Photosynthetic sucrose acts as cotyledon-derived

long-distance signal to control root growth during

early seedling development in Arabidopsis
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Stefan Kircher1 and Peter Schopfer1

Department of Plant Physiology, Faculty of Biology, Albert-Ludwigs-University, D-79104 Freiburg, Germany

Edited by Philip N. Benfey, Duke University, Durham, NC, and approved May 29, 2012 (received for review March 2, 2012)

The most hazardous span in the life of green plants is the period This conclusion was further supported by amputation experiments
after germination when the developing seedling must reach the in which root growth during global irradiation was followed over
state of autotrophy before the nutrients stored in the seed are a period of 3 d after dissecting either the visible leaf primordia
exhausted. The need for an economically optimized utilization of (“apex”), one cotyledon, the entire apex plus one cotyledon, both
limited resources in this critical period is particularly obvious in cotyledons, or the entire apex plus both cotyledons (Fig. 3).
species adopting the dispersal strategy of producing a large amount The results shown in Figs. 1 and 2 demonstrate that light pro-
of tiny seeds. The model plant Arabidopsis thaliana belongs to this duces a reversible growth-promoting signal in the cotyledons,
category. Arabidopsis seedlings promote root development only raising questions about the nature of this signal and its transport
in the light. This response to light has long been recognized and from the cotyledons to the root tip, where growth occurs. Using
recently discussed in terms of an organ-autonomous feature of photomorphogenic mutants, we first tested the previously sug-
photomorphogenesis directed by the red/blue light absorbing gested possibility (3, 5–7) that the established photomorphogenic
photoreceptors phytochrome and cryptochrome and mediated by pigments phytochrome (Phy) and cryptochrome (Cry) serve as
hormones such as auxin and/or gibberellin. Here we show that the photoreceptors for root growth responses. Compared with the
primary root of young Arabidopsis seedlings responds to an inter- wild type (WT, Columbia-0), the quadruple mutant phyA,B/cry1,2
organ signal from the cotyledons and that phloem transport of lacks the most prominently acting photomorphogenic photo-
photosynthesis-derived sugar into the root tip is necessary and suf- receptors and thus shows skotomorphogenesis of the shoot also in
ficient for the regulation of root elongation growth by light. the light (10). As illustrated in Fig. 4A, phyA,B/cry1,2 mutant
seedlings produce short roots both in light and darkness, arguing
he storage materials of the Arabidopsis seed (∼30 μg) support
T seedling development for not more than 4–5 d (25 °C). After
germination in the soil (i.e., in darkness), stored nutrients are
against the possible involvement of photoreceptors besides PhyA,
PhyB, Cry1, and Cry2 in the root growth response to light. To
further investigate whether well established light-signaling cas-
primarily invested in the elongation of the shoot axis (hypocotyl) cades of these sensors are responsible for root elongation in the
while root growth remains repressed (skotomorphogenesis). light (11, 12), we used the mutant constitutive photomorphogenic1
When the hypocotyl reaches the light, its growth stops and the (cop1-4). COP1 represses the default program of photomorpho-
cotyledons are converted into photosynthetically active leaves genesis in darkness resulting in skotomorphogenesis. Accordingly,
(photomorphogenesis). Concomitantly, elongation of the root is cop1 mutants show photomorphogenesis of the shoot also in

DEVELOPMENTAL
induced, allowing the exploration of the soil for water and min- darkness (13), and its genome-expression profile in darkness is

BIOLOGY
erals. In contrast to photomorphogenesis of shoot organs, the similar to that of light-grown WT seedlings (14). Thus, if root
impact of light on the development of the root has so far not been growth is part of this developmental program, cop1-4 seedlings
extensively investigated (1, 2). Recent investigators have con- should produce long roots also in darkness. Instead, Fig. 4A shows
cluded that the effect of light on root development in seedlings is that the roots of cop1-4 seedlings are short, indicating that primary
an organ-autonomous feature of photomorphogenesis controlled root growth does not follow the photomorphogenic program ex-
by the red/blue light absorbing photoreceptors phytochrome and ecuted in the shoot via the light-mediated elimination of COP1
cryptochrome (3–7) and mediated by hormones such as auxin and/ function, in line with observations of Miséra et al. (15).
or gibberellin (7–9). Our conclusion that the conventional photoreceptors Phy and
Cry may not be directly involved in the light-mediated root growth
Results response directed our attention to another plant light-sensitive
Fig. 1 shows the time course of primary root elongation of seedlings system that is often disregarded in photomorphogenesis research:
grown on vertical agar plates transferred from the light chamber to photosynthesis. Sugars synthesized in the green parts of plants are
darkness or vice versa. For investigating the reversible changes in known to have important roles as signaling molecules in addition
growth rate in more detail, we determined root elongation with an to their metabolic functions (16–18), for example, acting as a sys-
infra-red video camera system allowing monitoring growth kinetics temic signal for promoting root development in response to
in light and darkness with a high temporal and spatial resolution. phosphorus starvation (19). We tested the hypothesis that the light
Fig. 2A shows that growth attenuation induced by the transition stimulus emerging in the cotyledons and transmitted to the root is
from light to dark and growth enhancement by dark to light photosynthetically produced sugar. In a first experiment, we grew
transfer can be detected with this technique after a lag of 60–90
min. As shown in Fig. 2B, a light spot of 5 mm diameter of similar
fluence rate directed to the whole shoot (trace 1), a single cotyle- Author contributions: S.K. and P.S. designed research, performed research, analyzed data,
don (trace 2), or the cotyledon of a seedling from which the other and wrote the paper.
cotyledon including the entire shoot apex was removed (trace 3), The authors declare no conflict of interest.
was similarly effective in inducing root elongation after dark ad- This article is a PNAS Direct Submission.
aptation. When the light spot was directed to various regions of the 1
To whom correspondence may be addressed. E-mail: [email protected].
seedling, the root started to grow only if the cotyledons received de or [email protected].
the light (Fig. 2C). These results indicate that the light stimulus This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
inducing root growth is perceived specifically by the cotyledons. 1073/pnas.1203746109/-/DCSupplemental.

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Fig. 1. Root growth in light and darkness 3–8 d after initiation of germi-
nation (daig). After 3 d in the light, seedlings were kept in continuous light
(cL) or darkness (cD) and transferred from light to darkness (D) or darkness
to light (L) after 4 and 5 daig as indicated.

WT, phyA,B/cry1,2, and cop1-4 seedlings on agar plates containing

sucrose. Fig. 4B shows that, in all cases, the short-root morpho-
types demonstrated in Fig. 4A could be converted to long-root
morphotypes by supplementary sucrose. To further test the hy-
pothesis, we used three physiological treatments for inhibiting
various sections of the photosynthetic apparatus in WT seedlings:
(i) removal of CO2 from the atmosphere in the light, (ii) pre-
venting greening with the carotenoid-biosynthesis inhibitor nor-
flurazone in the light (20), and (iii) preventing greening, but not
PhyA-mediated photomorphogenesis, by growing the seedlings in
far-red light (Fig. 5). In all three treatments, the inhibition of
photosynthetic assimilation produced short roots that could be
converted to long roots by adding sucrose to the medium. Root
growth in the light and hypocotyl growth in light and darkness
were not affected by the sucrose treatment (except a slight pro-
motion in far-red light). Thus, sucrose promotes growth specifi-
cally in the root where it interacts synergistically with light. The
concentration-effect curve for sucrose (Fig. 6) indicates that the
sucrose effect on root growth in darkness can be detected already
at 1 mM and may not yet be saturated at 100 mM, a sucrose
concentration that produced about 90% of the root length in the Fig. 2. Short-term kinetics of root growth (representative single measure-
light without sucrose. However, because the hypocotyl growth was ments). (A) Intact light-grown seedlings were transferred to darkness 3 daig
inhibited at ≥100 mM, we routinely used 30 mM as a standard (D) and back to the light (broad field) 4 daig (L). (B) Perception of the light
concentration in this type of experiment. We also tested the pos- stimulus by the cotyledons. Light-grown seedlings were transferred to
sibility that the potentially growth-promoting plant hormones darkness 5 daig. At day 6 (L), a spotlight beam was directed to the whole
auxin and gibberellin contribute to root growth (8) in addition to shoot (1), a single cotyledon of an intact seedling (2), or the cotyledon of
a seedling from which the other cotyledon + the shoot apex were dissected 5
sucrose. We found that auxin (IAA) inhibits root elongation in daig (3). The dark control seedling (4) was growing next to the seedling of
darkness at concentrations ≥0.01 μM (as known from light-grown trace 1. (C) Selective irradiation of seedling parts. Intact seedlings grown as
seedlings), whereas gibberellin (GA3) had no significant effect up in B were partially irradiated with a spot light beam as outlined. In seedling
to 10 μM (Table S1). 1, the visible leaf primordia at the shoot apex were dissected 5 daig. The
The data presented so far suggest that root growth depends on distance between measuring points was 32 min.
photosynthetic sugar, presumably sucrose, which is delivered from
the cotyledons to the root. Alternatively, it could be hypothesized
that sugar gives rise to a growth factor X in the cotyledons, which from the cotyledons to the root. In agreement with this conclusion,
can be transported to the root tip. To discriminate between these we found that the roots respond to high sucrose concentrations in
possibilities, we fed sucrose specifically either to the cotyledons or the range normally present in the sieve tube sap (up to 1 M). Note
the root (close to the growth zone) of light-grown, dark-adapted that, in these experiments, the growth zone of the root was not in
seedlings and determined root elongation in darkness. Fig. 7 touch with the applied sucrose, avoiding osmotic side effects.
shows that root growth can be induced by feeding sucrose to the A critical step in sugar transport to the root is phloem loading
cotyledons and that sugar acts as a direct growth stimulus in the in the cotyledons. Arabidopsis is known as an “apoplastic loader”
root. Thus, conventional source-to-sink transport of sucrose in the in which sucrose secreted by the mesophyll cells can be pumped
phloem seems to be sufficient to explain the signal transmission into the sieve tubes by the H+-sucrose transporter SUC2 (21).

11218 | www.pnas.org/cgi/doi/10.1073/pnas.1203746109 Kircher and Schopfer

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Fig. 3. Effect of cotyledon and apex amputation on root growth. After 5 daig
in the light, the following seedling parts were dissected: visible leaf primordia
(−apex), one cotyledon (−1 cot), entire apex and one cotyledon (−apex, 1 cot),
two cotyledons (−2 cots), entire apex and two cotyledons (−apex, 2 cots). Root
elongation was followed for further 3 d in the light. If present, the leaf pri-
mordia started to expand between day 1 and day 2 after amputation.

We used a SUC2-deficient mutant for testing the involvement of

this transporter in the growth-signal transfer to the root. As
expected (22, 23), a fraction of the segregating progeny of het-
erozygous (SUC2/suc2) plants grown on sucrose-free medium in
the light showed a strong retardation of root growth (Fig. 8 A Fig. 5. Effect of photosynthesis inhibition on root and hypocotyl growth
and B). This mutant phenotype could be rescued by growing the and its reversal by sucrose. Seedlings were grown for 4 daig in light (L) or
seedlings on sucrose medium (Fig. 8C). darkness (D) with (gray bars) or without (white bars) 30 mM sucrose. (A)
Without further treatment (control). (B) In a CO2-depleted atmosphere
Discussion (−CO2). (C) With 0.1 μM norflurazone (San 9789) in the medium (20) (+NF).
Our results suggest a hierarchical order of steps in the execution of (D) Under far-red light (FR) with or without CO2.
the light-dependent developmental program during early seedling
development (Fig. 9). In darkness, the limited resources are mainly
allocated to hypocotyl growth for pushing the cotyledons toward the from direct photoreceptor signaling and put under the command of
light, whereas growth of the nearly functionless root is stalled. After photosynthesis. Moreover, the emerging role of Phy/Cry-mediated

DEVELOPMENTAL
reaching the light, photoreceptor signaling effects photomorpho- photomorphogenesis as a prerequisite for photosynthetic activity

BIOLOGY
genesis in the shoot, including the establishment of photosynthesis may explain why the involvement of these photoreceptors shows up
in the cotyledons. Subsequently, photosynthetically generated su- under particular experimental conditions (3–7).
crose acts as an interorgan signal as well as fuel to initiate growth of In contrast to general belief and in disagreement with published
the root that is now needed for capturing nutrients from the soil. results (8, 24), our amputation experiments (Figs. 2 and 3) provide
This interpretation explains why root growth control is uncoupled

Fig. 4. Effect of light on root elongation of mutants impaired either in the

photomorphogenesis program (phyA,B/cry1,2) or the skotomorphogenesis
program (cop1-4) grown in the absence (a) or presence (b) of 30 mM sucrose Fig. 6. Root and hypocotyl growth in darkness as a function of sucrose
(suc). WT and mutant seedlings were kept either in darkness (D) or light (L) concentration in the medium. Seedlings were grown for 4 daig on media
for 4 daig. Arrowheads indicate root tip. containing 0–100 mM sucrose.

Kircher and Schopfer PNAS | July 10, 2012 | vol. 109 | no. 28 | 11219
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Fig. 9. Summarizing scheme to illustrate the dual role of light in early

seedling development. After seed germination, seedlings follow the skoto-
morphogenic program of growth in darkness (1). Near the soil surface, in-
cident light is perceived by phytochrome (Phy) and cryptochrome (Cry)
Fig. 7. Effect of sucrose application to the root (A) or the cotyledons (B).
photoreceptor systems (2) leading to onset of photomorphogenic de-
Sucrose (0–1 M) or mannitol (0.1–1 M, osmotic control) were applied to the
velopment including establishment of the photosynthetic apparatus. In
cotyledons or the root (above the growth zone) of seedlings grown for 5
consequence, photosynthesis generates sugars (S) acting as interorgan signal
daig in the light plus 1 d in darkness and subsequently kept in darkness for
and as fuel to drive root growth (3).
further 4 d.

The dominant role of sugar in the control of root growth may be

no evidence that the elongation growth of the root of light-grown
restricted to the cotyledon stage of seedling development. With
Arabidopsis seedlings is controlled by auxin derived from the shoot the onset of leaf development additional factors may come into
apex. However, this finding does not preclude a general require- play, indicated by the observation that external sucrose supply
ment of auxin (or cytokinin and gibberellin) as permissive, rather cannot replace light with respect to side root formation that
than regulating, factors with essential functions in meristem ac- commences 5–6 d after initiation of germination (daig) (Fig. S1).
tivity or cell elongation (24). A permissive role of gibberellin is Light required for promoting chlorophyll synthesis and other light-
evident from the finding that root growth in the light is impaired in dependent processes in addition to photosynthesis may then be-
the gibberellin-deficient ga1-3 mutant (8). come increasingly important also for root development (5, 6).
There is scattered evidence in the literature that sucrose feeding
can have beneficial effects on root development, for instance by
dampening the decrease in growth rate during the daily night in
rhythmically entrained plants (25) or promoting the emergence of
lateral root primordia (26). Sugar application has been shown to
increase root growth in the dark, reaching about 30% of the effect
of light (27). However, as in many other studies with Arabidopsis
seedlings, the routine of including sucrose into the culture medium
may have hindered the full recognition of its specific morphogenic
role in root growth. In this paper, we show that the allocation of
photosynthesis-derived sugar limits root growth already during the
first few days after germination and serves directly as a long-dis-
tance signal for coupling root growth to shoot growth in the light.

Materials and Methods

Materials. Wild-type Arabidopsis thaliana (Columbia-0), cop1-4, and phyA,B/
cry1,2 mutants were as described (10, 13, 28). Mutant Suc2 seeds (22) were
a gift from Brian Ayre (University of North Texas, Denton, TX).
Fig. 8. Phenotypes of SUC2-deficient mutant seedlings grown in the ab-
sence (A and B) or presence (C) of sucrose. Seeds from the progeny of het- Growth Conditions. Seeds were sterilized with 70% ethanol and sown on half-
erozygous SUC2/suc2 plants were germinated on medium without sucrose. strength MS medium + vitamins (Duchefa) with 1% agar and 10 mM Mes
After 4 daig in the light, seedlings differing from WT (10–12 mm root length) buffer (pH 6.1) and additions as indicated. After 2 d storage at 5 °C, the plates
by having 1- to 2-mm-long roots (apparent homozygous individuals (A), were incubated in vertical orientation in continuous white light (fluorescent
were selected and kept on medium without (B) or with (C) 30 mM sucrose tubes, 100 μmol m−2 s−1), far-red light (λmax = 730 nm; 25 μmol m−2 s−1; ref.
for further 4 d in the light. 29), or darkness at 25 °C (after 5 h white light). CO2 depletion was achieved

11220 | www.pnas.org/cgi/doi/10.1073/pnas.1203746109 Kircher and Schopfer

 by enclosing the plates in hermetically closed, transparent plastic bags con- with a focusing lens. Picture sequences were captured with AVT software
taining 10 g of NaOH/CaO pellets. For local sucrose application, 50-μl drops of (AVT Universal Package 2.0) and analyzed using ImageJ software (NIH).
sterilized solutions fortified with boiled starch slurry (60 mg ml−1) were placed
on cotyledons or a 10-mm region of the root 5 mm above the tip. Amputation Experiments. Cotyledons were excised under a stereomicroscope
using fine scissors or scalpels. Microknives prepared by flattening 0.3-mm
Growth Measurements. Macroscopic root elongation was measured by injection needles were used for excising the visible leaf primordia at the
marking root tips daily at the backside of the plates. For kinematic time-lapse shoot apex.
measurements, the plates were exposed from behind to weak IR radiation
(880-nm LED array, Advanced Illumination; 0.5 μmol m−2 s−1). Pictures were Statistics. Data points are means of 20 seedlings from four to six independent
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taken automatically with an IR-sensitive CCD camera (Marlin F146B, AVT) experiments. SEs were between 3% and 10%.
equipped with a 720-nm cutoff filter (Hoya R-72, Tokina) following the set-
up proposed by Edgar Spalding (Phytomorph; http://phytomorph.wisc.edu/ ACKNOWLEDGMENTS. We thank B. Ayre for providing mutant suc2 seeds
hardware/fixed-cameras.php). The seedlings were irradiated with white LED and E. Schäfer and T. Kretsch for critical discussions and reading of the
light (100 μmol m−2 s−1) either globally or partially with a spot beam of 5- manuscript. S.K. is funded by SFB 592 of the Deutsche Forschungsgemein-
mm diameter emitted from a LED source attached to fiber optics equipped schaft (DFG) and the Wissenschaftliche Gesellschaft, Freiburg.

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Kircher and Schopfer PNAS | July 10, 2012 | vol. 109 | no. 28 | 11221