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Shoot meristem formation and maintenance
Michael Lenhard and Thomas Laux*
The shoot apical meristem of higher plants is a self-maintaining
stem cell system which gives rise to the entire aboveground
part of a plant. In the past year, genetic and molecular studies
have provided increasing insight into the processes of shoot
meristem formation and maintenance, as well as into the
relation between the apical meristem and its products.
Addresses
Lehrstuhl für Entwicklungsgenetik, Universität Tübingen, Auf der
Morgenstelle 1, D-72076 Tübingen, Federal Republic of Germany
*e-mail: [email protected]
Current Opinion in Plant Biology 1999, 2:44–50
http://biomednet.com/elecref/1369526600200044
© Elsevier Science Ltd ISSN 1369-5266
Abbreviations
CZ
central zone
KAPP
kinase-associated protein phosphatase
PZ
peripheral zone
Introduction
One of the fundamental features of postembryonic development of higher plants is the reiterative formation of new
organs by the shoot meristem [1]. The shoot meristem is
formed during embryogenesis and subsequently gives rise
to internodes, leaves, axillery shoot meristems and flowers
(Figure 1). The bases for this activity are the abilities of
the shoot meristem to: firstly, maintain a set of pluripotent
stem cells in a central zone (CZ); secondly, to initiate
organs from the progeny of the stem cells in a peripheral
zone (PZ); and thirdly, to balance these two processes
(reviewed in [2–5]). In the following review, we will discuss papers of the past year with regard to four aspects: the
organization of the shoot meristem; its formation during
embryogenesis; the maintenance of an active shoot meristem in postembryonic growth; and finally the inter-relation
between the shoot meristem and its products.
Organization of the shoot meristem
As stated above, the shoot meristem contains two cell populations with distinct behaviors, that is, those in the center
which remain pluripotent and those in the periphery which
contribute to organ formation and eventually differentiate.
Thus, cell behavior must be co-ordinated within one population and distinguished from that of the other
population, implying regulated intercellular communication. To address the question of whether specific
cytoplasmic coupling is involved in this process, Rinne and
van Schoot microinjected fluorescent dyes into single epidermal cells of the birch shoot meristem and followed the
fluorescence spread [6 ••]. Intercellular coupling was
observed within a central and a peripheral region, but not
between these two regions, except for a transient period,
possibly during the initiation of each new leaf. This sug-
gests the existence of at least two ‘communication compartments’ in the shoot meristem. Although it is not clear
whether these compartments coincide with the classical
CZ and PZ, an important conclusion of this work is that
selective symplasmic coupling of cells could provide a
mechanism to restrict the spread of potential morphogens
to separate regions in the shoot meristem.
Clonal analyses in a number of plant species, including
Arabidopsis thaliana, provided evidence that all vegetative
and generative structures of the shoot are derived from one
common set of stem cells [7–9]. These findings contradict
the ‘méristème d’attente’ concept put forward by Buvat
and colleagues some decades ago [10], which holds that
the germ cells are produced by a pool of stem cells set
aside very early in development, similar to the germ line in
animals. Recent clonal analysis in maize, however, has
taken up this concept again. The maize shoot meristem
forms a limited number of vegetative leaves before a terminal inflorescence, the tassel, is produced on the main
axis. It was shown that the upper part of the tassel is
derived from a set of cells in the shoot meristem that does
not contribute to postembryonic vegetative growth, even if
the extent of vegetative growth is artificially increased
[11••]. The author concludes that some apical cells are set
aside in the shoot meristem early in development to exclusively form tassel. This does not imply, however, that these
cells become committed to the formation of the upper tassel early in development, rather that they could simply be
located in a position where they are not recruited during
the vegetative phase of the maize shoot meristem.
Formation of the shoot meristem during
embryogenesis
The origin and development of the shoot meristem in
the embryo have been discussed controversially
(reviewed in [12,13]). On the basis of comparative morphology, it has been argued that when the shoot
meristem is first differentiated, the partitioning of the
embryo apex simultaneously defines two regions of the
shoot meristem with separate functions, the cotyledonary primordia at the periphery and the ‘apical initials
per se’ in the center, required for meristem perpetuation
[13]. Kaplan concluded that the cotyledons represent the
first products of the shoot meristem, a view which is consistent with the observation that the shoot meristem
specific gene SHOOTMERISTEMLESS (STM) [14] is
only expressed in the central cells, and not in the precursor cells of the cotyledons [13]. Recent molecular
studies of various genes implicated in embryonic shoot
meristem development, however, have demonstrated
that shoot meristem formation involves a succession of
events and that at the stage of cotyledon initiation not all
aspects are in place.
Shoot meristem formation and maintenance Lenhard and Laux
45
Figure 1
*
*
*
Late heart stage
Mature embryo
Seedling
Inflorescence meristem
Development of the Arabidopsis shoot
meristem. The shoot meristem (arrow) arises
between the outgrowing cotyledonary
primordia during embryogenesis. In the
mature embryo, the shoot meristem (arrow)
has initiated the first true leaf primordia (*). In
seedlings, the shoot meristem forms a shallow
dome and gives rise to leaves (*). The
inflorescence meristem initiates floral
meristems at its flanks. The oldest floral
meristem (at right) has already formed the first
whorl of organ primordia, the sepals (*).
Scanning electron microscopy images.
*
Floral meristems
Expression analysis of the shoot meristem gene
WUSCHEL (WUS) has indicated a considerably earlier
start of shoot meristem development than previously
thought [15••]. WUS is expressed in the four inner apical
cells of the 16-cell embryo and through several asymmetric cell divisions its expression segregates with a subset of
daughter cells which become located in the center of the
shoot meristem primordium (Figure 2). Mutant analysis
indicated that WUS is only necessary for the development
of the shoot meristem, but not for those cell lineages
derived from early WUS-expressing cells that contribute
to the cotyledons [16]. The function of WUS at very early
embryo stages, before a shoot meristem is evident, is
unclear. One possibility is that WUS functions to preserve
a pluripotent state in the cells required later in the emerging shoot meristem.
At the late globular stage, when the embryo consists of
about 100 cells, expression of the STM gene is initiated
(Figure 2, [17••]), and this step is independent of WUS
activity at earlier embryo stages [15••]. STM is expressed in
a central region of the embryo apex that may correspond to
the apical cells per se as well as in cells separating the
cotyledon primordia [17••]. In its absence these cells differentiate and fused organs are formed, suggesting that
STM may keep these cells from participating in organ formation. This interpretation is consistent with models
derived from genetic analysis [18] and with the proposed
role of the maize knotted1 (kn1) gene, a putative STM
ortholog [19]. STM appears to be functional from early
stages on, since at least the expression of another meristem
gene, UNUSUAL FLORAL ORGANS (UFO), requires STM
activity as early as the late globular stage [17••].
In the heart stage embryo, when cotyledonary primordia
are apparent, expression of a further meristem gene,
CLAVATA1 (CLV1), is initiated within the embryo apex
independently of STM activity (Figure 2 [17••]). Mutations
in CLV1 result in a progressive enlargement of the meristem during postembryonic development (see below). The
late onset of its expression in the embryo suggests, however, that CLV1 may not play a prominent role in very early
stages of shoot meristem development. By contrast, the
PRIMORDIA TIMING (PT) gene affects meristem size at
these stages. pt-mutations cause a progressive enlargement
of the shoot meristem region from the globular embryo
stage onward, but this defect regresses during later plant
development [20•]. Consistent with the temporal difference in the manifestation of the respective phenotypes,
double mutant analysis suggests that PT and CLV1 function in two independent processes.
In zll mutants [21] (allelic to pinhead [22]), the cells in
the shoot meristem primordium do not maintain STM
46
Growth and development
Figure 2
Shoot meristem formation during Arabidopsis
embryogenesis. The first indication of shoot
meristem development is the onset of
WUS expression at the 16-cell stage, long
before a shoot meristem is evident.
Subsequently, expression of STM and CLV1
is initiated. Initiation of STM expression is
independent of WUS activity and onset of
CLV1 expression is independent of STM. The
ZLL gene is necessary to maintain shoot
meristem development at later embryo
stages. Bars represent stages at which
mRNA is detected (WUS, STM, CLV1) or
phenotypic defects are observed (ZLL).
Shaded regions in embryos represent
approximate expression domains.
Shoot
meristem
Cotyledon
Shoot
Protoderm
Hypocotyl
Apical
Basal
Root
Zygote One-cell
8-cell
16-cell
Globular
Heart
Seedling
WUS
STM
CLV1
ZLL
Current Opinion in Plant Biology
expression and differentiate, indicating that ZLL is
required to maintain the meristematic cell status in the
apex of the embryo [23••]. ZLL codes for a member of a
novel gene family, including ARGONAUTE1, a gene
involved in leaf development [24••], and sequences
derived from genomic sequencing projects, e.g. in
humans and C. elegans. The recently cloned rabbit translation initiation factor eIF2C turned out to be another
member of this family [25], suggesting that ZLL and
AGO1 could be implicated in translational control. As
mutations in ZLL result in specific defects, the gene
could be involved in tissue- and/or stage-specific translational control. ZLL is expressed in the vascular precursor
cells underlying the shoot meristem primordium from
earliest embryo stages on and in the embryo apex at later
stages [23••]. In which cells its expression is needed for
meristem development remains to be determined.
Interestingly, the requirement for ZLL in primary shoot
meristem development is only transient. Once the first
true leaf primordia are present, the shoot meristem
appears to be able to self-maintain independently of ZLL
activity [23••].
Thus, from these studies it follows that shoot meristem
formation is a prolonged, dynamic process which begins
during early embryo pattern formation. Also, whereas some
aspects of the formation of cotyledons are strikingly similar to that of leaves, important differences should not be
overseen, such as that not all molecular mechanisms of the
postembryonic shoot meristem are in place when the
cotyledons are initiated.
The shoot meristem in
postembryonic development
Clonal analysis indicated that stem cells of the shoot meristem are not permanent but are instructed by positional
information as ‘temporary occupants of a permanent office’
as Newman elegantly put it [26], raising the question of
how the identity of these cells is specified. In wus mutants,
stem cells appear to be mis-specified and to have differentiated [16]. In contrast to stm mutations, however, cells in
wus apices are not recruited into organs, suggesting that
WUS positively regulates cell fate rather than preventing
organ formation. WUS was cloned and shown to encode a
putative homeodomain protein of a novel subtype [15••].
WUS is expressed in a small group of cells in the meristem
center underneath the presumed position of the stem cells.
A conceiveable model derived from these data is that
WUS-expressing cells act as an organizing center conferring stem cell fate to overlying neighbors (Figure 3). This
model implies similarities in the organization of shoot and
root meristems, since in the root meristem the stem cells
also appear to be maintained by signaling from a central
organizing cell group, the quiescent center [27 ••]
(Figure 4). Similarities between shoot and root meristem
regulation have also been concluded from the study of the
Defective embryo and meristems (Dem) gene of tomato which
affects cell divisions in both meristems [28•]. Because
organ primordia are also affected in the dem mutant, however, the significance of Dem for meristem development
still needs to be determined.
Once the progeny of the stem cells have left the center of
the shoot meristem, they are recruited into organogenesis
and eventually differentiate. In Arabidopsis, this process is
promoted by the CLV and MGOUN (MGO) genes.
CLV1, encoding a putative receptor kinase, and CLV3,
which interacts genetically with CLV1, are likely to be components of a common signaling pathway, with mutations in
either gene causing a progressive increase in meristem size
[29,30]. Previously two mutually not exclusive models for
their role had been proposed: CLV signaling could promote the entry of cells into organogenesis and/or
Shoot meristem formation and maintenance Lenhard and Laux
negatively regulate the proliferation of meristem cells
[29,31]. The latter alternative has recently been refuted by
Laufs et al. These authors find that in clv3 meristems the
size of the central region of low mitotic activity is increased
and the cells in this region divide even less frequently than
in wild type [32••]. Thus, it appears likely that the CLV
pathway primarily enhances the rate of a differentiation
step during organ formation (Figure 3).
To gain first insight into how CLV signaling is processed
within the cell, two laboratories examined the biochemical properties of CLV1 and its interaction with the
kinase-associated protein phosphatase KAPP [33••,34••].
The CLV1 intracellular domain can autophosphorylate
and appears to oligomerize with and transphosphorylate
other CLV1 molecules. KAPP was found to be able to
dephosphorylate CLV1 in vitro and the results of transgenic studies point at a role of KAPP as a negative
regulator of CLV1 signaling in planta. As KAPP interacts
with various receptor-like kinases similar to CLV1 [35],
however, it may be a more general modulator of different
receptor kinase pathways.
Mutations in the CLV2 gene result in an increase of shoot
meristem height and an extra whorl of organs in flowers,
similar to weak clv1 and clv3 alleles [36•]. Organ development is also affected in clv2, however; for example the
pedicel length of flowers is increased compared to wild
type. clv1 and clv3 are epistatic to clv2 with respect to floral organ number, but additive with respect to pedicel
length. This suggests that CLV2 acts in the same pathway
as CLV1/3 to regulate meristem activity, whereas it seems
to affect further organ development independently. The
initiation of lateral organs by the shoot meristem also
requires the MGOUN (MGO) genes. mgo1 and mgo2 result
in a reduction of the number of leaves and floral organs,
larger meristems and fasciation [37•]. In contrast to clv3
(see above), mgo2 shoot meristems accumulate cells in
the PZ [32••]. As clv3 mgo double mutants are additive,
the genes appear to be involved in different steps of
organ formation: whereas CLV3 affects the rate of the
transition of cells from CZ to PZ, the MGO genes may
affect the partitioning of PZ cells into organ
primordia (Figure 3).
The maize homeobox gene kn1 appears to counteract differentiation of meristem cells and organ formation [19].
Recent overexpression studies, however, are consistent
with differences in the action of kn1 as well as in the developmental plasticity of leaf cells in monocotyledonous and
dicotyledonous plants. Whereas overexpression of kn1 in
tobacco produced ectopic meristems on leaves [38], no
such effect has been observed in studies with transgenic
maize [39•] and barley [40•]. In barley, the only effect of
ectopic expression of maize kn1 was the formation of additional florets on the awn of primary spikelets, suggesting
that kn1 might have induced inflorescence meristem fate
in cells of the normally determinate awn [40•].
47
Figure 3
STM/kN1
CLV
MGO
sc
p
(PHAN)
CZ
PZ
p
WUS
PZ
RZ
Current Opinion in Plant Biology
Genes involved in the regulation of shoot meristem activity. WUS
expression in the basal part of the central zone (CZ) affects the state
of the overlying stem cells. The CLV signaling pathway, including
CLV1and CLV3, promotes a differentiation step reflected by the
transition of cells from the CZ to the PZ. This step is counteracted by
STM in Arabidopsis, and the maize kn1 possibly plays a similar role.
The MGO genes promote formation of organ primordia (p) from cells
of the PZ. Expression of the PHAN gene in leaf primordia is required
for maintenance of shoot meristem activity. The figure combines data
from Arabidopsis (WUS, STM, CLV, MGO), Antirrhinum (PHAN) and
maize (kn). See text for details. sc, stem cells; RZ, rib zone.
In contrast to Arabidopsis, in some species the shoot meristem only forms an intrinsically limited number of
structures. How is the meristem program terminated in
such species? One example is the maize spikelet meristem
which gives rise to two floral meristems only. Mutations in
the indeterminate spikelet1 (ids1) gene abolish spikelet
meristem determinacy such that it gives rise to additional
floral meristems, indicating a role of ids1 in meristem termination. Chuck et al. showed that ids1 codes for a gene
related to APETALA2, which is required in Arabidopsis
flower development [41••]. Although the precise regulatory mechanism for spikelet meristem determinacy is
unknown, one attractive hypothesis is that ids acts as a negative regulator of those factors necessary for maintaining
indeterminacy, such as kn1.
The relationship between the shoot meristem
and leaves
Is the shoot meristem autonomous and independent from
its products, or is there a mutual interaction between shoot
meristem and organs? The latter view is supported by classical studies demonstrating that continued activity of the
shoot meristem depends on hormonal supply from young
leaf primordia [42]. Recent studies on mutations primarily
affecting leaf development point into the same direction.
The phantastica (phan) mutation of Antirrhinum partly disrupts dorsoventrality of lateral organs, with ventral (abaxial,
lower leaf side) tissue present on the upper side of leaves,
and blocks the outgrowth of leaf primordia [43••]. The gene
48
Growth and development
Figure 4
p
PZ
CZ
PZ
WUS
p
lrc
lrc
QC
RZ
crc
Current Opinion in Plant Biology
codes for a putative MYB transcription factor and is
expressed uniformly in young primordia of leaves and floral
organs. When the formation of leaves is disrupted in conditional phan alleles, shoot development discontinues,
indicating that leaf development is required for shoot meristem activity (Figure 3). The dominant phabulosa mutation of
Arabidopsis affects leaf development in a manner opposite to
that of phantastica, causing a transformation of ventral into
dorsal (adaxial, upper leaf side) leaf tissue to varying degrees
[44••]. Interestingly, in such dorsalized leaves, ectopic
meristems are formed opposite to the leaf axils, at the lower
side of the petiole base, indicating a correlation between
dorsal leaf fate and the development of axillary shoot meristems and as the authors put it, “a cyclical model for shoot
development: the shoot meristem makes leaves which in
turn are responsible for generating new shoot meristems”.
Conclusions
The literature reviewed provides new insights into the
mechanisms underlying the formation and maintenance of
the shoot meristem. Several interesting new mutants have
been identified and several genes have been isolated that
will considerably add to our understanding of these processes. Nevertheless, despite extensive screens by several
laboratories, the number of regulators specific for shoot
meristem development that have been identified appears
small. Finding further novel components may require specific screening strategies, as exemplified by the isolation of
suppressors of the clv1 mutation [45]. With several important genes cloned which are involved in the regulation of
meristem cell fate and organ formation, the important questions can now be addressed of what is their cellular function,
which genes and processes are their targets and how are
their functions integrated in an active shoot meristem.
Acknowledgements
We gratefully acknowledge support from grants by the Deutsche
Forschungsgemeinschaft to Thomas Laux and by a stipend from the
Boehringer Ingelheim Fond to Michael Lenhard. We thank the member of the
Laux laboratory for helpful comments on the manuscript. We apologize to
those colleagues working in the field whose work was not mentioned due to
space constraints.
Model for the maintenance of stem cells in
shoot and root meristems. Analysis of the
WUS gene and cell ablation studies allow for
a model in which maintaining the state of stem
cells (lightly shaded) in shoot and root
meristems requires information (white arrows)
from neighboring cell groups (darkly shaded),
the WUS expressing cells and the quiescent
center (QC), respectively. Progeny of the
stem cells in the surrouding regions (white
areas) undergo differentiation, presumably
integrating information (shaded arrows) from
more mature tissues (for review see [2]). CZ,
central zone; crc, central root cap; lrc, lateral
root cap; p, leaf primordia; PZ, peripheral
zone; RZ, rib zone.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
1.
Steeves TA, Sussex IM: Patterns in Plant Development. Cambridge:
Cambridge University Press; 1989.
2.
Laux T, Mayer KFX: Cell fate regulation in the shoot meristem. Sem
Cell Dev Biol 1998, 9:195-200.
3.
Barlow PW: The concept of the stem cell in the context of plant
growth and development. In Stem Cells and Tissue Homeostasis.
Edited by Lord BI, Potten CS, Cole RJ. Cambridge: Cambridge
University Press; 1978:87-113.
4.
Meyerowitz EM: Genetic control of cell division patterns in
developing plants. Cell 1997, 88:299-308.
5.
Clark SE: Organ formation at the vegetative shoot meristem.
Plant Cell 1997, 9:1067-1076.
6.
••
Rinne PL, van der Schoot C: Symplasmic fields in the tunica of the
shoot apical meristem coordinate morphogenetic events.
Development 1998, 125:1477-1485.
This paper suggests the existence of symplasmic isolation between a central and peripheral zone in the epidermis of the birch shoot meristem, which
is only broken briefly with the initiation of each new leaf. The far-reaching
potential of such ‘communication compartments’ for the regulated
exchange of potential morphogens and for the segregation of cell fates in
the apex is discussed.
7.
Tilney-Basset RAE: Plant Chimeras. Baltimore: Edward Arnold; 1986.
8.
Irish VF, Sussex IM: A fate map of the Arabidopsis embryonic shoot
apical meristem. Development 1992, 115:745-753.
9.
Furner IJ, Pumfrey JE: Cell fate in the shoot apical meristem of
Arabidopsis thaliana. Development 1992, 115:755-764.
10. Buvat R: Structure, évolution et functionnement du méristème
apical de quelques dicotylédones. Annu Sci Nat Bot 1952,
13:199-300. [Title translation: Structure, evolution and function of
apical meristems of some dicotyledons.]
11. Irish EE: Additional vegetative growth in maize reflects expansion
•• of fates in preexisting tissue, not additional divisions by apical
initials. Dev Biol 1998, 197:198-204.
This paper reports a clonal analysis of extra vegetative leaves formed from
determinate maize meristems after explantation and in vitro culture. As these
leaves are found not to be related to the apical cells which form the generative structures of the tassel, the author suggests that in contrast to the situation in many other plant species the reproductive organs are formed by
cells in the maize apex that were set aside early in development.
12. Laux T, Jürgens G: Embryogenesis: A new start in life. Plant Cell
1997, 9:989-1000.
13. Kaplan DR, Cooke TJ: Fundamental concepts in the
embryogenesis of dicotyledons: a morphological interpretation of
embryo mutants. Plant Cell 1997, 9:1903-1919.
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14. Long JA, Moan EI, Medford JI, Barton MK: A member of the
KNOTTED class of homeodomain proteins encoded by the STM
gene of Arabidopsis. Nature 1996, 379:66-69.
15. Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T:
•• Role of WUSCHEL in regulating stem cell fate in the Arabidopsis
shoot meristem. Cell 1998, in press.
The WUSCHEL gene, required for the specification of stem cells in the
Arabidopsis shoot meristem, codes for a novel homeodomain protein. Its
expression pattern suggests that stem cells in the shoot meristem are specified by an underlying cell group which is established as early as in the 16cell embryo and becomes localized to its prospective domain of function by
asymmetric cell divisions. These findings suggest profound similarities
between different stem cell systems in animals and plants.
16. Laux T, Mayer KFX, Berger J, Jürgens G: The WUSCHEL gene is
required for shoot and floral meristem integrity in Arabidopsis.
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17. Long JA, Barton MK: The development of apical embryonic pattern
•• in Arabidopsis. Development 1998, 125:3027-3035.
An excellent analysis of the molecular patterns in the embryonic shoot meristem primordium by extensive in situ hybridizations for the STM, UFO, ANT
and CLV1 genes. The complex role of STM in the establishment of this early
pattern is addressed.
18. Endrizzi K, Moussian B, Haecker A, Levin J, Laux T: The SHOOT
MERISTEMLESS gene is required for maintenance of
undifferentiated cells in Arabidopsis shoot and floral meristems
and acts at a different regulatory level than the meristem genes
WUSCHEL and ZWILLE. Plant J 1996, 10:967-979.
19. Vollbrecht E, Veit B, Sinha N, Hake S: The developmental gene
Knotted-1 is a member of a maize homeobox gene family. Nature
1991, 350:241-243.
20. Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, van Went J,
•
Koornneef M, de Vries SC: Somatic embryogenesis in Arabidopsis
thaliana is facilitated by mutations in genes repressing
meristematic cell divisions. Genetics 1998, 149:549-563.
A detailed study of the effects of the pt, clv1 and clv3 mutations on
somatic embryogenesis is reported, as well as an analysis of the genetic
interactions between these genes, indicating a temporal succession in
their functions.
21. Jürgens G, Torres-Ruiz RA, Laux T, Mayer U, Berleth T: Early events
in apical-basal pattern formation in Arabidopsis. In Plant Molecular
Biology: Molecular-Genetic Analysis of Plant Development and
Metabolism. Edited by Coruzzi G, Puigdomènech P. Berlin: SpringerVerlag; 1994: 95-103.
22. McConnell JR, Barton MK: Effects of mutations in the PINHEAD
gene of Arabidopsis on the formation of shoot apical meristems.
Dev Genet 1995, 16:358-366.
23. Moussian B, Schoof H, Haecker A, Jürgens G, Laux T: Role of the
•• ZWILLE gene in the regulation of central shoot meristem cell fate
during Arabidopsis embryogenesis. EMBO J 1998, 17:1799-1809.
The ZLL gene is specifically required to maintain a meristematic cell state in
the shoot meristem primordium. It is expressed from early embryo stages on
in the vascular precursor cells and also in the embryonic apex in bent-cotyledon stage. Together with AGO1 and several animal sequences, it defines a
novel protein family.
24. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C:
•• AGO1 defines a novel locus of Arabidopsis controlling leaf
development. EMBO J 1998, 17:170-180.
This paper describes the cloning and functional analysis of the ARGONAUTE1 gene that is required for leaf development in Arabidopsis.
Together with ZLL and several animal sequences, AGO1 defines a novel
protein family.
25. Zou C, Zhang Z, Wu S, Osterman JC: Molecular cloning and
characterization of a rabbit eIF2C protein. Gene 1998,
211:187-194.
26. Newman IV: Patterns in the meristems of vascular plants. III.
Pursuing the patterns where no cell is a permanent cell. J Linn
Soc Bot 1965, 59:185-214.
27.
••
van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B:
Short-range control of cell differentiation in the Arabidopsis root
meristem. Nature 1997, 390:287-289.
This important paper describes the effects of cell ablation in the quiescent
center of the root meristem on the neighboring stem cells. The results indicate that short range signaling from the quiescent center to its immediate
neighbors prevents their differentiation.
49
28. Keddie JS, Carroll BJ, Thomas CM, Reyes ME, Klimyuk V, Holtan H,
•
Gruissem W, Jones JD: Transposon tagging of the Defective
embryo and meristems gene of tomato. Plant Cell 1998,
10:877-888.
The phenotype of the tomato dem mutant is described which exhibits a
severly disturbed organization and development of both shoot and root
meristems. Dem, encoding a novel protein, is not specific for meristems,
but is expressed in all tissues with organized cell division. However, the
mRNA is notably absent from callus, suggesting a role in the coordination
of cell division.
29. Clark SE, Williams RW, Meyerowitz EM: The CLAVATA1 gene
encodes a putative receptor-kinase that controls shoot and floral
meristem size in Arabidopsis. Cell 1997, 89:575-585.
30. Clark SE, Running MP, Meyerowitz EM: CLAVATA3 is a specific
regulator of shoot and floral meristem development affecting the
same processes as CLAVATA1. Development 1995,
121:2057-2067.
31. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM: The CLAVATA and
SHOOT MERISTEMLESS loci competitively regulate meristem
activity in Arabidopsis. Development 1996, 122:1565-1575.
32. Laufs P, Grandjean O, Jonak C, Kieu K, Traas J: Cellular parameters
•• of the shoot apical meristem in Arabidopsis. Plant Cell 1998,
10:1375-1390.
An excellent description of the morphology and distribution of mitoses in the
Arabidopsis shoot apex based on confocal laser scanning microscopy is
reported. The results obtained for the wild type are then used as a framework
for analyzing the defects in clv3 and mgo2 apices in greater detail, allowing
important novel conclusions about the functions of these genes.
33. Stone JM, Trotochaud AE, Walker JC, Clark SE: Control of meristem
•• development by CLAVATA1 receptor kinase and
kinase-associated protein phosphatase interactions. Plant Physiol
1998, 117:1217-1225.
Biochemical analysis demonstrates protein kinase activity for CLV1 and
the physical interaction of phosphorylated CLV1 with KAPP. KAPP probably functions as a negative regulator of CLV signaling, since reducing
KAPP mRNA can rescue the clv1 phenotype in a dose-dependent manner.
These findings provide important insights into the intracellular processing
of CLV1 signals.
34. Williams RW, Wilson JM, Meyerowitz EM: A possible role for kinase
•• associated protein phosphatase in the Arabidopsis CLAVATA1
signaling pathway. Proc Natl Acad Sci USA 1997,
94:10467-10472.
The powerful biochemical analysis reported in this paper provides evidence
that CLV1 functions as a protein kinase and that this activity is important for
CLV1 function. CLV1 associates with and is dephosphorylated by KAPP. A
functional significance of this interaction is suggested by the observation
that overexpression of KAPP produced a weak clv1 phenotype, implying a
negative regulation of CLV signaling by KAPP.
35. Becraft PW: Receptor kinases in plant development. Trends Plant
Sci 1998, 3:384-388.
36. Kayes JM, Clark SE: CLAVATA2, a regulator of meristem and organ
•
development in Arabidopsis. Development 1998, 125:3843-3851.
A detailed phenotypical and genetic characterization identifies the CLV2
gene as important regulator of meristem activity. clv2 mutants resemble
weak clv1 and clv3 alleles. CLV2 shows complex genetic interactions with
other meristem regulatory genes, precluding straightforward interpretations.
37.
•
Laufs P, Dockx J, Kronenberger J, Traas J: MGOUN1 and MGOUN2:
two genes required for primordium initiation at the shoot apical
and floral meristems in Arabidopsis thaliana. Development 1998,
125:1253-1260.
The mgo mutations cause a phenotype similar to that of clv with a severe
enlargement of the shoot meristem. Interestingly, the underlying defects
appear to be distinct, with MGO apparently acting in the PZ to partition cells
into organ primordia.
38. Sinha NR, Williams RE, Hake S: Overexpression of the maize
homeobox gene, KNOTTED-1, causes a switch from determinate
to indeterminate cell fates. Genes Dev. 1993, 7:787-795.
39. Zhang S, Williams-Carrier R, Jackson D, Lemaux PG: Expression of
•
CDC2Zm and KNOTTED1 during in vitro axillary shoot meristem
proliferation and adventitious shoot meristem formation in maize
(Zea mays L.) and barley (Hordeum vulgare L.). Planta 1998,
204:542-549.
Examining the expression patterns of CDC2Zm and knotted1 during the formation of adventitious shoot meristems in vitro, the authors find no difference
to the expression patterns observed in planta. kn1 overexpressing maize
plants show no signs of ectopic meristem formation.
50
Growth and development
40. Williams-Carrier RE, Lie YS, Hake S, Lemaux PG: Ectopic
•
expression of the maize kn1 gene phenocopies the Hooded
mutant of barley. Development 1997, 124:3737-3745.
Constitutive expression of maize kn1 in barley results in ectopic flowers, a
defect similar to that of the Hooded mutation of barley. Notably, no ectopic
shoot meristem formation is observed, as it has been reported in overexpression studies in tobacco.
41. Chuck G, Meeley RB, Hake S: The control of maize spikelet
•• meristem fate by the APETALA2-like gene indeterminate
spikelet1. Genes Dev 1998, 12:1145-1154.
This paper describes the cloning and analysis of the indeterminate spikelet1
gene, that is required for determinacy of the first two branches (spikelets) of
the maize inflorescence. The possible implications of ids1 for inflorescence
architecture in other grass species are discussed.
42. Shabde M, Murashige T: Hormonal requirements of excised
Dianthus caryophyllus L. shoot apical meristem in vitro. Am J
Botany 1977, 64:443-448.
43. Waites R, Selvadurai HR, Oliver IR, Hudson A: The PHANTASTICA
•• gene encodes a MYB transcription factor involved in growth and
dorsoventrality of lateral organs in Antirrhinum. Cell 1998,
93:779-789.
The PHAN gene, required for leaf dorsoventrality, was cloned and shown to
encode a putative MYB transcription factor. Its expression pattern and the
mutant phenotype suggest a role in the specification of leaf identity. PHAN
is necessary for sustained meristem activity in a non-cell-autonomous manner, reinforcing the observation that shoot meristem activity is affected by
signaling from leaves.
44. McConnell JR, Barton MK: Leaf polarity and meristem formation in
•• Arabidopsis. Development 1998, 125:2935-2942.
The dominant phb-d mutation which disrupts dorsoventrality of lateral organs
leads to the ectopic formation of axillary meristems on the lower side of leaf
petioles. This interesting effect suggests that dorsal (adaxial) leaf fate promotes the formation of axillary shoot meristems.
45. Pogany JA, Simon EJ, B KR, De Guzman BM, Yu LP, Trotchaud AE,
Clark SE: Identifying novel regulators of shoot meristem
development. J Plant Res 1998, 111:307-313.