351 Koshland Hall, University of California at Berkeley, Berkeley, CA 94720, USA
* Author for correspondence (e-mail: freeling{at}nature.berkeley.edu)
Accepted 28 November 2002
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SUMMARY |
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Key words: rgo, Maize inflorescence development, Nonallelic noncomplementation, Spikelet, Meristem identity, Gene dosage, ids1
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INTRODUCTION |
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Maize is a monoecious species that has two types of inflorescences, the
male tassel at the apex of the plant, and female ears in the axils of leaves.
Tassel and ear development are similar until after flowers are initiated, at
which point organ abortion in the tassel and the ear produce separate
unisexual inflorescences (Dellaporta and
Calderon-Urrea, 1994; Irish,
1996
). At the top of the plant the SAM elongates and converts into
an IM, which gives rise to the tassel. At approximately the same time, the
axillary meristems initiate a prophyll (the first leaf on a shoot) and eight
to 14 husk leaves, and then convert into a lateral IM, which produces the ear.
The top (youngest) ear primordium grows faster than lower primordia and often
develops into a single dominant ear. The IM gives rise to 2°, 3°, and
4° meristems (Fig. 1A).
Each IM produces an indeterminate number of spikelet pair meristems (SPM,
2°) in an acropetal (from the base to the apex), polystichous (multiple
rows) manner. In the tassel, the first few SPMs become branch meristems and
produce long tassel branches that initiate SPMs in a distichous pattern. All
other SPMs initiate one spikelet meristem (SM, 3°) and then convert into
SMs. Each SM then initiates a pair of bract-like glumes. Subsequently, each SM
initiates the lower floret meristem (FM, 4°) and converts into the upper
FM. The FMs make the floral organs, the palea/lemma, lodicules, anthers and
pistils. The pistils abort in the tassel, while the anthers and lower pistil
abort in the ear (Cheng et al.,
1983
). This results in a single kernel developing from each ear
spikelet. A large number of mutants that affect these meristem initiation and
identity conversion events have been identified and make the maize
inflorescence a powerful system for studying meristem function
(McSteen et al., 2000
;
Veit et al., 1993
).
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Maize inflorescence mutants affect tassel and ear development in many ways.
Interestingly, mutant phenotypes often differentially affect the two
inflorescence types (Postlethwait and
Nelson, 1964). These mutants interact with each other, often
synergistically. The class II tasselseed mutants (ts4, Ts6) affect
both floral organ abortion and branching. Pistil abortion in the tassel is
inhibited resulting in a feminized tassel with seeds. In addition, SPMs fail
to convert into SMs in ts4, and SM to FM transitions are delayed in
Ts6. Both of these mutations result in extra branching in the ear
(Irish, 1997a
;
Irish, 1997b
). The ramosa
mutants (ra1, ra2, ra3) have indeterminate SPMs; these make long
branches that produce many SMs
(Postlethwait and Nelson,
1964
; Veit et al.,
1993
). indeterminate spikelet1 (ids1) mutants
delay the SM to FM conversion resulting in the production of extra florets,
which is a more branched and less determinate condition
(Chuck et al., 1998
).
indeterminate floral apex1 (ifa1) affects determinacy of all
inflorescence meristems, resulting in extra SPMs, SMs and an indeterminate FM.
ids1 and ifa1 interact synergistically, with SMs converting
into branch meristems in the ear and into SPMs in the tassel
(Laudencia-Chingcuanco and Hake,
2002
).
Perturbations of regular rowing and kernel orientation are sensitive
indicators of defects in inflorescence development. Increased or decreased
numbers of florets produce an easily recognizable reversed germ orientation
(rgo) phenotype (Fig. 2D).
Several reversed germ and fused kernel mutants have been previously described
in maize. Kiesselbach describes the occurrence of reversed and fused kernels
in various inbreds and hybrids, as well as documenting reports of these
phenotypes dating back to 1810
(Kiesselbach, 1926). In this
and subsequent reports (Jackson,
1996b
; Joachim,
1956
), the reversed orientation of the kernels was attributed to
the development of the lower instead of the upper floret. Fused kernels were
attributed to the development of both florets in a spikelet. The development
of both florets occurs in Country Gentleman sweet corn and results in reversed
kernels (Micu et al., 1983
).
Diverse patterns of floret development are found in the grasses; basal fertile
florets with non-fertile apical florets are found in the pooids, while the
opposite pattern occurs in the panicoids
(Chapman and Peat, 1992
).
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The reversed germ orientation1 (rgo1) mutant was isolated
by Sachan and Sarkar. They suggested that the phenotype was due to the
differential growth of the integuments and the nucellus causing rotation of
the kernel (Sachan and Sarkar,
1980). In this paper, we show that the rgo1 reversed
kernel phenotype is actually due to the production of an extra floret by the
spikelet meristem. We demonstrate that rgo1 and ids1 have
overlapping functions in regulating meristem identity. The rgo1; ids1
double mutant is synergistic and affects more meristem types than either
mutant alone. A dosage based model is proposed for the regulation of meristem
identity conversion in the maize inflorescence.
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MATERIALS AND METHODS |
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rgo1 mapping
Wx1 rgo1 plants were crossed to a wx1 stock and 33
wx1 translocation lines representing 18 chromosome arms. The progeny
of these crosses were self-pollinated and the resulting waxy (wx1)
and opaque (Wx1) seed were planted separately. Linkage to an arm is
indicated by repulsion from a given translocation marked by wx1
(Laughnan and Gabay-Laughnan,
1996). After mapping to a chromosome arm, finer molecular mapping
was performed using RFLP and SSR markers.
Scanning electron microscopy
1-3 cm developing ears were dissected from 6- to 8-week old plants and
fresh tissue was used for imaging. 1-3 cm tassel primordia were fixed in FAA
(3.7% formaldehyde, 5% glacial acetic acid, 50% ethanol) overnight at 4°C,
dehydrated through an ethanol series, and critical-point dried. Glumes were
dissected away to expose the floret primordia, and the samples were then
sputter coated with 15 nm of gold/palladium (Polaron SEM coating system). An
Electroscan E3 Environmental Scanning Electron Microscope (ESEM) was used to
image samples at 20 kV. Images were digitally captured using IAAS software
(Electroscan Corp.). Electron microscopy was performed in the Electron
Microscope Laboratory at the University of California at Berkeley.
Histology
Tissue was fixed overnight at 4°C in FAA, dehydrated through an ethanol
series, and stained with 0.1% Safranin. The samples were then embedded in
paraffin (Paraplast, Oxford Labware, St Louis, MO). The samples were mounted
on stubs, and 10 µm sections were cut and then mounted on slides. The
slides were deparaffinized in Histoclear (National Diagnostics, Atlanta, GA),
hydrated through an ethanol series, and stained for 30 seconds to 1 minute
with 0.05% Toluidine Blue O. Slides were then rinsed, dehydrated, and mounted
with Merckoglas (Mikroskopic, Germany)
(Ruzin, 1999). Images were
digitally captured using a Zeiss Axiophot light microscope.
Quantitative analysis
Tassel phenotypes were quantified by counting the number of tassel
branches, the number of spikelets on the central spike of the tassel, and the
number of florets per spikelet. Between 20 and 50 spikelets from the central
spike were counted to determine the number of florets per spikelet, and the
numbers from siblings were pooled.
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RESULTS |
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In wild-type female spikelets the upper floret develops into the kernel with the embryo facing the tip of the ear, while the lower floret arrests and aborts. In wild-type male spikelets, two florets develop and produce three anthers each (Fig. 2G). In rgo1 tassels spikelets have three florets, each with three anthers, for a total of nine anthers per spikelet (Fig. 2H). The penetrance of the tassel phenotype is background dependent, and ranges from 39% in B73 to 91% in Gaspe Bay Flint (GBF). The total number of spikelets and number of tassel branches are not affected in rgo1 mutants (Table 1).
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rgo1 is a single recessive mutation and maps to chromosome
9
Self pollinations of heterozygous rgo1/+ plants produced 25%
(n=48) mutant progeny, and crosses of rgo1/+ heterozygotes
to rgo1 homozygotes produced 50.6% (n=81,
2=0.012, d.f.=1, P=0.91) mutant progeny. This
indicates that rgo1 behaves as a single recessive mutation when
introgressed into B73. waxy1 (wx1) marked reciprocal
translocation stocks were used to map rgo1 to a chromosome arm.
rgo1 was in repulsion to all of the wx1 marked
translocations as well as to a wx1 stock, indicating that
rgo1 is located on chromosome 9 and linked to wx1. Test
crosses place rgo1 and wx1 approximately 11 cM apart.
Further mapping with RFLP and SSR molecular markers locate rgo1
within 2 cM of the SSR marker umc1267 in bin 3, close to the centromere.
The spikelet meristem initiates an extra flower in rgo1
mutants
To define the developmental defects in rgo1 mutants, early ear
development was observed using electron microscopy and histology.
Inflorescence meristems (IMs) of rgo1 ears initiate multiple rows of
SPMs in the normal polystichous pattern and appear identical to wild-type IMs
(Fig. 3A,B). SPMs in
rgo1 plants initiate a SM correctly from the flank of each SPM
(Fig. 3C,D), and are thus not
responsible for the disrupted rowing observed in rgo1 ears
(Fig. 2B).
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Differences between normal and mutant development become evident upon
examination of the SM. Normally each SM initiates a set of outer and inner
glumes, and then the lower floret meristem
(Fig. 3E). The SM itself
converts into the upper floral meristem. rgo1 SMs also initiate two
glumes and a FM, but then continue to make a second FM at 180° from the
first FM (Fig. 3F).
Subsequently both wild-type and rgo1 SMs become FMs and initiate
floral primordia (Fig. 3G,H).
However, the orientation of the floral organs on rgo1 spikelets is at
180° from normal, with the middle anther primordium on the same side as
the outer glume (Fig. 3H), as
opposed to the inner glume as in wild-type spikelets
(Fig. 3G). Later in development
(further down the developing ear), the FM makes the gynoecial ridge, two fused
carpels that elongate to become the silk
(Nickerson, 1954). Like the
anther primordia, the orientation of the developing silk on the top flower is
reversed in rgo1 spikelets (Fig.
3I,J). In rgo1 spikelets the lowest FM arrests and aborts
similar to wild-type development, but in many spikelets the second flower
continues to develop (arrowheads in Fig.
3J). The developmental defects in tassel spikelets mirror those
observed in ear spikelets, with no defects observed until FMs are initiated.
Wild-type SMs initiate only one FM (Fig.
4A), while rgo1 SMs initiate two
(Fig. 4B). The orientation of
the third flower in rgo1 tassel spikelets is reversed compared to
wild-type apical florets (Fig.
4C,D).
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rgo1 affects floral abortion of subapical florets producing
fused kernels and disorganized rowing
During normal development the lower flower aborts while the upper flower
makes a silk (Fig. 5A). The
flower is then fertilized, and develops into a kernel. The lower flower
undergoes programmed cell death which is detectable using the TUNEL assay for
DNA fragmentation (Jones et al.,
2001) and the accumulation of autoflorescent compounds in the cell
wall (data not shown). After cell death, collapsed cell walls are all that
remains of the aborted flower (af in Fig.
5E). In rgo1 plants, developing flowers have several
fates, reflecting the variable expressivity of the mutation. Mirroring
wild-type development, the apical flower can develop while the two lower
flowers abort (Fig. 5B,F).
However, in many rgo1 spikelets the second flower does not abort and
the two upper flowers develop while the lowest flower aborts
(Fig. 5C,G). Two kernels are
produced in spikelets where the two apical flowers develop. The top (third)
flower produces a reversed kernel, while the middle (second) flower's kernel
has a normal orientation (Fig.
1). These two flowers can fuse during development, producing fused
kernels (Fig. 5D,H). In
spikelets with two developing flowers, the flowers are crowded and displace
each other resulting in the disrupted rows of kernels observed in mature
rgo1 ears (Fig.
2B).
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rgo1 and ids1 exhibit nonallelic
noncomplementation
indeterminate spikelet1 (ids1) is a maize gene with
homology to the AP2 class of transcription factors. Mutations of the
ids1 gene produce more than the usual two florets per spikelet. This
phenotype has been interpreted as having less determinate SMs. In some
backgrounds the spikelet becomes totally indeterminate. ids1 is
expressed in both SPMs and SMs, although the ids1 phenotype only
affects spikelet meristems (Chuck et al.,
1998). Because of the production of extra florets, ids1
mutant ears also have a reversed germ and disturbed rowing phenotype
(Fig. 6). The lack of a SPM
phenotype despite ids1 mRNA expression suggests redundancy with
another gene or genes, and given the similarity of the rgo1 and
ids1 phenotypes, we investigated whether the double mutant would
display a SPM phenotype.
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Homozygous rgo1 and ids1 mutants were crossed to each
other. The resulting ids1/+; rgo1/+ plants were grown and
self-pollinated to produce the double mutant. Since ids1 maps to
chromosome 1 and rgo1 maps to chromosome 9, it was a surprise that
the ears of the doubly heterozygous plants had disturbed rows and reversed
kernels, reminiscent of the ids1 and rgo1 single mutants
(Fig. 6). When two recessive
mutations at different loci fail to complement each other, the genetic
behavior is known as nonallelic noncomplementation
(Yook et al., 2001).
Penetrance of this phenotype was 26% in ids1-Burr, 84% in
ids1-mum1 and 100% with ids1-VI. Penetrant ids1-VI
and ids1-mum1 ears were used for further studies. Nonallelic
noncomplementation suggests that genetically, rgo1 and ids1
have overlapping functions. The occurrence of a mutant phenotype with the loss
of two functional copies (either a rgo1 or ids1 homozygote
or the ids1/+; rgo1/+ double heterozygote) implies that at least
three wild-type copies of these two genes are needed for correct regulation of
spikelet meristem activity.
rgo1; ids1 double mutants affect multiple meristems in the
ear
In order to observe double mutants, families of the selfed progeny of
double heterozygote plants were grown. Three classes of F2 ears
were observed in these families: normal ears, ears with reversed kernels and
disrupted rowing like rgo1 or ids1 single mutants, and ears
with proliferated spikelets and long branches
(Fig. 6). The expectation based
on the observation of nonallelic noncomplementation is that 11/16 of the
plants (all plants missing two or more copies of ids1 or
rgo1) would exhibit a mutant phenotype, and 1/16 would be double
mutants. Table 2 lists the
observed numbers of ears in each of these phenotypic classes. All families
segregated the three phenotypic classes as expected, although the severity of
the double mutant phenotype varied from family to family.
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While single mutants only affect the SM, the ids1; rgo1 phenotype affects the SM as well as the SPM. To analyze the double mutants, we define meristems that produce glumes or florets as SMs, and meristems that produce spikelets as SPMs. A range of effects on the SM is observed, from retardation of identity transitions to identity reversions. As expected from the single mutant phenotypes, extra florets are produced by each SM, resulting in reversed and fused kernels (Fig. 7A,E). In addition, the double mutant SMs make supernumerary glumes (Fig. 7B,G). The SM can initiate one or more florets, elongate into a branch, and then initiate one or more spikelets (Fig. 7C,E). Both the primary and reiterated spikelets are identified by the presence of subtending glumes (Fig. 7C,D). In cases where the SM is producing spikelets, it reverts to SPM identity.
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SPMs produce too many spikelets in the double mutant. This phenotype can be restricted to the base of the ear (Fig. 6, Fig. 7A) where the SPM produces multiple SMs. In the most severe cases, all of the SPMs on the ear become indeterminate (Fig. 7F), and produce multiple spikelets (Fig. 7G). These spikelets make many glumes (arrowheads, 7G) and only rarely produce florets as evidenced by the absence of silks. Since glumes are produced by the SM, in these spikelets the transition from producing glume primordia to floret primordia is delayed.
Unlike the synergistic interaction observed in the ear, rgo1; ids1 tassels have an additive phenotype. More florets are produced by each spikelet, but there is no evidence that the SMs in the tassel have changed identities or that SPMs are affected (Table 1).
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DISCUSSION |
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If ids1 is placed into the framework of meristem identity changes
it would perform a similar role as rgo1
(Fig. 7C), promoting the SM to
FM change. The overlapping functions of rgo1 and ids1
revealed by their mutants and genetic interactions support the idea that these
genes perform similar biological functions. In some double mutant spikelets,
the SM reiterates more SMs (Fig.
7D,E) or makes supernumerary glumes
(Fig. 7G) before initiating any
FMs. The phenotype indicates that SM identity changes are inhibited or even
reversed. This is consistent with a meristem identity role for both
rgo1 and ids1. In addition, in the double mutant the SPM
also produces long branches with multiple SMs
(Fig. 7A,F). Like the SM, SPM
conversion is defective in ids1 and rgo1 mutant plants
(Fig. 8D). The ids1;
rgo1 double mutant phenotype resembles the ids1; ifa1 phenotype
in several ways. In the latter, the ear SM is converted into an indeterminate
branch meristem which makes SPMs, while the tassel SM is converted into a SPM
(Laudencia-Chingcuanco and Hake,
2002). Both double mutants have more severe effects in the ear
than in the tassel. In both cases, meristem identity has changed and results
in a decrease in determinacy. rgo1 and ifa1 do not exhibit a
synergistic interaction like ids1 and ifa1 do (data not
shown), although ids1 interacts synergistically with both
rgo1 and ifa1. This illustrates that although rgo1
and ids1 functions overlap, these genes play unique roles in
inflorescence development.
The conversion model of maize inflorescence development proposes that SPMs
initiate a SM and then convert into SMs, and SMs intiate a FM and then convert
into FMs (Fig. 8A). This model
is based on the class II tasselseed phenotypes, in which meristem identity
conversions are delayed (Irish,
1997a). Determinacy is simply a function of correct identity
transitions in the conversion model. A SM that converts into a FM is
determinate, while a SM that never changes its identity is indeterminate. An
alternative model of inflorescence development, the lateral branching model,
does not involve identity conversion (Chuck
et al., 1998
). Instead, Chuck et al., suggest that all florets,
including the terminal floret, are initiated laterally by the SM. A band of
ids1 expression between the developing upper and lower floret was
interpreted to be the remnant SM, which is not suppressed in ids1
mutants. This theory was partially reconciled with the conversion model by
Irish who suggested that the remnant of the SM is morphologically
indistinguishable but still present on the flank of the FM
(Irish, 1998
). In the lateral
branching model, ids1 functions to suppress indeterminate growth of
the SM. One of the predictions of this model is that ids1 mutant SMs
should make more FMs, but as SM identity does not change, only FM primordia
should be produced by the SM.
Observations from our research favor the conversion model, which can explain mutant behavior without invoking remnant meristems. In the double mutant, SMs produce supernumerary FMs, but also initiate additional glumes and SMs, indicating that SM identity has changed (Fig. 8D). The lateral branching model does not implicate ids1 in meristem identity changes because in this model the SM never becomes a FM. The conversion model explicitly implicates identity change as a mechanism, and thus can explain the double mutant phenotype. The lateral branching model was partially based on the observation that ids1-mum1 spikelets do not terminate in florets, because in this model the florets are lateral branches of the spikelet. Upon introgression into B73, ids1-mum1 plants can make functional terminal florets, as do the ids1-Burr and ids1-VI alleles. ids1-VI ears make kernels and do not exhibit indeterminate spikelets on the ear (Fig. 6). Thus, in certain genetic backgrounds, ids1 mutant spikelets can terminate in fertile florets, suggesting that ids1 is involved in the conversion of SMs into FMs.
Meristem identity is regulated in a dosage-sensitive manner by
multiple genes
Nonallelic noncomplementation can be explained by a genetic pathway that is
sensitive to the total dosage of two genes
(Stearns and Botstein, 1988;
Yook et al., 2001
). Based on
the nonallelic noncomplementation and synergistic double mutant phenotypes of
rgo1 and ids1, we propose a dosage based model for meristem
conversion. In this model, SPM
SM and SM
FM conversions are
regulated by both ids1 and rgo1, although the threshold for
normal behavior is lower in SPMs than in SMs
(Fig. 9). Signals from the
vegetative portion of the maize plant are known to affect meristem identity
transitions. In the maize indeterminate 1 (id1) mutant the
transition from vegetative to reproductive development is extremely delayed or
never happens. id1 is expressed in immature leaves, but acts in a non
cell-autonomous manner and affects the apical meristem
(Colasanti et al., 1998
).
Meristem culture experiments also support the idea that the SAM integrates
signals from the whole plant and does not keep track of its identity
internally (Irish and Karlen,
1998
; Irish and Nelson,
1991
). If rgo1 and ids1 are in the genetic
pathway that responds to these signals coming from the rest of the plant,
these mutants could make the meristem less sensitive to the signal needed for
meristem conversion (this is equivalent to raising the signaling
threshold).
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Control of meristem identity transitions in the maize inflorescence is
under the combinatorial control of multiple genes. The penetrance of the
ids1/+; rgo1/+ nonallelic noncomplementation phenotype and the
severity of the ids1; rgo1 double mutant phenotype are variable
(Fig. 7), suggesting that there
are genetic modifiers in the maize genome (and probably environmental effects
as well) that affect this phenotype. Three additional lines of experimental
evidence provide support for the presence of modifiers. To test the dosage
model of nonallelic noncomplementation, we produced plants missing one copy of
the long arm of chromosome 1 (which carries ids1) using B centromere
translocation lines (Birchler,
1996). Chromosome 1L hypoploids exhibited a reversed kernel
phenotype. This shows that there are other genes on 1L (possibly tb1,
kn1, and/or ts6, which all have effects on meristematic
behavior) that in combination with a missing dose of ids1 have an
effect on spikelet meristem identity. Similarly, a directed Mutator
transposon mutagenesis experiment aimed at cloning rgo1 produced
hundreds of plants with rgo1-like phenotypes. Only one or two
disruptions of the rgo1 gene would be expected, suggesting that
rgo1 heterozygotes uncover many branching modifiers. Finally, a large
screen of over 50,000 F1 Mutator active ears for dominant
or semi-dominant reversed germ phenotypes identified several ears with strong
reversed germ phenotypes. These ears transmit fascicled (ears with more than
one main spike due to multiple IMs), ramosa (ears with long branches at their
base due to indeterminate SPMs), and reversed germ (SM) phenotypes in the
F2 families in a recessive manner. In these families, heterozygotes
uncover a reversed germ (i.e. SM) phenotype. However, homozygotes affect both
the SM and SPM and IMs. These data suggest there are many genes in the maize
genome that, when disrupted, can contribute to the dosage effect that creates
reversed kernels.
Several other examples of dosage-sensitive developmental pathways have been
described in plants. LEAFY (LFY) is an Arabidopsis gene that
regulates the transition to flowering by promoting and maintaining floral
meristem identity (Weigel et al.,
1992). Heterozygous lfy/+ plants are normal under long
day conditions. However, in short day conditions floral reversion results in
inflorescences being elaborated from the floral meristem
(Okamuro et al., 1996
). A
second example can be found in the regulation of meristem maintenance. The
CLAVATA1 (CLV1) and CLV3 genes in Arabidopsis are
involved in maintaining meristem size by balancing the rates of cell division
and primordial initiation. CLV1 encodes a receptor kinase, and
CLV3 is its ligand (Trotochaud et
al., 2000
). CLV1 and CLV3 exhibit a form of
dosage sensitivity. The weak clv1/+ phenotype is strongly enhanced in
a clv3/+ background (Clark et al.,
1995
). In addition, stm/+ heterozygotes suppress
clv1 semidominance (Clark et al.,
1996
). Finally, hemizygosity of either liguleless1 or
liguleless2, genes necessary for ligule development in maize, affect
the null phenotype of the other mutant
(Harper and Freeling, 1996
).
These examples may reflect a general sensitivity to dosage in many aspects of
meristem function.
Conclusion
Kellogg (Kellogg, 2000) has
proposed a generalized model for inflorescence development. The model states
that meristems can produce either more meristems or a set of determinate
floral organs on their flanks. In a reiterative manner, any subsequent
meristems must make the same developmental decision. This simple model can
explain the wide variety of inflorescence forms found in plants. If our
results can be generalized, then progress through the various orders of
meristem identity will depend on the dosage of ids1 and
rgo1-like genes and the concentration of their products. Meristem
identity is established by varying a threshold, with different thresholds for
different identities. Duplication or loss of these genes would explain
variations in the number of iterations of this basic process, and thus could
be responsible for the great diversity in inflorescence forms.
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ACKNOWLEDGMENTS |
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