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First published online 1 November 2006
doi: 10.1242/dev.02676
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Meeting Review |
Salk Institute for Biological Studies, Plant Molecular and Cellular Biology, 10010 North Torrey Pines Road, La Jolla, California 92037, USA.
e-mail: long{at}salk.edu
SUMMARY
In August 2006, plant biologists gathered at the FASEB `Mechanisms in Plant Development' meeting in Vermont, which was organized by Laurie Smith and Ueli Grossniklaus. A variety of plant developmental mechanisms were presented at this meeting and, although many talks focused on Arabidopsis thaliana as a primary model in which to study plant development, research in maize, tomato, Chlamydomonas and other plants also provided insight into various topics, such as cell-type specification, small RNA biosynthesis and action, hormone perception and transport, and cell and organ size.
From the beginning: fertilization and embryonic development
Like animals, plant embryos develop from the fertilization of an egg cell
by a sperm. Unlike animals, the sperm is delivered to the egg from the tip of
a growing pollen tube. To reach the egg, the pollen tube must first germinate
and then seek out the egg cell by growing through the tip of the female organ
(the gynecium) to find the ovule that houses the egg. This seeking process
involves a complex interplay between the pollen tube and the female
reproductive tissues, with signals coming from both sides. The nature of these
signals and the ability of a plant to distinguish its own pollen is still
largely unknown. June Nasrallah (Cornell University, Ithaca, NY, USA)
presented her laboratory's work on the mechanisms of self-incompatibility
(SI). Although Arabidopsis thaliana is self-fertile, many plant
species can recognize their own pollen and prevent pollen-tube development.
One such system uses signaling from a receptor kinase expressed at the tip of
the gynecium (the stigmatic tissue) that recognizes a cysteine-rich ligand
that is localized to the pollen coat. These two proteins (which are encoded by
two closely-linked genes that are referred to collectively as the S
locus) co-evolve in such a way that the pollen ligand binds and activates only
the receptor kinase encoded in the same S-locus haplotype,
consequently triggering the arrest of self pollination. Although this
ligand/receptor pair was discovered several years ago, the signal transduction
events downstream of the receptor are poorly understood
(Kusaba et al., 2001
;
Nasrallah et al., 1988). June
Nasrallah described an elegant system that can be used to investigate this
process further. Her group has recreated the SI system from A.
lyrata, a species that exhibits SI, in A. thaliana by creating
transgenic lines that express the A. lyrata S locus
(Nasrallah et al., 2002).
These plants are now amenable to genetics, and several mutants have been
isolated at unique loci that show varying degrees of self-fertility.
As the pollen tube invades the stigma, it must travel through the gynecium
and seek out the ovules. Tetsuya Higashiyama (University of Tokyo, Tokyo,
Japan) described an in vitro system to study this process using Torenia
fournieri, a plant with exserted embryo sacs
(Higashiyama et al., 1998).
Using this system, his group discovered that the pollen tube must first pass
through the maternal tissue in order to gain competence to seek out the
ovules. A 70 kDa protein derived from the ovule [activation molecule for
response-capability (AMOR)] is also necessary for the pollen tube to gain
competence. Once competent, the pollen tube can then respond to a
species-specific attractant produced from the synergid cell to find the ovule
(Higashiyama, 2002;
Higashiyama et al., 2006).
Higashiyama's group is currently in the process of collecting over 65 million
Torenia ovules in order to identify the AMOR protein.
After the egg is fertilized, the diploid embryo starts to develop. Polarity
becomes apparent at the first cell division, which is asymmetric - giving rise
to a small apical cell and a larger basal cell. The apical cell will give rise
to most of the resulting embryo, whereas the basal cell will give rise to a
nutritive structure (the suspensor) and a portion of the root meristem. Martin
Bayer (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA) described
his work on SHORT SUSPENSOR (SSP), which helps to specify the extraembryonic
suspensor. ssp mutants have reduced, or no, suspensor growth and can
be rescued by a constitutively active form of the MAPKK kinase protein YODA
(YDA) (Lukowitz et al., 2004).
yda mutants resemble ssp mutants, and YDA is probably
downstream of SSP in suspensor specification. Bayer then showed that the
ssp phenotype is observed only when the mutant allele is derived from
the pollen, regardless of the genotype of the egg cell. This novel mode of
inheritance may therefore shed light on a new mechanism of cell-type
specification in the embryo. Dolf Weijers (Wageningen University, Wageningen,
The Netherlands) described a mechanism that occurs later in embryogenesis:
root stem cell specification. Previous work has shown that the auxin response
factor MONOPTEROS (MP, also known as ARF5 and IAA24) is necessary for root
apical meristem formation and is antagonized by the AUX/IAA protein BODENLOS
(BDL, also known as IAA12 - Arabidopsis thaliana Database)
(Hamann et al., 2002;
Hardtke and Berleth, 1998). The
mystery was that neither of these proteins are found in the cells where the
first defects in cell division are observed (see
Fig. 1)
(Weijers et al., 2006). By
analyzing microarray data sets from mp, bdl and wild-type seedlings,
Weijers and colleagues have studied a set of transcription factors [referred
to as targets of MONOPTEROS (TOM)] that are expressed in the same cells as MP
in embryos and require MP for their expression. Weijers reported that one of
these transcription factors, TOM3, may explain the noncell autonomous action
of MP, as TOM3 appears to move into the cells directly below those that
express MP - the same cells that undergo aberrant cell divisions in a
mp mutant.
Cell-type specification in the epidermis
A question common to both plant and animal development is: how does a cell
become different from its neighbors in a seemingly homogenous context? The
development of root hairs from the root epidermis, and of trichomes and
stomates from the leaf epidermis, are excellent systems in which to study this
question. John Schiefelbein (University of Michigan, Ann Arbor, MI, USA) drew
on the work from his laboratory and from several others to describe how root
hairs form. The epidermis of the root contains both hair cells and non-hair
cells. Positional cues are thought to arise from the underlying cortex, as
hair cells sit above two cortex cells (the H position) and non-hair cells sit
above only one (the N position) (Galway et
al., 1994). Although several proteins are required for N and H
cell specification, many of them can move between cells, resulting in nearly
identical complexes in all epidermal cells. Schiefelbein presented on how the
negative regulation of these complexes ultimately defines the cell type. A
major regulator of this process is a receptor-like kinase called SCRAMBLED
(SCM) that probably receives a signal from the cortex cells and negatively
regulates the transcription factor WEREWOLF (WER) in the H position
(Kwak et al., 2005;
Lee and Schiefelbein, 1999).
This tips the balance of the transcriptional complexes and allows the root
hair to form. Many of these same regulators are involved in trichome
initiation and spatial patterning in the leaf epidermis. Martin Hülskamp
(University of Cologne, Cologne, Germany) described how the TRANSPARENT TESTA
GLABRA 1 (TTG1) protein is initially found in all cells, but then moves and is
concentrated in the trichome cells
(Schnittger et al., 1999).
Using a TTG1/yellow florescent protein fusion, his group was able to visualize
this movement, and he showed that TTG1 expressed in the subepdermis could
rescue the ttg mutant. Finally, Dominique Bergman (Stanford
University, Palo Alto, CA, USA) discussed the role of two related basic
helix-loop-helix proteins [SPEECHLESS (SPCH) and FAMA] in stomate formation in
the leaf epidermis (Fig. 2).
Although related, these two proteins act at distinct steps in stomatal
patterning, and FAMA cannot rescue spch when under the control of the
SPCH promoter. Ongoing research should reveal which other proteins
regulate the specific actions of these two genes.
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The hormone auxin has been implicated in almost all aspects of plant growth
and development. In the past several years, new tools and technologies have
allowed plant biologists to investigate how auxin may be involved in the
particular developmental process that they study. The discovery of auxin
biosynthetic genes, the cloning of the PINFORMED (PIN) family of auxin efflux
carriers and the creation of an auxin-responsive reporter (DR5) has advanced
the field considerably, and these new reagents have been used extensively to
answer specific developmental questions
(Galweiler et al., 1998;
Muller et al., 1998;
Palme and Galweiler, 1999;
Ulmasov et al., 1997;
Zhao et al., 2001). Three
groups presented work on computer models, based on the flow and localized
concentration of auxin, that can simulate a growing shoot apical meristem
(SAM) and the pattern (or phyllotaxy) of emerging primordia. Elliot Meyerowitz
(California Institute of Technology, Pasadena, CA, USA) presented a model from
his laboratory based on live imaging of PIN1-GFP and other cell type-specific
reporters (Heisler et al.,
2005). Drawing from data on PIN1 localization, PIN1 concentration,
and PIN1 trafficking between the membrane and internal cellular compartments,
Meyerowitz and his collaborators generated a model of the SAM that produced
primordia in a phyllotactic pattern
(Jonsson et al., 2006). The
model also accurately reproduced the changes in PIN1 subcellular localization
and concentration that occur as primordia are established. Cris Kuhlemeier
(University of Bern, Bern, Switzerland) and his collaborator Przemyslaw
Prusinkiewicz (University of Calgary, Calgary, Canada), presented their own
computer model, which took into account cell division patterns observed in
live meristems, the localization of PIN1 and the pattern of a DR5-GFP
reporter (Smith et al., 2006).
This model could reproduce the switch from distichous to spiral phyllotaxy and
mimic defects observed in live meristems, such as the loss of PIN1. These
`computable' plant meristems should allow researchers to predict how live
meristems will react to perturbations introduced into the computer model.
Michael Sauer (University of Tubingen, Tubingen, Germany) showed data
indicating that the flow of auxin either towards or away from an auxin source
may be tissue dependent. When roots were exposed to exogenous auxin, the PIN2
protein (located in the outer cell layers of the root) relocalized to the
plasma membrane nearest the auxin source, whereas the PIN1 protein (expressed
in the center of the root) relocalized from the bottom of cells to the top,
pointing away from the auxin source. Angela Hay (University of Oxford, Oxford,
UK) discussed how auxin gradients control leaf initiation and shape. By
combining mutations in genes known to affect leaf shape. such as
asymmetric leaves 1 (as1), and those involved in auxin
transport and perception, such as pin1 and auxin resistant 1
(axr1), she showed that these proteins all function to keep the
meristem-specific transcription factor BREVIPEDICELLUS (BP,
also known as KNAT1 - Arabidopsis thaliana Database) out of leaves
(Hay et al., 2006). John
Bowman (Monash University, Melbourne, Australia) presented data that
implicated auxin flow in the outgrowth of ectopic organs as well. By combining
mutations in a related family of transcription factors that play a role in
leaf polarity [KANADI1 (KAN1, also known as KAN -
Arabidopsis thaliana Database), KAN2 and KAN4 (also
known as ABBERANT TESTA SHAPEI; ATS)], the resulting plants produced
ectopic leaves from the seedling stem
(Emery et al., 2003;
McAbee et al., 2006). PIN1-GFP
was ectopically expressed in these outgrowths and appeared to be transporting
auxin to the tips, just as in normal leaf development. Although auxin flow has
been well researched, the timing and location of auxin production has remained
largely unknown. Yunde Zhao (University of California San Diego, San Diego,
CA, USA) presented his work on a family of flavin mono-oxygenases (the YUCCA
proteins) that are the possible rate-limiting step in tryptophan-dependent
auxin biosynthesis (Zhao et al.,
2001). Zhao showed that many of these genes, initially identified
by their overexpression phenotypes, are expressed in unique patterns, and
their loss-of-function phenotypes indicate that the site of auxin production
is as important as where it is transported to
(Cheng et al., 2006).
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How does a cell know what size it should be, and how is the overall size
and shape of an organ or organism determined? Plants provide an excellent
system to study these questions, as tissue-specific genetic screens can be
performed. Domestication and recent selections have also resulted in closely
related cultivars of crop plants that differ in organ size and shape. Esther
van der Knaap (Ohio State University, Wooster, OH, USA) presented work that
identified the tomato sun locus, which controls whether fruit shape
is elongated rather than being typically round
(van der Knaap et al., 2004).
sun, however, does not control fruit size, indicating that the gene
underlying this locus controls organ shape via a redistribution of fruit mass
(Fig. 3). High-resolution fine
mapping and sequencing of the sun locus by van der Knaap and
colleagues has revealed that a segmental duplication causes the altered fruit
shape. Two genes in this duplicated region are differentially expressed, and
are therefore probably responsible for the fruit-shape phenotypes. These
findings provide a starting point for identifying other fruit-shape genes in
plants. Michael Lenhard (University of Freiburg, Freiburg, Germany) reported a
mutant called kluh (klu), which formed smaller floral organs
because of a decreased number of cell divisions. KLU encodes a
cytochrome P450, which, when overexpressed in petals, increases their size.
Although the substrate of KLU is currently unknown, it may generate a non-cell
autonomous signal for growth, as organs that do not express KLU, but
are near those that do, can also grow larger. James Umen (Salk Institute for
Biological Studies, La Jolla, CA, USA) introduced the audience to the utility
of Chlamydomonas reinhardtii as a system in which to study cell-size
specification. Chlamydomonas mother-cell sizes can vary widely, but
they divide to produce daughter cells with a similar size distribution over a
population. Therefore the number of cell divisions a mother cell undergoes is
controlled by a sizing mechanism, and several mutants defective in this
process were presented. One mutant, mat3, produces abnormally small
daughter cells, and the MAT3 locus was shown to encode a
retinoblastoma (RB)-related protein (Umen
and Goodenough, 2001). Screens for suppressors of mat3
identified alleles of DP1- and E2F-related proteins - conserved targets of
RB-related proteins. On their own, these two mutants result in larger daughter
cells than normal. With these and other mutants in hand, a genetic and
biochemical framework is emerging for how Chlamydomonas and,
probably, other organisms regulate cell size.
The roles of small RNAs in development
Plants continue to be a rich source of information for how small RNAs are
generated and regulate the function of other genes. Small interfering RNAs
(siRNAs), micro RNAs (miRNAs) and trans-acting siRNAs (ta-siRNAs) play diverse
roles in plants, including in viral defense and cell-type specification, and
are produced through the action of four dicer-like (DCL) proteins with
specialized functions (Bouche et al.,
2006; Gasciolli et al.,
2005; Voinnet,
2002). Olivier Voinnet (CNRS, Strasbourg, France) presented the
results of large forward and reverse genetic screens designed to identify new
factors that play a role in small RNA activities and biogenesis. In one
screen, a miRNA sensor was constructed that contained a ubiquitously expressed
form of GFP that had a miRNA binding site at the 3' end. In wild-type
plants, the reporter was only active in cells that did not express the miRNA.
Mutants were then isolated that showed increased accumulation of the sensor
and fell into two classes. In class-1 mutants, the sensor RNA and protein were
increased, whereas in class- 2 mutants, the sensor RNA levels did not increase
significantly, but protein levels were increased. This indicates that there
may be separable pathways present for transcript cleavage and translational
inhibition. Scott Poethig (University of Pennsylvania, Philadelphia, PA, USA)
discussed the role of miRNAs and ta-siRNAs in juvenile-to-adult transition in
plants. In Arabidopsis, this phase change is manifested by increased
numbers of abaxial (or ventral) trichomes, as more adult leaves are produced.
Mutations in ZIPPY [ZIP, also known as ARGONAUTE7
(AGO7) Arabidopsis thaliana Database] had previously been
shown to produce precocious trichomes, and a suppressor screen of zip
yielded mutations in two genes, ETTIN (ETT) and AUXIN
RESPONSE FACTOR 4 (ARF4)
(Hunter et al., 2003).
ETT and ARF4 mRNA accumulation is controlled by a ta-siRNA
(tasiR-ARF) derived from the TAS3 locus, and Poethig showed
that zip mutants had an increased level of ETT and
ARF4, and a reduced level of tasiR-ARF
(Hunter et al., 2006). Marja
Timmermans (Cold Spring Harbor Laboratories, Cold Spring Harbor, NY, USA)
discussed the role of miRNAs and ta-siRNAs on the correct adaxial/abaxial
(dorsal/ventral) patterning of the leaf. miR166 controls the
accumulation of the class III homeodomain leucine-zipper gene rolled
leaf1 (rld1), and Timmermans showed that miR166 is
abaxially expressed in a pattern complementary to rld1 and that it
appears to accumulate in a gradient
(Juarez et al., 2004). A
second gene, leafbladeless1 (lbl1), is necessary for adaxial
fate and for the production of ta-siRNA2142
(Timmermans et al., 1998).
lbl1 mutants in maize misexpress miR166 throughout the leaf
primordial, indicating that leaf polarity in maize is under the control of two
opposing small regulatory RNAs. Timmermans also showed that the ta-siRNA
pathway is active in the SAM, and postulated that ta-siRNA2142, like
other DCL4-dependent siRNAs, may act as a mobile signal to set up leaf
polarity by restricting miR166 expression. Finally, Yuval Eshed
(Weizmann Institute of Science, Rehovot, Israel) showed the power of using
synthetic miRNAs to overcome genetic redundancy in plants
(Alvarez et al., 2006;
Schwab et al., 2006). By using
synthetic miRNAs, Eshed reduced the expression of nine genes from two
different families involved in growth and uncovered phenotypes not observed in
any single-mutant line. These sorts of experiments should rapidly advance
research on closely related gene families and uncover roles that are difficult
to discern through classical genetics.
Conclusions
In the 2 years since the last FASEB conference, a remarkable amount of progress has been made in our understanding of plant development. The roles of hormones, small RNAs and moving transcription factors have been carefully dissected, and problems with genetic redundancy have been tackled. It has become clear that, work in many plant model organisms strengthens the field and provides insight into not only plant developmental mechanisms, but also into questions that arise in the development of all organisms.
ACKNOWLEDGMENTS
I apologize to the many speakers whose results I could not include due to space constraints. I would like to thank H. Szemenyei and M. Hannon for sharing their notes on the meeting.
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