Evolution and expression of the MADS-box flowering transition genes AGAMOUS-like 24/SHORT VEGETATIVE PHASE with emphasis in selected Neotropical orchids

In angiosperms the reproductive transition results in the transformation of a vegetative apical meristem (SAM) into an inflorescence meristem (IM), capable of forming floral meristems (FM). Two key players in the flowering transition are AGAMOUS-like 24 (AGL24) and SHORT VEGETATIVE PHASE (SVP). They are eudicot MADS-box paralogs performing opposite roles, as AGL24 positively regulates flowering while SVP represses the reproductive transition in Arabidopsis. We confirm that the Arabidopsis functional reference cannot be readily extrapolated to all eudicots as there are additional duplications of AGL24 in early divergent eudicots and core eudicots with significant sequence variation. In addition, we found that in monocots, two additional independent duplication events have resulted in at least three clades of AGL24/SVP homologs, some only found in Orchidaceae. Protein sequence analyses and comparative evolutionary rates point to higher rates of relaxed negative selection in the Core Eudicot AGL24 B and the Orch SVP-like B clades, in eudicots and monocots respectively. On the other hand, expression data points to plesiomorphic pleiotropic roles of AGL24/SVP genes likely similar to SVP core eudicot genes, and the acquisition of new roles as flowering positive regulators in Core Eudicot AGL24 A genes. Our research presents evidence on the diversification and recruitment of AGL24/SVP homologs in flowering transition in orchids. Although, broad expression of most copies does not allow to determine if they act as flowering repressors or promoters, the restricted expression of some homologs in the SAM suggests putative roles in maintaining the vegetative phase. If so studying in detail the function of AGL24/SVP homologs in orchids is critical to identify putative flowering repressors in a lineage where other canonical repressors remain elusive.

Automated summary

The study highlights the diverse roles of AGL24 and SVP in the flowering transition in angiosperms, with variations in different lineages. Independent duplication events in monocots have resulted in at least three clades of AGL24/SVP homologs, some specific to Orchidaceae. The analysis suggests higher evolutionary rates and potential pleiotropic roles of these genes in maintaining the vegetative phase and promoting flowering in different plant groups.