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TitleStem cell activation by light guides plant organogenesis
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Stem cell activation by light guides
plant organogenesis

Saiko Yoshida, Therese Mandel, and Cris Kuhlemeier1

Institute of Plant Sciences, University of Bern, CH-3013 Bern, Switzerland

Leaves originate from stem cells located at the shoot apical meristem. The meristem is shielded from the
environment by older leaves, and leaf initiation is considered to be an autonomous process that does not depend
on environmental cues. Here we show that light acts as a morphogenic signal that controls leaf initiation and
stabilizes leaf positioning. Leaf initiation in tomato shoot apices ceases in the dark but resumes in the light, an
effect that is mediated through the plant hormone cytokinin. Dark treatment also affects the subcellular
localization of the auxin transporter PIN1 and the concomitant formation of auxin maxima. We propose that
cytokinin is required for meristem propagation, and that auxin redirects cytokinin-inducible meristem growth
toward organ formation. In contrast to common wisdom over the last 150 years, the light environment controls
the initiation of lateral organs by regulating two key hormones: auxin and cytokinin.

[Keywords: light signaling; stem cells; organ initiation; cytokinin; auxin; shoot apical meristem]

Supplemental material is available for this article.

Received March 16, 2011; revised version accepted May 20, 2011.

The plant shoot culminates in the shoot apical meristem,
a dome-shaped organ that generates the aerial parts of the
plant. Pluripotent stem cells are harbored in the central
zone at the tip of the meristem, while organ initiation
takes place below the tip in the peripheral zone (Carles
and Fletcher 2003; Rieu and Laux 2009; Sablowski 2011).
Because of its dynamic properties, the maintenance of the
shoot apical meristem requires a precise coordination of
growth and differentiation.

In the central zone, cytokinin has a role in the main-
tenance of the stem cell pool. The loss of meristem
function in the stm mutant is rescued by exogenous
cytokinin application as well as expression of a cytokinin
biosynthesis gene from the STM promoter (Yanai et al.
2005). Rice log mutants have smaller shoot meristems.
The LOG gene encodes a cytokinin biosynthesis enzyme,
and its transcripts are localized in the shoot meristem
tips (Kurakawa et al. 2007). A negative feedback loop
involving the CLV ligand–receptor system limits expres-
sion of the homeobox gene WUS and thereby prevents
accumulation of excess stem cells (Lenhard and Laux
2003). Local cytokinin perception by AHK4 and type A
cytokinin response regulators maintains the WUS ex-
pression domain at a predictable distance from the L1
layer (Gordon et al. 2009). A computational model
showed that, in a network in which cytokinin simulta-
neously activates WUS and represses CLV1, WUS ex-

pression increases steeply above a critical cytokinin
concentration.

In the peripheral zone, a positive feedback loop be-
tween auxin and its transporter, PIN1, is required for
organ patterning and initiation (Reinhardt et al. 2000,
2003; Heisler et al. 2005; de Reuille et al. 2006; Bayer et al.
2009). Treatment of tomato shoot apices with the auxin
transport inhibitor NPA blocks organ formation, result-
ing in the formation of a radially symmetric pin-like
structure. Similarly, mutations in the Arabidopsis PIN1
gene, which encodes an auxin efflux carrier, result in
a pin-like shoot. The application of auxin to the flank of
such pins induces organ formation (Okada et al. 1991;
Reinhardt et al. 2000, 2003). PIN1 was detected pre-
dominantly in the epidermal L1 layer and vascular tissues
of the developing primordia (Reinhardt et al. 2003). In the
L1 layer, PIN1 localizes toward sites of incipient primor-
dia, causing accumulation of auxin at these so-called
convergence points (Reinhardt et al. 2000, 2003; Heisler
et al. 2005; de Reuille et al. 2006; Bayer et al. 2009). The
local auxin maxima generate the regular organ arrange-
ment called phyllotaxis. Mathematical modeling sup-
ports a molecular mechanism in which the phyllotactic
pattern is self-organized by positive feedback between
auxin and PIN1 (Jönsson et al. 2006; Smith et al. 2006;
Heisler et al. 2010).

Recent studies indicate cross-talk between auxin and
cytokinin. In the Arabidopsis shoot apical meristem, WUS
directly represses the transcription of type A ARR genes
(ARR5, ARR6, ARR7, and ARR15), negative regulators of
cytokinin signaling. Overexpression of a constitutively

1Corresponding author.
E-mail [email protected]
Article is online at http://www.genesdev.org/cgi/doi/10.1101/gad.631211.

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active form of ARR7 disrupts meristem activities simi-
larly to wus mutants (Leibfried et al. 2005). These ARRs
are under negative control of auxin. Accordingly, mutants
in auxin biosynthetic enzymes, the auxin response regu-
lator MP, or PIN1 have enhanced ARR expression. Silenc-
ing of ARR7 and ARR15 caused enlargement of the shoot
apical meristem and restored organ formation in the mp
mutant. Thus, ARR7 and ARR15 integrate cytokinin and
auxin signals, connect them to the CLV–WUS network,
and mediate shoot apical meristem activity.

In maize, a loss-of-function mutation in ABPH1, a type
A ARR, caused enlargement of the shoot apical meristem
and changed phyllotaxis (Giulini et al. 2004). In the abph1
mutant, PIN1 expression at the incipient primordia was
reduced, indicating that ABPH1 is required for normal
expression of PIN1. Maize PIN1 was rapidly induced by
cytokinin, suggesting that ABPH1 acts as a positive
regulator of PIN1 and auxin accumulation in leaf primor-
dia (Lee et al. 2009). NPA treatment reduced ABPH1
expression. Therefore, in contrast to Arabidopsis, auxin
enhances a type A ARR in maize, although the effect may
be indirect. Despite this discrepancy, the ARRs appear to
be part of a regulatory network that connects auxin and
cytokinin signaling.

Auxin and cytokinin not only function as endogenous
regulators of the shoot meristem, they are also involved
in perceiving information from the environment and
relaying it to a wide variety of developmental programs
(Argueso et al. 2009; Shibasaki et al. 2009; Wolters and
Jurgens 2009). Of the various environmental cues, light
plays a particularly important role (Jiao et al. 2007). When
mature plants compete with their neighbors, the de-
creased red/far red ratio of the incident radiation causes
a shade avoidance response and leaf primordia transiently
stop growing, accompanied by rapid arrest of leaf cell
division. This response involves downstream activation
of auxin signaling as well as auxin-inducible cytokinin
degradation in the vascular procambium (Carabelli et al.
2007). Light also affects auxin biosynthesis, signaling, and
transport (Bandurski et al. 1977; Jones et al. 1991; Behringer
and Davies 1992; Gil et al. 2001; Salisbury et al. 2007;
Laxmi et al. 2008; Stepanova et al. 2008; Tao et al. 2008;
Halliday et al. 2009).

Surprisingly little is known about the effect of light on
leaf initiation and leaf positioning in mature plants. The
long-standing consensus has been that the shoot meri-
stem, as the source of the all-important stem cells, is
shielded from the ‘‘outward danger and vicissitudes’’ of
the environment (Airy 1873), and that phyllotaxis is not
affected by environmental cues. In a rigorous series of
experiments published 40 years ago, it was shown that
pea plants stopped leaf formation in the dark. Leaf
formation resumed when the plants were returned into
light (Low 1970). The arrest of leaf initiation in the dark
could be due to the lack of energy, but it is also possible
that light acts as an environmental signal of leaf initiation.

Microarray analysis of light- and dark-grown Arabidop-
sis seedlings showed that ;1150 genes were up-regulated
by light, whereas ;800 genes were down-regulated by
light (Ma et al. 2001). Some genes were regulated dis-

tinctly by light between adult leaves and seedlings.
During light-induced greening of etiolated seedlings,
microarray analysis also demonstrated rapid hormone
responses in the shoot apex: Genes implicated in auxin
and ethylene action were repressed, and genes associated
with cytokinin and gibberellin actions were activated
(Lopez-Juez et al. 2008).

Considering that light affects many hormonal path-
ways in different ways, we ask whether light modulates
hormonal pathways to control organogenesis at the shoot
apical meristem. Recently, we reported that the aux1
lax1lax2lax3 quadruple mutant, which is defective in
auxin influx carriers, has a much stronger phyllotactic
phenotype in short days than in long days (Bainbridge
et al. 2008). This suggests that light has an influence on
the shoot apical meristem by affecting auxin distribution.
This prompted us to investigate the influence of light on
auxin-dependent leaf initiation and positioning.

The common model plant Arabidopsis has a small
shoot apical meristem that is deeply buried between
rosette leaves, is virtually impossible to access, and
cannot be grown in culture. Thus, most studies on
Arabidopsis organ initiation concern the induction of
floral meristems from the inflorescence apex, which is
more easily accessed (Reddy et al. 2004; Heisler et al.
2005, 2010; Hamant et al. 2008). We use tomato as an
experimental system because its vegetative shoot apical
meristem is relatively large and therefore can be easily
dissected, grows vigorously under defined culture condi-
tions, and is well suited for a wide variety of microma-
nipulations. We show that light is strictly required for leaf
initiation and stabilizes organ positioning, and that the
light signal is transduced via cytokinin and PIN1 in-
tracellular trafficking.

Results

Shoot apices stop producing leaf primordia
in the absence of light

In order to investigate the effects of light on leaf initia-
tion, we analyzed the number of newly initiated leaf
primordia in long days and darkness. Soil-grown tomato
seedlings produced approximately one primordium per
day, while leaf initiation was arrested in the dark (Fig.
1A,B,H). The results supported the data from Low (1970):
Shoot apices cease to make leaves in the dark, and light
reverses the effects of dark and restarts leaf initiation.
The lack of organ formation in the dark could be
a photomorphogenic response or due to a lack of photo-
synthetic energy production. To avoid potential depletion
of energy, we cultured shoot apices in the presence of
sucrose (Fleming et al. 1997). When the apices were
cultured in long days, primordium initiation continued
(Fig. 1C,I). In contrast, when the apices were transferred
into the dark, the production of leaf primordia arrested
even in the presence of sucrose (Fig. 1D,I). When the dark-
treated seedlings and apices were returned to the light,
they resumed producing leaves (Fig. 1F,E), confirming that
dark treatment did not affect the viability of the apices.

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However, when zeatin was applied to the summit or
flank of dark-cultured NPA pins, the distance between
the lanolin dots increased like in the light-cultured NPA
pins, showing that the meristem tip grew in the dark (Fig.
3S; Table 1). Note that this growth was not accompanied
by organ induction. Thus, in dark-grown NPA pins,
exogenous cytokinin induced apical growth. In addition,
there were no obvious differences in cell shape between

light-grown NPA pins and cytokinin-treated dark-cul-
tured NPA pins, confirming that the effect of cytokinin
is similar to that of light. We calculated the rate of
meristem tip growth by measuring the distance between
the summit and the lanolin dot in the flank (see the
Supplemental Material). The rate of meristem tip growth
per day was as follows: in light-cultured NPA pins: 48 6
18 mm; in dark-cultured NPA pins with zeatin applied to

Table 1. Induction of primordia on tomato NPA pins by local treatment of auxin and cytokinin

Flank Summit Number of effects (%)

Condition IAA Zeatin IAA Zeatin Number of treatments Primordia induction No effect Meristem tip growth

Light 10 mM — — — 9 7 (78) 2 (22) 0 (0)
Mocka Mocka 42 3 (7) 8 (19) 31 (74)

Dark 10 mM — — — 95 5 (5) 89 (94) 1 (1)
10 mM 1 mM — — 16 11 (69) 5 (31) 0 (0)

— 1 mM — — 42 2 (5) 31 (74) 9 (21)
— — — 1 mM 38 0 (0) 25 (66) 13 (34)

Mocka Mocka 25 0 (0) 23 (92) 2 (8)

Apices were cultured in the presence of 10 mM NPA for 8 d to make NPA pins and were transferred to the light or the dark for 6 d. The
resulting pins were locally treated with IAA or zeatin. NPA pins were examined 5 d after microapplication.
aDMSO 1%.

Figure 3. Induction of primordium formation
and meristem tip growth by auxin and cytokinin.
(A–I) Microapplication of auxin and cytokinin to
dark-cultured apices. Dissected tomato apices
were precultured in the light and transferred to
darkness for 6 d. Lanolin containing 1% DMSO
(A), 10 mM IAA (B,C), 1 mM zeatin (D–F), or 10
mM IAA plus 1 mM zeatin (G–I) was applied in
the dark. These apices were further cultured in
the dark for 10 d. (White asterisks) Pre-existing
primordia. (F,I) Note that apices treated with 10
mM IAA plus 1 mM zeatin and with 1 mM
zeatin alone continued to grow in the dark. (A,B)
However, apices treated with 1% DMSO or 10
mM IAA did not grow. (C,E,H) In addition, 10
mM IAA alone, 10 mM IAA plus 1 mM zeatin,
and 1 mM zeatin alone promoted the develop-
ment of pre-existing P1 and I1. The numbers in
the bottom left corner show the number of apices
that show the displayed phenotype out of the
total number of samples. Thus cytokinin induces
leaf initiation in the dark, and auxin promotes
leaf initiation in the presence of cytokinin. (J–O)
Microapplication of auxin and cytokinin to the
flank of the meristems of tomato NPA pins.
Dissected apices were cultured in the presence
of NPA. Resulting pin-shaped apices (NPA pins)
were precultured in the light or the dark, and
microapplication of IAA and cytokinin was per-
formed. Microapplication of 1% DMSO (mock)

lanolin in the light (J), 10 mM IAA lanolin in the light (K), 1% DMSO lanolin in the dark (L), 10 mM IAA lanolin in the dark (M), 10 mM
IAA plus 1 mM zeatin lanolin in the dark (N), and 10 mM IAA plus 10 mM zeatin lanolin in the dark (O). (P–S) Microapplication to the
flank and the summit of the meristem of NPA pins. Microapplication of 1% DMSO lanolin to the flank and the summit in the light (P),
1% DMSO lanolin to the flank and the summit in the dark (Q), 10 mM IAA lanolin to the flank and 1% DMSO lanolin to the summit
in the dark (R), and 1 mM zeatin lanolin to the summit and 1% DMSO lanolin to the flank in the dark (S). (A–I) Scanning electron
microscope images. (J–S) Stereomicroscope images. Lanolin dots applied to the flank are colored red, and those applied to the summit
are colored blue. Bars, 100 mm.

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the summit: 35 6 15 mm. The results clearly show that, in
the absence of light, cytokinin is required to promote
meristem tip growth. In the absence of NPA, cytokinin
induced organ initiation but not meristem tip growth
in the dark (Fig. 3F). Together, this suggests that cytoki-
nin promotes leaf initiation in the presence of active
auxin transport.

Auxin redirects cytokinin-induced growth

Next, we asked why auxin could not induce organ
initiation in the dark. Microapplication of IAA alone
promoted PIN1 and DR5 expression in the dark-cultured
NPA pins (Fig. 4B,C,G,H). Similarly, both PIN1 and DR5
expression were up-regulated by IAA plus zeatin treatment
in the dark (Fig. 4D,I). The longitudinal and transverse
sections of DR5-expressing NPA pins showed up-regulation
of the DR5 signal in the L1 layer and a gradient in the DR5
signal at the site of microapplication (Supplemental Fig.
3A,B). Notably, PIN1 and DR5 expression were up-regu-
lated by IAA to the same extent in the absence or
presence of cytokinin (Fig. 4, cf. C and D, H and I).
Therefore, the results indicate that auxin promotes
downstream signaling in the dark; however, for organ
initiation, cytokinin is also required.

According to Figure 3S, cytokinin treatment promotes
meristem tip growth of NPA pins in the dark. Is activa-
tion of auxin signaling necessary for meristem tip
growth? Application of auxin alone induced PIN1 and
DR5 (Fig. 4C,H) but did not induce tip growth. Further-
more, microapplication of zeatin promoted neither DR5
nor PIN1 expression in the dark-cultured NPA pins (Fig.
4E,J). Therefore, auxin signaling is not necessary for
induction of meristem tip growth. We conclude that (1)

cytokinin induces growth, but (2) cytokinin in the ab-
sence of auxin causes the tip to grow, while, in its
presence, the lateral organs initiate and grow out at the
expense of tip elongation.

In addition, expression of PIN1 was higher in the light
than in the dark (Fig. 4A,B). Expression of DR5 was low in
the light and the dark (Fig. 4F,G). This suggests that light
is required for PIN1 expression; however, as long as the
auxin level is low, the meristem tip continues to grow
without producing organs.

Light controls expression of key regulatory genes
of the shoot apical meristem

The results so far show that light controls organogenesis
via activation of cytokinin signaling. This signaling is
likely to involve well-known regulators of meristem
activity and organogenesis. Because no tomato lines
carrying relevant reporter gene constructs are available,
we switched to the Arabidopsis inflorescence meristem.

Compared with the apices in the light, the number of
newly initiated flower primordia was lower in the dark.
Local cytokinin treatment restored primordium initia-
tion (Supplemental Fig. 4A). Furthermore, microapplica-
tion of IAA to the tip of the pin1 mutant induced organ
formation in the light but not in the dark (Supplemental
Fig. 4B–E). In contrast, microapplication of IAA plus zeatin
induced organ formation in dark-cultured pin1 mutants
(Supplemental Fig. 4F–H). These results confirmed that
the light response in the shoot apical meristem is con-
served between the vegetative tomato shoot meristem
and the Arabidopsis inflorescence meristem.

To determine whether alterations in meristem activity
in the light and the dark were evident at the level of gene

Figure 4. Induction of auxin signaling by local auxin
and cytokinin treatment on tomato NPA pins. Maximal
projections of transversal confocal sections of NPA pins
expressing PIN1-GFP (A–E) and DR5-YFP (F–J). Confo-
cal image with GFP signal in green (top) and GEO look-
up tables (bottom). In GEO look-up tables, blue in-
dicates low intensity, and red indicates high intensity.
Microapplication of 1% DMSO lanolin to the flank of
a light-cultured NPA pin (A,F), 1% DMSO lanolin to the
flank of a dark-cultured NPA pin (B,G), 10 mM IAA
lanolin to the flank of a dark-cultured NPA pin (C,H), 10
mM IAA plus 1 mM zeatin lanolin to the flank of
a dark-cultured NPA pin (D,I), and 1 mM zeatin lanolin
to the summit of the meristem of a dark-cultured NPA
pin (E,J). The numbers in the bottom right corner show
the number of apices that display the shown expression
pattern out of the total number of samples. Bars, 50 mm.
Lanolin pastes are colored white.

Leaf initiation requires light

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Saiko Yoshida, Therese Mandel and Cris Kuhlemeier

Stem cell activation by light guides plant organogenesis


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