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First published online 24 January 2007
doi: 10.1242/dev.02774
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Research Report |
Laboratoire de Biologie Cellulaire UR501, Institut J. P. Bourgin, INRA, F-78000 Versailles, France.
* Author for correspondence (e-mail: laufs{at}versailles.inra.fr)
Accepted 5 December 2006
SUMMARY
In plants, the arrangement of organs along the stem (phyllotaxy) follows a predictable pattern. Recent studies have shown that primordium position at the meristem is governed by local auxin gradients, but little is known about the subsequent events leading to the phyllotaxy along the mature stem. We show here that plants expressing a miR164-resistant CUP-SHAPED COTYLEDON2 (CUC2) gene have an abnormal phyllotactic pattern in the fully grown stem, despite the pattern of organ initiation by the meristem being normal. This implies that abnormal phyllotaxy is generated during stem growth. These plants ectopically express CUC2 in the stem, suggesting that the proper timing of CUC2 expression is required to maintain the pattern initiated in the meristem. Furthermore, by carefully comparing the phyllotaxy in the meristem and along the mature inflorescence in wild types, we show that such deviation also occurs during wild-type development, although to a smaller extent. We therefore suggest that the phyllotactic pattern in a fully grown stem results not only from the organogenetic activity of the meristem, but also from the subsequent growth pattern during stem development.
Key words: Phyllotaxy, CUP-SHAPED COTYLEDON, Boundary domain, Internode, miRNA, Arabidopsis
INTRODUCTION
A feature of plant architecture that has puzzled scientists for centuries
is the strikingly regular position of the lateral organs along the stem. A
group of undifferentiated cells - the shoot apical meristem (SAM) - plays a
crucial role in the formation of this pattern by initiating organ primordia on
its flanks in a temporally and spatially controlled manner. The mechanisms
controlling organ positioning in the SAM (hereafter referred to as the
meristematic phyllotaxy) are beginning to be unravelled
(Reinhardt, 2005
). Little is
known, however, about the maintenance of relative organ position during the
subsequent growth and differentiation of the shoot and the generation of the
final phyllotaxy (hereafter referred to as the phyllotactic pattern)
(Reinhardt, 2005).
Many mutants with abnormal phyllotactic patterns have been described. The
bellringer [blr; also known as larson
(lsn), pennywise (pny) and vaamana
(van)] mutant (Bhatt et al.,
2004; Byrne et al.,
2003; Smith and Hake,
2003) has internodes of variable lengths, some being very short
and resulting in the formation of organ clusters. The positions of the organs
in the meristems of blr mutants are abnormal, although the meristem
appears to have a normal shape and size
(Byrne et al., 2003). This
contrasts with most mutants, in which abnormal meristem size or organisation
lead to defects in organ position from their initiation onwards
(Chaudhury et al., 1993;
Clark et al., 1993;
Clark et al., 1995;
Jeong et al., 1999;
Moussian et al., 1998;
Para and Sundas-Larsson,
2003).
Here, we describe a novel mechanism leading to changes in phyllotactic
pattern. The CUC2 gene, together with two other members of the NAC
family of transcription factors - CUC1 and CUC3 - are
required for the specification of the boundary domain surrounding organ
primordia (Aida et al., 1997;
Takada et al., 2001;
Vroemen et al., 2003).
miR164 is a microRNA (miRNA) that targets the transcript of the
CUC1 and CUC2 genes for endonucleotide cleavage, a role that
is important during the development of the organ boundaries, flowers and
leaves (Baker et al., 2005;
Kasschau et al., 2003;
Laufs et al., 2004;
Mallory et al., 2004;
Nikovics et al., 2006;
Rhoades et al., 2002). We show
here that plants expressing a miR164-resistant CUC2 gene
show abnormal phyllotactic patterns due to post-meristematic perturbations of
stem growth. Furthermore, in wild-type plants, the position of the organs
along the mature stem is more variable than in the meristem, suggesting that
variability in the phyllotaxy also occurs during wild-type stem development,
although to a smaller degree. This shows that the phyllotaxy initiated at the
meristem has to be maintained during stem growth and differentiation, and
suggests that this requires the proper timing of CUC2 expression.
MATERIALS AND METHODS
Plant material and growth conditions
CUC2g-m4 and CUC2-wt transgenic plants
(Nikovics et al., 2006), and
the LFY::ALCR alcA::erGFP
(Deveaux et al., 2003) and
DR5::GFP (Benkova et al.,
2003) lines have all been described previously. Plant growth in
controlled chambers was conducted according to Laufs et al.
(Laufs et al., 2003) and
ethanol induction according to Deveaux et al.
(Deveaux et al., 2003).
Phyllotactic pattern and meristematic phyllotaxy measurements
Phyllotactic pattern was assessed on fully grown stems of 2-month-old
plants. The top 5 cm of the stem was not assessed, as elongation was
incomplete. Divergence angle and internode length were measured
simultaneously, using the device presented in Fig. S1A in the supplementary
material. The divergence angle was measured between the insertion points of
two successive floral pedicels and is therefore independent of the outgrowth
direction of the pedicel (see Fig. S1B in the supplementary material).
Phyllotaxy orientation can be either clockwise or anticlockwise. For each
individual, the phyllotaxy orientation was set to the direction giving the
smallest average divergence angle.
To analyse the meristematic phyllotaxy, we determined the order of primordium formation by studying phyllotaxy in plants producing erGFP under the control of the primordium marker LFY. GFP observations were made with a Leica MZFIII fluorescence stereomicroscope with a 450-490 nm excitation filter set and a 525-550 nm bandpass, or with a 480 nm long-pass emission filter set. Digital pictures were taken with a Nikon Coolpix995 camera. The divergence angle at the meristem was measured using Optimas software (version: 6.51.199, Media Cybernetics).
The distributions were compared using the Kolmogorov-Smirnov test (K-S test) at http://home.ubalt.edu/ntsbarsh/Business-stat/otherapplets/ks.htm.
Epidermal cell- and meristem-structure observations
Epidermal cells were observed on an imprint produced by applying
transparent nail polish to the surface of the plant. Digital pictures were
taken with a Nikon Coolpix995 camera. Cell length was measured with Optimas
software (version: 6.51.199, Media Cybernetics). Cell length that was measured
at the two ends and in the middle of the internode was found to be uniform.
Therefore, the number of cells per internode in a row of cells could be
calculated by dividing the internode length by the cell length.
Meristem size and structure were analysed on partially dissected and cleared apices. Alternatively, sections of paraffin-embedded material were observed.
Scanning electron microscopy
Scanning electron microscopy was carried out as previously described
(Bertrand et al., 2003).
In situ hybridisation
CUC2 in situ hybridisation was performed as described by Nikovics
et al. (Nikovics et al.,
2006).
RESULTS AND DISCUSSION
Plants expressing a miR164-resistant CUC2 gene have an abnormal phyllotactic pattern
Plants expressing a miR164-resistant CUC2 gene
(CUC2g-m4) showed multiple phenotypical defects, including serrated
leaves, enlarged boundaries around the floral organs and defects in carpel
development (Nikovics et al.,
2006). In addition, they showed abnormal phyllotaxy defects
(Fig. 1). Out of the 60
CUC2g-m4 lines that we generated (11 and 49 in the Col and WS
backgrounds, respectively), three showed extremely compact inflorescences with
very short internodes and long floral pedicels
(Fig. 1C). None of the 52
CUC2g-wt control lines (21 and 31 in the Col and WS backgrounds,
respectively) that were transformed with an unmodified CUC2 gene had
such a phenotype. Weaker CUC2g-m4 lines also showed abnormal
inflorescence architecture. In wild-type Arabidopsis, a cauline leaf
subtends the side branches. By contrast, one or two additional smaller leaves
growing on the sides of the normal cauline leaves were frequently observed in
CUC2g-m4 lines (32%) and less often in CUC2g-wt lines (12%)
(Fig. 1A,B). In the
Arabidopsis inflorescence, organs are arranged following a spiral
pattern. Organs of CUC2g-m4 lines showed a less regular distribution
along the inflorescence (Fig.
1D,E). In some cases, flowers formed clusters that were separated
with longer internodes (Fig.
1D,E). There was no strict separation between these two types of
abnormal phyllotactic pattern, as siblings of the same transgenic lines could
show either phenotype and individual plants could show both phenotypes at
different moments of their development. This suggests that these variations
are extremely sensitive to the level of CUC2 expression. These
modifications were observed in at least 17 independent CUC2g-m4
transgenic lines (two and 15 in the Col and WS backgrounds, respectively), but
in none of the CUC2g-wt lines.
Precise characterisation of the phyllotactic pattern in wild-type and CUC2g-m4 plants
We characterised the phyllotactic pattern of the flowers by measuring the
divergence angle and internode length between successive organs along the main
inflorescence stem (Fig. 1F,
and see Fig. S2 in the supplementary material). The divergence angle was
measured between the insertion points of the pedicel of two successive organs
and is therefore independent from the growth direction of the flower (see Fig.
S1 in the supplementary material for details). For each inflorescence, we
determined the orientation of the generative spiral and measured divergence
angles according to this orientation.
In wild-type WS, the mean divergence angle (149°, n=217) was surprisingly far from the theoretical angle of 137.5°, and we also observed considerable variability (Fig. 1F). Only 48% of the divergence angles fell into the 120-150° class, which contains the theoretical angle. This proportion increased to 82% if the class was enlarged to encompass angles ranging from 90-180°. In total, 18% of the measured angles fell outside of this class, with a second maximum in the angle distribution observed for the 210-300° class, which contained 11.5% of all of the measured angles. The expected angle in the case of the reversal of the direction of phyllotaxy (360°-137.5°=222.5°) falls into this class, suggesting that the phyllotactic pattern may have been transiently reversed. Most of the divergence angles falling into this 210-300° class were not isolated. Instead, they formed groups of three to 11 successive angles in 65% of cases. This observation is consistent with the transient inversion of phyllotaxy orientation, followed by a reversion to the original orientation.
Internode length was highly variable in WS, ranging from less than 0.5 mm to 2 cm, and no major class of internode length could be identified (Fig. 1F). No correlation was observed between internode length and divergence angle (see Fig. S3 in the supplementary material). Thus, abnormal divergence angles are not preferentially associated with a decrease or an increase in internode length.
From this, we concluded that the phyllotactic pattern is to some extent variable in wild-type WS Arabidopsis. We observed a similar variability in the phyllotactic pattern of plants grown under three other environmental conditions, including growth chambers (see Fig. S4 in the supplementary material). This suggests that the variability is unlikely to result from some particularity or from variations in the environment. In addition, variability of the phyllotactic pattern was also observed in a second ecotype, Col (see Fig. S2 in the supplementary material). Altogether, this suggests that the observed variability is an intrinsic property of the phyllotactic pattern of Arabidopsis.
We next examined two representative CUC2g-m4 transgenic lines (Fig. 1F, and see Fig. S2 in the supplementary material). The WS CUC2g-m4 line had a strong increase in the frequency of short internodes (77% less than 3 mm, versus 19% in wild type), which accounts for the organ clusters. Long internodes were also more frequent (6% greater than 2.1 cm, versus 1.5% in wild type). The divergence-angle distribution was also strongly affected, as the maximum in the 90-180° class observed in wild type was not observed in the mutant, which showed a more uniform distribution (Fig. 1F). Similar changes of the internode length and divergence angle were observed in the Col CUC2g-m4 line (see Fig. S2 in the supplementary material).
Meristem function is unaffected in CUC2g-m4 plants
Because abnormal phyllotactic pattern is often associated with perturbed
meristem size or organisation, we analysed the meristem of CUC2g-m4
plants. Meristems of transgenic plants showed typical layered organisation
(Fig. 2A) and their size was
not modified compared to the wild-type control
(Fig. 2B).
Variability in divergence angle principally results from post-meristematic defects
Because the meristem appeared to be unaffected in the CUC2g-m4
lines, we next analysed primordium initiation. As auxin has been implicated in
the control of the primordium initiation site in the meristem
(de Reuille et al., 2006;
Jonsson et al., 2006;
Reinhardt et al., 2000;
Reinhardt et al., 2003;
Smith et al., 2006;
Vernoux et al., 2000), we
first analysed auxin response using an auxin-sensitive promoter (DR5)
controlling the expression of a GFP reporter gene
(Benkova et al., 2003). In both
wild-type and CUC2g-m4 meristems, similar strong GFP staining was
observed in two to three distinct groups of cells
(Fig. 2C). This suggests that
the auxin-response peaks associated with primordium initiation are not
disturbed in CUC2g-m4 apices.
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In order to identify the point at which internode development in CUC2g-m4 plants deviated from that in wild type, we observed internodes on partially dissected inflorescences (Fig. 3B). Internode length increased gradually and regularly down the stem in wild-type plants, whereas it was more variable in CUC2g-m4 inflorescences. Interestingly, this variability between internodes on the same stem became clear in the subapical region. This suggested that abnormal internode length mainly resulted from post-meristematic defects in internode growth.
Variability of internode length in CUC2g-m4 plants is due to changes in both cell number and cell size
We investigated the cellular basis of variation in internode length by
measuring epidermal-cell length and calculating the cell number on wild-type
internodes (mean size 10 mm), and on long (mean size 30 mm) and short (less
than 1 mm) internodes of CUC2g-m4 plants
(Fig. 3C). The long
CUC2g-m4 internodes were formed by approximately 3-times more cells,
which all had normal lengths (Fig.
3C). The short internode of CUC2g-m4 plants contained
approximately 2.5 fewer cells, which were only about a third the wild-type
length. If cell elongation and division are variable in the inflorescence, it
would be expected that an asymmetrical distribution of regions of shorter
cells or longer cells leads to the twisting of the inflorescence. Such
twisting was observed in CUC2g-m4 plants and the cells on the inner
part were shorter than those on the outer part of the twisted stem
(Fig. 3D). We therefore
conclude that internodelength variation results from a combination of
cell-elongation and cell-division defects.
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CUC2g-m4 plants showed an increase in the level of CUC2 expression, as well as a severely modified expression pattern (Fig. 4B). The number of cells expressing CUC2 in the meristem was increased, which is consistent with an enlargement of the boundary domain. CUC2 expression was maintained for longer in the axils of the floral pedicels during stem development compared to wild type, as it was detected in lower nodes. CUC2 expression also expanded in the adaxial region of the flower pedicel. CUC2 was expressed in the epidermal and cortical cells of the internode. Twisted CUC2g-m4 stems showed an asymmetrical distribution of CUC2 expression, with maximum expression on the inner part of the bent stem (Fig. 4C,D).
These observations show that, in the apex, all cells between two flowers
initially express CUC2. These CUC2-expressing cells are the
source for the internode and node cells. During later stages, a region with no
CUC2 expression appears and grows rapidly (the internode), while
CUC2 expression is maintained for slightly longer in the axils of the
flower pedicels. Thus, differentiation of the internodes involves the
establishment of a cell population that no longer expresses CUC2.
miR164 has a central role in the clearing of CUC2 mRNA from
internode cells, as CUC2g-m4 plants show ectopic CUC2 mRNA
accumulation in the internode. We suggest that post-meristematic changes of
the phyllotaxy result from this ectopic expression of CUC2 in cells
derived from the boundary domain and that give rise to the internode. How
could this occur? It has been suggested that CUC2 genes repress
growth during embryogenesis, resulting in the formation of two separated
cotyledons (Aida et al., 1997;
Aida et al., 1999). The
enhanced reduction of internode elongation in strong CUC2g-m4 plants
(Fig. 1C) and the reduction of
stem growth on the side with the strongest CUC2 expression
(Fig. 4C,D) suggest a similar
CUC2-mediated growth inhibition.
CONCLUSION
By characterising plants expressing a CUC2 gene modified to be resistant to the microRNA miR164, we show that an abnormal phyllotactic pattern can be generated despite the plants having an initial normal meristematic phyllotaxy. Interestingly, wild-type Arabidopsis showed some variability in the phyllotactic pattern, whereas the meristematic phyllotaxy was more robust. This indicates that, in the transgenics, and to a lower level in the wild type, variability of the phyllotaxy is generated during stem growth. We therefore suggest that the phyllotactic pattern in the fully grown stem results not only from the organogenetic activity of the meristem, but also from subsequent events during stem growth. This pattern may either be well-maintained (as in wild-type Arabidopsis) or be maintained less efficiently (as in CUC2g-m4 plants). Furthermore, our work shows that rapid clearing of the CUC2 transcript from internode cells is required for the efficient maintenance of the phyllotactic pattern during stem development.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/134/6/1045/DC1
ACKNOWLEDGMENTS
We thank D. Barabé and B. Jeune for discussion on the analysis of the phyllotaxy; R. Simon, M. Aida, V. Pautot, J. D. Faure and J. C. Palauqui for discussions; B. Letarnec for plant care; O. Grandjean for help with the confocal microscope; and S. Domenichini for SEM assistance. This work was partially supported by an ACI Jeunes Chercheurs award to P.L. and by the trilateral Genoplante GENOSOME program TRIL-046.
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