The gibberellins (GAs) receptor GA INSENSITIVE DWARF1 (GID1) plays a central role in GA signal perception and transduction. The typical photoperiodic plant chrysanthemum (Chrysanthemum morifolium) only flowers when grown in short-day photoperiods. In addition, chrysanthemum flowering is also controlled by the aging pathway, but whether and how GAs participate in photoperiod- and age-dependent regulation of flowering remain unknown. Here, we demonstrate that photoperiod affects CmGID1B expression in response to GAs and developmental age. Moreover, we identified PHOTOLYASE/BLUE LIGHT RECEPTOR2, an atypical photocleavage synthase, as a CRYPTOCHROME-INTERACTING bHLH1 interactor with which it forms a complex in response to short days to activate CmGID1B transcription. Knocking down CmGID1B raised endogenous bioactive GA contents and GA signal perception, in turn modulating the expression of the aging-related genes MicroRNA156 and SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3. We propose that exposure to short days accelerates the juvenile-to-adult transition by increasing endogenous GA contents and response to GAs, leading to entry into floral transformation.

The decision to flower in chrysanthemum (Chrysanthemum morifolium) is controlled by the photoperiod imposed by the outside environment along with endogenous gibberellin levels. Small peptides have broad and critical functions throughout the plant life cycle, but whether and how small peptides are involved in photoperiod- and gibberellin-dependent regulation of flowering remain unclear. Here, we demonstrate that a GIBBERELLIC ACID-STIMULATED TRANSCRIPT (GAST) peptide family member, CmGAST1, promotes flowering in chrysanthemum by interacting with SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9), a key regulator of flowering in the age-dependent pathway. CmGAST1 expression was induced under short-day photoperiods and by gibberellin treatment. In addition, we show that a negative regulator of GA signaling GIBBERELLIC ACID INSENSITIVE (GAI) interacts with CALMODULIN 7 (CAM7), a key factor in calcium signaling, and the resulting CmCAM7–GAI complex directly suppresses CmGAST1 expression. Notably, short-day photoperiods induce the accumulation of bioactive gibberellins and Ca2+ in the shoot apex, thereby inhibiting CmGAI and CmCAM7, respectively, and releasing their inhibition of CmGAST1 expression. We propose that the peptide CmGAST1 integrates gibberellin and calcium signals, coordinating the photoperiod and aging pathways to accelerate chrysanthemum maturation and flowering.

Gibberellins (GAs) is a key endogenous hormone regulating chrysanthemum flowering, and Gibberellin INSENSITIVE DWARF1 (GID1) is the core receptor of the gibberellin (GA) signaling pathway. However, the functional mechanism of CmGID1A remains unelucidated. Here, we constructed CmGID1A-RNAi silencing lines, and characterized the biological function of CmGID1A by phenotypic identification, protein interaction assays, qRT-PCR and RNA-seq. The results of RT-qPCR showed that CmGID1A responds to short days and gibberellins. Inhibition of the expression of CmGID1A can significantly promote the transition of chrysanthemum from the vegetative growth stage to the reproductive growth stage and accelerate its flowering process. Bimolecular fluorescence complementation (BiFC) and yeast two-hybrid (Y2H) assays confirmed that CmGID1A interacts with the DELLA protein CmRGL1 in a gibberellin-dependent manner. RNA-seq results revealed that silencing of CmGID1A leads to a significant up-regulation of downstream Ethylene Response Factor 6 (ERF6) expression. Collectively, CmGID1A acts as a GA receptor to mediate GA signal transduction via interacting with CmRGL1, and regulates the expression of CmERF6 and other downstream genes, thereby participating in the regulation of floral transition in chrysanthemum. This study clarifies the core role of CmGID1A in the GA signaling pathway and provides novel experimental data for enriching the molecular regulatory mechanism of GA in floral transition in chrysanthemum.

Gibberellins (GAs) are key endogenous hormones regulating chrysanthemum flowering, and Gibberellin INSENSITIVE DWARF1 (GID1) is the core receptor of the gibberellin (GA) signaling pathway. However, the functional mechanism of CmGID1A remains unelucidated. Here, we constructed CmGID1A-RNAi silencing lines and characterized the biological function of CmGID1A by phenotypic identification, protein interaction assays, qRT-PCR and RNA-seq. The results of RT-qPCR showed that CmGID1A responds to short days and gibberellins. Inhibition of the expression of CmGID1A can significantly promote the transition of chrysanthemum from the vegetative growth stage to the reproductive growth stage and accelerate its flowering process. Bimolecular fluorescence complementation (BiFC) and yeast two-hybrid (Y2H) assays confirmed that CmGID1A interacts with the DELLA protein CmRGL1 in a gibberellin-dependent manner. RNA-seq results revealed that silencing of CmGID1A leads to a significant up-regulation of downstream Ethylene Response Factor 6 (ERF6) expression. Collectively, CmGID1A acts as a GA receptor to mediate GA signal transduction via interacting with CmRGL1, and regulates the expression of CmERF6 and other downstream genes, thereby participating in the regulation of floral transition in chrysanthemum. This study clarifies the core role of CmGID1A in the GA signaling pathway and provides novel experimental data for enriching the molecular regulatory mechanism of GA in floral transition in chrysanthemum.