FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar

Abstract

Annual plants grow vegetatively at early developmental stages and then transition to the reproductive stage, followed by senescence in the same year. In contrast, after successive years of vegetative growth at early ages, woody perennial shoot meristems begin repeated transitions between vegetative and reproductive growth at sexual maturity. However, it is unknown how these repeated transitions occur without a developmental conflict between vegetative and reproductive growth. We report that functionally diverged paralogs FLOWERING LOCUS T1 (FT1) and FLOWERING LOCUS T2 (FT2), products of whole-genome duplication and homologs of Arabidopsis thaliana gene FLOWERING LOCUS T (FT), coordinate the repeated cycles of vegetative and reproductive growth in woody perennial poplar (Populus spp.). Our manipulative physiological and genetic experiments coupled with field studies, expression profiling, and network analysis reveal that reproductive onset is determined by FT1 in response to winter temperatures, whereas vegetative growth and inhibition of bud set are promoted by FT2 in response to warm temperatures and long days in the growing season. The basis for functional differentiation between FT1 and FT2 appears to be expression pattern shifts, changes in proteins, and divergence in gene regulatory networks. Thus, temporal separation of reproductive onset and vegetative growth into different seasons via FT1 and FT2 provides seasonality and demonstrates the evolution of a complex perennial adaptive trait after genome duplication.ife cycles of higher plants display a great diversity in morphological and seasonal adaptation. Annual plants grow, reproduce, and senesce within a growing season, whereas woody perennials display successive years of vegetative growth before reaching sexual maturity (1-3). After this time, shoot meristems begin cyclical transitions between vegetative and reproductive growth. Consequently, shoots may repeatedly form early vegetative buds (Vegetative Zone I), reproductive buds (Floral Zone), and late vegetative buds (Vegetative Zone II) in a sequential manner (3). However, our understanding of the mechanisms underlying such complex phenotypes, and thus variation in growth habits and adaptation, remain rudimentary. In the herbaceous perennial Arabis alpina, repeated transcriptional repression and activation of PERPETUAL FLOWERING 1 (PEP1), an ortholog of the floral repressor FLOWERING LOCUS C (FLC) in annual Arabidopsis thaliana (4), controls recurring seasonal transitions between reproductive and vegetative phases (5). However, a true functional ortholog of FLC has not been reported in trees, nor does phylogenetic analysis point to a clear structural ortholog of FLC in poplar (Populus spp.) (6).Previous results showed that FLOWERING LOCUS T1 (FT1) (7) and FLOWERING LOCUS T2 (FT2) (8) under the cauliflower mosaic virus 35S (CaMV 35S) constitutive overexpression promoter induce early flowering in poplar. Transcript abundance of both genes gradually increases in the growing season as poplar trees mature....

Mutation inTERMINAL FLOWER1Reverses the Photoperiodic Requirement for Flowering in the Wild StrawberryFragaria vesca

“…However, its up-regulation in the LDs of spring is crucial for perennialism, because it prevents further floral initiation in the newly emerged axillary shoots until SD conditions return. Our results on FvTFL1 and earlier findings that seasonal changes in the expression of two Populus FTlike genes regulate the perennial growth cycle in Populus (Hsu et al, 2011) highlight the importance of CETS proteins in the control of perennialism. Also, in A. alpina, TFL1 contributes to perennialism by regulating the age-dependent sensitivity of meristems to vernalization; but transient silencing of the FLC ortholog, PEP1, by vernalization has a major role in the cycling between vegetative and generative phases in this species (Wang et al, 2009(Wang et al, , 2011.…”

“…Detailed analyses of two Populus FT paralogs have shown that seasonal changes in their expression control the cycling of reproductive and vegetative growth. Winter cold (vernalization) activates FT1, which promotes flowering, whereas LD and high temperature activate FT2, which promotes vegetative growth and prevents bud set (Hsu et al, 2011). In Arabis alpina, the return to vegetative development after flowering is regulated by transient silencing of the FLOWERING LOCUS C (FLC) ortholog PERPETUAL FLOWERING1 (PEP1) by vernalization (Wang et al, 2009).…”

Dual role of tree florigen activation complex component FD in photoperiodic growth control and adaptive response pathways

“…Interestingly, FT homologs are also involved in the control of diverse developmental transitions distinct from flowering, such as tuberization in potatoes (6), bulb formation in onions (7), stomatal opening (8), and photoperiodic control of seasonal growth in trees (9)(10)(11). These observations suggest that complexes of FT are not only important to the control of flowering but have a broader functionality.…”

TheFragaria vescaHomolog of SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 Represses Flowering and Promotes Vegetative Growth

“…In perennials, which undergo repeated cycles of vegetative and reproductive phases, flowering time is controlled by seasonal regulation of flowering genes (Böhlenius et al, 2006;Wang et al, 2009;Koskela et al, 2012). Moreover, homologous genes, or genes classified in the same gene family, may have roles during the seasonal cycle beyond those that are known in annual species (Böhlenius et al, 2006;Hsu et al, 2011). Therefore, careful analysis of gene functions in the different phases of seasonal cycles is required to better understand perennial growth.…”