Download Meristematic sculpting in fruit development

Journal of Experimental Botany, Vol. 60, No. 5, pp. 1493–1502, 2009
Perspectives on Plant Development Special Issue
doi:10.1093/jxb/erp031 Advance Access publication 26 February, 2009
REVIEW PAPER
Meristematic sculpting in fruit development
Thomas Girin*, Karim Sorefan* and Lars Østergaard†
Crop Genetics Department, John Innes Centre, Colney Lane, Norwich NR4 7UH, UK
Received 9 December 2008; Revised 22 January 2009; Accepted 26 January 2009
Abstract
The diversity of shape in life is astounding, and this is particularly vivid when the varied forms observed in our fruit
bowls are examined. How some of the tissues of the Arabidopsis fruit are moulded is starting to be understood,
revealing how plants may sculpt plant form by modulating the degree of meristematic properties. In this fruit the
KNOX I and BLH meristem identity genes promote medial tissue proliferation by maintaining these tissues in
a ‘quasi-meristematic’ fate. The action of these genes is opposed by ASYMMETRIC LEAVES activity that promotes
valve formation together with JAGGED/FILAMENTOUS FLOWER and FRUITFULL activities. This is reminiscent of the
function of these genes in the shoot apical meristem and in leaf development. In this review, the aim is to present the
medial tissues of the Arabidopsis fruit as a modified meristem and extrapolate our knowledge from other plant
organs to fruit development.
Key words: ASYMMETRIC LEAVES, REPLUMLESS/BELLRINGER, fruit development, gynoecium, JAG/FIL, KNOX I,
quasi-meristem, replum, SAM, tissue patterning.
Introduction
To understand the end, we must return to the beginning
and, for most plants, the beginning is the meristem. The
meristem is a tissue in which cells are actively dividing and
giving rise to relatively undifferentiated cells (Oxford
English Dictionary, Online edition http://dictionary.oed.
com). Plant meristems can be thought of as specific regions
of pluripotent cells (or stem cell niches) and are commonly
regarded as generating fountains of new cells. However,
recent work suggests that some plant organs are sculpted by
creating zones of intermediate or ‘quasi-meristematic’
activity.
Various types of meristematic tissue have been defined in
plants, all of which contribute to the overall structure/
function of the plant. The establishment and maintenance
of root and shoot apical meristems (respectively, RAM and
SAM) have been the subject of intense studies. These
primary meristems develop during embryogenesis and the
entire biomass of the plant can be traced back to them.
Although these meristems are vital to increase plant size,
secondary meristems are essential for producing specialized
tissues. One example is the (pro)cambium, which is impor-
tant for vascular development and increasing stem diameter.
Although secondary meristems function like meristems,
generating a source of new cells, a molecular description
was required to reveal that they are indeed related to
primary meristems (Baucher et al., 2007). The primary and
secondary meristems are indeterminate in nature because
the organs they produce can vary in size and shape
depending on local environments (Sablowski, 2007a).
Unlike indeterminate meristems, determinate meristems
produce new cells for a predetermined period and form
organs and tissues of predictable size and form, such as the
floral meristem. Another group of determinate meristems
are found within organs. Their fuzzy and fleeting nature
makes them difficult to define and, like the procambium,
require molecular markers to help to reveal their presence.
The cells of these meristems are partially differentiated, but
they have meristematic characteristics allowing prolonged
proliferation. These ‘quasi-meristems’ are important for leaf
development and have recently been shown to be important
for development of the central tissues of the fruit (Donnelly
et al., 1999; Ori et al., 2000; Hay and Tsiantis, 2006;
* These authors contributed equally to this work.
y
To whom correspondence should be addressed: [email protected]
ª The Author [2009]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved.
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1494 | Girin et al.
Alonso-Cantabrana et al., 2007). In this review, research on
Arabidopsis that supports the notion that the final morphology of the fruit is dependent on its initial meristematic and
quasi-meristematic qualities is highlighted.
Fruit and meristem morphology
The shoot apical meristem (SAM) is a complex structure
that has been extensively described (reviewed by Carles and
Fletcher, 2003, and Sablowski, 2007b). In most dicots,
including Arabidopsis, it consists of three distinct layers: the
external L1 and L2 layers, which compose the tunica, and
the inner L3 layer corresponding to the corpus. The tunica
layers are characterized by anticlinal cell divisions, whereas
cells of the corpus can divide in all planes. Superimposed on
this layer structure, the SAM can be divided into three
functional zones. The central zone is maintained by a low
cell division rate that generates cells for the peripheral zone
and the rib meristem. The peripheral zone is responsible for
the formation of lateral organ primordia, whereas the rib
meristem sustains stem growth, thus pushing the SAM
upward (Sablowski, 2007a).
The Arabidopsis silique is one of the best understood
fruit. It is vital for seed protection before maturity, and
enables seed dissemination as it breaks apart when mature.
Its structure is conserved in many species of the Brassicaceae family, including Cardamine hirsuta and the crop
species Brassica napus (oilseed rape). It is composed of the
gynophore at its base, the ovary, the style, and the stigma at
the top (Fig. 1A, B). At the end of development, the ovary
Fig. 1. Structure of the mature Arabidopsis fruit. (A) Stage 17b
fruit. Medial and lateral tissues are indicated. (B) Scanning electron
micrograph of dehiscing fruit (stage 18). The valves (V, green) have
partially separated from the replum (R, red) at the valve margins
(VM, blue) revealing the internal septum (S, yellow) and seeds (Sd).
The apical stigma (Stg) and style (Sty) tissues are coloured orange.
(C) Transverse section of a stage 17b fruit.
is composed of three external tissues with distinct morphologies. The valves are the largest part of the fruit and their
epidermis has long wide irregular cells interspersed with
stomata. The two valves are separated by two medial repla,
composed of long rectangular cells. The valves and repla are
divided by the valve margins, composed of a few rows of
small cells that later differentiate into the dehiscence zone.
The dehiscence zone is responsible for regulating the timing
of valve separation from the replum, and subsequent seed
dispersal. Internally, the two congenitally fused carpels are
separated by the septum, which joins one replum to the
other (Fig. 1B, C). The septum and repla (medial tissues)
remain attached to the plant after pod shattering.
Much of the patterning of the fruit is established at the
onset of gynoecium development, although it is still not
clear precisely from where the different tissues arise. The
layered structure of the gynoecium and the multipotent
nature of its cells, which produce ovules, suggest it has
meristematic qualities (Pautot et al., 2001). The gynoecium
is made of two congenitally fused carpels that arise from the
terminating floral meristem after initiation of the other
flower organ whorls. It appears as a circular roll of cells
enclosing a small depression [stage 6 of flower development;
the stages have been defined by Smyth et al. (1990) and
nicely reviewed by Roeder and Yanofsky (2006)]. It then
grows to form a cylinder (stage 8) and becomes closed at its
tip (stage 10). Interestingly, the layered structure of the
SAM is conserved in the growing cylinder, suggesting they
are mechanistically similar (Pautot et al., 2001). At stage 8,
the presumptive repla give rise to two medial ridges on their
adaxial side (i.e. inside the tube) flanked on both sides by
placental tissues. The medial ridges will grow towards each
other and post-genitally fuse at stage 9 in the centre of
the gynoecium. This internal structure will later form
the septum, and the ovule primordia will develop from the
placenta. The style and stigma, which form when the
gynoecium post-genitally fuses at its tip, are also derived
from the medial tissues. Therefore, the meristematic activity
of the early repla is essential for development of all the
marginal tissues of the fruit (medial tissues, style, and
stigma).
The valves and valve margins are the only fruit tissues
that develop independently of this meristematic activity.
Interestingly, the valves have a leaf-like structure with an
adaxial/abaxial polarity and the presence of stomata. As it
is widely accepted that the carpels are modified leaves,
the gynoecium can thus be seen as two modified leaves (the
presumptive valves) fused to two modified meristems (the
presumptive repla).
Many of the key regulators of fruit development have
now been identified (Gu et al., 1998; Ferrandiz et al., 2000a;
Liljegren et al., 2000, 2004; Rajani and Sundaresan, 2001;
Roeder et al., 2003; Dinneny et al., 2005; Dinneny and
Yanofsky, 2005). Several of them have roles in patterning
both the SAM and fruit medial tissues, or leaves and fruit
lateral tissues, supporting the notion that these organs have
a common origin (Fig. 2A, B) (Gu et al., 1998; Ferrandiz
et al., 2000b; Balanza et al., 2006; Roeder and Yanofsky,
Quasi-meristems regulate fruit development | 1495
Fig. 2. Comparison between the genetic and molecular pathways
controlling SAM identity and medio-lateral patterning of the fruit in
Arabidopsis. (A) Genetic pathways in the SAM (longitudinal
section). STM promotes SAM identity by excluding leaf primordia
factors, JAG/FIL activity, AS1 and AS2. CUC and KNAT6 maintain
the boundaries of the stem cell niche. An auxin maximum (purple)
predicts the position of the leaf primordia where STM is excluded.
(B) Genetic pathways of medio-lateral patterning in Arabidopsis
fruit (transverse section). Valves are shown in green (V), replum in
red (R), valve margins in blue (VM), and septum in yellow (S). The
purple zone represents an auxin maximum. The gene interactions
that have been demonstrated are designated with solid lines and
possible genetic interactions are indicated with a dashed line. See
text for details.
AS1 has recently been involved in medio-lateral patterning of the fruit (Alonso-Cantabrana et al., 2007). Valve and
replum width are, respectively, reduced and increased in as1
mutants, which underline a specific role of AS1 in promoting valve initiation. Similarly to leaf specification, AS1
is likely to act on valve formation through repression of
KNOX I genes and replum development (Fig. 2B; see
below).
Leaf development is also regulated by the JAG/FIL
transcription factor families. JAGGED (JAG) acts redundantly with the related C2H2 zinc-finger NUBBIN (NUB) in
promoting leaf formation and regulating leaf shape
(Dinneny et al., 2004, 2006; Ohno et al., 2004). FILAMENTOUS FLOWER (FIL) acts redundantly with the related
YABBY transcription factor YAB3 in promoting abaxial
leaf specification (Siegfried et al., 1999). JAG/FIL activity
also promotes leaf development by repressing KNOX I gene
expression and SAM identity in the lateral organ primordia
(Fig. 2A) (Kumaran et al., 2002).
In the fruit, JAG/FIL activity promotes valve and valve
margin formation; the analogous structures to leaves
(Dinneny et al., 2005). JAG/FIL activity positively regulates
the valve-promoting gene FRUITFULL (FUL) and the
valve margin identity genes SHATTERPROOF1 (SHP1),
SHP2, INDEHISCENT (IND), and ALCATRAZ (ALC)
(Ferrandiz et al., 2000a; Liljegren et al., 2000, 2004; Rajani
and Sundaresan, 2001). JAG/FIL activity may also promote
valve specification through repression of KNOX I genes
(Fig. 2B) (Alonso-Cantabrana et al., 2007).
The replum has meristematic properties
2006; Alonso-Cantabrana et al., 2007; Østergaard, 2008).
Understanding how these genes function in the SAM and
leaves has provided insight into their function in fruit
development.
Valves are analogous to leaves
Shoot apex development is governed by the mutual
exclusion of SAM and leaf-promoting factors. Leaf primordia formation is promoted by a complex involving the MYB
domain protein ASYMMETRIC LEAVES1 (AS1; ARP
family) and the Lateral Organ Boundary transcription
factor AS2 (Fig. 2A) (Byrne et al., 2000; Semiarti et al.,
2001; Phelps-Durr et al., 2005; Guo et al., 2008). The AS1/
AS2 complex epigenetically silences in leaf primordia the
class I KNOX meristem identity genes (KNOTTED-LIKE
HOMEOBOX; KNOX I). In this way, the AS1/AS2
complex promotes cellular differentiation and leaf initiation. Interestingly, this pathway is highly conserved in
angiosperms, as KNOX I and ARP proteins share the same
functions in Arabidopsis, maize, and Antirrhinum (Schneeberger et al., 1998; Timmermans et al., 1999; Tsiantis et al.,
1999), suggesting a fundamental role for these transcription
factors.
In addition to leaf/valve specification, JAG/FIL activity
may be linked to replum formation as fil yab3 double
mutants have enlarged repla. Replum development is promoted by the exclusion of JAG/FIL activity and valve
margin identity genes (Dinneny et al., 2005). This exclusion
from the replum is mediated by the BEL1-like homeodomain transcription factor REPLUMLESS (RPL, also
known as PENNYWISE, BELLRINGER, and VAAMANA).
rpl mutants have a reduced replum width and septum
development, and strong alleles have a complete absence
of outer replum (Roeder et al., 2003). This replumless
phenotype is rescued when rpl is combined with mutations
in valve and valve margin promoting genes, including
JAG and FIL (Fig. 2B) (Roeder et al., 2003; Dinneny et al.,
2005; Alonso-Cantabrana et al., 2007). This suggests
that the role of RPL is strictly to repress valve and valve
margin development, and not to induce replum formation
directly.
RPL also has important roles in SAM organization and
function, such as maintenance of stem cell fate, phyllotaxy
establishment, internode patterning and response to floral
induction (Byrne et al., 2003; Smith and Hake, 2003; Bhatt
et al., 2004; Smith et al., 2004). RPL has been demonstrated
to function in the SAM by interaction with KNOX I
meristem genes. This interaction may be direct as KNOX I
1496 | Girin et al.
and BELL1-like homeodomain can form heterodimers
in vivo (Bellaoui et al., 2001; Chen et al., 2003; Smith and
Hake, 2003; Hackbusch et al., 2005; Kanrar et al., 2006).
KNOX proteins are transcription factors containing a highly
conserved homeobox domain. They are named after the
founder member KNOTTED1 from maize and can be
subdivided into two classes (Vollbrecht et al., 1991;
Kerstetter et al., 1994). The KNOX I class is important for
the establishment and maintenance of meristems in all
angiosperms studied so far (Hake et al., 2004). In Arabidopsis the KNOX I genes include KNAT2 (KNOTTED IN
ARABIDOPSIS THALIANA2), KNAT6, BP (BREVIPEDICELLUS, also known as KNAT1), and STM (SHOOTMERISTEMLESS). Mutations in these genes lead to loss
of meristematic identity whereas misexpression induces
ectopic meristem formation (Long et al., 1996; Ori et al.,
2000; Hake et al., 2004; Belles-Boix et al., 2006; Scofield and
Murray, 2006; Scofield et al., 2007). Their expression
patterns are restricted to overlapping domains of the
vegetative SAM. They are repressed in leaves and leaf
primordia by the action of AS1/AS2 complex and JAG/FIL
activity (Fig. 2A).
It has recently been suggested that this regulatory module
involving RPL, KNOX I, and AS1 acts on the fruit mediolateral patterning as it does on the SAM/primordia patterning. Alonso-Cantabrana et al. (2007) showed that AS1 and
the KNOX I gene BP have antagonistic effects on replum
development. Whereas BP promotes replum development,
AS1 represses it. Analysis of the as1 mutant showed that
BP expression is restricted to the replum by the repressing
action of AS1 in the valves (Fig. 2). BP ectopic expression,
either by overexpression under the 35S promoter or in the
as1 mutant, increases replum width. AS1 probably acts in
the valves through a complex involving AS2, since as1 and
as2 mutants show a similar enlarged replum. The AS1/AS2
complex therefore has a similar role in the fruit as it has in
the SAM region, promoting lateral tissues by inhibiting BP
expression.
BP probably acts on replum development by interacting
with RPL, but also through a separate mechanism. This is
first suggested by the fact that interaction between BP and
RPL proteins regulates meristem function (Smith and Hake,
2003; Bhatt et al., 2004; Kanrar et al., 2006). It is also
consistent with the strong replumless phenotype of the rpl
bp double mutant (Alonso-Cantabrana et al., 2007). In
addition, BP ectopic expression in the valves and valve
margins drives a similar expression pattern for RPL, which
correlates with an enlargement of replum width. However,
the replumless phenotype of rpl mutant can be rescued by
the as1 mutation, and this is probably because of BP
ectopic expression in this background. In other words, BP
overexpression caused by as1 mutation is able to trigger
replum formation in the absence of a functional RPL gene.
This suggests that BP and RPL act in a partially independent manner.
Extension of the regulatory network from leaves could
further explain the spatial expression pattern observed for
BP. In addition to repression by AS1, BP expression in the
valves could be further quenched if JAG/FIL repressed BP
as it does in the leaves. High BP expression in the replum
could then be promoted by JAG/FIL repression by RPL.
This leads to a positive feedback loop: BP induces RPL
which indirectly blocks BP repression.
Alonso-Cantabrana et al. (2007) proposed an attractive
‘overlap’ model in which the medio-lateral patterning of the
fruit is organized by two opposing gradients (Fig. 3A), thus
modifying the French flag model for pattern formation
proposed by Wolpert (1969) on a single gradient basis.
Accordingly, the valves and the repla would, respectively,
be defined by high activities of valve factors (JAG/FIL) and
replum factors (BP being one of these). The valve margins
would form in a narrow stripe where the activities overlap,
being weakly expressed in this tissue or diffusing from
adjacent tissues. This is consistent with the observation of
Dinneny et al. (2005) that activation of FUL and SHP
require, respectively, a high and a low level of JAG/FIL
Fig. 3. Models for medio-lateral patterning of the Arabidopsis fruit.
(A) ‘Overlap’ model proposed by Alonso-Cantabrana et al. (2007).
Two opposing gradients of antagonistic factors delimit three
domains of the fruit. Valves factors (JAG/FIL activity, green) and
replum factors (BP, STM, and possibly RPL) specify, respectively,
valve and replum formation; the domain in which both factors
overlap develops into valve margin. (B) ‘Threshold’ model, inspired
by the overlap model. JAG/FIL activity on its own promotes both
valve and valve margin formation through a gradient. A low activity
induces valve margin development, whereas an activity above
a threshold (dashed line) promotes valve formation via the
activation of FUL and the repression of valve margin identity
genes. In this modified model, the activity of replum factors is not
required for valve margin specification but rather to delimit JAG/FIL
activity, thereby to position the valve margins and regulate replum
and valve widths. This is illustrated by BP over-expresser lines, as1
mutants and rpl mutants, in which variations of the replum factor
activity affect replum width and valve margin position. In the ant
lug double mutant, the absence of replum has no effect on valve
margin formation at the edges of the valves.
Quasi-meristems regulate fruit development | 1497
activity, thus defining valve and valve margin territories.
Furthermore, the high BP expression in the replum is likely
to produce the necessary gradient through the valve
margins since KNOX I proteins can diffuse via plasmodesmata (Bolduc et al., 2008).
If BP was the only replum factor, the model would
predict that the bp mutant has a reduced replum, but this is
not the case (Alonso-Cantabrana et al., 2007). The authors
suggest that other KNOX I genes act redundantly with BP,
as it has been shown for the SAM. KNAT2 and KNAT6 are
unlikely candidates, as knat2 knat6 bp triple mutants exhibit
no reduction of the replum (Ragni et al., 2008). Moreover,
the knat6 mutant rescues the reduction of replum width of
rpl and rpl bp mutants, suggesting that KNAT6 is a suppressor of replum formation. KNAT2 and KNAT6 are exclusively expressed in the valve margins. Therefore, they may
be partially involved in valve margin formation occurring at
the boundaries between the valves and replum. This is
reminiscent of the role of KNAT6 in the establishment of
the boundaries between the SAM and the cotyledons
(Belles-Boix et al., 2006).
An additional KNOX I gene which could be a candidate
for promoting replum development is STM. Indeed, STM is
expressed in the presumptive replum at the early stages of
gynoecium development, is partially redundant with BP in
regulating stem cell function, and interacts both genetically
and at the protein level with RPL to regulate inflorescence
stem growth and stem cell fate (Long et al., 1996; Byrne
et al., 2002, 2003; Bhatt et al., 2004). Until recently, a role
of STM has not been shown in gynoecium patterning
because most stm mutants do not develop normal inflorescences and flowers. Moreover, the study of weak stm
mutant alleles has revealed that STM is involved in early
floral patterning and carpel initiation which makes the
study of its function in the replum even more difficult
(Endrizzi et al., 1996; Pautot et al., 2001). Scofield et al.
(2007) obtained inducible STM-RNAi lines to study late
STM functions. In the most affected flowers, the floral
meristem aborted before initiating the gynoecium, but
weakly affected flowers developed two independent structures instead of the gynoecium. These structures correspond
to unfused valves topped with a stigma and flanked by
residual replum, placenta, and ovules. The septum is
completely absent and the repla are highly reduced and
divided into two parts. A related phenotype is found in the
weak stm-6 mutant in which the carpels are partially
unfused at the top of the replum (Endrizzi et al., 1996).
STM is thus involved in the formation of medial tissues of
the fruit. It is unfortunately impossible to conclude whether
it is strictly necessary for replum formation, as stm-6 and
the STM-RNAi lines still have some medial tissue that
could have been promoted by residual STM activity. In the
SAM, STM functions in part by restricting AS1 expression
to the leaf primordia, preventing the differentiation of the
stem cells (Clark et al., 1996; Endrizzi et al., 1996; Byrne
et al., 2000). STM could have a similar role in the fruit,
restricting AS1 expression to the valves thus enabling BP
expression in the replum.
The KNOX I genes BP and STM are clearly involved in
replum development. However none of them have been
shown to be strictly necessary as all the single mutants
studied so far still have some replum tissue. In the SAM,
these two genes act redundantly to maintain stem cell fate
(Byrne et al., 2002), suggesting a similar mechanism in the
replum. It would then be interesting to study the effect on
replum development in the absence of both BP and STM.
It could also be interesting to test the implication of the
KNOX II genes and the newly discovered KNATM gene. The
encoded proteins differentially interact in a yeast 2 hybrid
experiment with KNOX I and RPL, but no developmental
function have yet been reported (Hackbusch et al., 2005;
Scofield and Murray, 2006; Magnani and Hake, 2008). The
relative importance of the different KNOX genes could
provide a difference between SAM and replum developments.
In addition to KNOX and AS1 transcription factors,
a key factor regulating SAM activity and leaf initiation is
the phytohormone auxin (Reinhardt et al., 2000; Reinhardt
et al., 2003; Furutani et al., 2004; Heisler et al., 2005). The
position of lateral primordia is predicted by the production
of auxin maxima and the boundaries between them are
characterized by auxin minima. The ebb and flow of auxin
within the meristem to generate the auxin maxima is mainly
directed by the PIN-FORMED1 (PIN1) auxin efflux carrier
(Petrasek et al., 2006). The dynamic nature of PIN1:GFP
polar localization is controlled by direct phosphorylation by
the PINOID (PID) protein kinase family (Benjamins et al.,
2001; Friml et al., 2004; Michniewicz et al., 2007).
Disturbance of auxin transport by mutations in PIN1 and/
or PID cause the loss of lateral primordia (Christensen
et al., 2000; Furutani et al., 2004). A negative correlation
between STM and PIN1 expression domains in the
meristem has been observed (Heisler et al., 2005). Moreover, STM is ectopically expressed at the periphery of the
meristem in auxin transport mutants or after auxin transport inhibitor treatment, suggesting that auxin flow is
important in limiting STM expression (Scanlon, 2003;
Heisler et al., 2005; Schuetz et al., 2008). PIN-dependent
auxin fluxes are also required, together with AS1, to repress
BP expression in leaf primordia (Hay et al., 2006). It is
particularly interesting that the complete lack of lateral
floral primordia in pin1 mutants may be a consequence of
ectopic KNOX function, since mutations in BP or in its
binding partner RPL, both involved in replum development,
are known to partially rescue pin1 mutant influrescences
(Hay et al., 2006). These data highlight the interdependency
of KNOX I gene function and auxin dynamics.
Replum development in Arabidopsis is regulated by auxin
action. Disruption of polar auxin transport (PAT) by pin1 or
pid mutations or by auxin transport inhibitor treatment leads
to an expansion of the replum and a reduction of the lateral
valves (Bennett et al., 1995; Nemhauser et al., 2000; K
Sorefan, unpublished data). This is similar to the floral
meristem where disruptions in PAT cause an enlargement of
the meristem and reduction of lateral primordia. However,
there are some notable differences between the SAM and the
replum. In the SAM, auxin maxima are associated with
1498 | Girin et al.
lateral organ primordia, where AS1 is highly expressed and
KNOX I genes are repressed. By contrast, an auxin
maximum can be visualized in the replum by DR5::GFP
whereas the lateral valves have low GFP signals (T Girin,
unpublished data). The auxin maximum in the fruit is
therefore associated with a low AS1 expression and a high
STM and BP expression.
Other meristem-associated genes involved
in fruit development
The CUP SHAPED COTYLEDON 1 (CUC1) and CUC2
genes provide another interesting link between gynoecium
medial tissues and stem cell niches. These two transcription
factors of the plant-specific NAC family are indispensable
for the initiation of the embryonic SAM, and the separation
of cotyledons (Aida et al., 1997, 1999; Takada et al., 2001;
Hibara et al., 2003). CUC1/2 are expressed in the presumptive embryonic SAM, and initiate SAM formation by
activating STM expression. Their expression is later restricted to the SAM boundaries, maintaining the cells in an
undifferentiated state. Accordingly, the SAM fails to form
in the cuc1 cuc2 double mutant, and the stem cells are used
to produce fused cotyledons. Ishida et al. (2000) studied
their role in late developmental stages by producing cuc1
cuc2 plants from calli. The mutants have a defect in the
growth of the gynoecium medial ridges, thus failing to form
a septum. Interestingly, the fruit also often lack the repla in
their upper parts. The CUC1 expression pattern in the
gynoecium is currently unknown. CUC2 is expressed at
stage 7 in the presumptive medial ridges, then at the tip of
these ridges until stage 11 (after the fusion that forms the
septum). Accordingly, CUC genes are believed to maintain
the presumptive septum cells in an undifferentiated state.
An intriguing question is how cuc1 cuc2 mutations can
affect the replum development since CUC2 is not expressed
in this tissue. This could be explained by CUC1 activity or
by a putative transitory expression of CUC2 in the presumptive replum at an early stage of gynoecium development. The mutant phenotype could then result from a lack
of KNOX I activation by CUC1/2 in the replum, as for the
embryonic SAM.
To our knowledge, the only known mutant that completely lacks replum tissues is the ant lug double mutant
(Liu et al., 2000). ANT encodes a protein of the AP2/ERF
transcription factor family. It is involved in cell proliferation in lateral organ primordia and is also linked to
meristem maintenance as ant mutants have smaller floral
meristems. It is thought to regulate cell proliferation by
maintaining meristematic activity during organogenesis
(Krizek, 1999, 2003; Long and Barton, 2000; Nole-Wilson
and Krizek, 2006). The LUG transcriptional co-repressor is
involved in the growth of lateral organ primordia, but its
role is less well understood (Cnops et al., 2004). Both ANT
and LUG were first identified for their role in floral organ
identity and growth (Elliott et al., 1996; Klucher et al.,
1996; Chen et al., 2000; Conner and Liu, 2000). In addition
to their homeotic conversions, the single ant and lug
mutants have septum defects due to a lack of medial ridge
fusion and replum development appears to be reduced. The
gynoecium of the double mutant has two independent
valves completely lacking all the marginal tissues (repla,
septum, placenta, ovules, style, and stigma) (Liu et al.,
2000). These valves are similar to wild-type valves, with
long wide epidermal cells interspersed with stomata, and are
flanked by small cells similar to valve margin cells. This
suggests that ANT and LUG are involved in the maintenance of the meristematic activity in the replum primordia,
which is similar to their role during leaf organogenesis.
Interestingly, the ant lug double mutant phenotype helps
to define the relationships between tissues during gynoecium
development. Firstly, it helps to understand the relationship
between marginal tissues. It is the only known mutant that
completely lacks the replum, and it also lacks all the other
marginal tissues. On the other hand, many mutants lacking
some marginal tissues have been described, but these all have
replum tissue. It strongly suggests that replum initiation is
a prerequisite for the development of all marginal tissues,
including style and stigma. Secondly, it helps to understand
the relationship between marginal and lateral tissues. Lateral
tissues are unaffected in the double mutant. This suggests
that valves and valve margins can develop independently of
repla. The valve margins are also correctly placed at the edge
of the valves. These data do not fit the ‘overlap’ model
proposed by Alonso-Cantabrana et al. (2007) which postulate that valve margins develop where both valve and replum
factors are active (Fig. 3A). A modified ‘threshold’ model
(Fig. 3B) could account for the ant lug double mutant
phenotype. In this model, a single gradient of valve factors
(JAG/FIL) promotes both valve and valve margin development. Below a certain threshold, JAG/FIL activity promotes
valve margin formation. Above the threshold, FUL is
activated, leading to the repression of valve margin identity
genes and the formation of valve tissues. In this model, the
repressive action of replum factors (BP, STM, and RPL)
delimits the JAG/FIL domain, and therefore defines the
borders of lateral tissues. In other words, the interaction of
replum and valve signals is not involved in valve margin
tissue formation but rather in relative positioning of the
valve margins, thus affecting valve and replum sizes.
Quasi-meristems as key modulators of plant
development
The presence of meristematic activity outside proper
meristems is not specific to the gynoecium/fruit, as many
meristematic regions in organs have been described. It is
proposed that these regions are named ‘quasi-meristems’. A
quasi-meristem corresponds to a zone of active cell proliferation within an organ, giving birth to specialized and
determinate tissues. Contrary to true-meristems, all the cells
of quasi-meristems will eventually differentiate.
Quasi-meristems are important for determining the structure of plants. Such zones are important for leaf
Quasi-meristems regulate fruit development | 1499
morphogenesis, where the marginal meristem initiates the
leaf blade before the plate meristem expands it (Donnelly
et al., 1999). They are also found at the base of monocotyledon leaves, and determine the final size of the leaf
blade. Ovule primordia arise and develop from a meristematic zone (Brambilla et al., 2007). To some extent the rib
meristem can be considered as a quasi-meristem, which
drives stem growth. It is often considered part of the SAM
but was initially defined as an independent structure within
the stem (Ruonala et al., 2008). All its cells will differentiate
rapidly and its apparent indeterminate activity is only due
to the provision of new cells from the SAM.
These quasi-meristems share key regulatory genes with
true-meristems, but also require some specific genes. The
SAM and the replum both require KNOX I gene function,
whereas the SAM and ovule primordia both require
WUSCHEL activity. ANT and LUG on the other hand are
specifically required for quasi-meristem activity in the leaf
and the medial part of the fruit.
Another good example of quasi-meristems is illustrated by
dissected leaf species. Some of the molecular mechanisms for
SAM identity have been diverted in these species to control
organ morphology. In the Arabidopsis relative Cardamine
hirsuta, which has a dissected leaf form, ChBP was expressed
not only in the SAM, as in Arabidopsis, but also in leaf
primordia. ChBP is first repressed in leaf founder cells, but
this repression is not maintained later in leaf primordia. This
re-establishment of KNOX I expression is thought to maintain
a degree of meristematic activity, promoting leaflet outgrowth
and repressing precocious differentiation (Champagne and
Sinha, 2004). The molecular mechanisms of KNOX I gene
regulation have been investigated. The chas1 mutant had
additional leaflets and the ChBP was ectopically expressed
(Hay and Tsiantis, 2006). Auxin maxima predict the positions
of lateral leaflet formation. Disruption of auxin transport with
chemical inhibitors or mutations in the ChPIN1 gene blocks
the auxin maxima and reduces lateral leaflet formation.
Conversely, application of exogenous auxin induces auxin
maxima and leaflet production. The exclusion of STM
expression from positions of auxin maxima in the SAM is
also maintained in leaflet formation of C. hirsuta (Barkoulas
et al., 2008). The establishment of a quasi-meristem with
partial meristematic activity is thus a key regulatory mechanism to drive leaf morphology in some species.
The establishment of the quasi-meristem allows for the
timing of tissue differentiation to be fine-tuned. In the
SAM, developmentally ‘simple’ primordia can form in
a matter of hours. Morphologically ‘complex’ leaves and
fruit on the other hand can take days and weeks to develop.
Therefore, the prolonged quasi-meristematic state may
allow for the organ to modulate growth during this time.
meristems are clearly important for leaf and fruit development and may be involved in stem growth. Controlling the
degree of meristematic identity may allow the moulding of
desirable plant traits in crops. For example, premature pod
shattering in oilseed rape crops is a major cause of yield
loss. In some Brassica cultivars, the replum is reduced and
the valves become partially fused, which is similar to the
rpl-3 mutant in Arabidopsis. These plants have much
reduced pod shatter. Therefore, it may be possible to
modulate pod shatter in Brassica crops by manipulating
replum meristematic activity, possibly by reducing Brassica
RPL or KNOX I gene function. It has already been
demonstrated that knowledge from Arabidopsis can be
transferred to other Brassicaceae. It is possibly not surprising that modulating FUL transcription in Brassica juncea
abolished valve margin development and therefore pod
shattering as it does in Arabidopsis (Østergaard et al, 2006).
What is more exciting and valuable is that soft fruit species
may regulate fruit development through shared mechanisms
with Arabidopsis but this is something that needs more
attention (Seymour et al., 2008).
Research has focused on the beginning and ends of celltype differentiation, and it is indeed much more difficult to
analyse the intermediate states. Ground-breaking work on
plant growth using computer models is now allowing us to
record these transient stages of development. Petal formation in Antirrhinum, for example, can now be replayed to
demonstrate how small localized changes in growth rate,
perhaps by quasi-meristems, help to mould the final petal
shape (Coen et al., 2004). The discovery of quasi-meristems
in leaves and fruit highlights the importance of understanding the journey from stem cells to terminally differentiated
cells, if we are to fully understand plant development.
Quasi-meristems as targets for crop
improvement
Alonso-Cantabrana H, Ripoll JJ, Ochando I, Vera A,
Ferrandiz C, Martinez-Laborda A. 2007. Common regulatory
networks in leaf and fruit patterning revealed by mutations in the
Arabidopsis ASYMMETRIC LEAVES1 gene. Development 134,
2663–2671.
An important goal for plant biology is to translate our
fundamental knowledge from model plants to crops. Quasi-
Acknowledgements
This work was supported by grants from the Biotechnological and Biological Sciences Research Council and core
strategic funds from the John Innes Centre to LØ.
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