BBX9 forms feedback loops with PIFs and BBX21 to promote photomorphogenic development.

Light is one of the most essential environmental factors that tightly and precisely control various physiological and developmental processes in plants. B-box CONTAINING PROTEINs (BBXs) play central roles in the regulation of light-dependent development. In this study, we report that BBX9 is a positive regulator of light signaling. BBX9 interacts with the red light photoreceptor PHYTOCHROME B (phyB) and transcription factors PHYTOCHROME-INTERACTING FACTORs (PIFs). phyB promotes the stabilization of BBX9 in light, while BBX9 inhibits the transcriptional activation activity of PIFs. In turn, PIFs directly bind to the promoter of BBX9 to repress its transcription. On the other hand, BBX9 associates with the positive regulator of light signaling, BBX21, and enhances its biochemical activity. BBX21 associates with the promoter regions of BBX9 and transcriptionally up-regulates its expression. Collectively, this study unveiled that BBX9 forms a negative feedback loop with PIFs and a positive one with BBX21 to ensure that plants adapt to fluctuating light conditions.

B-BOX proteins:Multi-layered roles of molecular cogs in light-mediated growth and development in plants.

B-box containing proteins (BBXs) are a class of zinc-ligating transcription factors or regulators that play essential roles in various physiological and developmental processes in plants. They not only directly associate with target genes to regulate their transcription, but also interact with other transcription factors to mediate target genes' expression, thus forming a complex transcriptional network ensuring plants' adaptation to dynamically changing light environments. This review summarizes and highlights the molecular and biochemical properties of BBXs, as well as recent advances with a focus on their critical regulatory functions in photomorphogenesis (de-etiolation), shade avoidance, photoperiodic-mediated flowering, and secondary metabolite biosynthesis and accumulation in plants.

COP1 SUPPRESSOR 6 represses the PIF4 and PIF5 action to promote light-inhibited hypocotyl growth.

Light signaling precisely controls photomorphogenic development in plants. PHYTOCHROME INTERACTING FACTOR 4 and 5 (PIF4 and PIF5) play critical roles in the regulation of this developmental process. In this study, we report CONSTITUTIVELY PHOTOMORPHOGENIC 1 SUPPRESSOR 6 (CSU6) functions as a key regulator of light signaling. Loss of CSU6 function largely rescues the cop1-6 constitutively photomorphogenic phenotype. CSU6 promotes hypocotyl growth in the dark, but inhibits hypocotyl elongation in the light. CSU6 not only associates with the promoter regions of PIF4 and PIF5 to inhibit their expression in the morning, but also directly interacts with both PIF4 and PIF5 to repress their transcriptional activation activity. CSU6 negatively controls a group of PIF4- and PIF5-regulated gene expressions. Mutations in PIF4 and/or PIF5 are epistatic to the loss of CSU6, suggesting that CSU6 acts upstream of PIF4 and PIF5. Taken together, CSU6 promotes light-inhibited hypocotyl elongation by negatively regulating PIF4 and PIF5 transcription and biochemical activity.

PIFs- and COP1-HY5-mediated temperature signaling in higher plants.

Plants have to cope with the surrounding changing environmental stimuli to optimize their physiological and developmental response throughout their entire life cycle. Light and temperature are two critical environmental cues that fluctuate greatly during day-night cycles and seasonal changes. These two external signals coordinately control the plant growth and development. Distinct spectrum of light signals are perceived by a group of wavelength-specific photoreceptors in plants. PIFs and COP1-HY5 are two predominant signaling hubs that control the expression of a large number of light-responsive genes and subsequent light-mediated development in plants. In parallel, plants also transmit low or warm temperature signals to these two regulatory modules that precisely modulate the responsiveness of low or warm temperatures. The core component of circadian clock ELF3 integrates signals from light and warm temperatures to regulate physiological and developmental processes in plants. In this review, we summarize and discuss recent advances and progresses on PIFs-, COP1-HY5- and ELF3-mediated light, low or warm temperature signaling, and highlight emerging insights regarding the interactions between light and low or warm temperature signal transduction pathways in the control of plant growth.

A missense mutation in WRKY32 converts its function from a positive regulator to a repressor of photomorphogenesis.

CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) mediates various cellular and physiological processes in plants by targeting a large number of substrates for ubiquitination and degradation. In this study, we reveal that a substitution of Pro for Leu at amino acid position 409 in WRKY32 largely suppresses the short hypocotyls and expanded cotyledon phenotypes of cop1-6. WRKY32P409L promotes hypocotyl growth and inhibits the opening of cotyledons in Arabidopsis. Loss of WRKY32 function mutant seedlings display elongated hypocotyls, whereas overexpression of WRKY32 leads to shortened hypocotyls. WRKY32 directly associates with the promoter regions of HY5 to activate its transcription. COP1 interacts with and targets WRKY32 for ubiquitination and degradation in darkness. WRKY32P409L exhibits enhanced DNA binding ability and affects the expression of more genes compared with WRKY32 in Arabidopsis. Our results not only reveal the basic role for WRKY32 in promoting photomorphogenesis, but also provide insights into manipulating plant growth by engineering key components of light signaling.

HY5: A Pivotal Regulator of Light-Dependent Development in Higher Plants.

ELONGATED HYPOCOTYL5 (HY5), a bZIP-type transcription factor, acts as a master regulator that regulates various physiological and biological processes in plants such as photomorphogenesis, root growth, flavonoid biosynthesis and accumulation, nutrient acquisition, and response to abiotic stresses. HY5 is evolutionally conserved in function among various plant species. HY5 acts as a master regulator of light-mediated transcriptional regulatory hub that directly or indirectly controls the transcription of approximately one-third of genes at the whole genome level. The transcription, protein abundance, and activity of HY5 are tightly modulated by a variety of factors through distinct regulatory mechanisms. This review primarily summarizes recent advances on HY5-mediated molecular and physiological processes and regulatory mechanisms on HY5 in the model plant Arabidopsis as well as in crops.

BBX11 promotes red light-mediated photomorphogenic development by modulating phyB-PIF4 signaling.

phytochrome B (phyB) acts as the red light photoreceptor and negatively regulates the growth-promoting factor PHYTOCHROME INTERACTING 4 (PIF4) through a direct physical interaction, which in turn changes the expression of a large number of genes. phyB-PIF4 module regulates a variety of biological and developmental processes in plants. In this study, we demonstrate that B-BOX PROTEIN 11 (BBX11) physically interacts with both phyB and PIF4. BBX11 negatively regulates PIF4 accumulation as well as its biochemical activity, consequently leading to the repression of PIF4-controlled genes' expression and promotion of photomorphogenesis in the prolonged red light. This study reveals a regulatory mechanism that mediates red light signal transduction and sheds a light on phyB-PIF4 module in promoting red light-dependent photomorphognenesis. Supplementary Information: The online version contains supplementary material available at 10.1007/s42994-021-00037-2.

BBX28/BBX29, HY5 and BBX30/31 form a feedback loop to fine-tune photomorphogenic development.

Light is one of the key environmental cues controlling photomorphogenic development in plants. A group of B-box (BBX) proteins play critical roles in this developmental process through diverse regulatory mechanisms. In this study we report that BBX29 acts as a negative regulator of light signaling. BBX29 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) and undergoes COP1-mediated degradation in the dark. Mutant seedlings with loss of BBX29 function show shortened hypocotyls, while transgenic plants overexpressing BBX29 display elongated hypocotyls in the light. Both BBX28 and BBX29 interfere with the binding of ELONGATED HYPOCOTYL 5 (HY5) to the promoters of BBX30 and BBX31, consequently leading to the upregulation of their transcript levels. BBX30 and BBX31 associate with the promoter regions of BBX28 and BBX29, which in turn promotes the expression of these genes. Taken together, this study reveals a transcriptional feedback loop consisting of BBX28, BBX29, BBX30, BBX31, and HY5 that serves to fine-tune photomorphogenesis in response to light in plants.

B-box proteins: Pivotal players in light-mediated development in plants.

Light signals mediate a number of physiological and developmental processes in plants, such as flowering, photomorphogenesis, and pigment accumulation. Emerging evidence has revealed that a group of B-box proteins (BBXs) function as central players in these light-mediated developmental processes. B-box proteins are a class of zinc-coordinated transcription factors or regulators that not only directly mediate the transcription of target genes but also interact with various other factors to create a complex regulatory network involved in the precise control of plant growth and development. This review summarizes and highlights the recent findings concerning the critical regulatory functions of BBXs in photoperiodic flowering, light signal transduction and light-induced pigment accumulation and their molecular modes of action at the transcriptional and post-translational levels in plants.