Download Axioms and axes in leaf formation? Andrew Hudson

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Axioms and axes in leaf formation?
Andrew Hudson
Formation of leaves and floral organs involves down-regulation
of meristem-specific homeobox genes, and de novo expression
of genes for organ identity, growth and patterning. Genes
required for all these aspects of organ formation have been
identified. The challenge now is to establish how they interact
to direct organogenesis.
Addresses
Division of Biological Sciences, Institute of Cell and Molecular Biology,
The University of Edinburgh, Daniel Rutherford Building, King’s
Buildings, Mayfield Road, Edinburgh EH9 3JH, UK;
e-mail: [email protected]
Current Opinion in Plant Biology 1999, 2:56–60
http://biomednet.com/elecref/1369526600200056
© Elsevier Science Ltd ISSN 1369-5266
Abbreviation
SAM
shoot apical meristem
Introduction
Leaves, and related floral organs, arise from groups of initial cells within the peripheral zone of the shoot apical
meristem (SAM) or floral meristem (Figure 1). Leaf initials, numbering less than 50 in Arabidopsis [1,2] and over
200 in maize [3], follow a different developmental fate to
SAM cells or initials of the stem and form two new axes of
asymmetry — proximodistal and dorsoventral. Here, I
review recent evidence for the genetic control of organ, as
opposed to meristem, identity and for specification and
elaboration of proximodistal and dorsoventral organ axes.
Specification of organ identity
Meristematic cells at the shoot apex are characterised by
expression of knox genes (a family of homeobox genes
including the knotted1 gene of maize) and, conversely, loss
of knox gene expression has provided a faithful marker for
organ fate. The Arabidopsis knox gene SHOOT MERISTEMLESS (STM) [4] is required for the formation and
maintenance of a functional SAM [4–7], consistent with a
role in specifying meristem identity. STM transcripts are
detectable in SAM cells, but not in those which will form
the next leaf primordium (P0 initials) [4], suggesting that
the P0 cells have lost meristem identity and assumed that
of organ, although they have yet to show morphological
signs of organ formation.
Two genes, AINTEGUMENTA (ANT) and PHANTASTICA
(PHAN), that might specify organ identity have been identified in Arabidopsis and Antirrhinum, respectively. ANT
encodes a putative transcription factor of the AP2-like family [8,9,10] and is expressed in the P0 initials and older
primordia of leaves and floral organs. ant mutants produce
fewer floral organs suggesting the gene is required for
organ identity or initiation. Mutations in the related floral
homeotic gene AP2, which is required to specify the identity of sepals and petals in the outer two whorls of the
flower, also cause similar reductions in floral organ number
[10]. This has been attributed to ectopic expression of a
second homeotic gene, AGAMOUS (AG) [11], which is normally confined to the inner two floral whorls, because loss
of AG activity restores normal organ number to ap2
mutants. Ectopic AG expression is also partly responsible
for the homeotic effects on organ identity in the outer two
whorls of ap2 mutants. As ant mutants show no floral
homeotic phenotypes characteristic of ectopic AG expression, ANT and AP2 functions appear unlikely to overlap in
repressing AG. ant:ap2 double mutants, however, show a
more severe organ loss phenotype than either single
mutant [9] suggesting that ANT and AP2 do share roles in
organ formation. Although ANT is expressed in leaf and
cotyledon initials, it is not required for normal leaf development, presumably because of the activity of other,
independently expressed genes.
The PHAN gene of Antirrhinum encodes a MYB-like transcription factor [12••] and its expression is confined to
organs from before primordium initiation, in a pattern reciprocal to that of an Antirrhinum STM gene. Because the
phan mutant phenotype is conditional on temperature, it
was possible to demonstrate a requirement for PHAN in
initiation of all lateral organs (i.e. elaboration of the proximodistal axis) and for dorsoventral asymmetry in leaves
and petals. These findings suggest that the primary role of
PHAN is to specify lateral organ identity and that elaboration of proximodistal and dorsoventral axes is a
consequence of this. It also appears that organ initials or
primordia produce a PHAN-dependant signal, of unknown
identity, required to maintain SAM activity because phan
mutant meristems become quiescent at restrictive temperatures. A similar pleiotropic effect on organ formation and
SAM activity results from mutations in the REVOLUTA
and ARRESTED DEVELOPMENT genes of Arabidopsis
[13,14], supporting the view that SAM function and organ
formation are inter-dependent. This contrasts with the
phenotypes of mgoun (mgo1 or mgo2) mutants of
Arabidopsis, however, which produce fewer leaves and floral organs [15] and accumulate more cells in the peripheral
zone of the SAM from which organs would normally form
[16•] — suggesting that MGO1 and MGO2 are required for
organ fate but not meristem activity. One explanation for
the difference in the effects of these mutations would be
that the MGO genes are required only for organ formation
and act downstream of genes like PHAN that specify organ
fate and are needed for signalling. Isolation of the MGO
loci should allow this to be tested.
It remains to be determined whether organ-specific genes
are required to repress meristem-specific knox genes (or
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Axioms and axes in leaf formation? Hudson
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Figure 1
P1
P1
P1
Dorsal
PO
P1
PO
P1
P2
PO
Ventral
Lateral
PO
P2
P2
P3
P2
P3
Distal
Proximal
Current Opinion in Plant Biology
(Formation of leaves at the shoot apical meristem. Leaves develop from
groups of initial cells within the flanks of the shoot apical meristem
(SAM). These form a primordium growing away from the SAM,
elaborating its proximodistal axis. The primordia of monocots are
usually flattened at emergence, those of dicots grow laterally to
become flattened in a plane perpendicular to the dorsoventral axis of
the leaf soon after emergence.
vice versa), or whether the two classes of genes respond
independently to an existing pre-pattern in the apex.
Because such a pre-pattern would be a major determinant
of organ position (phyllotaxy), its nature has been the
source of much speculation (e.g. [17,18]). Indirect evidence suggests that meristem-specific knox genes might
interact with genes specifying organ identity. STM appears
necessary to prevent organ fate in the SAM because
reduced activity in weak stm mutants or in zwille (zll)
mutants unable to maintain STM expression leads to formation of ectopic leaves ([6,7,19]; zll is allelic to pinhead
[20]). Loss-of-function mutations in the STM-like knotted1
(kn1) gene of maize have less severe effects (presumably
due to redundancy of kn1) but lead to formation of ectopic
leaves and carpels [21•], suggesting a similar role in
repressing organ formation. Down-regulation of STM, however, is also seen in initials that will subsequently form
floral meristems indicating that it is not sufficient for organ
identity in all contexts (see [15] for example). Conversely,
PHAN might be sufficient to repress STM (their expression
domains are complementary), although the same cannot be
true of ANT which is expressed with STM in some cells of
the embryo [22•], and probably also in vascular initials in
the stem.
Figure 2
Ectopic knox gene expression alters proximodistal pattern in leaves.
(a) The wild-type maize leaf consists of sheath tissue (s) at the base,
proximal to the stem, and blade tissue (b) distally. The ligule (lg) and
auricle (a) form at the blade/sheath boundary. Ectopic expression of
one of several knox genes shift the blade/sheath boundary distally,
producing a mutant phenotype similar to that conditioned by the
dominant Gnarley1-R mutant shown in (b). (c) The petiole, stipules
and axillary meristem develop proximally in the wild-type Arabidopsis
leaf. Ectopic expression of the knox gene KNAT1 from the constitutive
35S promoter causes lobing of leaves and these proximal identities to
be expressed more distally at the base of the lobes (d). Pictures kindly
provided by Sarah Hake.
Further evidence for organ-specific repression of the knox
genes kn1, rough sheath1 (rs1) and liguleless3 (lg3) is provided by the rough sheath2 (rs2) mutant of maize which
ectopically accumulates RS1 protein in leaf primordia from
the earliest stage after initiation (P1), and kn1, rs1 and lg3
transcripts in older leaves [23••]. Although rs2 is necessary
for repression of knox expression in leaf primordia, it does
not appear to be required for setting the early expression
pattern of RS1 or KN1, because these proteins are reduced
as normal in P0 leaf initials of strong rs2 mutants. These
findings add to a growing body of evidence suggesting that
regulation of knox genes is complex and may occur at the
levels of both transcription and RNA stability [24,25••].
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Growth and development
Regulation also appears differs between parts of the maize
leaf. In wild-type initials, Kn1 mRNA and protein is first
lost from P0 initial cells that will form the centre of the
leaf, and subsequently from cells that will form the leaf
margins. Down-regulation of Kn1 in marginal initials
requires the activity of narrow sheath and leaf bladeless1
genes [26,27•], whereas that in the central initials does not.
Recent isolation of the maize terminal ear1 (te1) gene of
maize has identified an additional class of gene with a role
in leaf initiation [28•]. Loss of te1 function causes increased
leaf production at ectopic positions, suggesting te1 is
required to repress leaf identity. te1 mRNA is confined to
cells opposite P0 initials, consistent with this role, although
these cells will later assume identities as marginal leaf initials and therefore te1 is not sufficient to prevent leaf
identity. TE1 protein contains RNA binding motifs suggesting a role in post-transcriptional gene regulation.
Formation of the proximodistal organ axis
The first morphological sign of proximodistal axis formation
is initiation of primordium growing away from the SAM and
stem axis and, therefore, the proximodistal axis appears to
be specified in organ initials within the meristem. One consequence of this is that mutations which prevent
specification or early elaboration of the proximodistal axis
may disrupt initiation of primordia and, therefore, be difficult to distinguish phenotypically from those affecting organ
identity. Gain-of-function phenotypes, however, implicate
knox genes in proximodistal axis formation.
The maize leaf consists of sheath tissue proximal to the
stem and blade tissue distally (Figure 2). This pattern is
specified early in development because the blade/sheath
boundary, at which the auricle and ligule will form, is apparent in the second youngest primordium (P2) [29].
Gain-of-function mutations in a number of knox genes
including kn1 and rs1 [30,31] cause expression in leaves
from stage P1 and result in distal cells developing with more
proximal identities (e.g. sheath in place of blade, Figure 2).
Freeling and co-workers interpret this as evidence that positional values along the proximal–distal axis reflect the
developmental age of cells and that the competency of cells
to make different tissues changes as they mature. Proximal
cells of the wild-type leaf, therefore, assume different fates
to distal ones because they mature much later. As knox gene
expression is usually confined to the most immature stage
of development — that of SAM cells — ectopic expression
in leaves is proposed to slow maturation and result in acquisition of more proximal fates [32].
Analysis of marked clones of cells carrying a ligueless3 (Lg3)
gain-of-function mutation (which, like similar mutations in
knl and rsl, is reported to result in ectopic expression in
leaves) has been used to support this hypothesis [33•]. If
lg3 expression were responsible for specifying positional
information, mutant clones might have been expected to
express a more distal identity uniformly; however, this was
not observed. Clones retain proximodistal pattern
(although this is displaced distally relative to surrounding
wild-type tissue), suggesting that lg3 expression allows
cells to respond to positional information, and consistent
with reduction, rather than prevention of maturation.
Large mutant clones, established early in development,
also showed more severe distal to proximal conversions
than smaller clones established later, as would be expected to result from longer exposure to a maturation inhibitor;
however, the alternative view — that knox genes are
involved in specifying positional information — cannot be
ruled out. Knox genes might be needed for signals that
specify proximal identity in organ initials closest to their
domain of expression in the wild-type SAM and ectopic
expression could signal proximal cell fate at more distal
positions in the leaf. The incomplete loss of proximodistal
pattern in Lg3-expressing clones could reflect the requirement for other signals in proximodistal patterning, which
remains unaffected in Lg3 mutant cells. This view, in
which knox genes are responsible for proximodistal signals, is consistent with the finding that Kn1, Rs1 and Lg3
gain-of-function mutations act non cell-autonomously to
influence cell fate [31,33•,34•].
Similar proximodistal shifts in leaf pattern result from
ectopic expression of the knox gene KNAT1 in the dicot
Arabidopsis [24], resulting in formation of leaf lobes with
ectopic stipules and SAMs at their bases (Figure 2).
Because stipules and axillary SAMs are normally associated with the most proximal part of the wild-type leaf, this
phenotype implies a shift of proximal identity distally and
suggests that knox genes also have a role in proximodistal
patterning of dicot leaves. Although the compound leaf of
tomato differs from that of simple-leaved plants in retaining knox gene expression in developing leaf primordia,
overexpression of knox genes in transgenic plants or spontaneous mutants also confers proximal identity (that of
branching rachis) to more distal parts, resulting in a more
highly branched structure [35,36•,37•].
Specification of the dorsoventral organ axis
Leaves are generally flattened perpendicular to their
dorsoventral axis. This flattening is usually the first morphological indication of dorsoventral polarity within
organs, although dorsoventral patterning of tissues
appears later (e.g. palisade cells differentiate dorsally and
spongy mesophyll ventrally in most dicot leaves). In
monocots such as maize, the leaf primordium is flat at
emergence, suggesting that dorsoventral polarity of initials is specified within the SAM. Even though dicot
leaves usually become flattened as primordia grow laterally after emergence, evidence from surgical studies [38]
suggests that their dorsoventral polarity is also specified
within the SAM.
In the dicot Antirrhinum, the PHAN gene is required for
dorsal cell identity in leaf and petal initials as shown by
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phan mutant organs, which can develop with only ventral
cell types. PHAN is not sufficient for this identity, however, because it is also transcribed in initials that develop
with ventral identities [12]. Because phan mutant leaves,
which are mosaics of normal dorsal and ectopic ventral tissues, form ectopic leaf blades at dorsal ventral boundaries,
interaction between dorsal and ventral initial cells was proposed to be responsible for the lateral growth which
flattens the wild-type leaf blade [39]. Mutations, such as
lam-1 in tobacco [40], that prevent lateral growth of the primordium but do not affect dorsoventrality may, therefore,
identify genes downstream of dorsoventral interactions
required for growth. In Arabidopsis, loss of ARGONAUTE1
(AGO1) activity also leads to production of narrow, ventralised organs, suggesting a similar role in dorsal cell
identity [41••]. AGO1 encodes a ZWILLE-like protein of
unknown function that is conserved in multicellular organisms and likely to be located in the cytosol. Although
AGO1, which encodes a ZLL-like protein of unknown biochemical function, is transcribed in various tissues,
overexpression caused ventral cells to assume dorsal fates,
indicating that it is sufficient for this fate.
tials, but is also required for identity of leaf margin cells
[26,44]. Because marginal cell types are formed in lb1
mutants, the relationship between ns and lb1 activities is
currently unclear.
A similar gain of dorsal identity occurs in the Phabulosa1D (Phab-1D) mutant of Arabidopsis [42••]. The Phab-1D
mutation is semi-dominant and, therefore, the mutant
phenotype might also result from ectopic ventral expression of gene sufficient for dorsal identity. In both Phab-1D
and ago mutants, ectopic lateral growth occurs at ectopic
dorsoventral boundaries, supporting the view that interaction between cells with these identities is responsible
for flattening of organs. Phab-1D mutants form axillary
meristems ventrally at the boundary between ectopic
dorsal tissues and the stem, suggesting that dorsal organ
identity might be required for normal axillary meristem
formation. In maize, recessive leaf bladeless1 (lb1) mutations result in variable loss of dorsal identity in leaves
[27•], whereas the dominant Lax midrib1-O mutation
results in gain of dorsal identity by ventral cells [43]. The
lb1 and Lxm1-O mutations, therefore, may identify genes
required and sufficient for dorsal identity, respectively.
As in dicots, ectopic leaf blades are produced by cell divisions at the boundaries between normal dorsal cells and
ectopic ventral of primordia of these mutants suggesting
that cell divisions that produce lateral growth of the
maize leaf may be regulated in the same way as those in
a dicot. Cell division in the maize primordium, however,
contributes mainly to growth in the proximodistal axis little to growth in width, as in the dicot leaf. Cells which
form the lateral margins of the maize leaf are recruited
from within the SAM and the primordium is, therefore,
flattened at emergence. Interestingly, lb1 also appears to
be needed for recruitment of lateral leaf initial cells,
because these cells neither show reduced kn1 expression
nor participate in primordium formation in lb1 mutants,
suggesting that lateral recruitment may also require dorsal cell identity. Loss of narrow sheath (ns) activity,
however, has a similar effect on recruitment of lateral ini-
References and recommended reading
Conclusions
Identification of genes that are expressed in organ initials
and required for organ formation have added a missing
piece to the picture of meristematic patterning. How
these genes might interact with each other and with
homeobox genes required for meristematic identity, however, remain to be examined. The two major axes of
organ growth and patterning appear to be specified within the meristem. Gain-of-function studies implicate
homeobox genes in patterning the proximodistal organ
axis and genes required for dorsoventral asymmetry have
also been identified. To understand how these genes
direct polar organ growth and specification of cell type
will be a major undertaking.
Acknowledgement
Thanks to Sarah Hake for providing the pictures for Figure 2.
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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•
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Confocal microscopy was used to determine mitotic indices in the
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•
leaf initiation by the terminal ear 1 gene of maize. Nature 1998,
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Suggests a novel component of meristem patterning. te1 is expressed opposite leaf initials, encodes a putative RNA binding protein and is required for
inhibition of leaf initiation.
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33. Muehlbauer GJ, Fowler JE, Freeling M: Sectors expression the
•
homeobox gene liguleless3 implicate a time-dependent
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•
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Previous work [35] showed that overexpression of the maize knox gene knotted1 increased compounding of tomato leaves. Here, the semi-dominant
Mouse-ear mutation of tomato, which conditions a similar phenotype, is
shown to correlate with misexpression of a related knox gene, (LeT6, also
known as TKn2) probably as a result of fusion to a metabolic gene.
Misexpression of LeT6 in transgenic plants has similar effects.
21. Kerstetter RA, Laudencia-Chingcuanco D, Smith LG, Hake S: Loss
•
of-function mutations in the maize homeobox gene, knotted1, are
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The first description of loss-of-function phenotypes for a maize knox gene.
Reveals a similar role to STM in Arabidopsis, although there appears to be
less requirement for kn1.
22. Long JA, Barton MK: The development of apical embryonic pattern
•
in Arabidopsis. Development 1998, 125:3027-3035.
Detailed molecular epistasis in embryos reveals that ANT expression in
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during maize leaf development. Development 1998,
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Although gain-of-function mutations giving rise to ectopic knox gene expression in leaves have been well documented, this is the first identification of a
loss-of-function mutation with a similar effect. It suggests that rough sheath2
acts as a negative regulator of several knox genes in leaves.
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ectopic meristems when overexpressed in Arabidopsis. Plant Cell
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25. 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.
Includes the surprising finding that knotted1 RNA expressed from a constitutive promoter, or Hooded RNA from a gain-of-function allele, accumulate
ectopically only in certain cell types, suggesting post-transcriptional regulation homeobox gene expression that is conserved between barley and maize
26. Scanlon MJ, Schneeberger RG, Freeling M: The maize mutant
narrow sheath fails to establish leaf margin identity in a
meristematic domain. Development 1996, 122:1683-1691.
27.
•
Timmermans MCP, Schultes NP, Jankovsky JP, Nelson T:
Leafbladeless1 is required for dorsoventrality of lateral organs in
maize. Development 1998, 125:2813-2823.
Suggests that dorsal cell identity has a similar effect on growth of maize
leaves as was proposed for dicot leaves.
37.
•
Parnis A, Cohen O, Gutfinger T, Hareven D, Zamir D, Lifschitz E:
The dominant developmental mutants of tomato, Mouse-ear and
Curl, are associated with distinct modes of abnormal transcriptional
regulation of a knotted gene. Plant Cell 1997, 9:2143-2158.
A more thorough analysis of the knox mutant described in [36•] in comparison to a second gain-of-function mutant, Curl involving the same gene.
Phenotype differences correlate with overexpression in Curl and ectopic
expression in Mouse-ear.
38. Sussex IM: Experiments on the cause of dorsoventrality in leaves.
Nature 1954, 174:351-352.
39. Waites R, Hudson A: phantastica: a gene required for dorsoventrality
of leaves in Antirrhinum majus. Development 1995 121:2143-2154.
40. McHale N: LAM-1 and FAT genes control development of the leaf
blade in Nicotiana sylvestris. Plant Cell 1993, 5:1029-1038.
41. 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.
ago1 mutants produce narrower organs with loss of some dorsal characters.
Evidence for the role of AGO1 in dorsal cell identity is strengthened by the
dorsalising effects of its overexpression.
42. McConnell JR, Barton MK: Leaf polarity and meristem formation in
•• Arabidopsis. Development 1998, 125:2935-2942.
Describes the Phab-1D mutant phenotype involving ectopic dorsal identity
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