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First published online 6 June 2007
doi: 10.1242/dev.006759
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Research Report |
University of Toronto, Department of Cell and Systems Biology, 25 Willcocks Street, Toronto, Ontario M5S 3B2, Canada.
Author for correspondence (e-mail:
thomas.berleth{at}utoronto.ca)
Accepted 8 May 2007
SUMMARY
AUXIN RESPONSE FACTOR (ARF)-mediated signaling conveys positional information during embryonic and postembryonic organogenesis and mutations in MONOPTEROS (MP/ARF5) result in severe patterning defects during embryonic and postembryonic development. Here we show that MP patterning activity is largely dispensable when the presumptive carboxypeptidase ALTERED MERISTEM PROGRAM 1 (AMP1) is not functional, indicating that MP is primarily necessary to counteract AMP1 activity. Closer inspection of the single and double mutant phenotypes reveals antagonistic influences of both genes on meristematic activities throughout the Arabidopsis life cycle. In the absence of MP activity, cells in apical meristems and along the paths of procambium formation acquire differentiated identities and this is largely dependent on differentiation-promoting AMP1 activity. Positions of antagonistic interaction between MP and AMP1 coincide with MP expression domains within the larger AMP1 expression domain. These observations suggest a model in which auxin-derived positional information through MP carves out meristematic niches by locally overcoming a general differentiation-promoting activity involving AMP1.
Key words: amp1, Arabidopsis, Embryogenesis, Meristem, mp, Stem cells
INTRODUCTION
Cell division is unequally distributed in the plant body. Growth regions
with controlled patterns of dividing cells, termed apical meristems, elongate
the plant axis and an extended meristem, the procambium, retains pluripotent
cells for subsequent vascular differentiation. In many locations,
proliferative activity is inversely correlated with the differentiation status
of cells and their balance defines the sizes of meristematic regions. In some
meristematic tissues, as for example in the procambium, dividing cells give
rise to limited cell numbers in specialized tissues
(Esau, 1965
), whereas in
apical meristems permanent stem cells give off daughter cells indefinitely
(Weigel and Jürgens,
2002).
The controls regulating the balance between proliferating and
differentiating cells are only partially understood. Where amenable to genetic
dissection, as in the shoot apical meristem (SAM), these controls seem to
comprise antagonistic activities acting in specific zones (reviewed by
Bäurle and Laux, 2003;
Williams and Fletcher, 2005).
Antagonistic activities might also control the size of other meristems. A
mechanism related to that in the SAM has been proposed for the root meristem
(Casamitjana-Martinez et al.,
2003), and the formation of procambium in the leaf seems to occur
in competition with mesophyll differentiation
(Scarpella et al., 2004).
Mutations in the presumptive glutamate carboxypeptidase AMP1 are
associated with diverse morphological abnormalities including supernumerary
cotyledons, shortened plastochrons and a bushy appearance, and are further
characterized by cytokinin overproduction and upregulation of CYCD3;1
(Chaudhury et al., 1993;
Chin-Atkins et al., 1996;
Nogué et al., 2000a;
Nogué et al., 2000b;
Riou-Khamlichi et al., 1999).
However, amp1 mutants are phenotypically distinct from both cytokinin
or CYCD3;1-overproducing plants and it is unclear what primary defect could
account for the various aspects of the amp1 phenotype. Despite a
wealth of phenotypic data, AMP1 function has not been genetically
linked to other genes in embryo or meristem patterning. The AMP1 product bears
similarities to mammalian N-acetyl 
-linked acidic dipeptidases
(NAALADases) (Helliwell et al.,
2001), but neither its organismal or cellular localization nor the
molecular identity of its targets is known.
Auxin distribution patterns have been implicated in positioning of lateral
organs in shoots and roots (Reinhardt et
al., 2003; Benkova et al.,
2003), the formation of vascular tissues
(Aloni et al., 2003;
Avsian-Kretchmer et al., 2002;
Mattsson et al., 2003) and in
the generation of the root stem cell niche
(Aida et al., 2004). In all
these positions, robust patterns of auxin accumulation were found associated
with patterned cell fate specification, including positioning of meristematic
activities. Other plant hormones, specifically cytokinins, are also essential
for promoting cell division (Bishopp et
al., 2006), but their distribution patterns have not been as
precisely correlated to cellular responses. Auxin regulates gene expression
through auxin response factors (ARFs) and their nuclear co-regulators of the
Aux/IAA family (Guilfoyle and Hagen,
2001; Liscum and Reed,
2002). Although most ARF functions are still elusive, patterning
functions involving organ initiation and growth have been assigned to some
ARFs, including MONOPTEROS (MP/ARF5). Mutations in
MP lead to the absence of an embryonic root, the formation of reduced
vascular systems and flowerless shoots
(Berleth and Jürgens,
1993; Przemeck et al.,
1996). Among other ARFs, ARF7/NON-PHOTOTROPIC
HYPOCOTYL 4 and ARF19 are required for local cell proliferation
in the pericycle to produce lateral roots
(Okushima et al., 2005a;
Wilmoth et al., 2005). By
contrast, ARF2 has been shown to restrict the size of
Arabidopsis ovules and seeds and to negatively regulate certain cell
proliferation genes (Ellis et al.,
2005; Okushima et al.,
2005b; Schruff et al.,
2005).
Here we identify amp1 as a first loss-of-function suppressor of an arf mutant and present evidence that AMP1 has a role in balancing and restricting the meristem-promoting activity of auxin signaling. We document that MP has an important role in promoting meristematic niches in diverse locations and that this activity is dispensable in the absence of a counteracting pathway involving AMP1.
MATERIALS AND METHODS
Plant material and growth conditions
Unless otherwise noted, seeds were plated and plants grown as previously
described (Hardtke et al.,
2004). Origin of transgenic lines: CycB1;1::CycB1;1-GUS
(Donnelly et al., 1999),
pCLV3::GUS (Brand et al.,
2002), SNO-GFP
(Cutler et al., 2000).
UBI3::Lti6b-GFP was generated by M. Aida in the laboratory of B.
Scheres (Utrecht University, Utrecht, The Netherlands) by fusion of membrane
marker 29-1 (Cutler et al.,
2000) to the potato UBI3 promoter (L22576).
Microtechniques and microscopy
Cleared whole-mount samples were prepared as described in Berleth and
Jürgens (Berleth and Jürgens,
1993). Detection of ß-glucuronidase (GUS) activity was as in
Scarpella et al. (Scarpella et al.,
2004) with the following modifications to the concentration of
potassium ferro- and ferricyanide and incubation times: 10 mM for 1 hour
(pCLV3::GUS), 0.5 mM for 16 hours (MP::MP-GUS embryos), 2 mM
for 2 hours (CycB1;1:CycB1;1-GUS), 5 mM for 2 hours
(MP::MP-GUS seedlings) or 5 mM plus 1% Triton X-100 for 1 hour
(MP::MP-GUS nuclear localization). Scanning electron microscopy and
confocal laser scanning microscopy were performed as described
(Douglas et al., 2002;
Gazzarrini et al., 2004).
Sizes of inflorescence meristems were determined on images taken from above
the meristem by measuring the distance from the centre of the youngest
recognizable floral primordium to the centre of the furrow separating the
fifth flower primordium from the meristem as described
(Yu et al., 2000). SAM sizes
were determined on cleared medium longitudinal images using ImageJ 1.33
software
(http://rsb.info.nih.gov/ij/)
as being the area formed by the dome of the meristem connected by a straight
line between the cotyledon primordia.
RESULTS AND DISCUSSION
A survey of the molecular lesions and phenotypic strengths of amp1 mutations, including six new alleles, identified amp1-10 and amp1-13 as likely null alleles with no recognizable AMP1 transcripts and amp1-1 as an allele with pronounced residual gene activity (see Fig. S1 and Table S1 in the supplementary material). As there are no apparent AMP1 paralogs in the Arabidopsis genome, the two allele-strength categories probably reflect partial and complete loss of NAALADase activity in the AMP1 pathway.
AMP1 function stabilizes suspensor cell fate and restricts cell numbers in embryos
Cell numbers and cell division patterns in the early wild-type
Arabidopsis embryo are almost invariable. A particularly reproducible
feature of the Arabidopsis embryonic fate map is the restriction of
the descendents of the apical and basal daughter cells of the zygote. Basal
cell descendents form the suspensor, but, except for the central portion of
the root meristem, they do not contribute to the seedling pattern
(Scheres et al., 1994). In
amp1 embryos, abnormal divisions of basal cell derivatives gave rise
to additional cell tiers in the embryo proper and basal cell derivatives
regularly contributed to large parts of the seedling, including the hypocotyl
and cotyledons (Fig. 1I,J,P-S;
frequency of extra tiers in amp1-13: 36/42, 42/54, 63/63, 96/96 at
4-, 8-, 16-cell and globular stages, respectively). Conversely, cells from the
apical part of the globular embryo (framed cells in
Fig. 1G,H,I) no longer
contributed to cotyledons but became incorporated into an oversized SAM
(Fig. 1Q,R,S). At lower
frequency, abnormal divisions of basal derivatives led to the formation of a
complete second embryo from the same zygote, which was reflected in the
appearance of twin seedlings from single seeds in amp1 mutant lines
(Fig. 1V,W and see Table S1B in
the supplementary material). Except for the oversized shoot meristem and
frequent supernumerary cotyledons, the architecture of amp1
late-stage embryos is remarkably normal
(Fig. 1Y)
(Conway and Poethig, 1997).
These features suggest that the mutant phenotype is primarily a consequence of
the increased cell numbers in early pro-embryos.
In conclusion, the patterning defects in amp1 mutant embryos can be traced back to the failure of basal cell descendents to attain suspensor cell fate. Instead of displaying suspensor-specific differentiation features, some of those cells proliferate and either generate additional embryos or contribute to inappropriately large portions of the embryo proper.
AMP1 negatively regulates meristematic activities in shoots and roots
The enlarged SAM is not solely a consequence of abnormal cell specification
in the embryo. As shown in Fig.
2B,F,J and Table
1A, in amp1 mutants, SAMs continued to increase in
diameter post-embryonically and were enlarged in the central stem cell
regions, as visualized by expression of pCLV3::GUS. In addition,
expression of pCLV3::GUS was generally extended towards the flanks of
the SAM (Fig. 2F). In extreme
cases, the pCLV3::GUS expression domain was five times wider than in
wild type and became concentrated in concrete spots
(Fig. 2M). These spots might be
correlated with the formation of multiple SAMs
(Fig. 2N), which we observed in
all amp1 alleles, reminiscent of what has been described for the
corona mutant (Green et al.,
2005). By contrast, the sizes of the amp1 inflorescence
and floral meristems were not markedly abnormal [mean inflorescence meristem
diameter±s.e.m.: wild type, 52.6±0.7 mm (n=16);
amp1-9, 51.4±1.2 mm (n=12)]
(Fig. 2V,W).
|
; Himanen et al.,
2002). In amp1 mutants, the proportion of pericycle cells
that were actually proliferating was greatly increased. Lateral roots were
initiated very early (Fig. 2AA,
Table 1C) and adventitious
roots from hypocotyls were frequent (Fig.
2AE, Table 1B).
Once established, amp1 mutant root meristems were not expanded in
diameter (data not shown). In summary, our results document that AMP1 restricts stem cell pool sizes in the SAM and keeps division-competent cells dormant in the pericycle.
MP promotes meristem formation in roots and shoots
Mutations in mp are associated with the absence of an embryonic
root (Berleth and Jürgens,
1993) and MP has been implicated in the generation of a
stem cell niche in the root meristem (Aida
et al., 2004). As shown in Fig.
2D,H,L, MP was found to promote stem cell formation not
only in the root meristem, but also in the SAM. In wild type, the SAM is
initiated during embryogenesis and produces the first two leaf primordia
approximately at the time of germination
(Laux et al., 1996). In
mp mutants, the SAM was typically not visible at germination and SAMs
were also smaller in mp seedlings
(Fig. 2D,H,L,
Table 1A). As previously
reported, mutant inflorescence meristems are unable to produce normal numbers
of flowers, floral meristems produce fewer floral organs
(Fig. 2U,Y)
(Przemeck et al., 1996) and
mp mutants have incomplete vascular systems
(Fig. 3A). This defect has been
traced back to a reduced procambium, the meristematic precursor tissue of
vascular strands (Przemeck et al.,
1996). Finally, we found that mp mutants produce
adventitious roots only after many weeks in culture, in sharp contrast to the
enhanced production of adventitious roots in amp1 mutants
(Table 1B). In summary,
mp mutants are defective in the generation of appropriately sized
meristems in various locations.
amp1 uncouples embryo and meristem development from MP dependence
We assessed the possibility that MP and AMP1 activity
antagonize each other in the control of meristematic activities by
constructing amp1 mp double mutants of various allelic combinations.
We found that amp1 suppresses the phenotype of mp and can
even restore viability and fertility in an mp mutant background.
Whereas rootless mp mutant seedlings were not viable under normal
growth conditions, amp1 mp double mutants frequently formed
hypocotyls and roots (Fig. 1Z,
Fig. 2AB,
Table 1D) and could be grown on
soil (Fig. 2O-Q). In fact,
amp1 mp double-mutant embryo development could be indistinguishable
from amp1 embryogenesis (data not shown). Further, in contrast to the
generally flower-defective and invariably sterile mp mutants,
inflorescences of amp1 mp double mutants had abundant fertile flowers
with partially restored numbers of floral organs
(Fig. 2T,X,
Table 1E). Mutations in
AMP1 also increased the reduced cotyledon numbers in mp
mutants (Table 1F) and we
observed a restoration of adventitious root formation in amp1 mp
double mutants (Table 1B).
Finally, loss of AMP1 function significantly restored vascular tissue
formation in the mp mutant background
(Fig. 3A). Whereas the mature
vascular system in cotyledons of mp mutants was typically restricted
to a short midvein and occasional short side branches, cotyledon venation of
amp1 mp double mutants comprised several lateral circular veins
similar to wild-type cotyledons.
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|
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), molecular
details of the AMP1 pathway and the nature of the interaction with
MP might also not be immediately tractable. At this point, we can
rule out three obvious possibilities for this interaction. First, as explained
above, the interaction cannot be reduced to the superimposition of opposite
controls. Second, MP does not seem to overcome AMP1 activity
by transcriptional downregulation of AMP1, because AMP1
transcript levels are unaffected in mp seedlings
(Fig. 3D). Third, MP and AMP1
are unlikely to interact physically, as they are localized to different
cellular compartments (see Fig. S4B,C in the supplementary material). This
finding is also reflected in the absence of semidominant suppressive effects,
which are frequently associated with direct interaction, in amp1 mp
double mutants. Both gene products are, however, co-expressed in many
locations and their respective pathways could therefore interact in those
cells (see Fig. S5 in the supplementary material). In summary, mutant phenotypes and expression patterns suggest that MP locally interferes with AMP1-promoted cell differentiation to maintain meristematic niches.
Supplementary material
Supplementary material for this article is available at
http://dev.biologists.org/cgi/content/full/134/14/2561/DC1
ACKNOWLEDGMENTS
We thank John Celenza, Sean Cutler, Thomas Laux, Mitsuhiro Aida, Ikram Blilou and Ben Scheres for seeds, Enrico Scarpella and Annemarie Meijer for plasmid pC1300-35S-GFP and Enrico Scarpella for helpful comments on the manuscript. This work was supported by an NSERC Discovery Grant and a Premier's Research Excellence Award to T.B.
Footnotes
* Present address: The University of North Carolina, Department of Biology,
Coker Hall, Chapel Hill, NC 27599-3280, USA 
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