Download The mating game: pollination and fertilization in flowering plants

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The mating game: pollination and fertilization in flowering plants
Laura K Wilhelmi and Daphne Preuss*
Recent work has revealed signaling molecules that control
pollination, including small peptides that mediate pollen
recognition and glycoproteins that support pollen tube growth.
The polarized growth of pollen tubes requires a calciummediated signal cascade, and cues derived from the haploid
and diploid ovule cells guide pollen tubes to the eggs.
Addresses
Department of Molecular Genetics and Cell Biology, University of
Chicago, Chicago, IL 60637, USA
*e-mail: [email protected]
Current Opinion in Plant Biology 1999, 2:18–22
http://biomednet.com/elecref/1369526600200018
© Elsevier Science Ltd ISSN 1369-5266
Abbreviations
AGP
arabinogalactan protein
PCP
pollen coat protein
SI
self-incompatibility
SLG
S-locus glycoprotein
SRK
S-locus receptor kinase
TTS
transmitting tissue-specific glycoprotein
Introduction
Plants, like other organisms, invest enormous resources to
find the most suitable mate. Although regulation of flowering time and insect pollination help ensure that pollen
arrives at an appropriate flower, recent studies reveal the
importance of communication between male and female
cells in controlling plant mating. Cell signaling regulates
recognition of pollen by the stigma, migration of pollen
tubes through the pistil, delivery of sperm to the ovules,
and finally, co-ordinated development of the zygote,
endosperm, seed, and fruit (Figure 1). In this review, we
summarize recent insights into the mechanisms that control pollination and fertilization.
for SI: SLG encodes an extracellular glycoprotein and SRK
encodes a receptor kinase localized to the plasma membrane [1•,2]. Mutations in either gene result in
self-compatibility, as do transgenic constructs that reduce
their expression levels [1•,3,4].
How do SLG and SRK enable plants to reject incompatible pollen? Current models propose an interaction with a
pollen-specific S locus gene, initiating a phosphorylation
cascade that results in pollen rejection. Although the SI
response is often accompanied by a rapid and localized
production of β-1,3 glucan, or callose, in the stigma, surprising recent studies demonstrate that callose is not
required for SI [5]. In addition, though adhesion of pollen
to the stigma is species specific [6], pollen binding affinity
does not correlate with SI [7•].
One approach used to identify pollen-specific SI components relied on characterizing the structure of the S locus
itself. This resulted in the identification of one promising
gene, SLA (S-locus anther), that is disrupted by a retrotransposon insertion in several self-compatible mutants
[8]. Linkage of this SLA sequence defect with a mutant
phenotype initially led to proposals that SLA mediates SI
in pollen [8]. Subsequent investigations, however, showed
that many wild-type strains have a similar insertion within
SLA, indicating that SLA is not necessary for a functional
SI response [9]. Nonetheless, exploring the S-locus for
other genes active in SI remains a valuable approach.
Stigma cells use a variety of mechanisms to limit the success of inappropriate pollen. On dry stigmas, the transfer of
water and nutrients to pollen grains is also controlled —
foreign pollen often remains dehydrated. The invasion of
pollen tubes into stigma cells is regulated in many species,
including those with wet stigmas. These early checkpoints
serve to block pollination before pollen consumes valuable
resources within the pistil.
Purification of pollen components that bind to SLG and
SRK led to the exciting discovery that peptide signals may
regulate SI [10••]. The extracellular pollen coating contains several proteins, including a large family of
cysteine-rich peptides (pollen coat proteins or PCPs)
released onto the stigma surface upon pollination
[10••,11,12•]. Purified fractions containing these peptides
bind to SLG, although their function remains undefined.
Curiously, the PCP genes neither map to the S locus, nor
do their products bind to SLG in an allele-specific manner.
Because genetic evidence suggests the male determinant
of SI ought to be polymorphic and within the S-locus, a
search for additional SLG-binding components may prove
fruitful. Nonetheless, the strong sequence similarity
between the PCPs and defensins, plant polypeptides with
antifungal activity [12•], presents an intriguing possibility
for peptide signaling during pollination.
In self-incompatible Brassica species, self fertilization is
inhibited at the stigma surface. A genetic and molecular
characterization of self-incompatibility (SI) defined a complex polymorphic locus, which contains both male and
female-specific genes [1•]. Recent studies conclusively
demonstrate that two stigma-specific genes are necessary
Immediately after pollination, compatible pollen grains
absorb water and begin to form a pollen tube that invades
the stigma. Whether stigma surfaces are wet or dry, lipids
have been implicated in mediating pollen hydration
[13,14,15•]. Mutations that eliminate the lipid-rich exudate of wet Nicotiana stigmas result in female sterility, and
Pollen recognition at the stigma surface — the
first line of defense
The mating game Wilhelmi and Preuss
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Figure 1
Anatomy of fertilization in flowering plants.
(a) Representation of a typical pistil, consisting
of a stigma, style, and ovary. Pollen grains land
on the stigma surface and germinate pollen
tubes which grow into the style through a
central transmitting tract which contains the
ovules. (b) Desiccated pollen grains land on
the stigma cell surface; once compatible
grains are hydrated, they are able to produce a
pollen tube that carry two sperm to each ovule.
sc, stigma cell; dp, desiccated pollen grain;
hp, hydrated pollen grain; pt, pollen tube. (c)
After exiting the style, pollen tubes enter the
ovary, where they approach individual ovules.
Each ovule contains a haploid female
gametophyte, consisting of the egg and
central cell nuclei (cn), that is surrounded by
diploid integument tissue (it). The tubes grow
up the funiculus and enter the micropyle, an
opening in the ovule that allows the tube
access to the female gametophyte. Fertilization
of the egg by one sperm cell forms the zygote,
and fusion of a second sperm cell with the two
central cell nuclei forms the endosperm. fu,
funiculus; pt, pollen tube.
(a)
(b)
Stigma
dp
Pollen
grain
Growing
pollen
tube
sc
hp
pt
Style
Transmitting
tract
(c)
it
cn
Ovary
Ovule
egg
fu
pt
Current Opinion in Plant Biology
addition of lipids to the surface of these stigmas restores
fertility [15•,16]. In plants with dry stigmas, long-chain
lipids in the pollen coating are required for hydration
[13,14]; delivery of those lipids may require oleosins — oil
binding proteins that solubilize lipid droplets [17–19].
Though the application of short-chain lipids can cause
pollen hydration even on dry stigmas [15•], it remains to be
demonstrated if lipids alone can trigger a normal series of
hydration events. Lipids may serve to form a water-tight
seal between pollen and the stigma, facilitating the rapid
transport of water through channels in the stigma and
pollen membranes. The recent identification of an aquaporin-like gene within the Brassica S-locus may provide
clues toward the regulation of this process [20]. Self-compatible mutants show reduced expression of this
aquaporin, though the nature of the mutant defect remains
to be demonstrated. Finally, it is reasonable to expect that
several components contribute to pollen germination,
some such as lipids or water channels that are shared
among all plants and others, like flavonols, that play a
species-specific role [21,22].
Pollen tube growth —organizing cell polarity
Once pollen tubes invade the stigma, they grow through
the style at rates that can approach 1 cm/hr. This polarized
cell growth has been the focus of recent investigations:
revealing parallels with systems as diverse as root hairs,
yeast buds, and neural outgrowths. Small GTP-binding
proteins are required for polarized secretion in many
organisms; similarly, Rho GTPases are localized at the tips
of pollen tubes and are essential for tube growth [23,24].
Rapid pollen tube growth also requires remodeling of pistil cell walls, and expansin and extensin-like activities
required for cell wall loosening have been purified from
maize pollen tubes [25,26].
Although polarized secretion and cell wall loosening are
clearly required for pollen tube growth, additional activities are likely to provide signals that orientate the growing
tubes. Calcium has long been implicated in directing tube
growth, and exciting new evidence reveals the pathways
and mechanisms by which pollen tubes react to calcium
gradients [27,28]. Intriguingly, calcium gradients within
pollen tubes oscillate in phase with pulses of tube
growth [29,30•]. Identifying the source, concentration, and
destination of the calcium ions that pulse across the pollen
tube tip may provide important clues as to how calcium
regulates cell polarity. Pathways known to be regulated by
calcium are also under investigation, and a calcium-dependent protein kinase has been implicated in pollen tube
reorientation [31]. Growing pollen tube tips exhibit high
levels of a calcium-dependent, calmodulin-independent
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Growth and development
protein kinase (CDPK); localization of kinase activity
changes with pollen tube orientation. Further, release of
caged calcium ions on one side of the pollen tube apex
induces a localized increase in calcium concentration, tube
reorientation, and a corresponding increase in kinase activity adjacent to the site of release [28,31].
Pollen tube guidance — from the style to
the ovules
As pollen tubes travel through the style, many interactions between male and female cells facilitate inhibition
of incompatible pollen tubes. In Nicotiana species, selfincompatible pollen tubes are arrested by S locus RNases
[32,33]. These RNase molecules vary with each S allele,
and current models suggest their import into or activity
within incompatible pollen is regulated by a male-specific S-encoded protein. An intense search for this putative
pollen component is underway. Unfortunately, analysis of
the structure and function of the S-RNase genes themselves reveal few clues. Though active site residues have
been identified [32], construction of chimeric RNases
from different S alleles failed to identify functional
domains [34].
Compatible pollen tubes import nutrients from the style
extracellular matrix and respond to guidance signals as
they travel through the transmitting tract. Arabinogalactan
proteins (AGPs), abundant in stylar secretions, may provide important directional cues. The Yariv reagent, which
binds AGPs, inhibits growth of lily and maize pollen,
although a similar effect was not observed in all plants [35].
In Nicotiana tabacum, a transmitting tissue specific glycoprotein, TTS, exhibits a gradient of glycosylation that may
attract and stimulate growth of pollen tubes to the base of
the pistil [36,37]. Similar results, however, were not
obtained with Nicotiana alata; despite 97% sequence identity and similar sugar modifications, the TTS homolog
GaRSGP fails to exhibit a glycosylation gradient, attract
pollen tubes or stimulate tube growth [38]. These recent
studies warrant careful consideration and substantial work
will be required to identify conserved style components
that regulate the growth of pollen tubes.
After exiting the style, pollen tubes grow toward the
ovules, diploid structures that contain haploid female
gametophytes (Figure 1). Though it was previously
unclear which ovule tissues contribute to pollen tube guidance, recent studies show that both diploid and haploid
female cells are important. Several diploid-specific mutations have been identified that alter ovule structure and
function (see K Schneitz review, this issue pp 13–17, and
[39•]). Some of these dramatically affect ovule morphology; not surprisingly, pollen tube guidance is also aberrant
[40]. Other diploid-specific alterations reveal that morphologically normal ovules can also be defective in guiding
pollen tubes [40,41]. In one case, female tissues from a
self-sterile Arabidopsis mutant exhibit aberrant pollen tube
guidance only in the presence of mutant pollen [41]. This
suggests diploid pistil cells, including those that comprise
the funiculus and integuments (Figure 1), may be required
to attract, bind, and promote the growth of pollen tubes.
Conclusive evidence that the haploid gametophyte is also
required for pollen tube targeting has come from the identification of an Arabidopsis strain that contains a balanced
chromosomal translocation [42••]. Heterozygotes that carry
this translocation have a normal genetic complement; in
these plants, half of the meioses undergo adjacent chromosome segregation, resulting in lethal chromosome
imbalances in the meiotic products. Consequently, although
all of the ovules have genetically normal diploid cells, half
contain aborted gametophytes. In these plants, pollen tubes
fail to approach the abnormal gametophytes, though normal
ovules have associated pollen tubes. Although these studies
reveal that a female gametophyte is important for guidance,
the female gametophyte might induce the surrounding
diploid tissue to emit guidance cues.
The next generation — from gametophytes
to seeds
Gene expression in pollen tubes and female gametophytes
is required for successful reproduction, but few genetic
screens aimed at identifying haploid-specific (gametophytic) mutants have been performed. Diploid-specific
(sporophytic) mutations dramatically reduce fertility and
are relatively easy to isolate; in contrast, male or femalespecific gametophytic defects cause at most a 50%
reduction in seed yield. Recently, progress has been made
toward identifying large numbers of defects in Arabidopsis
gametophytes. One approach has relied on following the
transmission of a heterozygous T-DNA insertion to the
next generation; biased transmission indicates a defect in
the fertility of the male and/or female gametophytes that
carry the insertion [43,44]. Alternatively, genes with interesting haploid-specific roles in development can be
identified by careful characterization of mutants with
defective pollen morphology [45,46].
The genomes contributed by the male and female gametophytes may be fundamentally different, due to
heritable epigenetic modifications (genetic imprinting)
that alter gene expression patterns. In a recent study,
crosses between Arabidopsis diploids, tetraploids, and
hexaploids were performed to cause imbalances in the
maternal and paternal contributions to the embryo and
endosperm [47•]. An excess of maternal genomes (for
example when a tetraploid female is pollinated by a
diploid male) inhibits the development of the endosperm
and results in the formation of small embryos, whereas an
excess of paternal genomes causes embryos and
endosperm to grow larger than normal. More severe
imbalances can result in seedling lethality; for example,
tes (tetraspore) and std (stud) mutants are defective in
pollen cytokinesis and form polyploid sperm that lead to
genetic imbalances and embryo abortion [48,49]. Finally,
maternal effect genes that regulate embryonic
The mating game Wilhelmi and Preuss
development in Arabidopsis have been identified through
gene trapping, a transposon insertion screen that results
in the fusion of a reporter gene carried on the transposon
to chromosomal genes [50]. Mutations in MEDEA, a
homolog of Drosophila Polycomb genes, cause embryo
abortion when transmitted through females. Though the
number of genes that can be imprinted is unknown,
genetic strategies aimed at isolating maternally or paternally imprinted loci will likely prove worthwhile.
The co-ordinated formation of embryos, endosperm,
seeds, and fruit is likely to require the exchange of multiple developmental signals, and mutations that affect
this signaling have been identified. Arabidopsis mutants
known as fie (fertilisation-independent endosperm) or fis (fertilisation-independent seed) [51•,52], inappropriately initiate
development of the endosperm before fertilization takes
place. Mutant fie and fis alleles often fail to be transmitted through female gametophytes. Even when
fertilization of these aberrant gametophytes takes place,
the defect in developmental co-ordination results in
embryo lethality. Regulation of fruit development likely
requires a distinct set of genes; mutation of a MADS-box
gene (AGL8 or FRUITFULL) was recently shown to
interrupt fruit development, without affecting the formation of seeds [53].
Conclusion
Plant reproduction occurs in a competitive environment —
choosing among the available mating partners requires an
amazing array of cell signaling interactions. Recent investigations of pollination in self-compatible and self-incompatible
plants have unearthed a complex set of genetic and molecular controls, active in both diploid and haploid cells. Though
many important molecules have been defined, discerning
those that play general, rather than species-specific, roles
remains a challenge for the future.
References and recommended reading
Papers of particular interest, published within the annual period of review,
have been highlighted as:
• of special interest
•• of outstanding interest
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21
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An elegant bioassay was developed, that enabled purification and characterization of the pollen component of self-incompatibility. For this assay, the
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•
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•
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Growth and development
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•
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•
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•
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Although the resulting seeds do not contain a viable embryo, this approach is
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