Asymmetric expansions of FT and TFL1 lineages characterize differential evolution of the EuPEBP family in the major angiosperm lineages

Abstract

Background In flowering plants, precise timing of the floral transition is crucial to maximize chances of reproductive success, and as such, this process has been intensively studied. FLOWERING LOCUS T (FT) and TERMINAL FLOWER1 (TFL1) have been identified as closely related eukaryotic phosphatidylethanolamine-binding proteins (‘EuPEBPs’) that integrate multiple environmental stimuli, and act antagonistically to determine the optimal timing of the floral transition. Extensive research has demonstrated that FT acts similar to hormonal signals, being transported in the phloem from its primary site of expression in leaves to its primary site of action in the shoot meristem; TFL1 also appears to act as a mobile signal. Recent work implicates FT, TFL1, and the other members of the EuPEBP family, in the control of other important processes, suggesting that the EuPEBP family may be key general regulators of developmental transitions in flowering plants. In eudicots, there are a small number of EuPEBP proteins, but in monocots, and particularly grasses, there has been a large, but uncharacterized expansion of EuPEBP copy number, with unknown consequences for the EuPEBP function. Results To systematically characterize the evolution of EuPEBP proteins in flowering plants, and in land plants more generally, we performed a high-resolution phylogenetic analysis of 701 PEBP sequences from 208 species. We refine previous models of EuPEBP evolution in early land plants, demonstrating the algal origin of the family, and pin-pointing the origin of the FT/TFL1 clade at the base of monilophytes. We demonstrate how a core set of genes (MFT1, MFT2, FT, and TCB) at the base of flowering plants has undergone differential evolution in the major angiosperm lineages. This includes the radical expansion of the FT family in monocots into 5 core lineages, further re-duplicated in the grass family to 12 conserved clades. Conclusions We show that many grass FT proteins are strongly divergent from other FTs and are likely neo-functional regulators of development. Our analysis shows that monocots and eudicots have strongly divergent patterns of EuPEBP evolution.

The FLOWERING LOCUS T gene expression is controlled by high‐irradiance response and external coincidence mechanism in long days in Arabidopsis

“…With the advent of molecular genetics utilizing Arabidopsis and rice ( Oryza sativa ), florigen was finally revealed to be a small mobile protein encoded by FLOWERING LOCUS T ( FT ) gene in Arabidopsis and its homolog, Heading day 3a ( Hd3a ) gene in rice (Corbesier et al ., 2007; Tamaki et al ., 2007). FLOWERING LOCUS T belongs to a gene family found in all angiosperms (Bennett & Dixon, 2021; Jin et al ., 2021). This family contains FT orthologs and paralogs with inhibitory roles in flowering.…”

CRISPR/Cas9 mutants delineate roles ofPopulus FTandTFL1/CEN/BFTfamily members in growth, dormancy release and flowering

“…Recently, mutagenesis of FT2 showed its essential role in maintaining shoot growth in long days (LDs; Andre et al 2022a; Gomez-Soto et al 2021). FT2 is a member of the PHOSPHATIDYLETHANOLAMINE-BINDING PROTEIN (PEBP) family that in angiosperms consists of three major clades, here named for family members: FT, T ERMINAL FLOWER1 (TFL1)/ C ENTRORADIALIS(CEN)/ B ROTHER OF FT AND TFL1 (BFT) (TCB clade) and MOTHER OF FT AND TFL1 (MFT) (Bennett and Dixon 2021). The balance between florigen FT and indeterminacy-promoting TCB members is a broadly conserved mechanism to control flowering time and plant architecture; however, gene duplication and evolution have resulted in functional diversification among paralogs and orthologs (reviewed in Jin et al 2021; Wickland and Hanzawa 2015).…”

Identification and Functional Characterization of FLOWERING LOCUS T in Platycodon grandiflorus

“…In addition, segment A (LGRQTVYAPGWRQN), which forms an external loop and is required for FT proteins to act as a floral activator [ 26 ], and LYN, which is required for FT full functionality with segment A [ 25 ], were found in PlgFT protein. In flowering pathways, FT and TFL1 act as flowering regulators with homology to phosphatidylethanolamine-binding proteins [ 20 , 21 ]. Although Arabidopsis FT exhibits protein sequence similarity of ~60% with Arabidopsis TFL1, they function in an opposite manner [ 21 , 27 ].…”

“…Similarly, the day-natural tomato flowering is regulated by the FT-homologue SFT/SP3D gene, which is regulated independently of CO and day length [ 11 , 19 ]. In plants, the flowering transition and inflorescence architecture are modulated by eukaryotic phosphatidylethanolamine-binding protein family, which contains TWIN SISTER OF FT (TSF), TERMINAL FLOWER 1 (TFL1), ARABIDOPSIS THALIANA CENTRORADIALIS (ATC), BROTHER OF FT AND TFL1 (BFT), and MOTHER OF FT AND TFL1 (MFT) [ 20 ]. Among them, FT functions as the mobile flower-promoting signal, which promotes the transition to reproductive development and flowering, whereas TFL1 plays as a repressor of this transition [ 21 ].…”