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ScienceDirect
FT and florigen long-distance flowering control in plants
Joanna Putterill1 and Erika Varkonyi-Gasic2
The great hunt for florigen, the universal, long distance
flowering regulator proposed by Chailakhan in the 1930s,
resulted in the discovery a decade ago that FT-like proteins
fulfilled the predictions for florigen. They are small (175
amino acids), globular, phosphatidylethanolamine-binding
(PEBP) proteins, phloem-expressed, graft-transmissible and
able to move to the shoot apex to act as potent stimulators
of flowering in many plants. Genes that regulate Arabidopsis
FT protein movement and some features of Arabidopsis FT
protein that make it an effective florigen have recently
been identified. Although floral promotion via graft transmission
of FT has not been demonstrated in trees, FT-like genes have
been successfully applied to reducing the long juvenile
(pre-flowering) phase of many trees enabling fast track
breeding.
Addresses
1
The Flowering Lab, School of Biological Sciences, University of
Auckland, Auckland, New Zealand
2
The New Zealand Institute for Plant & Food Research Limited (Plant &
Food Research) Mt Albert, Private Bag 92169, Auckland Mail Centre,
Auckland 1142, New Zealand
Corresponding author: Putterill, Joanna (j.putterill@auckland.ac.nz)

i. Plants usually have several FT-like genes that play

overlapping and/or distinct roles in promoting flowering. For example, FT and TSF promote Arabidopsis
flowering, as do Hd3a and RFT1 in rice and GmFT2a
and GmFT5a in soybean [916].
ii. Some FT-like genes repress flowering (antiflorigens). For
example, sugar beet has two FT-like genes, FT1 that
represses flowering and FT2 that promotes flowering
[17].
iii. The balance of activity of florigens and antiflorigens is
important for overall growth, architecture, and/or
flowering. This was first elucidated for FT and TFL1like genes in the tomato model [1820].
iv. Not all FT-like genes regulate flowering. For example, FT
gene family members in potato and onion have roles
in storage organ differentiation [21,22] and poplar FT
genes have diverse roles in seasonal phenology [23].
v. There is diversity in the regulators of FT. For example,
CO promotes long day photoperiodic flowering
control of Arabidopsis FT and rice CO (Hd1)
functions in short day induction of rice FT (Hd3a)
and flowering [7]. However, CO-like genes do not
regulate FT in all plants including the temperate long
day legumes pea and Medicago [10,11,24].

Current Opinion in Plant Biology 2016, 33:7782

This review comes from a themed issue on Cell signalling and gene
regulation
Edited by Kimberley Snowden and Dirk Inze

Building on recent reviews on FT and flowering time

control [911,19,23,2528], here we provide an update on
two important aspects of FT research; first, how FT
functions as a mobile florigen and second the applications
of FT/TFL1-like genes to flowering control in woody
perennial plants.

http://dx.doi.org/10.1016/j.pbi.2016.06.008
1369-5266/# 2016 Elsevier Ltd. All rights reserved.

Introduction
The timing of flowering is critical for successful sexual
reproduction, crop productivity and yield [1,2]. A decade
ago FT, a gene first described in the pioneering Koornneef paper on late flowering Arabidopsis mutants and
then identified as a major integrator of flowering signals,
was discovered to encode a protein that functioned as a
major florigen a universal, long distance flowering activator in different plants including tomato, rice and
Arabidopsis [38].
Today, FT research is progressing in many directions.
Some major insights from studies in different plants are:
www.sciencedirect.com

Update on FT protein as a major florigen

FT protein was identified in the vascular stream of several

annual plants and key proof that mobile FT protein,
rather than its RNA, was the major florigen came from
experiments performed in tomato, Arabidopsis, rice and
cucurbits [3,15,19,2934]. Once FT protein enters the
sieve elements from the phloem companion cells, it
travels with the phloem translocation stream to the shoot
apex. FT unloads from the phloem and moves cell-to-cell
to interact with the bZIP transcription factor FD and
switch on the floral development program [6].
An important advance in FT biology in 2011 was the
crystal structure of the proposed florigen activation complex (FAC) at the rice shoot apex comprised of two of
each FT, FD and 14-3-3 proteins [26,27,35]. The complex stimulates flowering by activating transcription of
OsMASDS15 and in Arabidopsis the floral integrator gene
SOC1 and the floral meristem identity gene AP1 [6,35].
Current Opinion in Plant Biology 2016, 33:7782

78 Cell signalling and gene regulation

The predicted spatio-temporal aspects of the proposed

FAC and targets in the rice shoot apex were recently
confirmed [36]. FT, as a PEBP protein might also be
expected to bind lipids. A recent report demonstrated that
FT also binds to the phospholipid phosphatidylcholine in
vitro, and in vivo manipulation of phosphatidylcholine
availability and type at the Arabidopsis shoot apex affects
flowering time, in a partly FT-dependant manner [37].
In addition, 2014 saw the most comprehensive functional
mutagenesis on FT protein to date built on previous
structural and mutagenesis studies of FT and TFL1
proteins [38]. The effect of overexpression of hundreds
of FT point mutations on flowering time was determined.
The majority of the mutants remained functional, but
inactive and neomorphic mutants were obtained; four
new point mutations affected the surface charge of FT,
potentially impacting on docking of regulatory ligands
such as TCP proteins, converting FT to a TFL1-like
repressor.
The mechanisms controlling FT movement are not well
understood overall. However, in 2013 the first FT mutagenesis to focus on mobility was reported [39]. Triple FT
movement mutants carrying mutations at the following
residues; V69A, S75A and R82A in pumpkin FTL2 or
V70A, S76A and R83A in Arabidopsis FT entered the
pumpkin sieve tube system, but did not move beyond
the terminal phloem and were unable to stimulate flowering. However, they promoted flowering when expressed
throughout the plant. In addition, two mutants in adjacent
FT residues in a different region, D17K and V18A, did not
accelerate flowering nearly as well from the phloem-specific SUC2 promoter than the CaMV35S or FD (shoot apex
specific) promoters, implying a defect in movement [38].
A recent study using micrografting showed that two
highly related (82% identical) Arabidopsis FT proteins
that promote flowering, FT and TSF, were not equal with
regard to their florigenic ability [40]. When over
expressed from the CaMV35S promoter, both genes
caused transgenic plants to flower very early. However,
only CaMV35S:FT rootstocks (donors) could stimulate
flowering of grafted ft tsf scions, while CaMV35S:TSF
rootstocks virtually lacked activity (Figure 1). Swapping
Region 2 of FT (L28-G98) into TSF imbued it with
better florigenic activity and chimeric proteins were detectable in the shoot apex. However, insertion of TSF
Region 2 into FT did not block FT movement, indicating
the influence of other FT regions.
Turning to other regulators of FT movement, the Arabidopsis genes FTIP1 and FE both promote flowering in
long days and are expressed in the phloem [41,42]. Less
FT protein was present in the shoot apex of ftip1 mutant
plants because of a reduction in the amount of FT protein
entering the sieve elements from the phloem companion
Current Opinion in Plant Biology 2016, 33:7782

cells, while single-leaf induction of FT protein, saw fe

mutants accumulating less FT protein in their shoot
apices than wild type plants.
FTIP1 [41] was first identified as a FT interactor in yeast
two hybrid experiments. An in situ Proximity Ligation
Assay (PLA) indicated that FTIP1 and FT proteins also
interact in phloem companion cells. FTIP1 protein localises to the phloem companion cells and plasmodesmata
connecting companion cells and sieve elements. It is an
ER-localised membrane protein with a PRT_C membrane-targeting domain and predicted C2 domains reminiscent of membrane-trafficking synaptotagmins and may
function as a movement chaperone for FT [19,41]. FE,
the last of the classical flowering time genes [5] to be
molecularly characterised, encodes a MYB-like transcription factor expressed in the phloem [42]. By promoting
the transcription of both FTIP and FT in long days, FE
positively influenced the production and transport of FT
and the transition to flowering. Genetic analysis found
that the fe-1 ftip1-1 double mutant was slightly later
flowering than either of the single mutants and it was
described as more-than-additive, indicating independent
and common functions.
Application of FT genes to flowering regulation in trees

Much less is known about regulation of flowering time in

woody perennial plants. However, flowering control is of
particular interest because of their long juvenile period
before they become competent to flower, followed by
seasonal vegetative and reproductive growth and coexistence of vegetative and floral meristems on the same
shoot. Shortened juvenility and precocious flowering are
important breeding goals in fruit trees and vines; on the
other hand, understanding flowering-time regulation can
provide practical means to prevent flowering to improve
the biomass and quality of wood in forestry and biofuel
crops. Here, we focus on regulation of flowering with FT
genes and their perceived role as florigen in woody
perennials.
Ample evidence confirms the role of some FT genes as
activators of flowering in woody perennial plants. For
example, constitutive expression of endogenous FT
genes in poplar and citrus resulted in early flowering
[43,44]. Similarly constitutive expression of Arabidopsis
FT promoted flowering in Eucalyptus [45] as did expression from a heat-inducible promoter in juvenile poplar
[43] (Figure 2) or by viral delivery into cotton, apple and
pear [46,47,48,49]. Constitutive expression of poplar
FT1 also gave early maturity and continuous flowering
in plum [50] and its inducible expression promoted
flowering in apple [51] (Figure 2).
Studies in woody perennials also highlight the importance
of TFL1-like repressor genes in flowering. Down regulation of TFL1 accelerated the onset of first flowering in
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FT and florigen long-distance flowering control Putterill and Varkonyi-Gasic 79

Figure 1

Figure 2

Poplar

Arabidopsis

Scion

ft tsf

ft tsf

ft tsf

Rootstock

ft tsf

35S:TSF

35S:FT

Current Opinion in Plant Biology

Scion

Greater florigenic activity of FT compared to TSF demonstrated by

grafting in Arabidopsis. Very late flowering Arabidopsis ft tsf double
mutant, homo-grafted, produces a high number of leaves before
flowering (left), a grafted plant with CaMV35S:TSF rootstock and ft tsf
scion flowers slightly more rapidly (middle), but is still very delayed
compared to the very early flowering grafted plant with CaMV35S:AtFT
rootstock and ft tsf scion (right).

poplar, apple and pear [5254]. Using virus delivery,

simultaneous down regulation of TFL1 combined with
over expression of Arabidopsis FT greatly increased the
efficiency of floral promotion in apple and pear and led to
continuous flowering [48,49].

Rootstock

Indirect evidence on possible mobility of FT protein over

long distances in woody perennials is very scarce. There
are no reports on detection of FT in the phloem or xylem
sap in perennials. Some answers have been provided by a
recent study of mobility of pear FT-like protein PcFT2 in
tobacco and apple [56]. Ectopic expression of PcFT2
fused to YFP promoted flowering in tobacco, this effect
was graft-transmissible and the fusion protein, but not
PcFT2 RNA, was identified in the non-transgenic scion.
In a similar experiment in apple, movement of the fusion
protein was detected. Although it did not promote flowering, this indicated the presence of the mechanism for FT
movement in the vascular tissue in woody perennials.
The accessibility of signal conduits provides one possible
regulatory mechanism for intercellular signal delivery in
trees; reopening of conduits and transcription of FT are
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pHSP:AtFT

WT

pHSP:PtFT1

pHSP:AtFT

Apple

Scion
Rootstock

Remarkably, there is little evidence that any FT protein

(or RNA) moves in trees. One exception is graft-transmissible early flowering in a small woody shrub Jatropha
[55]. Expression of Jatropha JcFT under the control of
the relatively weak synthetic G10-90 promoter reduced
flowering time from 8 months to 12 months and induced
early flowering in non-transgenic scions (Figure 3). By
contrast, grafting experiments in poplar and apple with
rootstocks expressing FT transgenes under the control of
a heat-shock inducible promoter did not result in flowering in receptor scions [43,51] (Figure 2).

WT
WT

WT
pHSP:PtFT1

Current Opinion in Plant Biology

FT induced by heat shock promotes flowering in transgenic apple and

poplar but not by grafting. Upper panel: Poplar plants; wild type (left),
early flowering heat-shocked pHSP:AtFT plants with Arabidopsis FT
expressed from the heat shock promoter (middle) and non-flowering
heat-induced grafted plants with pHSP:AtFT rootstock and wild type
scion (right). Lower panel: Apple plants; wild type (left), early flowering
plants after heat shock induction of pHSP:PtFT1 (Populus trichocarpa
(poplar) FT), (middle) and non-flowering heat-shocked grafted plants
with pHSP:PtFT1 rootstock grafted to a wild type scion (right). Double
lines indicate the graft junction.

believed to jointly regulate growth and dormancy cycles

in poplar [57].
Perspectives

In annual plants, there has been recent progress on the

mechanisms of long distance FT protein transport and
FT floral promotion at the shoot apex. FT stability
[40,58], shape, size, ability to pass through plasmodesmata or interact with the phloem transport machinery,
such as FTIP1, and/or other regulators including the justdescribed NaKR1 [59] are all likely to contribute to
florigenic potential. The specifics of how FT movement
is controlled beyond the terminal phloem into the shoot
apex remains a gap in knowledge.
Current Opinion in Plant Biology 2016, 33:7782

80 Cell signalling and gene regulation

Figure 3

Acknowledgements
We thank Andrew Allan and Karine David for interesting discussions and
apologise to authors not cited due to word and reference limits. The
research on flowering in our labs was funded by the New Zealand
Foundation for Research Science and Technology (http://www.msi.govt.nz/)
contract number C10X0816 MeriNET and in addition for JP the New
Zealand Marsden Fund (http://www.royalsociety.org.nz/programmes/funds/
marsden/) contracts 10-UOA-200 and 14-UOA-125.

Jatropha

References and recommended reading

Papers of particular interest, published within the period of review,
have been highlighted as:
 of special interest
 of outstanding interest

Scion

X834

Rootstock

WT

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82 Cell signalling and gene regulation

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