1 John Innes Centre, Colney, Norwich NR4 7UH, UK
2 Department of Plant Sciences, University of Oxford, South Parks Rd, Oxford OX1
3RB, UK
* Author for correspondence (e-mail: jane.langdale{at}plants.ox.ac.uk)
SUMMARY
This year, the biannually organized FASEB meeting `Mechanisms in Plant Development' took place in August in Vermont, USA, organized by Martin Hulskamp (University of Köln, Köln, Germany) and John Schiefelbein (University of Michigan, Ann Arbor, MI, USA). The meeting covered numerous topics, ranging from patterning and differentiation to the evolution of developmental mechanisms. Despite apparent distinctions between the sessions, many of the talks were broad ranging and most highlighted unifying developmental concepts.
Fertilization and epigenetic regulation of development
After a pollen grain lands on the stigma of a receptive plant, it grows
through the transmitting tract towards an ovule, where it penetrates the
embryo sac and releases sperm cells. Given that pollen of many different
species may land on a stigma, plants have complex mechanisms with which to
identify compatible pollen. Ueli Grossniklaus (University of Zurich, Zurich,
Switzerland) described a gene that may be involved in such a process. In
feronia (fer) mutants of Arabidopsis, sperm cells
are not released into the synergid where the FER gene is transcribed
(Huck et al., 2003). As
FER encodes a putative receptor kinase, it may represent the first
identified part of a gametophyte-gametophyte recognition system. Following
double fertilisation, flowering plants develop a diploid embryo and a triploid
endosperm, the development of which is repressed prior to fertilization. Ramin
Yadegari (University of Arizona, Tucson, AZ, USA) described recent progress
towards understanding the epigenetic control of this repression by the
Polycomb-group (PcG) proteins FIS1/MEA, FIE and FIS2. Paternal alleles of PcG
genes are repressed during early endosperm development, and Yadegari is
currently identifying regions of the FIS2 gene that are required for
this negative regulation. Rob Martienssen (Cold Spring Harbor Laboratories,
Cold Spring Harbor, NY, USA) accounted for a further a mechanism for the
epigenetic regulation of gene expression in plants via transposable
elements which indicates that the general mechanism of heterochomatin
(silent chromatin) regulation is conserved among eukaryotes
(Lippman et al., 2004
).
Stem cells and patterning: the root and shoot of it
As embryogenesis proceeds, the root and shoot apical meristems are
generated. Three talks focussed on the genetic mechanisms responsible for
spatially positioning stem cell populations within the developing root or
shoot meristem. In the first, Gerd Jurgens (University of Tübingen,
Tübingen, Germany) discussed how auxin plays a role in establishing the
root meristem. PIN-FORMED (PIN) proteins, which are hypothesized to regulate
auxin efflux from cells, are required for the formation of a polar axis during
Arabidopsis embryogenesis
(Geldner et al., 2003).
PIN-regulated auxin transport then controls the expression of two
transcription factors, MONOPTEROS (MP) and
BODENLOS, which specify the basal embryonic pole that develops into
the root meristem. Ben Scheres (Utrecht University, Utrecht, The Netherlands)
developed this theme to discuss how coordinates along both the proximodistal
(PD) and radial axes are interpreted to position the quiescent centre (QC)
within the root meristem. In the radial axis, the GRAS-type transcription
factor SCARECROW (SCR) is necessary and sufficient for QC specification
(Heidstra et al., 2004
).
However, as the QC occupies only a single cell layer in the PD axis, other
factors must influence specification. Using promoter trap lines, Scheres has
identified PLETHORA1 (PLT1), which encodes an APETALA2-type
transcription factor that is specifically expressed in the QC and stem cells.
Double mutants of plt1 and its duplicate plt2 display
aberrant stem cell populations in the root, and fail to express QC markers.
Notably, early spatial restriction of PLT expression depends on four
PIN genes and later expression requires MP. As an auxin-responsive
reporter gene construct is expressed normally in plt double mutants,
PLT probably acts downstream of auxin to establish the PD coordinates for QC
specification. Thus, QC specification is mediated by an overlap between auxin
and SCR pathways.
Overlapping pathways that specify stem cell populations were also discussed
by Steve Clark (University of Michigan, Ann Arbor, MI, USA). He introduced two
proteins that are related to the CLAVATA1 (CLV1) receptor kinase. CLV1 acts in
a feedback pathway with the homeodomain protein WUSCHEL (WUS) to specify stem
cell fate in the shoot apical meristem (SAM) of Arabidopsis
(Carles and Fletcher, 2003).
WUS promotes stem cell fate and CLV3 activity, whereas CLV restricts the
WUS expression domain and thus the size of the stem cell population.
Mutational analysis has shown that the CLV1-related BAM1 and BAM2 proteins act
with CLV1 in the SAM. Paradoxically, clv1 mutants have larger
meristems than do wild-type plants, whereas bam double mutants have
smaller meristems. This observation can be explained if the CLV1 receptor is
able to respond to BAM ligands. If so, loss of bam receptor function
could lead to hyperactivation of CLV1 by its own ligand (CLV3) and by the BAM
ligands. As a consequence, CLV1 would `over'-repress WUS activity and meristem
size would be reduced. The dynamics of CLV/WUS interactions were elegantly
displayed by Venugopala Reddy (Caltech, Pasadena, CA, USA) using real-time
confocal microscopy (Reddy et al.,
2004
). By using constitutively expressed WUS and a
CLV3-reporter gene construct, Reddy showed that WUS-induced expansion
of the CLV3 expression domain involves a respecification of the
peripheral zone of the SAM. An additional player in the WUS pathway was
introduced by Cristel Carles (Plant Gene Expression Centre, Albany, CA, USA).
The ULTRAPETALA1 (ULT1) gene restricts the WUS
expression domain in the inflorescence meristem of Arabidopsis in a
CLV-independent manner. ULT1 also acts in the AGAMOUS (AG)/WUS pathway that
operates in the floral meristem. Previous work has shown that WUS acts with
LEAFY to promote AG function in early floral development and that later in
floral development AG acts to repress WUS activity, and thus to terminate
floral development (Lohmann et al.,
2001
; Lenhard et al.,
2001
). Mutant and transgenic analysis suggest that ULT1,
which encodes a putative transcription factor, is a novel temporal component
of AG induction in the centre of the flower and of the subsequent
WUS-dependent stem cell termination (Carles
et al., 2004
).
In addition to maintaining stem cells, the SAM also produces the aerial
organs of the plant. The distinction between meristem and organs is a crucial
component of the switch from indeterminate to determinate growth. In this
context, Patty Springer (University of California, Riverside, CA, USA)
discussed the role of LATERAL ORGAN BOUNDARIES (LOB), a gene
whose expression is regulated by the homeodomain proteins SHOOTMERISTEMLESS
(STM) and BREVIPEDICELLUS (BP) (Shuai et
al., 2002). Interactions between STM and the 3' region of
the LOB gene, and between BP and the 5' region of LOB,
restrict LOB expression to the region between the stem cells and
developing organ primordia. Springer has identified two further genes
expressed in this region that may interact with LOB to demarcate the
meristem/organ primordia boundary.
From boundaries to specialized tissues
Once boundaries are established between meristems and organ primordia,
patterning can occur in an organ-specific manner. The developmental decisions
that occur during organogenesis were highlighted in talks by Kathy Barton
(Carnegie Institute, Washington, DC, USA) and Kay Schneitz (Technical
University, Munich, Germany). Barton discussed the regulation of HD ZIP genes
such as PHABULOSA (PHB), the spatial expression of which is
restricted to the adaxial side of the leaf primordium, which is crucial for
establishing the adaxial/abaxial axis of the leaf
(Shuai et al., 2002). The
localization of PHB mRNA reportedly involves miRNA-induced
posttranscriptional gene silencing. Somewhat controversially, Barton proposes
an alternative mechanism whereby miRNA binding leads to the methylation of
downstream regions of the PHB gene and its subsequent transcriptional
repression. Interestingly, this explanation is more compatible with the
phenotype of dominant gain-of-function phb mutants. Schneitz
presented an analysis of factors that facilitate differentiation along the PD
axis of ovules. Three domains are apparent in this axis: the distal nucellus,
the middle chalaza and the basal funiculus. In early development, WUS
is expressed in the distal domain, yet WUS activity influences integument
outgrowth from the chalaza. Therefore, WUS most probably acts non
cell-autonomously to specify chalazal and hence integument fate
(Sieber et al., 2004
).
Within developing organs, several processes specify cell fate, and at least
eight talks addressed this issue. In one of the best presentations of the
meeting, Adrienne Roeder (University of California, San Diego, CA, USA)
discussed fruit development in Arabidopsis. The Arabidopsis
fruit comprises two large seedpod walls known as valves that are joined to the
replum at the valve margins. The valve margins form narrow stripes of cells
that are specialized for seed dispersal. When the fruit matures, the valve
margin cells separate, allowing the valves to detach from the replum and the
seeds to be released. Specification of valve margin cell fate is controlled by
a group of transcription factors. SHATTERPROOF (SHP) is a MADS domain
transcription factor that is initially expressed broadly, but becomes
restricted to the valve margin. SHP positively regulates the expression of two
basis helix-loop-helix (bHLH) transcription factors, INDEHISCENT
(IND) and ALCATRAZ (ALC), which are also required
for valve margin differentiation
(Liljegren et al., 2004). The
negative regulation of SHP by the homeodomain protein REPLUMLESS
(RPL) in the replum and by another MADS factor, FRUITFULL (FUL), in the valves
limits SHP expression to the valve margin
(Roeder et al., 2003
). The
coordinated action of these transcription factors thereby leads to the
formation of the line of specialized valve margin cells precisely at the
border between the valve and the replum (see
Fig. 1).
|
Two further talks discussed the specification of vascular tissue. Vascular
traces contain xylem strands, and a fundamental question is how individual
xylem cells [tracheary elements (TE)] fit together to form a contiguous tube.
Using Zinnia elegans, Hiroo Fukuda (University of Tokyo, Tokyo,
Japan) showed that cultured cells undergoing xylem differentiation secrete a
protein that induces the differentiation of TEs in neighbouring cells. The
secreted protein (xylogen) is induced by auxin and has a polar distribution in
the cell. This suggests that during tube formation, developing TEs secrete
xylogen and induce neighbouring cells to also develop as TEs.
Arabidopsis plants lacking xylogen cannot develop contiguous xylem
and instead form discontinuous vascular strands
(Motose et al., 2004). Further
insight into the mechanism of vascular cell differentiation might come from a
mutagenesis screen in Arabidopsis described by Tim Nelson (Yale
University, New Haven, CT, USA). Nelson reported the existence of two mutant
classes those with discontinuous venation and those with parallel,
rather than networked, venation.
In the final talks on cell-type differentiation Fred Sack (Ohio State
University, Columbus, OH, USA) and Lynn Pillitteri (University of Washington,
Seattle, WA, USA) discussed how the patterning of stomata and epidermal
pavement cells depends upon the balance between asymmetric cell divisions,
symmetric cell divisions and terminal differentiation
(Fig. 2). Pillitterri
highlighted the role of ERECTA (ER)-like receptor kinases in stomatal
patterning and Sack described TOO MANY MOUTHS (TMM), a different type of
extracellular receptor (Nadeau and Sack,
2002). The ligand for the TMM receptor may be created through the
action of the STOMATAL DENSITY AND DISTRIBUTION (SDD) protease and TMM may act
upstream of YODA, a MAPKKK (Bergmann et
al., 2004
). Later in development, the transcription factors FOUR
LIPS and FAMA limit symmetric divisions. Possibly, these transcription factors
are targets of the signal transduction cascade defined by ER, TMM, SDD and
YODA proteins.
|
Cellular differentiation processes modulate not just cell type but also cell size and cell shape. Increase in cell size in plants is accompanied by an increase in the amount of DNA in the nucleus (endoreduplication). Yuki Mizukami (University of California, Berkeley, CA, USA) identified a group of proteins required for endoreduplication in Arabidopsis. Fizzy genes control the cell cycle in Drosophila. Arabidopsis plants that lack the two FIZZY-RELATED (FZR) genes have reduced endoreduplication, whereas overexpression of FZR1 induces endoreduplication in cultured cells. Neither perturbation affects cell-type differentiation, demonstrating that increased DNA content is not essential for cell differentiation.
The cytoskeleton plays an important role in determining cell shape, and
this issue was the focus of many talks. Tobias Baskin (University of
Massachusetts, Amherst, MA, USA) discussed the roles of cellulose and
microtubules in determining cell growth directions. Experiments with low doses
of anti-microtubule drugs suggest that the degree of cellular growth
anisotropy (the degree to which cell expansion is not uniform, i.e. isometric
on all surfaces) is determined by how well aligned cellulose microfibrils are
across fields of cells rather than in individual cells, and that microtubules
somehow promote the establishment of transcellular cellulose alignments.
(Baskin et al., 2004). Both Jie
Le (Purdue University, West Lafayette, IN, USA) and David Oppenheimer
(University of Florida, Gainesville, FL, USA) discussed the role of the
cytoskeleton in the morphogenesis of Arabidopsis trichomes
branched epidermal hair cells. Actin filaments form bundles in elongating
trichome branches, and the drug-induced depolymerisation of these bundles
results in the formation of fat trichomes with short branches that resemble
those that form on distorted (dis) mutants. Four of the DIS
genes encode components of the Arp2/3 complex, which nucleates polymerization
of actin filaments in vitro. To stimulate actin polymerization, the Arp2/3
complex must be activated. Laurie Smith (University of California, San Diego,
CA, USA) described a family of WAVE/Scar-related proteins found in both
Arabidopsis and maize that can activate the Arp2/3 complex in vitro.
These proteins also bind to BRICK 1 (BRK1), a protein required for
localized actin polymerization and for the proper morphogenesis of maize
epidermal pavement cell lobes (Frank and
Smith, 2002
). BRK1 is the plant homolog of a mammalian protein
found in a complex with WAVE that regulates WAVE activity. Jie Le reported
that two additional DIS genes [PIROGI (PIR) and
GNARLED (GRL)] encode other components of this WAVE
regulatory complex. Together, these observations suggest that a WAVE complex
containing PIR, GRL and BRK1 is crucial for the activation of the plant Arp2/3
complex during trichome morphogenesis in Arabidopsis and during
pavement cell formation in maize. The formation of epidermal pavement cell
lobes in Arabidopsis involves both F-actin and microtubules, both of
which are controlled by ROP-GTPases. So how does ROP-GTPase control two
different cytoskeletal systems in the same cell? Zhenbiao Yang (University of
California, Riverside, CA, USA) described two ROP INTERACTING PROTEINs (RIC2
and RIC4), one of which controls microfilament assembly and the other
microtubule organization. The interaction of ROP with different proteins can
coordinate the activity of these two cytoskeletal systems.
Hormonal and environmental influences on development
Several speakers highlighted advances in our understanding of both hormonal
and environmental influences on plant development. In the case of hormones,
brassinosteroids and auxin were discussed at length. The brassinosteroid
signal transduction cascade was discussed by Jianming Li (University of
Michigan, Ann Arbor, MI, USA) who presented an impressive experimentally
supported model in which the receptor kinases BRASSINOSTEROID RECEPTOR1 (BRI1)
(Li and Chory, 1997) and
BRASSINOSTEROID INSENSITIVE 1-ASSOCIATED RECEPTOR KINASE 1 (BAK1) are present
in the plasma membrane as monomers until the steroid is present. The binding
of brassinosteroid promotes receptor dimerization and its consequent
activation. Activated BRI1 then phosphorylates TRANSTHYRETIN-LIKE (TTL), which
is similar to the vertebrate thyroid carrier protein
(Nam and Li, 2004
), and
inhibits BRASSINOSTEROID INSENSITIVE2 (BIN2), a GSK3 kinase
(Li and Nam, 2002
). As a
consequence, BIN2 cannot phosphorylate BRASSINAZOLE-RESISTANT1 (BZR1)
(Wang et al., 2002
) and
BRI1-EMS-SUPPRESSOR1 (BES2) (Yin et al.,
2002
; Zhao et al.,
2002
). In the non-phosphorylated state, BZR1 and BES2 are stable
and are transferred to the nucleus, where they are hypothesized to regulate
the transcription of brassinosteroid-responsive genes.
Auxin also controls development by regulating the stability of
transcription factors and other proteins. For example, auxin treatment induces
the degradation of AUX/IAA proteins through their ubiquitination
(Gray et al., 2001). When
present, AUX/IAA proteins bind to AUXIN RESPONSE FACTOR (ARF) proteins and
prevent the ARFs from regulating the transcription of auxin response genes. In
the presence of auxin, AUX/IAA proteins are degraded and ARF proteins promote
or repress transcription. Details of how the AUX/IAA proteins feed into the
ubiquitin pathway in response to auxin have emerged over the past few years
(Kepinski and Leyser, 2002
).
Essentially, auxin stimulates an interaction between the AUX/IAA proteins and
a ubiquitin protein ligase (E3) SCFTIR1. Mark Estelle (Indiana
University, Bloomington, IN, USA) described recent data to show that at least
three transport inhibitor response 1 (TIR1)-related proteins
are involved in auxin signalling as part of E3 ligase complexes. Furthermore,
on the basis of assays in a cell-free system, he indicated that auxin
interacts directly with the SCFTIR complex or with a tightly
associated protein. If true, the hunt for at least one type of auxin receptor
may soon be over.
With respect to environmental influences on development, both temperature
and light were discussed. Rick Amasino (University of Wisconsin, Madison, WI,
USA) discussed temperature effects in the context of vernalization
requirements for flowering. Whilst rapid-cycling Arabidopsis has no
vernalization requirement, winter annuals must be exposed to the cold to gain
competence to respond to day length in spring. Cold treatment represses
activity of FLOWERING LOCUS C (FLC), a repressor of flowering
(Michaels and Amasino, 1999;
Sheldon et al., 1999
), and
this repression is mediated by two distinct methylation events and one
deacetylation event (Bastow et al.,
2004
; Sung and Amasino,
2004
). The epigenetic nature of these modifications permits the
memory of winter to be perpetuated into spring.
The effect of light was highlighted in three talks. Rob McClung (Dartmouth
College, Hanover, NH, USA) and Julin Maloof (University of California, Davis,
CA, USA) demonstrated how quantitative trait loci (QTL) analysis can be used
to identify genomic regions responsible for natural variation in response to
light (Michael et al., 2003;
Borevitz et al., 2002
;
Maloof et al., 2001
). Xing
Wang Deng (Yale University, New Haven, CT, USA) went on to report that
function had now been assigned to all of the loci that were initially
identified in genetic screens for de-etiolated (DET) and CONSTITUTIVELY
PHOTOMORPHOGENIC (COP) mutants (Chory,
1993
; Wei and Deng,
1996
). In particular, he showed that in addition to the COP9
signalosome (Chamovitz et al.,
1996
) and the COP1 complex
(Saijo et al., 2003
;
Seo et al., 2003
), another
multisubunit complex acts to degrade proteins upon exposure to light (see
Fig. 3). COP10 interacts with
DEETIOLATED1 (DET1) and DDB1 to form a complex that enhances
ubiquitin-conjugating enzyme E2 activity
(Suzuki et al., 2002
;
Yanagawa et al., 2004
). These
observations suggest that the ability to etiolate evolved as a consequence of
gaining mechanisms to specifically degrade proteins involved in
photomorphogenesis.
|
The modification of developmental mechanisms to mediate evolutionary change
was discussed in four talks. Jane Langdale (University of Oxford, Oxford, UK)
demonstrated that the genetic pathway required for the switch from
indeterminate shoot to determinate leaf growth was conserved in two plant
lineages that diverged over 400 million years ago. Kirsten Bomblies
(University of Wisconsin, Madison, WI, USA) showed that one of the QTL
corresponding to morphological change in ear phyllotaxy from teosinte to maize
maps to one of two maize LFY genes. Although zfl1 and zfl2
act redundantly in the floral transition
(Bomblies et al., 2003), by
comparing single mutations in different maize backgrounds, Bomblies was able
to distinguish gene-specific functions. Consistent with the idea that
zfl2 underlies the previously identified QTL, ear number and ear rank
are associated more strongly with zfl2 than with zfl1. David
Baum (University of Wisconsin, Madison, WI, USA) also discussed the role of
LFY in morphological change. He used a transgenic approach to determine
whether differences in LFY gene function facilitate a conversion from the
ancestral inflorescence flowering phenotype to a rosette-flowering phenotype.
Using LFY promoters from rosette-flowering species, he demonstrated that at
least partial rosette phenotypes could be induced in transgenic
Arabidopsis. However, conversion was not complete and differed
depending on which donor species was used
(Yoon and Baum, 2004
). Vivian
Irish (Yale University, New Haven, CT, USA) went on to discuss the ancestral
and derived roles of the floral homeotic genes APETALA3
(AP3) and PISTILLATA. In Arabidopsis, the two genes
act together to define petals and stamens. Irish has previously reported that
the ancestral (paleo) AP3 gene found in basal eudicots differs from
the two genes (euAP3 and TM6) found in core eudicots
(Kramer et al., 1998
). As
Arabidopsis does not have a copy of TM6, gene function has
not previously been ascribed. Using tomato, Irish showed that whereas
euAP3 regulates both petal and stamen formation, TM6 only
regulates stamen development. This suggests paleoAP3 function was
restricted to stamen development.
Conclusions
As the meeting concluded, it was apparent that things had moved quickly over the past 2 years and that we are achieving an ever more in-depth understanding of developmental mechanisms in Arabidopsis. Over the next 2 years, we expect that the discoveries made in this plant will be translated to other organisms, providing insight into the mechanism by which morphological diversity has been generated in land plants over the past 450 million years.
ACKNOWLEDGMENTS
We apologise to speakers whose results we could not include because of space constraints. We thank M. Yanofsky for Fig. 1, M. Pernas-Ochoa and P. Linstead for Fig. 2, and X. W. Deng for Fig. 3.
REFERENCES
Baskin, T. I., Beemster, G. T., Judy-March, J. E. and Marga,
F. (2004). Disorganization of cortical microtubules
stimulates tangential expansion and reduces the uniformity of cellulose
microfibril alignment among cells in the root of Arabidopsis. Plant
Physiol. 135,2279
-2290.
Bastow, R., Mylne, J. S., Lister, C., Lippman, Z., Martienssen, R. A. and Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427,164 -167.[CrossRef][Medline]
Bergmann, D. C., Lukowitz, W. and Somerville, C. R.
(2004). Stomatal development and pattern controlled by a MAPKK
kinase. Science 304,1494
-1497.
Bomblies, K., Wang, R. L., Ambrose, B. A., Schmidt, R. J.,
Meeley, R. B. and Doebley, J. (2003). Duplicate
FLORICAULA/LEAFY homologs zfl1 and zfl2 control
inflorescence architecture and flower patterning in maize.
Development 130,2385
-2395.
Borevitz, J. O., Maloof, J. N., Lutes, J., Dabi, T., Redfern, J.
L., Trainer, G. T., Werner, J. D., Asami, T., Berry, C. C., Weigel, D. et
al. (2002). Quantitative trait loci controlling light and
hormone response in two accessions of Arabidopsis thaliana.Genetics 160,683
-696.
Carles, C. C. and Fletcher, J. C. (2003). Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci. 8,394 -401.[CrossRef][Medline]
Carles, C. C., Lertpiriyapong, K., Revelle, K. and Fletcher, J.
C. (2004). The ULTRAPETALA1 gene functions early in
Arabidopsis development to restrict shoot apical meristem activity and acts
through WUSCHEL to regulate floral meristem determinacy.
Genetics 167,1893
-1903.
Chamovitz, D. A., Wei, N., Osterlund, M. T., von Arnim, A. G., Staub, J. M., Matsui, M. and Deng, X.-W. (1996). The COP9 complex, a novel multisubunit nuclear regulator involved in light control of a plant developmental switch. Cell 86,115 -121.[Medline]
Chory, J. (1993). Out of darkness: mutants reveal pathways controlling light-regulated development in plants. Trends Genet. 9,167 -172.[CrossRef][Medline]
Frank, M. J. and Smith, L. G. (2002). A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr. Biol. 12,849 -853.[CrossRef][Medline]
Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A. and Jurgens, G. (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112,219 -230.[Medline]
Gray, W. M., Kepinski, S., Rouse, D., Leyser, O. and Estelle, M. (2001). Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 414,271 -276.[CrossRef][Medline]
Heidstra, R., Welch, D. and Scheres, B. (2004).
Mosaic analyses using marked activation and deletion clones dissect
Arabidopsis SCARECROW action in asymmetric cell division. Genes
Dev. 18,1964
-1969.
Huck, N., Moore, J. M., Federer, M. and Grossniklaus, U.
(2003). The Arabidopsis mutant feronia disrupts the
female gametophytic control of pollen tube reception.
Development 130,2149
-2159.
Kepinski, S. and Leyser, O. (2002).
Ubiquitination and auxin signaling: a degrading story. Plant
Cell 14,S81
-S95.
Kramer, E. M., Dorit, R. L. and Irish, V. F.
(1998). Molecular evolution of genes controlling petal and stamen
development: duplication and divergence within the APETALA3 and
PISTILLATA MADS-box gene lineages. Genetics
149,765
-783.
Lenhard, M., Bohnert, A., Jurgens, G. and Laux, T. (2001). Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105,805 -814.[CrossRef][Medline]
Li, J. and Chory, J. (1997). A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90,929 -938.[Medline]
Li, J. and Nam, K. H. (2002). Regulation of
brassinosteroid signaling by a GSK3/SHAGGY-Like kinase.
Science 295,1299
-1301.
Liljegren, S. J., Roeder, A. H., Kempin, S. A., Gremski, K., Ostergaard, L., Guimil, S., Reyes, D. K. and Yanofsky, M. F. (2004). Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116,843 -853.[CrossRef][Medline]
Lippman, Z., Gendrel, A. V., Black, M., Vaughn, M. W., Dedhia, N., McCombie, W. R., Lavine, K., Mittal, V., May, B., Kasschau, K. D. et al. (2004). Role of transposable elements in heterochromatin and epigenetic control. Nature 430,471 -476.[CrossRef][Medline]
Lohmann, J. U., Hong, R. L., Hobe, M., Busch, M. A., Parcy, F., Simon, R. and Weigel, D. (2001). A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105,793 -803.[CrossRef][Medline]
Maloof, J. N., Borevitz, J. O., Dabi, T., Lutes, J., Nehring, R. B., Redfern, J. L., Trainer, G. T., Wilson, J. M., Asami, T., Berry, C. C. et al. (2001). Natural variation in light sensitivity of Arabidopsis. Nat. Genet. 29,441 -446.[CrossRef][Medline]
Michael, T. P., Salome, P. A., Yu, H. J., Spencer, T. R., Sharp,
E. L., McPeek, M. A., Alonso, J. M., Ecker, J. R. and McClung, C. R.
(2003). Enhanced fitness conferred by naturally occurring
variation in the circadian clock. Science
302,1049
-1053.
Michaels, S. D. and Amasino, R. M. (1999).
FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a
repressor of flowering. Plant Cell
11,949
-956.
Motose, H., Sugiyama, M. and Fukuda, H. (2004). A proteoglycan mediates inductive interaction during plant vascular development. Nature 429,873 -878.[CrossRef][Medline]
Nadeau, J. A. and Sack, F. D. (2002). Control
of stomatal distribution on the Arabidopsis leaf surface.
Science 296,1697
-1700.
Nam, K. H. and Li, J. (2004). The Arabidopsis
transthyretin-like protein is a potential substrate of
BRASSINOSTEROID-INSENSITIVE 1. Plant Cell
16,2406
-2417.
Reddy, G. V., Heisler, M. G., Ehrhardt, D. W. and Meyerowitz, E.
M. (2004). Real-time lineage analysis reveals oriented cell
divisions associated with morphogenesis at the shoot apex of Arabidopsis
thaliana. Development 131,4225
-4237.
Roeder, A. H., Ferrandiz, C. and Yanofsky, M. F. (2003). The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr. Biol. 13,1630 -1635.[CrossRef][Medline]
Saijo, Y., Sullivan, J. A., Wang, H., Yang, J., Shen, Y., Rubio,
V., Ma, L., Hoecker, U. and Deng, X. W. (2003). The COP1-SPA1
interaction defines a critical step in phytochrome A-mediated regulation of
HY5 activity. Genes Dev.
17,2642
-2647.
Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K.,
Beermann, A., Thumfahrt, J., Jurgens, G. and Hulskamp, M.
(2002). TRIPTYCHON and CAPRICE mediate lateral inhibition during
trichome and root hair patterning in Arabidopsis. EMBO
J. 21,5036
-5046.
Seo, H. S., Yang, J. Y., Ishikawa, M., Bolle, C., Ballesteros, M. L. and Chua, N. H. (2003). LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423,995 -999.[CrossRef]
Sheldon, C. C., Burn, J. E., Perez, P. P., Metzger, J., Edwards,
J. A., Peacock, W. J. and Dennis, E. S. (1999). The
FLC MADS box gene: a repressor of flowering in Arabidopsis regulated
by vernalization and methylation. Plant Cell
11,445
-548.
Shuai, B., Reynaga-Pena, C. G. and Springer, P. S.
(2002). The LATERAL ORGAN BOUNDARIES gene defines a
novel, plant-specific gene family. Plant Physiol.
129,747
-761.
Sieber, P., Gheyselinck, J., Gross-Hardt, R., Laux, T., Grossniklaus, U. and Schneitz, K. (2004). Pattern formation during early ovule development in Arabidopsis thaliana. Dev. Biol. 273,321 -334.[CrossRef][Medline]
Sung, S. and Amasino, R. M. (2004). Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427,159 -164.[CrossRef][Medline]
Suzuki, G., Yanagawa, Y., Kwok, S. F., Matsui, M. and Deng, X.
W. (2002). Arabidopsis COP10 is a ubiquitin-conjugating
enzyme variant that acts together with COP1 and the COP9 signalosome in
repressing photomorphogenesis. Genes Dev.
16,554
-559.
Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y.,
Tachibana, T., Goto, K., Marks, M. D., Shimura, Y. and Okada, K.
(2002). Role of a positive regulator of root hair development,
CAPRICE, in Arabidopsis root epidermal cell differentiation.
Development 129,5409
-5419.
Wang, Z. Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T. et al. (2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2,505 -513.[Medline]
Wei, N. and Deng, X.-W. (1996). The role of
COP/DET/FUS genes in light control of Arabidopsis seedling development.
Plant Physiol. 112,871
-878.
Yanagawa, Y., Sullivan, J. A., Komatsu, S., Gusmaroli, G.,
Suzuki, G., Yin, J., Ishibashi, T., Saijo, Y., Rubio, V., Kimura, S. et
al. (2004). Arabidopsis COP10 forms a complex with DDB1 and
DET1 in vivo and enhances the activity of ubiquitin conjugating enzymes.
Genes Dev. 18,2172
-2181.
Yin, Y., Wang, Z. Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T. and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109,181 -191.[Medline]
Yoon, H. S. and Baum, D. A. (2004). Transgenic
study of parallelism in plant morphological evolution. Proc. Natl.
Acad. Sci. USA 101,6524
-6529.
Zhao, J., Peng, P., Schmitz, R. J., Decker, A. D., Tax, F. E.
and Li, J. (2002). Two putative BIN2 substrates are nuclear
components of brassinosteroid signaling. Plant
Physiol. 130,1221
-1229.