Yanjun Jing

Antagonistic Basic Helix-Loop-Helix/bZIP Transcription Factors Form Transcriptional Modules That Integrate Light and Reactive Oxygen Species Signaling in Arabidopsis

This study shows that PIF1/PIF3 and HY5/HYH physically interact and coordinately regulate the expression of ROS-responsive genes. It reveals that the PIF1/PIF3-HY5/HYH transcriptional modules mediate crosstalk between light and ROS signaling pathways and suggests a mechanism by which plants optimize their growth in response to excess light. The critical developmental switch from heterotrophic to autotrophic growth of plants involves light signaling transduction and the production of reactive oxygen species (ROS). ROS function as signaling molecules that regulate multiple developmental processes, including cell death. However, the relationship between light and ROS signaling remains unclear. Here, we identify transcriptional modules composed of the basic helix-loop-helix and bZIP transcription factors PHYTOCHROME-INTERACTING FACTOR1 (PIF1), PIF3, ELONGATED HYPOCOTYL5 (HY5), and HY5 HOMOLOGY (HYH) that bridge light and ROS signaling to regulate cell death and photooxidative response. We show that pif mutants release more singlet oxygen and exhibit more extensive cell death than the wild type during Arabidopsis thaliana deetiolation. Genome-wide expression profiling indicates that PIF1 represses numerous ROS and stress-related genes. Molecular and biochemical analyses reveal that PIF1/PIF3 and HY5/HYH physically interact and coordinately regulate the expression of five ROS-responsive genes by directly binding to their promoters. Furthermore, PIF1/PIF3 and HY5/HYH function antagonistically during the seedling greening process. In addition, phytochromes, cryptochromes, and CONSTITUTIVE PHOTOMORPHOGENIC1 act upstream to regulate ROS signaling. Together, this study reveals that the PIF1/PIF3-HY5/HYH transcriptional modules mediate crosstalk between light and ROS signaling and sheds light on a new mechanism by which plants adapt to the light environments.

Arabidopsis Chromatin Remodeling Factor PICKLE Interacts with Transcription Factor HY5 to Regulate Hypocotyl Cell Elongation

Light inhibits hypocotyl growth and the expression of genes that stimulate it. This study reveals that the CHD3 chromatin remodeling factor PKL/EPP1 is recruited by HY5, a master transcription factor of the light signaling pathway and represses H3K27me3 modification of cell elongation–related loci. PKL/EPP1 and HY5 work together to fine-tune hypocotyl cell elongation in response to light. Photomorphogenesis is a critical plant developmental process that involves light-mediated transcriptome changes, histone modifications, and inhibition of hypocotyl growth. However, the chromatin-based regulatory mechanism underlying this process remains largely unknown. Here, we identify ENHANCED PHOTOMORPHOGENIC1 (EPP1), previously known as PICKLE (PKL), an ATP-dependent chromatin remodeling factor of the chromodomain/helicase/DNA binding family, as a repressor of photomorphogenesis in Arabidopsis thaliana. We show that PKL/EPP1 expression is repressed by light in the hypocotyls in a photoreceptor-dependent manner. Furthermore, we reveal that the transcription factor ELONGATED HYPOCOTYL5 (HY5) binds to the promoters of cell elongation–related genes and recruits PKL/EPP1 through their physical interaction. PKL/EPP1 in turn negatively regulates HY5 by repressing trimethylation of histone H3 Lys 27 at the target loci, thereby regulating the expression of these genes and, thus, hypocotyl elongation. We also show that HY5 possesses transcriptional repression activity. Our study reveals a crucial role for a chromatin remodeling factor in repressing photomorphogenesis and demonstrates that transcription factor–mediated recruitment of chromatin-remodeling machinery is important for plant development in response to changing light environments.

Transposase-Derived Proteins FHY3/FAR1 Interact with PHYTOCHROME-INTERACTING FACTOR1 to Regulate Chlorophyll Biosynthesis by Modulating HEMB1 during Deetiolation in Arabidopsis

This study identifies FHY3 and FAR1 as positive regulators directly affecting chlorophyll biosynthesis through the activation of HEMB1. It shows that FHY3 protein physically interacts with PIF1, a negative regulator in the pathway, and they work coordinately to modulate the plant greening process. Successful chlorophyll biosynthesis during initial light exposure is critical for plant survival and growth, as excess accumulation of chlorophyll precursors in darkness can cause photooxidative damage to cells. Therefore, efficient mechanisms have evolved to precisely regulate chlorophyll biosynthesis in plants. Here, we identify FAR-RED ELONGATED HYPOCOTYL3 (FHY3) and FAR-RED IMPAIRED RESPONSE1 (FAR1), two transposase-derived transcription factors, as positive regulators of chlorophyll biosynthesis in Arabidopsis thaliana. We show that null mutations in FHY3 and FAR1 cause reduced protochlorophyllide (a precursor of chlorophyll) levels in darkness and less photobleaching in the light. We find that FHY3 directly binds to the promoter and activates expression of HEMB1, which encodes 5-aminolevulinic acid dehydratase in the chlorophyll biosynthetic pathway. We reveal that PHYTOCHROME-INTERACTING FACTOR1 physically interacts with the DNA binding domain of FHY3, thereby partly repressing FHY3/FAR1-activated HEMB1 expression. Strikingly, FHY3 expression is upregulated by white light. In addition, our genetic data indicate that overexpression, severe reduction, or lack of HEMB1 impairs plant growth and development. Together, our findings reveal a crucial role of FHY3/FAR1 in regulating chlorophyll biosynthesis, thus uncovering a new layer of regulation by which light promotes plant dark–light transition in early seedling development.

The Chromatin-Remodeling Factor PICKLE Integrates Brassinosteroid and Gibberellin Signaling during Skotomorphogenic Growth in Arabidopsis

This study reveals that the chromatin-remodeling factor PICKLE (PKL) functions as a signaling convergent point that integrates BR and GA signals that regulate skotomorphogenesis. PKL interacts with key transcription factors and modulates the chromatin state of their targets. It provides a direct molecular link between trimethylation of histone H3 Lys-27 and the BR and GA signaling pathways. Plant cell elongation is controlled by endogenous hormones, including brassinosteroid (BR) and gibberellin (GA), and by environmental factors, such as light/darkness. The molecular mechanisms underlying the convergence of these signals that govern cell growth remain largely unknown. We previously showed that the chromatin-remodeling factor PICKLE/ENHANCED PHOTOMORPHOGENIC1 (PKL/EPP1) represses photomorphogenesis in Arabidopsis thaliana. Here, we demonstrated that PKL physically interacted with PHYTOCHROME-INTERACTING FACTOR3 (PIF3) and BRASSINAZOLE-RESISTANT1 (BZR1), key components of the light and BR signaling pathways, respectively. Also, this interaction promoted the association of PKL with cell elongation–related genes. We found that PKL, PIF3, and BZR1 coregulate skotomorphogenesis by repressing the trimethylation of histone H3 Lys-27 (H3K27me3) on target promoters. Moreover, DELLA proteins interacted with PKL and attenuated its binding ability. Strikingly, brassinolide and GA3 inhibited H3K27me3 modification of histones associated with cell elongation–related loci in a BZR1- and DELLA-mediated manner, respectively. Our findings reveal that the PKL chromatin-remodeling factor acts as a critical node that integrates light/darkness, BR, and GA signals to epigenetically regulate plant growth and development. This work also provides a molecular framework by which hormone signals regulate histone modification in concert with light/dark environmental cues.

The VQ Motif-Containing Protein Family of Plant-Specific Transcriptional Regulators

Recent advances highlight the roles and mechanisms of the plant-specific VQ-motif-containing protein family in regulating stress and developmental processes. The VQ motif-containing proteins (designated as VQ proteins) are a class of plant-specific proteins with a conserved and single short FxxhVQxhTG amino acid sequence motif. VQ proteins regulate diverse developmental processes, including responses to biotic and abiotic stresses, seed development, and photomorphogenesis. In this Update, we summarize and discuss recent advances in our understanding of the regulation and function of VQ proteins and the role of the VQ motif in mediating transcriptional regulation and protein-protein interactions in signaling pathways. Based on the accumulated evidence, we propose a general mechanism of action for the VQ protein family, which likely defines a novel class of transcriptional regulators specific to plants.

Arabidopsis VQ MOTIF-CONTAINING PROTEIN29 Represses Seedling Deetiolation by Interacting with PHYTOCHROME-INTERACTING FACTOR1

A transcriptional regulator interacts with the transcription factor PIF1 to modulate hypocotyl cell growth in response to light. Seedling deetiolation, a critical process in early plant development, is regulated by an intricate transcriptional network. Here, we identified VQ MOTIF-CONTAINING PROTEIN29 (VQ29) as a novel regulator of the photomorphogenic response in Arabidopsis (Arabidopsis thaliana). We showed that 29 of the 34 VQ proteins present in Arabidopsis exhibit transcriptional activity in plant cells and that mutations in the VQ motif affect the transcriptional activity of VQ29. We then functionally characterized VQ29 and showed that the hypocotyl growth of plants overexpressing VQ29 is hyposensitive to far-red and low-intensity white light, whereas a vq29 loss-of-function mutant exhibits decreased hypocotyl elongation under a low intensity of far-red or white light. Consistent with this, VQ29 expression is repressed by light in a phytochrome-dependent manner. Intriguingly, our yeast (Saccharomyces cerevisiae) two-hybrid, bimolecular fluorescence complementation, and coimmunoprecipitation assays showed that VQ29 physically interacts with PHYTOCHROME-INTERACTING FACTOR1 (PIF1). We then showed that VQ29 and PIF1 directly bind to the promoter of a cell elongation-related gene, XYLOGLUCAN ENDOTRANSGLYCOSYLASE7, and coactivate its expression. Furthermore, the vq29 pif1 double mutant has shorter hypocotyls than either of the corresponding single mutants. Therefore, our study reveals that VQ29 is a negative transcriptional regulator of light-mediated inhibition of hypocotyl elongation that likely promotes the transcriptional activity of PIF1 during early seedling development.

A PIF1/PIF3-HY5-BBX23 Transcription Factor Cascade Affects Photomorphogenesis

Two PIF transcription factors activate the expression of HY5 and BBX23, the proteins of which interact to affect downstream gene expression in photomorphogenesis. Light signaling plays an essential role in controlling higher plants’ early developmental process termed as photomorphogenesis. Transcriptional regulation is a vital mechanism that is orchestrated by transcription factors and other regulatory proteins working in concert to finely tune gene expression. Although many transcription factors/regulators have been characterized in the light-signaling pathway, their interregulation remains largely unknown. Here, we show that PHYTOCHROME-INTERACTING FACTOR3 (PIF3) and PIF1 transcription factors directly bind to the regulatory regions of ELONGATED HYPOCOTYL5 (HY5) and a B-box gene BBX23 and activate their expression in Arabidopsis (Arabidopsis thaliana). We found that BBX23 and its close homolog gene BBX22 play a redundant role in regulating hypocotyl growth, and that plants overexpressing BBX23 display reduced hypocotyl elongation under red, far-red, and blue light conditions. Intriguingly, BBX23 transcription is inhibited by light, whereas its protein is degraded in darkness. Furthermore, we demonstrate that HY5 physically interacts with BBX23, and these two proteins coordinately regulate the expression of both light-induced and light-repressed genes. BBX23 is also recruited to the promoter sequences of the light-responsive genes in a partial HY5-dependent manner. Taken together, our study reveals that the transcriptional cascade consisting of PIF1/PIF3, HY5, and BBX23 controls photomorphogenesis, providing a transcriptional regulatory layer by which plants fine-tune their growth in response to changing light environment.

PICKLE is a repressor in seedling de-etiolation pathway

Light plays a vital role in seedling de-etiolation during which it remarkably inhibits hypocotyl growth and promotes cotyledon opening and the synthesis of chlorophyll and anthocyanin. After light perception, photoreceptors act to repress two main branches of the light signaling, PIFs and COP1-HY5. We recently identified PKL/EPP1, a chromatin remodeling factor, as a new component in regulating light-mediated hypocotyl growth. In this study, we found that EPP1 acts additively with SPA1 to repress seedling de-etiolation. Moreover, the expression of EPP1 is downregulated specifically in the hypocotyl region of the cop1 mutant compared with that of the wild type. We further found that EPP1 drastically inhibits both the protein and transcript levels of HY5, but not vice versa, indicating that HY5 acts downstream of EPP1. We thus propose a model in which EPP1 defines a new repressor and mediates a distinct signaling pathway of photomorphogenesis.

Glycosyltransferase‐like protein ABI8/ELD1/KOB1 promotes Arabidopsis hypocotyl elongation through regulating cellulose biosynthesis

Seedling de-etiolation (photomorphogenesis) is an important light-regulated developmental process in plants. Here, we showed that disruption of the gene encoding a glycosyltransferase-like protein, ABA INSENSITIVE 8 (ABI8)/ELONGATION EFFECTIVE 1 (ELD1)/KOBITO1 (KOB1), caused short-hypocotyl elongation under all light conditions examined and even in darkness. We found that the ABI8 transcript level was down-regulated by light in a phytochrome A-dependent manner. Furthermore, light destabilized ABI8 protein via the 26S proteasome degradation pathway. We showed that ABI8 promoted the expression of genes involved in cell elongation and cellulose synthesis. Consistently, the cellulose content was reduced in the abi8 mutants and application of 2, 6-dichlorobenzonitrile (an inhibitor of cellulose biosynthesis) mimicked the abi8 mutant phenotype. Moreover, we found that phytochrome and cryptochrome photoreceptors negatively, whereas CONSTITUTIVE PHOTOMORPHOGENIC 1 positively, regulated cellulose synthesis. We also showed that ELONGATED HYPOCOTYL 5 directly bound to the promoters of ABI8 and several cellulose synthesis genes and repressed their expression in light conditions. Taken together, our study reveals that ABI8 functions as a negative factor in light inhibition of hypocotyl elongation through modulating cellulose biosynthesis.