The transition from vegetative to reproductive growth Vegetative phase change is required to allow a shoot to be able to produce flowers English Ivy (Hedera helix) A shoot is only competent to flower once it has passed from the juvenile to

Adult the adult phase, a transition sometimes marked by gross morphological Juvenile leaf Adult leaf

changes Juvenile

The vegetative (juvenile to adult) phase transition is controlled by the relative abundance of microRNAs 156 and 172 Acacia koa Reprinted with permission friom Huijscer, P., and Schmid, M. (2011) The control of developmental phase transitions in plants. Development 138: 4117-4129. The nature of the flowering signal was elusive for decades Conversion of meristem vegetative to floral Environmental cues

“Florigen”

Julius von Sachs Mikhail Chailakhyan (1832-1897) (1901-1991) a.k.a. The “Father of Plant Physiology”. He was the first Proved the existence of a florigenic compound and to propose the existence of a chemical compound demonstrated that it is a small molecule, produced in capable of inducing flowering leaves and translocated to the shoot apex via the produced in leaves of illuminated plants phloem; he named it “florigen”

Credits: Romanov, 2012 Russian J Plant Phys 4:443-450; Redrawn from Ayre and Turgeon, 2004 Several physiological pathways regulate flowering These are called ‘enabling pathways’ as they regulate floral competence of the meristem Vernalization

Photoperiodic Autonomous GA-dependent pathway pathway pathway

Where is florigen? FLOWERING Molecular repressors LOCUS C (FLC) of flowering, also Note: This model called ‘anti-florigenic’ corresponds to signals, maintain the Arabidopsis but many of its modules have vegetative state of counterparts in other the meristem species Vegetative Florigen Flowering

Adapted from Reeves, P.H., and Coupland, G. (2001). Analysis of flowering time control in Arabidopsis by comparison of double and triple mutants. Plant Physiol. 126: 1085-1091. FLOWERING LOCUS T (FT) and its orthologs are considered the ‘florigen’ A mutation in Constitutive the tomato expression of ortholog SFT SFT using a leads to strong promoter delayed leads to early flowering and flowering and plants with plants with increased increased vegetative reproductive growth WT sft WT 35S::SFT growth

FT fulfills the criteria to be considered the ‘florigen’ hormone: • A graft-transmissible, phloem-mobile signal

• Synthesized in leaves and then transported to the shoot apical meristem • Promotes the transition from vegetative growth to flowering

Credits: Agustin Zsögön FT is part of the conserved CETS gene family of inducers and repressors

TFL1-like proteins: FT-like proteins: Flowering repressors Flowering inducers

Phylogenetic tree of the CETS protein family in 50 plant species

WT tfl1 WT ft Arabidopsis loss-of- Arabidopsis loss-of- function terminal flower-1 function ft mutant (right) mutant (tfl1, right) showing showing extended premature flowering vegetative growth

Benlloch, R., Berbel, A., Ali L., Gohari, G., Millán, T., and Madueño, F. (2015). Genetic control of inflorescence architecture in legumes. Front. Plant Sci. 6: 543; ; Wickland, D.P., and Hanzawa, Y. (2015). The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: Functional evolution and molecular mechanisms. Mol. Plant 8: 983-997. Matsoukas, I.G. (2015). Florigens and antiflorigens: a molecular genetic understanding. Essays In Biochemistry 58: 133-149.

FT and TFL1 are key floral integrators that compete for the same binding site

When FT binds to FD, flowering genes are activated and the switch from vegetative to reproductive growth is triggered at the apical meristem. TFL1 competes with FT for binding to FD.

FLOWERING LOCUS D: a bZIP TFL1 family receptor FD protein in the Vegetative meristem FT FD Flowering

Arabidopsis apical meristems Vegetative Inflorescence

Reproduced with permission from Hay, A., and Tsiantis, M. (2010). KNOX genes: versatile regulators of plant development and diversity. Development 137: 3153-3165. Expression of FT is under daylength control

In Arabidopsis, a long day plant, the CO transcription factor protein is stabilized in long days. CO accumulation leads to expression of FT and flowering. Expression of FT is under daylength control

In rice, a short day plant, CO accumulation represses expression of FT. Therefore, flowering is induced under short but not long days. The transition to flowering is controlled at the apical meristem

Flowering in tomato

SAM: shoot apical meristem TM: transitional meristem Meristems can produce SYM: vegetative axillary meristem inflorescences after a (sympodial meristem) succession of genetic IM: inflorescence meristem FM: floral meristem interconversions F: flowers

Périlleux, C., Lobet, G., Tocquin, P. (2014) Inflorescence development in tomato: gene functions within a zigzag model. Front. Plant Sci. 5: 121. The transition to flowering alters shoot architecture

Arabidopsis: Tends to form branches after floral transition Rice: Branches known Pea: Lateral as tillers form during branches form Leaves are shown in green, open vegetative growth. under flowering circles represent flowers, and Tillers may produce nodes arrows represent branches. inflorescences Drummond, R.S.M., et al. (2012) The expression of petunia strigolactone pathway genes is altered as part of the endogenous developmental program. Front. Plant Sci. 2: 115. Growth can by monopodial or sympodial

Sympodial Arabidopsis: Petunia: growth Monopodial Sympodial (literally, single (literally, joined foot). One apical feet). After the meristem initial apical produces all meristem primary tissues transitions to Initial flowing, monopodial vegetative growth until growth first flowering continues from an axillary branch Leaves are shown in green, open circles represent flowers, and arrows represent branches.

Drummond, R.S.M., et al. (2012) The expression of petunia strigolactone pathway genes is altered as part of the endogenous developmental program. Front. Plant Sci. 2: 115. Tomato is the classic example of sympodial growth, from multiple meristems

Sympodial growth in tomato

The apex terminates in a flower or inflorescence and In most tomatoes each vegetative growth {sympodium} is composed continues from a by three leaves (1-3) and subtending axillary an inflorescence meristem that assumes the top- most position.

Zsögön, A., Cermak, T., Voytas, D., Peres, L.E.P. (2017) Genome editing as a tool to achieve the crop ideotype and de novo domestication of wild relatives: Case study in tomato. Plant Sci. 256: 120-130 Summary: The transition from vegetative to reproductive growth

• The transition to flowering is determined by ecological strategies and dramatically alters shoot architecture • Monopodial species produce vegetative and reproductive structures from a single (“mono”) apical meristem • Sympodial species grow by a concatenation of different meristems which assume the top-most position sequentially • Florigen is a hypothetical molecule proposed by early plant physiologists as a trigger of the transition to flowering • FLOWERING LOCUS T (FT) in Arabidopsis and its orthologs in other species fulfill multiple tenets of the florigen • The FT gene family, called CETS, includes repressors of flowering such as TERMINAL FLOWER 1 (TFL1) • The FT/TFL1 genetic module is conserved in many species and influences shoot architecture by altering the vegetative/reproductive balance