Light and phytohormone are external and internal cues that regulate plant growth and development throughout their life cycle. BBXs (B-box domain proteins) are a group of zinc finger proteins that not only directly govern the transcription of target genes but also associate with other factors to create a meticulous regulatory network to precisely regulate numerous aspects of growth and developmental processes in plants. Recent studies demonstrate that BBXs play pivotal roles in light-controlled plant growth and development. Besides, BBXs have been documented to regulate phytohormone-mediated physiological procedures. In this review, we summarize and highlight the multi-faced role of BBXs, with a focus in photomorphogenesis, photoperiodic flowering, shade avoidance, abiotic stress, and phytohormone-mediated growth and development in plant.

B-box containing proteins (BBXs) integrate light and various hormonal signals to regulate plant growth and development. Here, we demonstrate that the photomorphogenic repressors BBX28 and BBX29 positively regulate brassinosteroid (BR) signaling in Arabidopsis thaliana seedlings. Treatment with the BR brassinolide stabilized BBX28 and BBX29, which partially depended on BR INSENSITIVE1 (BRI1) and BIN2. bbx28 bbx29 seedlings exhibited larger cotyledon aperture than the wild-type when treated with brassinazole in the dark, which partially suppressed the closed cotyledons of brassinazole resistant 1-1D (bzr1-1D). Consistently, overexpressing BBX28 and BBX29 partially rescued the short hypocotyls of bri1-5 and bin2-1 in both the dark and light, while the loss-of-function of BBX28 and BBX29 partially suppressed the long hypocotyls of bzr1-1D in the light. BBX28 and BBX29 physically interacted with BR-ENHANCED EXPRESSION1 (BEE1), BEE2, and BEE3 and enhanced their binding to and activation of their target genes. Moreover, BBX28 and BBX29 as well as BEE1, BEE2, and BEE3 increased BZR1 accumulation to promote the BR signaling pathway. Therefore, both BBX28 and BBX29 interact with BEE1, BEE2, and BEE3 to orchestrate light and BR signaling by facilitating the transcriptional activity of BEE target genes. Our study provides insights into the pivotal roles of BBX28 and BBX29 as signal integrators in ensuring normal seedling development.

Intron retention (IR) is the most common alternative splicing event in Arabidopsis. An increasing number of studies have demonstrated the major role of IR in gene expression regulation. The impacts of IR on plant growth and development and response to environments remain underexplored. Here, we found that IR functions directly in gene expression regulation on a genome-wide scale through the detainment of intron-retained transcripts (IRTs) in the nucleus. Nuclear-retained IRTs can be kept away from translation through this mechanism. COP1-dependent light modulation of the IRTs of light signaling genes, such as PIF4, RVE1, and ABA3, contribute to seedling morphological development in response to changing light conditions. Furthermore, light-induced IR changes are under the control of the spliceosome, and in part through COP1-dependent ubiquitination and degradation of DCS1, a plant-specific spliceosomal component. Our data suggest that light regulates the activity of the spliceosome and the consequent IRT nucleus detainment to modulate photomorphogenesis through COP1.

Light and brassinosteroid (BR) are external stimuli and internal cue respectively, that both play critical roles in a wide range of developmental and physiological process. Seedlings grown in the light exhibit photomorphogenesis, while BR promotes seedling etiolation. Light and BR oppositely control the development switch from skotomorphogenesis in the dark to photomorphogenesis in the light. Recent progress report that substantial components have been identified as hubs to integrate light and BR signals. Photomorphogenic repressors including COP1, PIFs, and AGB1 have been reported to elevate BR response, while photomorphogenesis-promoting factors such as HY5, BZS1, and NF-YCs have been proven to repress BR signal. In addition, BR components also modulate light signal. Here, we review the current research on signaling network associated with light and brassinosteroids, with a focus on the integration of light and BR signals enabling plants to thrive in the changeable environment.

BR-ENHANCED EXPRESSION1 (BEE1), BEE2, and BEE3, key transcriptional components of brassinosteroid signaling, have been shown to play critical roles in regulating light signaling. However, the precise molecular mechanism by which BEE1/2/3 repress photomorphogenesis remains elusive. In this study, we found that light triggers the degradation of BEE1/2/3 proteins through the 26S proteasome system. BEE1/2/3 interact with PHYTOCHROME A (phyA) and phyB, and this interaction promotes the degradation of BEE3. Mutations in BEE1/2/3 exhibit short hypocotyls and partially suppress the long hypocotyl phenotype of the phyA phyB double mutant. BEE1/2/3 attenuate the interaction between phyB and PHYTOCHROME-INTERACTING FACTOR 3 (PIF3), leading to PIF3 stabilization and subsequent repression of photomorphogenesis. In addition, BEE1/2/3 interact with SUPPRESSORs OF PHYTOCHROME A (SPAs) to disrupt the phyA/B-SPA1 association, thereby further attenuating the exaggerated light signaling. The COP1–SPAs complexes stabilize BEE1/3 under both dark and light conditions. Mutations in BEE1/2/3 enhance the constitutively photomorphogenic phenotype of spa1/2/4, whereas overexpression of BEE1/3 partially rescue the short hypocotyls of cop1 and spa1/2/4. Collectively, these findings demonstrate that BEE1/2/3 fine-tune the phyA/B-COP1/SPA1 signaling hub to negatively regulate photomorphogenesis in response to excessive light signaling. Our study provides insights into the pivotal roles of BEE1/2/3 as photomorphogenic repressors, facilitating adaptation to complex light conditions.