Hd3a Protein Is a Mobile Flowering Signal in Rice
Shojiro Tamaki, et al.
Science 316, 1033 (2007);
DOI: 10.1126/science.1141753

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an ft-7 shoot receiver. These receiver shoots flowered slightly earlier than receiver shoots on control
grafts (Fig. 3D and fig. S3), as observed previously
for grafts of wild-type plants to ft-7 mutants (24),and FT:GFP protein was clearly detected in thevascular tissue of the shoot receiver (Fig. 3, E and
F). The grafting experiments support long-distancemovement of FT:GFP protein in the phloem.
Two general models could explain the role of
FT in floral induction. The first proposes that a
product of FT expressed in the leaves moves tothe meristem and initiates flowering through theactivation of flowering-time genes such as SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) (7, 25, 26). Our data support
movement of the protein. The second model
suggests that FT expression in the leaves activatesa second messenger, which is transmitted to theapex and induces flowering, perhaps throughactivation of FT genes or genes similar to FT in
the meristem. We refer to this second model as arelay model: FT protein could move along with asecond messenger but not comprise a signal.
We used transgenic plants expressing FT and
FT:GFP from additional phloem promoters to test
the relay model. The GALACTINOL SYNTHASE(GAS1) promoter is active specifically in the phloem
companion cells of the minor veins of leaves (27)and not in the companion cells of the shoot or majorveins of the leaf. GAS1:CO promotes early flowering of co-1 mutants (28). We constructed GAS1:FT,
GAS1:FT:GFP, and GAS1:FT:GFP:GFP transgenes and introduced these into ft-7 mutants. In
plants expressing the fusion proteins, GFP was detected only in the minor veins of the leaves (Fig. 4,
A to D). GAS1:FT complemented the ft-7 mutation, and the transgenic plants flowered earlier
than did wild-type plants (Fig. 4E). However,
GAS1:FT:GFP ft-7 plants were as late flowering
as ft-7 mutants (Fig. 4E). Nevertheless, FT:GFP isbiochemically active in the leaves of GAS1:FT:GFP
plants. Expression of FRUITFULL (FUL) mRNA
is increased in the leaves of transgenic Arabidopsis
plants that express high levels of FT mRNA (29).
FUL mRNA levels were higher in GAS1:FT ft-7
and GAS1:FT:GFP ft-7 than in wild-type plants andft-7 mutants (Fig. 4F). Thus FT:GFP is active in theleaves of GAS1:FT:GFP plants, but in contrast to
GAS1:FT or SUC2:FT:GFP, this construct does notpromote flowering. The larger FT:GFP protein
may move less effectively to the meristem fromthe minor veins than from the larger veins in which
SUC2 is also active, or downloading from thecompanion cells to the minor veins may be differentially regulated compared with downloading
to major veins. Thus, FT:GFP activity in the leavesof GAS1:FT:GFP plants was not sufficient to promote flowering, arguing for direct movement of an
FT product to the meristem.
We conclude (i) that during floral induction of
Arabidopsis, transient expression of FT in a single
leaf is sufficient to induce flowering and (ii) that in
response to FT expression, a signal moves fromthe leaves to the meristem. This signal is unlikely
to be a second messenger activated by FT in theleaves given that GAS1:FT:GFP is active in leaves
but does not promote flowering (Fig. 4). In contrast, we propose that FT protein is transported
through the phloem to the meristem. Our data
provide evidence for movement of FT:GFP fromthe phloem companion cells of SUC2:FT:GFP
plants to the meristem that correlates with flowering, and of FT:GFP protein across graft junctions,consistent with the detection of proteins similar to
FT in the phloem of Brassica napus plants (30).
The data in the Report by Tamaki et al. (31) demonstrate that this function of FT is highly conserved
in rice. The presence of a wide range of different
proteins in phloem sap suggests that long-distancemovement of proteins is the basis of other signaling
processes in plants (23), in addition to the shorterdistance movement of proteins between neighboring
cells (32) and previous indications of the importanceof long-distance mRNA movement (33, 34).
References and Notes
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6. H. An et al., Development 131, 3615 (2004).
7. P. A. Wigge et al., Science 309, 1056 (2005).

Hd3a Protein Is a Mobile
Flowering Signal in Rice
Shojiro Tamaki, Shoichi Matsuo, Hann Ling Wong, Shuji Yokoi,* Ko Shimamoto†
Florigen, the mobile signal that moves from an induced leaf to the shoot apex and causes
flowering, has eluded identification since it was first proposed 70 years ago. Understanding thenature of the mobile flowering signal would provide a key insight into the molecular mechanism offloral induction. Recent studies suggest that the Arabidopsis FLOWERING LOCUS T (FT) gene is acandidate for encoding florigen. We show that the protein encoded by Hd3a, a rice ortholog of FT,
moves from the leaf to the shoot apical meristem and induces flowering in rice. These results
suggest that the Hd3a protein may be the rice florigen.

T

he flowering time of plants is determined bya number of environmental factors (1–3),
among which day length (photoperiod) is amajor factor (4). On the basis of the day length,
which promotes flowering, plants are grouped into
two major classes: long-day (LD) and short-day

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SCIENCEVOL 316

8. A. Samach et al., Science 288, 1613 (2000).
9. M. Abe et al., Science 309, 1052 (2005).
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Science 286, 1960 (1999).
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316, 367 (2007).
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(2006).
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pp. 1380–1536.
15. J. A. D. Zeevaart, Meded. Landbouwhogesch. Wageningen
58, 1 (1958).
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material on Science Online.
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S. A. Kay, Nature 426, 302 (2003).
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19. F. Valverde et al., Science 303, 1003 (2004).
20. M. J. Yanovsky, S. A. Kay, Nature 419, 308 (2002).
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24. C. G. N. Turnbull, S. Justin, Flower. Newsl. 37, 3 (2004).
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929 (2000).
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29. P. Teper-Bamnolker, A. Samach, Plant Cell 17, 2661 (2005).
30. P. Giavalisco, K. Kapitza, A. Kolasa, A. Buhtz, J. Kehr,Proteomics 6, 896 (2006).
31. S. Tamaki, S. Matsuo, H. L. Wong, S. Yokoi, K. Shimamoto,
Science 316, 1033 (2007).
32. K. L. Gallagher, P. N. Benfey, Genes Dev. 19, 189 (2005).
33. M. Kim, W. Canio, S. Kessler, N. Sinha, Science 293, 287(2001).
34. V. Haywood, T.-S. Yu, N.-C. Huang, W. J. Lucas, Plant J.
42, 49 (2005).
35. This work was funded by the Deutsche Forschungsgemeinschaft
through SFB 572 and by a core grant from the Max
Planck Society to G.C. We thank P. Schulze-Lefert, S. Davis,
F. Turck, and A. de Montaigu for valuable comments andK. Shimamoto for providing results before publication.

Supporting Online Materialwww.sciencemag.org/cgi/content/full/1141752/DC1
Materials and Methods
SOM Text
Figs. S1 to S3
References
26 February 2007; accepted 6 April 2007
Published online 19 April 2007;
10.1126/science.1141752
Include this information when citing this paper.

Downloaded from www.sciencemag.org on June 11, 2007

REPORTS(SD) plants. Arabidopsis is a LD plant and rice is
a SD plant. FT is a major floral activator (5, 6),
which is expressed in the vascular tissue of leaves(7, 8). FT protein interacts with a transcription
factor FD, which is expressed only in the shootapical meristem (SAM) (9, 10). The difference in
expression site implies that FT protein must moveto the SAM to interact with FD for flower induction. Therefore, FT is a primary candidate forencoding florigen (11), a mobile flowering signal.
Laboratory of Plant Molecular Genetics, Nara Institute of
Science and Technology, 8916-5 Takayama, Ikoma 6300101, Japan.
*Present address: Faculty of Agriculture, Iwate University,
Morioka 020-8550, Japan.
†To whom correspondence should be addressed. E-mail:simamoto@bs.naist.jp

18 MAY 20071033

A tomato ortholog of FT, SFT, induced early
flowering, and grafting sft mutant shoots to
35S::SFT donors induced normal flowering in thesft shoots (12). However, SFT mRNA was not detected in the SAM of the grafted tomato plants(12), suggesting that SFT mRNA does not movethrough graft junctions in tomato. Furthermore, aprevious study suggesting that florigen was an
RNA molecule has been retracted (13). Therefore, although FT is a candidate for encoding
florigen, the exact nature of florigen remains to be
determined.

Previous studies indicate that Hd3a is the
major activator of flowering in rice, a SD plant,
under SD conditions, and that Hd3a complements
Arabidopsis ft mutants (14–17). Therefore, we examined Hd3a transcript levels in several tissues byreal-time polymerase chain reaction (PCR) underinductive conditions for flowering (Fig. 1A). Hd3amRNA accumulates in leaf blade tissue, but ispresent at very low abundance in leaf sheath (Fig.
1A). Quantitative comparisons of Hd3a mRNA inleaves and the shoot apex indicate that its accumulation in the shoot apex is on the order of 10−4
Fig. 1. Expression of Hd3a mRNAin rice under SD conditions. (A)Real-time quantitative RT-PCR of
Hd3a mRNA accumulation in ricetissue. Samples of plants were harvested at ZT 0 to 4. Hd3a mRNA
was quantified relative to Ubiquitin(Ubq) mRNA. (B to D) GUS stainingof Hd3a::GUS. (B) Leaf blade of the
Hd3a::GUS transgenic rice plant at
ZT4 on day 35 under SD conditions.
(C) Transverse section of a leaf bladein (B). (D) Longitudinal section of
the SAM (arrow) of the same transgenic plant as in (B) and (C). Scalebars: 1 mm (B), 20 mm (C), 50 mm (D).

of that in leaf blade, indicating that Hd3a mRNAis virtually absent from the shoot apex of rice
plants when flowering is induced under SD conditions. Therefore, it is unlikely that Hd3a mRNA
moves from leaf to the SAM in any appreciable
amount.
To determine the tissue and cell specificity of
Hd3a mRNA expression, we analyzed the activity of an Hd3a::GUS transgene in leaf blades
and SAMs of transgenic rice. The promoter
activity of Hd3a was detected in phloem andxylem parenchyma cells of leaf blade (Fig. 1, B
and C), and no GUS activity was detected in the
SAM (Fig. 1D). This was consistent with thequantitative reverse transcription–polymerase
chain reaction (RT-PCR) results (Fig. 1A) andsimilar to the tissue specificity of FT expressionin Arabidopsis (7, 18). Hd3a expression is thus
restricted to the vascular tissues of rice leaves
under inductive SD conditions.
To study the function and localization of Hd3a
protein in rice, we fused the 1.7-kb Hd3a promoter used for GUS analysis to green fluorescentprotein and introduced the resulting construct(Hd3a:GFP) into rice plants by Agrobacteriummediated transformation. The leaf diurnal expression pattern of transgenic plants was similar tothat of the endogenous Hd3a gene (Fig. 2L), butvaried among transgenic plants. Transgenic rice
plants flowered (headed) significantly earlier thanwild-type plants (Table 1 and fig. S1A), suggesting that expression of Hd3a:GFP causes early
flowering, because expression of endogenous
Hd3a mRNA in transgenic rice plants did notchange relative to that in wild-type plants.
To examine tissue localization of the Hd3a
protein in Hd3a:GFP transgenic plants, we analyzed GFP fluorescence in the SAM, the upper
part of the stem, and in the leaf blade by confocal laser scanning microscopy. GFP fluorescence was limited to the inner conelike region of
the SAM in transgenic rice (Fig. 2, A to D, G
and H). The GFP signal was detected in the
SAM (Fig. 2, C and D) and stem vascular tissue(Fig. 2, I and J). GFP signal was also detected in
the vascular tissue of the upper part of the stem
and in the region just beneath the meristem
where nodes are present (Fig. 2, E and F), suggesting that Hd3a:GFP protein moves from theend of the vascular bundles through the basal
cells and into the SAM.
Table 1. Flowering (Heading) times of transgenic plants under SD conditions.
Genotype

Fig. 2. Confocal microscopy of Hd3a::Hd3a-GFP transgenic rice. (A to J) Confocal images of Hd3a::
Hd3a-GFP transgenic plants. (A to H) Longitudinal sections through the SAM. (I and J) Longitudinal
section through vascular bundles indicated by the red squares in (G) and (H). (A), (C), (E), (G), and (I)are composite images of the fluorescein isothiocyanate (FITC) and transmission channels. (B), (D), (F),(H), and (J) show the spectrally unmixed images. Hd3a-GFP fluorescence is shown in green, and plant
autofluorescence in red. Scale bars, 50 mm. Arrows indicate a SAM. (K) Diagram of the SAM and theupper part of the rice stem. V, vascular bundles; SAM, shoot apical meristem. (L) Real-time quantitative
RT-PCR of Hd3a-GFP and endogenous Hd3a mRNAs under SD conditions in Hd3a::Hd3a-GFP transgenic
rice plants. White and black bars at the bottom represent light and dark periods, respectively.

1034

18 MAY 2007

VOL 316SCIENCE

Wild type
Hd3a::Hd3a:GFP
RPP16::Hd3a:GFP
RPP16::GFP
rolC::Hd3a:GFP*
rolC::GFP*

Days to flowering(days ± SE)n50.4 ± 7.6
32.8 ± 11.2
14.8 ± 3.3
6419.5 ± 13.6
88.6 ± 11.3

5
6
5
2
11
5

*Indicates significant difference from control by Student’s t test
(P = 0.0000007).

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REPORTS

Hd3a:GFP protein is thus found in the inner
region of the SAM and in stem and leaf blade
vascular tissues, suggesting that it is produced in
the vascular tissue of the leaf blade, transported
through stem phloem tissue, unloaded at the upper
end of the vascular tissue, and translocated to theSAM, probably through the region just beneath theSAM. These results suggest that the Hd3a protein,
but not Hd3a mRNA, is a candidate for theflorigen in rice.
We expressed the Hd3a:GFP gene in phloem
tissue by fusing it with two phloem-specificpromoters, the Agrobacterium rhizogenes rolCpromoter (8, 18) and Rice Phloem Protein 16(RPP16) promoter (19). The rolC promoter is
specifically active in the phloem (18), androlC::CO is known to induce extremely early
flowering in Arabidopsis (8). The RPP16 geneencodes a phloem-specific protein in rice (19).

Rice plants expressing RPP16::Hd3a:GFP androlC::Hd3a:GFP flowered very early comparedto the wild-type plant (Table 1 and fig. S1, B
and C), indicating that the vascular-specific expression of the Hd3a:GFP gene induced early
flowering in rice. GFP signals were detected in
the vascular tissues of leaf blades and in the stemsof rolC::Hd3a:GFP and RPP16::Hd3a:GFP
transgenic plants (Fig. 3, B, D, J, and L). In
transverse sections of the leaf blade, GFP
signals were detected in cells near the phloem(Fig. 3, A, B, I, and J). The intact Hd3a:GFP
protein was detected by immunoblotting with
antibody to GFP in the leaf extract (fig. S2).
Fluorescence was detected in the SAMs of bothtransgenic lines (Fig. 3, E, F, M, and N), andin leaves adjacent to SAMs (Fig. 3, E, F, M,
and N). Because the free GFP protein diffusedin many tissues in rice, the Kaede reporter pro-

Fig. 3. Confocal microscopy of transgenic rice plants expressing a fusion of reporter protein withphloem-specific promoters. Confocal images of transgenic rice plants. (A), (C), (E), (G), (I), (K),(M), and (O) are composite images of FITC and transmission channels. (B), (D), (F), (H), (J), (L),(N), and (P) show the spectrally unmixed images. Hd3a-GFP and Kaede-green fluorescence areshown in green, and autofluorescence is in red. (A) and (B) Transverse sections through a leaf ofrolC::Hd3a-GFP. (C) and (D) Longitudinal sections through the stem and SAM of rolC::Hd3a-GFP. (E)and (F) Longitudinal section through a SAM of rolC::Hd3a-GFP. (G) and (H) Longitudinal sections
through a SAM of rolC::Kaede. (I) and (J) Transverse section through a leaf of RPP16::Hd3a-GFP. (K) and(L) Longitudinal sections through a stem, including the meristem of RPP16::Hd3a-GFP. (M) and (N)Longitudinal sections through a meristem of RPP16::Hd3a-GFP. (O) and (P) Longitudinal sections
through the SAM of RPP16::Kaede. Scale bars: 25 mm [(A), (B), (M), and (N)]; 50 mm [(C to L), (O),and (P)]. Arrows indicate SAM. Arrowheads indicate GFP fluorescence.
www.sciencemag.org

SCIENCEVOL 316tein (20, 21) was used to localize promoter
activity. The Kaede protein forms a monotetrameric complex of 116 kD and is retainedin cytoplasm (20). Kaede fluorescence was
not detected in the SAM (Fig. 3, G, H, O, andP) and was detected only in the vascular tissues of rolC::Kaede and RPP16::Kaede transgenic plants (fig. S3), demonstrating that therolC and RPP16 promoters are not active in
the SAM. This result confirms that Hd3a protein is translocated from stem vascular tissue
to the SAM.
Hd3a protein fulfills the requirements for aflorigen (11), but Hd3a mRNA cannot be completely ruled out as a florigen because Hd3atranscripts are present in the shoot apex in extremely low abundance. A recent proteomic studyof phloem sap obtained from the inflorescencestem of Brassica napus identified FT protein(22) as a sap constituent. The presence of FT
ortholog in the corresponding tissues of thisdistantly related plant supports our conclusionthat it is the Hd3a protein that acts as the main
florigen. Our results strongly suggest that theprotein encoded by FT/Hd3a acts universally asa florigen (23–25).
Because there is no vascular connection between the upper end of the vascular bundles andthe base of the SAM, there must be some mechanisms that regulate the movement of Hd3a
protein into the SAM. There may be intercellulartransport proteins which help Hd3a protein movetoward the center of the stem just beneath theSAM. Once Hd3a protein enters the SAM, it may
be localized in the nucleus. A recent report on themaize FD ortholog (26) shows that its mRNA islocalized in the inner region of the SAM, similar
to the region where GFP signal was detected in
Hd3a:GFP transgenic rice. These results suggest that an FD-like nuclear protein may regulate intracellular localization of Hd3a protein in
the SAM.
The morphology of vegetative organs changes
when there is a phase transition to flowering insome species. It has recently been shown thatFT overexpression induces changes in leaf morphology and stem branching in tomato (12) andin Arabidopsis leaf morphology (27). In aspen
trees, FT was shown to regulate growth cessation
and bud dormancy (28). We found that transgenic rice plants expressing RPP16::Hd3a:GFP
or rolC::Hd3a:GFP had alterations in multiple
traits in vegetative organs such as elongation ofinternodes, which is known to occur after thetransition to flowering and increased tillering.
These alterations were induced by ectopic expression of the Hd3a protein in the vascular tissues. These results may suggest that many, if notall, of the changes associated with the transition from vegetative to reproductive growth anddevelopment induced by day length are induced by Hd3a protein. Therefore, Hd3a/FT
protein may be a general mobile morphogenthat regulates multiple phases of plant growthby photoperiod.

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1035

REPORTS
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The Increasing Dominance ofTeams in Production of Knowledge
Stefan Wuchty,1* Benjamin F. Jones,2* Brian Uzzi1,2*†
We have used 19.9 million papers over 5 decades and 2.1 million patents to demonstrate that teams
increasingly dominate solo authors in the production of knowledge. Research is increasingly done inteams across nearly all fields. Teams typically produce more frequently cited research than individuals
do, and this advantage has been increasing over time. Teams now also produce the exceptionally highimpact research, even where that distinction was once the domain of solo authors. These results aredetailed for sciences and engineering, social sciences, arts and humanities, and patents, suggesting thatthe process of knowledge creation has fundamentally changed.
n acclaimed tradition in the history andsociology of science emphasizes the roleof the individual genius in scientific discovery (1, 2). This tradition focuses on guiding
contributions of solitary authors, such as Newton
and Einstein, and can be seen broadly in the tendency to equate great ideas with particular names,such as the Heisenberg uncertainty principle, Euclidean geometry, Nash equilibrium, and Kantian
ethics. The role of individual contributions is alsocelebrated through science’s award-granting institutions, like the Nobel Prize Foundation (3).
Several studies, however, have explored anapparent shift in science from this individualbased model of scientific advance to a teamwork
model. Building on classic work by Zuckerman
and Merton, many authors have established arising propensity for teamwork in samples ofresearch fields, with some studies going back acentury (4–7). For example, de Solla Price examined the change in team size in chemistry from1910 to 1960, forecasting that in 1980 zero percent of the papers would be written by solo au-A

thors (8). Recently, Adams et al. established thatover time, teamwork had increased acrossbroader sets of fields among elite U.S. research
universities (9). Nevertheless, the breadth anddepth of this projected shift in manpower remains
indefinite, particularly in fields where the size ofexperiments and capital investments remain
small, raising the question as to whether the
projected growth in teams is universal or
cloistered in specialized fields.
A shift toward teams also raises new questions of whether teams produce better science.
Teams may bring greater collective knowledge
and effort, but they are known to experience social network and coordination losses that make*These authors contributed equally to this work.
†To whom correspondence should be addressed. E-mail:uzzi@northwestern.edu

1036

Supporting Online Materialwww.sciencemag.org/cgi/content/full/1141753/DC1
Materials and Methods
Figs. S1 to S3
References
26 February 2007; accepted 6 April 2007
Published online 19 April 2007;
10.1126/science.1141753
Include this information when citing this paper.

them underperform individuals even in highly
complex tasks (10–12), as F. Scott Fitzgerald
concisely observed when he stated that “no grandidea was ever born in a conference” (13). From
this viewpoint, a shift to teamwork may be acostly phenomenon or one that promotes lowimpact science, whereas the highest-impact ideas
remain the domain of great minds working alone.
We studied 19.9 million research articles in
the Institute for Scientific Information (ISI) Web
of Science database and an additional 2.1 million
patent records. The Web of Science data covers
research publications in science and engineering
since 1955, social sciences since 1956, and artsand humanities since 1975. The patent data cover
all U.S. registered patents since 1975 (14). A teamwas defined as having more than one listed author(publications) or inventor (patents). Following the
ISI classification system, the universe of scientificpublications is divided into three main branches
and their constituent subfields: science andengineering (with 171 subfields), social sciences(with 54 subfields), and arts and humanities (with27 subfields). The universe of U.S. patents wastreated as a separate category (with 36 subfields).
See the Supporting Online Material (SOM) text
for details on these classifications.
For science and engineering, social sciences,and patents, there has been a substantial shift
toward collective research. In the sciences, teamsize has grown steadily each year and nearly

Table 1. Patterns by subfield. For the three broad ISI categories and for patents, we counted thenumber (N) and percentage (%) of subfields that show (i) larger team sizes in the last 5 years
compared to the first 5 years and (ii) RTI measures larger than 1 in the last 5 years. We show RTI
measures both with and without self-citations removed in calculating the citations received. Dashentries indicate data not applicable.
Increasingteam size

1

Northwestern Institute on Complexity (NICO), Northwestern University, Evanston, IL 60208, USA. 2Kellogg
School of Management, Northwestern University, Evanston,
IL 60208, USA.

27. P. Teper-Bamnolker, A. Samach, Plant Cell 17, 2661 (2005).
28. H. Böhlenius et al., Science 312, 1040 (2006).
29. We thank J. Kyozuka (University of Tokyo) for advice on
the experiments and comments on the manuscript,
K. Kadowaki (NIAS, Tsukuba) for the RPP16 promoter,
H. Uchimiya (University of Tokyo) for the rolC promoter,and members of the Laboratory of Plant Molecular
Genetics at NAIST for discussions. This research was
supported by Grants-in-Aid for Scientific Research on
Priority Areas of the Ministry of Education, Culture,
Sports, Science, and Technology of Japan (to K.S.).

Science and engineeringSocial sciences
Arts and humanities
Patents

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RTI > 1
(with self-citations)

RTI > 1(no self-citations)

Nfields

Nfields%

Nfields%

Nfields

%

171
54
27
36

170
54
24
36

99.4
100.0
88.9
100.0

167
54
23
32

97.7
100.0
85.2
88.9

159
51
18
–

92.4
94.4
66.7
–

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References and Notes
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(2006).
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316, 367 (2007).
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15. S. Kojima et al., Plant Cell Physiol. 43, 1096 (2002).