively expressed PIF4 or PIF7 to the promoters of genes such as PIL1 without affecting the accumulation of either protein (Nieto et al ., 2015; Huang et al ., 2016; Jiang et al ., 2019). These two different mechanisms of ELF3‐mediated inhibition of PIFs probably both contribute to repression of hypocotyl growth in response to light.…”

“…This contributes to a progressive rise in expression of PIF targets, namely PIL1 , XTR7 , and HFR1 , and to hypocotyl growth during the dark phase, particularly when phyB activity is at its lowest, that is, slightly before dawn (Soy et al ., 2012; Soy et al ., 2014; Leivar et al ., 2020). Reduced phyB activity later in the night also activates PIF7, which further contributes to the induction of PIF targets and growth at night in SDs (Jiang et al ., 2019; Leivar et al ., 2020).…”