Cryptochrome 1 interacts with PIF4 to regulate high temperature-mediated hypocotyl elongation in response to blue light

Abstract

Cryptochrome 1 (CRY1) is a blue light receptor that mediates primarily blue-light inhibition of hypocotyl elongation. Very little is known of the mechanisms by which CRY1 affects growth. Blue light and temperature are two key environmental signals that profoundly affect plant growth and development, but how these two abiotic factors integrate remains largely unknown. Here, we show that blue light represses high temperature-mediated hypocotyl elongation via CRY1. Furthermore, CRY1 interacts directly with PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) in a blue lightdependent manner to repress the transcription activity of PIF4. CRY1 represses auxin biosynthesis in response to elevated temperature through PIF4. Our results indicate that CRY1 signal by modulating PIF4 activity, and that multiple plant photoreceptors [CRY1 and PHYTOCHROME B (PHYB)] and ambient temperature can mediate morphological responses through the same signaling component-PIF4.ryptochromes are photolyase-like blue-light receptors first discovered in Arabidopsis and later found in all major evolutionary lineages (1-4). Arabidopsis cryptochrome 1 (CRY1) and cryptochrome 2 (CRY2) mediate primarily blue-light inhibition of hypocotyl elongation (5) and photoperiodic control of floral initiation (6) via modulation of gene expression. For example, Arabidopsis CRY2 undergoes blue light-dependent interaction with CIB1 (CRY2 Interacting bHLH1) to regulate flowering time (7-9). CRYs also suppress the E3 ubiquitin ligase activity of COP1 (CONSTITUTIVE PHOTOMORPHOGENIC 1) by forming a complex with SPA1 (SUPPRESSOR OF PHYA-105) and COP1 in a blue light-dependent manner (10-13). COP1 is a RING finger E3 ubiquitin ligase that acts downstream of phytochromes, cryptochromes, and UVR8 (UV Resistance Locus 8) (14,15) and is responsible for the degradation of various transcription factors in the dark, such as the bHLH transcription factor HFR1 (LONG HYPOCOTYL IN FAR RED1) and the bZIP factor HY5 (12,(16)(17)(18). Whether Arabidopsis CRY1 undergoes blue light-dependent interaction with transcription factors to regulate hypocotyl elongation is still unknown.In addition to light, ambient temperature serves as another key environmental cue that affects plant growth and development, but does not induce stress responses to any significant degree (19). Temperature regulates gene expression via chromatin remodeling and also regulation of transcription. It has been demonstrated that H2A.Z histone variant-containing nucleosomes act as thermosensors and mediate temperature induced transcriptome changes (20). PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) is a bHLH transcription factor directly link red light photoreceptor PHYTOCHROME B (PHYB) to light-regulated gene expression and plant development (21-23). PIF4 also plays a role in sensing high temperature, it not only regulates temperature-mediated floral induction in the short day condition through direct activation of FT (FLOWERING LOCUS T) (24), but it also controls high temperature-induced hypocotyl elongation by increasing free indo...

Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock

“…Blue light and CRYs were reported to be required for temperature compensation of the circadian clock (Gould et al, 2013), and phyB and CRY1 were shown to be critical for controlling growth in high temperature (Foreman et al, 2011). We showed recently that the blue light photoreceptor CRY1 interacted directly with PIF4 in a blue light-dependent manner to repress transcriptional activation by PIF4 and that multiple plant photoreceptors (CRY1 and phyB) and ambient temperature can mediate morphological responses through the same signaling component, PIF4 (Ma et al, 2016). Here, we showed that the cold-responsive genes COR27 and COR28 are induced not only by cold but also by reduced ambient temperature (Figure 1), indicating that they are involved in both cold response and ambient temperature response.…”

“…mRNA Expression Analyses mRNA expression analyses were performed as described previously (Ma et al, 2016). Total RNAs were isolated using the RNAiso Plus (Takara).…”

“…ChIP assays were performed as described before (Ma et al, 2016). Sevenday-old LD-grown seedlings harboring Pro35S:YFP-COR27, Pro35S: GFP-COR28, or wild-type genes were used for ChIP.…”

SUPPRESSOR OF PHYTOCHROME B4-#3 Represses Genes Associated with Auxin Signaling to Modulate Hypocotyl Growth

“…8). YUC8 functions in biosynthesis of the hormone and is essential for increasing endogenous auxin levels in response to warm temperatures, which in turn leads to hypocotyl elongation (Gray et al, 1998;Stavang et al, 2009;Franklin et al, 2011;Sun et al, 2012;Ma et al, 2016). Eleven YUC genes in Arabidopsis code for flavin monooxygenases, which function in the biosynthesis of auxin from Trp in what seems to be the major pathway for the synthesis of this hormone in plants (Zhao et al, 2001;Hofmann, 2011;Mashiguchi et al, 2011;Phillips et al, 2011;Stepanova et al, 2011;Won et al, 2011;Dai et al, 2013; for review, see Zhao, 2014).…”

A Negative Feedback Loop between PHYTOCHROME INTERACTING FACTORs and HECATE Proteins Fine-Tunes Photomorphogenesis in Arabidopsis

“…ELF3 also interacts with PIF4 and regulates plant growth independent of the evening complex (Nieto et al, 2015). Moreover, PIF4 and PIF5 interact with the blue light photoreceptors CRY1 and CRY2 to regulate shade avoidance under low blue light or hypocotyl elongation under high temperature (Ma et al, 2016;Pedmale et al, 2016). In addition, the bZIP transcription factor HY5 interacts with PIFs and functions antagonistically to regulate photomorphogenesis (Chen et al, 2013;Toledo-Ortiz et al, 2014;Xu et al, 2014).…”