Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK
* Author for correspondence (e-mail: miltos.tsiantis{at}plants.ox.ac.uk)
SUMMARY
The Society for Experimental Biology organised a `Plant Frontier' meeting, which was recently held at the University of Sheffield, UK. One of the sessions of this broad meeting was on plant meristems, which covered a range of topics, including stem cells, patterning, long distance signalling and epigenetic regulation of meristem development.
Introduction
Meristems are groups of organogenic cells that are established during plant embryogenesis. There are two apical meristems that reside in the growing shoot and root tips of plants, and produce the aerial and subterranean parts of the plant body, respectively. To fulfil this function, a meristem produces daughter cells that differentiate into distinct cell types, thus producing the different tissue types that make up the organs of the plant. However, a meristem must also regenerate itself to allow organogenic processes to continue throughout the life of a plant. This dual function requires a constant flow of cells through a meristem. This flow is maintained by an autoregulatory system that ensures a constant stem cell population (Fig. 1A) and by factors that prevent the premature differentiation of meristem cells (Fig. 1B). Mechanisms that underlie and direct meristem function were the focus of this meeting session on Plant Meristems organised by Keith Lindsey (University of Durham, Durham, UK).
Meristems from past to present
Nick Battey (University of Reading, Reading, UK) appropriately opened the meeting by discussing meristem action from a historical and philosophical perspective. Meristems act to iteratively form organs and, therefore, to ultimately produce the whole plant. This behaviour, Battey argued, embodies the Aristotelian `final cause', as it can be taken to represent the `purpose' of meristem function. Meristem activity also represents a key difference between plant and animal development because meristematic stem cells can generate new pattern throughout the life of a plant, whereas in animals, stem cell activity largely maintains existing patterns of development.
A key problem highlighted by Battey is whether phyllotaxis the
regular pattern of organ initiation at the shoot apical meristem (SAM)
is a cause or a consequence of growth. Over 100 years ago, Church established
the SAM as the origin of pattern with his equipotential theory of phyllotaxis
(Church, 1904), but he failed
to see that pattern could be generated merely as a consequence of regular
growth at the apex. The idea that phyllotaxis is generated via the graded
distribution of an inhibitor of primordium initiation at the SAM gained
prominence, and, for the past 50 years, auxin has been proposed to be this
inhibitor. Cris Kuhlemeier (University of Bern, Bern, Switzerland) has
recently turned this theory on its head by demonstrating that auxin is not an
inhibitor but an activator of primordium initiation
(Reinhardt et al., 2003
). As
Kuhlemeier reported, another key difference from the classical inhibitor
theory is the source of auxin distribution. Rather than diffusing from the
centre, elegant immunolocalisation experiments demonstrated that auxin is
transported basipetally by the PINFORMED1 protein through the epidermal layer
of the shoot up to the periphery of the SAM, where it induces primordium
initiation (Fig. 1B). The
scavenging of diffusible auxin by the putative auxin influx protein AUX1
confines these auxin gradients to the epidermis, and much evidence
demonstrates that these gradients are not only permissive but also instructive
for organ initiation (Reinhardt et al.,
2000
; Reinhardt et al.,
2003
). Kuhlemeier also highlighted several unanswered questions in
this area. Is the source of auxin localised? How is PIN1 polarised in the
cell? When do primordia switch from auxin sink to source? How are phyllotactic
patterns first established? His group is tackling these questions using the
combined approaches of computer modelling and mutagenesis.
Shoot meristems and organ growth: close connections
Organogenesis occurs at the SAM, raising the issue of how cell division,
differentiation and morphogenesis are coordinated to facilitate this process.
Andrew Fleming (University of Sheffield, Sheffield, UK) used an inducible
expression system to show that localised induction of the cell wall-loosening
protein, expansin, is sufficient to produce a leaf from the SAM
(Pien et al., 2001), whereas
induction of cell division or a reorientation of the cell division plane is
not (Wyrzykowska and Fleming,
2003
; Wyrzykowska et al.,
2002
). By performing identical experiments in the margins of young
leaves, Fleming has found that an inverse relationship exists between cell
division, which restricts growth, and cell expansion, which promotes growth,
in the generation of leaf shape. But what links the processes of cell growth,
differentiation and proliferation? Fleming suggests that the retinoblastoma
protein (AtRBR), which acts as a suppressor of cell proliferation
(Ebel et al., 2004
), provides
such a link in Arabidopsis because transient AtRBR
expression in the SAM suppresses growth and cell division while promoting cell
differentiation.
Miltos Tsiantis (University of Oxford, Oxford, UK) also discussed the
developmental transition from meristem to leaf cell fate and returned to
Battey's Aristotelian view of a meristem to argue that a Heraclitian view may
be more accurate that ordered development is produced through
`conflict'. Mutual antagonism between KNOTTED1-like homeobox (KNOX) meristem
and ASYMMETRIC LEAVES1/ROUGHSHEATH2/PHANTASTICA transcription factors regulate
meristem versus leaf fate (Byrne et al.,
2000; Timmermans et al.,
1999
; Tsiantis et al.,
1999
; Waites et al.,
1998
), and Tsiantis presented evidence that auxin may act within
this framework to repress meristem-promoting activities in the leaf. Lateral
growth is also driven by antagonism between adaxial- and abaxial-promoting
factors (Bowman et al., 2002
),
and Tsiantis proposed that gibberellin biosynthesis is confined to the leaf
via the repression by KNOX transcription factors
(Hay et al., 2002
), where it
mediates the activity of polar growth determinants.
|
Lucy Moore (University of Oxford, Oxford, UK) presented evidence that
interactions between three different families of homeodomain proteins might be
important for shoot development. BELLRINGER (BLR) and class I KNOX homeodomain
proteins interact with each other (Byrne et
al., 2003; Smith and Hake,
2003
), and Moore showed here that BLR also interacts with REVOLUTA
(REV), a member of the class III homeodomain leucine zipper (HD-Zip III)
family, but that REV does not interact with the KNOX proteins. This suggests
that BLR may act as an intermediate between KNOX and REV proteins to promote
SAM function. Keith Lindsey also discussed the possibility that HD-Zip III
proteins bind sterol ligands to specify embryo polarity. Lindsey showed how
sterols could affect ethylene receptors in a genetic analysis of the sterol
biosynthetic mutants hydra and fackel
(Schrick et al., 2000
;
Souter et al., 2002
). He
proposed that loss of sterol biosynthesis results in membrane defects that
render membrane-localised ethylene receptors `on'. His group is now using
laser capture on early embryos in order to carry out whole-genome expression
analysis to identify unique apically versus basally expressed genes and to
assess their role in embryo polarity.
How to know how much to grow?
Delphine Fleury [Flanders Interuniversity Institute for Biotechnology (VIB), Ghent, Belgium] used mutational analyses in Arabidopsis to demonstrate that the `Elongator' histone acetyl transferase transcriptional complex functions in leaf and root growth by regulating cell proliferation. Genetic epistasis and clustering of genome-wide expression analyses of elongata mutants indicate that the Elongator complex forms in plants and acts in the RNA polymerase II-mediated transcriptional process downstream of the Mediator complex. This work showed that, in plants, the Elongator complex acts in meristems and that the histone code is important for regulating organ growth.
|
Manuela Costa (John Innes Centre, Norwich, UK) discussed the problem of how
differential regulation of organ growth may have contributed to the evolution
of floral dorsoventral asymmetry, a trait that has evolved numerous
independent times in flowering plants, including Antirrhinum. Several
Antirrhinum mutants show loss of dorsal petal identity, and
combinations of these mutants result in symmetrical flowers
(Corley et al., 2005;
Galego and Almeida, 2002
;
Luo et al., 1999
;
Luo et al., 1996
). These
genetic interactions define a gene network that controls differential petal
growth in Antirrhinum and functions partly via the direct
transcriptional regulation of RADIALIS (RAD) by the
DNA-binding protein CYCLOIDEA (CYC). Costa investigated how this gene network
is configured in Arabidopsis, which unlike Antirrhinum has
symmetrical flowers. In Arabidopsis, the CYC orthologue
TCP1 is also expressed in the dorsal side of flowers, but only
transiently (Cubas et al.,
2001
). However, RAD-like genes are not expressed in
Arabidopsis flowers, indicating that the function of this
developmental network is at least partially diverged. Nevertheless, elements
of this network are conserved because inducible CYC expression in
Arabidopsis is sufficient to alter leaf and petal growth, and to
activate the expression of a RAD::RAD transgene. This talk also
highlighted the importance of the integrated study of developmental patterning
and organ growth in understanding plant development.
Stem cells and vascular development underground
Ben Scheres (Utrecht University, Utrecht, The Netherlands) reached the
heart of questions about meristem development by asking what specifies stem
cells. Patterning the stem cell niche in the Arabidopsis root
meristem requires radial coordinates from the SHORT ROOT (SHR) and SCARECROW
(SCR) GRAS-type transcription factors (Di
Laurenzio et al., 1996;
Helariutta et al., 2000
) and
apical-basal coordinates from feedback between PLETHORA (PLT) AP2-type
transcription factors and auxin (Aida et
al., 2004
; Blilou et al.,
2005
) (Fig. 3). But
what specifies stem cells? The NAC-domain putative transcription factors FEZ
and SOMBRERO (SMB) are expressed in root cap stem cells, and their loss
affects stem cell number. For example, fez mutants initiate fewer
stem cells and smb mutants initiate an excess. fez is
epistatic to smb and FEZ overexpression results in extra
stem cells, indicating that SMB acts downstream of FEZ to
promote stem cell activity and feeds back to repress FEZ. Expression
analysis showed that PLT proteins, but not SHR/SCR, regulate FEZ and
SMB (Fig. 3). All of
these patterning and stem cell-specific transcription factors are plant
specific, raising the issue of whether the mechanisms that specify plant stem
cells resemble those in animals. Scheres' results show that modulating the
expression of G1 regulators specifically affects stem cell number, and that
these genes act downstream of SCR (Fig.
3). Therefore, common cellular modules may be independently
recruited to facilitate stem cell function in multicellular eukaryotes.
The Arabidopsis root also emerged as the model of choice for
understanding the differentiation of provascular cells into the distinct
phloem and xylem tissues that form the vascular system. Yka Helariutta
(University of Helsinki, Helsinki, Finland) described the isolation of
suppressors of the short root mutant wooden leg (wol),
providing a powerful example of how forward genetic analyses are still
indispensable for dissecting development and understanding protein function.
WOL/CRE1 encodes a hybrid two-component signal transduction molecule
that acts as a receptor for the hormone cytokinin and is required for
provascular cell proliferation (Hwang and
Sheen, 2001; Inoue et al.,
2001
; Mahonen et al.,
2000
). The wol mutation produces a mutant protein that
abolishes cytokinin binding and prevents cell proliferation by blocking
activity not only of CRE1 but also of the related and redundantly acting AHK1
and AHK2 proteins (Higuchi et al.,
2004
). Helariutta also described an extragenic mutant
suppressor of wol1 (sow1), which allows the proliferation of
provascular cells and the development of phloem in wol. He was able
to show that cytokinin is required to maintain provascular stem cell identity
and prevent protoxylem differentiation, while SOW1 counteracts cytokinin
activity to allow protoxylem differentiation.
Liam Dolan (John Innes Centre, Norwich, UK) discussed the transcriptional patterning system that specifies root hair cells. He introduced the roles of the ROOT HAIR DEFECTIVE6 family (RDL) of bHLH proteins in root hair development and went on to show conservation of RDL-like gene function in tip growth of the moss Physcomitrella patens, demonstrating that the genetic pathways controlling tip growth may be conserved in plant lineages that diverged 450 million years ago.
Hormonal control of meristem function
In her presentation, Ottoline Leyser (University of York, York, UK)
explored the control of shoot branching. Branches form via the activity of
axillary meristems, which share functional attributes with the SAM but reside
in the leaf axils. The classical hormone auxin and a novel hormone
provisionally named `Mystery Compound X' (MCX) both inhibit branching. The
auxin resistant1 (axr1) mutant has excessive branching,
while the dominant auxin over-responding mutant axr3-1 has no
branching (Lincoln et al.,
1990). AXR1 and AXR3 are components of an auxin-signalling pathway
in which Aux/IAA repressor proteins, such as AXR3, are targeted for
proteolysis by a ubiquitin ligase SCFTIR1 complex (named after the
components SkpI, Cullin and the F-box protein TIR1)
(Gray et al., 2001
). AXR3
degradation de-represses AUXIN RESPONSE FACTOR transcription factors, enabling
auxin-responsive genes to be turned on. So what binds and senses auxin in this
pathway? Current results indicate that SCFTIR1 has a key role in
this process. Understanding auxin signalling is not, however, sufficient to
understand shoot branching, as auxin regulates this process by acting in the
stem and not the axillary bud. The key to discovering what happens in buds
might lie in understanding a novel developmental pathway that is defined by
the more axillary branching (max) mutants. Grafting
experiments have shown that MAX1, MAX3 and MAX4 act outside of the bud,
probably as biosynthetic enzymes of a carotenoid-derived signal currently
called MCX, which inhibits bud growth
(Booker et al., 2004
;
Booker et al., 2005
;
Sorefan et al., 2003
;
Stirnberg et al., 2002
).
Grafting experiments and clonal analysis show that MAX2 acts cell autonomously
in the bud to receive the MCX signal. MAX2 encodes an F-box protein
that also forms a SCF complex, indicating that MCX and auxin signalling may
both operate via regulated proteolysis. How, then, is MCX and auxin signalling
integrated to control bud development? As Leyser discussed, grafting either
axr1 mutant or wild-type roots to max3 shoots restores
normal branching, indicating that the interaction between auxin and MCX occurs
after MCX synthesis. One possibility being tested is whether MCX signalling
regulates auxin efflux from buds.
|
`Florigen' is another mystery compound that is produced in the leaf and
that signals long-distance to the shoot meristem to promote flowering. George
Coupland (Max Planck Institute for Plant Breeding, Köln, Germany) is
investigating how this elusive signal is integrated into the genetic hierarchy
of known flowering time genes in Arabidopsis. The transcriptional
regulator CONSTANS (CO) is sufficient to induce flowering when expressed in
the phloem but not in the SAM, whereas the CO-activated gene FLOWERING
LOCUS T (FT), encoding a phosphatidylethanolamine-binding
protein, induces flowering in either tissue
(An et al., 2004). This signal
acts quantitatively: the specific induction of CO activity in the phloem
tissue of a single leaf could activate FT expression but not
flowering. This signal is also strictly temporally controlled: CO is only
sufficient to induce FT expression at the end of the day because of
the antagonistic effects of the photoreceptors PHYTOCHROME B (PHYB) and
PHYA/CRYPTOCHROME1/2 on CO protein stability
(Valverde et al., 2004
).
Additionally, the bHLH protein PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) is
expressed at midday and represses PHYB action, potentially restricting the
effect of PHYB to the morning. Nevertheless, the phloem signal that triggers
flowering in the SAM in response to CO activity remains a mystery.
Epigenetic regulation of meristem development
Caroline Dean (John Innes Centre, Norwich, UK) presented a compelling
framework for how plants use a `memory' of winter to trigger flowering.
Vernalization is the facilitation of flowering by prolonged cold, and it acts
by establishing a mitotically stable gene expression state that is reset at
meiosis and is, therefore, epigenetic in nature. Vernalization represses the
MADS-box gene FLOWERING LOCUS C (FLC), which blocks
flowering by inhibiting genes required to switch the meristem from vegetative
to floral development (Michaels and
Amasino, 1999). Many regulators of FLC alter chromatin
structure or are involved in RNA processing (reviewed by
Henderson and Dean, 2004
). One
unanswered question is how these chromatin marks are erased from FLC
to allow expression again in the early embryo? Dean also highlighted the
substantial natural variation in the vernalization requirement of
Arabidopsis accessions, mostly owing to allelic variation at the
FLC and FRIGIDA (FRI) loci
(Gazzani et al., 2003
). FRI is
a novel nuclear protein that acts non-cell autonomously to promote
FLC expression and thus prevent flowering
(Johanson et al., 2000
).
Strikingly, 15 independent mutations in the FRI locus have been
identified in rapid cycling accessions.
Conclusions
The scope and breadth of this meeting reflected how, only a few decades after plant developmental genetics emerged as a discipline, it has moved to the forefront of modern biology. Current research is not only illuminating older problems, such as the mechanisms underlying the generation of canonical patterns in nature, in the case of phyllotaxis, but is also elucidating newer ones, such as how developmental patterning mechanisms are intertwined with the cell-division machinery to specify stem-cell identity or how transcriptional states are mitotically maintained. The meeting also prefigured future research. For example, it is not clear how cell fate allocation mechanisms defined in molecular genetic frameworks are translated into precise growth patterns that generate organismal form. The use of morphometric analyses in the context of molecular genetics appears to hold a lot of promise in this direction. How the genetic hierarchies discussed in the meeting are reconfigured during evolution to produce natural variation in form will also be a major challenge for the future. Research on natural variation in flowering time has shown, for example, how the use of wild accessions of plant model systems has much to offer in this respect.
ACKNOWLEDGMENTS
We thank Rüdiger Simon, Robert Sablowski and Nick Battey for comments, and Dorota Kwiatkowska and Ben Scheres for Figs 2 and 3, respectively. We apologise to speakers whose results we could not include due to space constraints.
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