Download Life after meiosis: patterning the angiosperm male gametophyte

Cell–Cell Communication in Plant Reproduction
Life after meiosis: patterning the angiosperm
male gametophyte
Michael Borg1 and David Twell
Department of Biology, University of Leicester, Leicester LE1 7RH, U.K.
Abstract
Pollen grains represent the highly reduced haploid male gametophyte generation in angiosperms. They play
an essential role in plant fertility by generating and delivering twin sperm cells to the embryo sac to undergo
double fertilization. The functional specialization of the male gametophyte and double fertilization are
considered to be key innovations in the evolutionary success of angiosperms. The haploid nature of the male
gametophyte and its highly tractable ontogeny makes it an attractive system to study many fundamental
biological processes, such as cell fate determination, cell-cycle progression and gene regulation. The present
mini-review encompasses key advances in our understanding of the molecular mechanisms controlling male
gametophyte patterning in angiosperms. A brief overview of male gametophyte development is presented,
followed by a discussion of the genes required at landmark events of male gametogenesis. The value of the
male gametophyte as an experimental system to study the interplay between cell fate determination and
cell-cycle progression is also discussed and exemplified with an emerging model outlining the regulatory
networks that distinguish the fate of the male germline from its sister vegetative cell. We conclude with a
perspective of the impact emerging data will have on future research strategies and how they will develop
further our understanding of male gametogenesis and plant development.
Introduction
Plant development is a continuous and highly plastic
process that originates from populations of undifferentiated
pluripotent stem cell niches called meristems. The interplay
between cell proliferation and differentiation is critical
for proper development and is tightly co-ordinated both
temporally and spatially in response to intrinsic and extrinsic
cues. This interrelationship dictates the patterning and
growth of single cells right through to their organization
at the multicellular level into tissues and organs [1]. Our
understanding of how these processes are integrated has
mostly come through observations at the individual cell level
[2].
The male gametophyte represents an excellent system to
exploit since its simple cell lineage and highly orchestrated
development makes it ideal to dissect the molecular control
of cellular patterning and its integration with the cell
cycle. In angiosperms, the male gametophyte plays a vital
role in plant fertility and crop production through the
generation and delivery of the male gametes to the embryo
sac for double fertilization. Major advances in genetic
and genomic technologies have fuelled significant progress
in our understanding of male gametophyte development
at the molecular level [3]. Comprehensive transcriptomic
Key words: Arabidopsis, asymmetric division, cell cycle, cell fate, germline, male gametophyte.
Abbreviations used: APC, anaphase-promoting complex; CDK, cyclin-dependent kinase; CYCB1;1,
cyclin B1;1; FBL17, F-box-like 17; GCS1, GENERATIVE CELL SPECIFIC 1; GEM1, GEMINI 1;
GEX2, GAMETE-EXPRESSED2; MGH3, MALE GAMETE-SPECIFIC HISTONE H3; PAKRP1, phragmoplastassociated kinesin-related protein 1; Rb, retinoblastoma; RBR, Rb-related; TIO, two in one; TUBG,
γ -tubulin.
To whom correspondence should be addressed (email [email protected]).
1
Biochem. Soc. Trans. (2010) 38, 577–582; doi:10.1042/BST0380577
datasets from Arabidopsis are readily available [4], including
those from the male gametophyte [5,6] and recently from isolated sperm cells [7]. Moreover, the identification of various
gametophytic mutants has been pivotal in identifying genes
required for cellular patterning of the male gametophyte.
In the present paper, we review some of the key advances
made in understanding male gametophyte development, with
a focus on genetic studies of landmark events required to
pattern the highly reduced male gametophyte. We refer
the reader to other reviews that comprehensively discuss
other aspects of male gametophyte patterning, including
transcriptomic advances [3,8–11]. We also outline a model of
the emerging regulatory network governing male germline
specification and maintenance during male gametophyte
development.
Overview of male gametophyte
development
In animals, germline cells are determined early in embryogenesis and remain as a distinct population of stem cells
throughout life [12,13]. In contrast, the male germline in
angiosperms is only established after meiosis, when haploid
microspores divide asymmetrically to form a small germ cell
and large vegetative cell. Unlike the animal germline, the plant
male germline is not regenerated through mitotic stem cell
divisions, but instead undergoes a single round of mitosis to
produce the functional pair of sperm cells required for double
fertilization.
Formation of the male gametophyte in angiosperms
takes place within the stamens and the landmark events
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Figure 1 Male gametophyte development in Arabidopsis
Schematic diagram representing the distinct morphological stages of male gametophyte development in Arabidopsis. Diploid
pollen mother cells undergo meiotic division to produce a tetrad of haploid microspores. The released microspores undergo
a highly asymmetric division to produce a bicellular pollen grain with a small germ cell engulfed within the cytoplasm of
a large vegetative cell. Whereas the vegetative cell exits the cell cycle, the germ cell undergoes a further mitotic division
to produce twin sperm cells. The sperm cells then continue through the cell cycle to reach G2 -phase before karyogamy
and double fertilization. A colour-coded timeline of the cell-cycle progression in each cell lineage is provided. Listed on the
timeline are mutations that affect male gametophyte development at the point at which they are known to act. PMI, pollen
mitosis I; PMII, pollen mitosis II.
are outlined in Figure 1. Diploid pollen mother cells first
undergo meiotic division to produce tetrads of haploid
microspores. The microspores released then enlarge, and
the microspore nucleus migrates to a peripheral position.
The microspore then undergoes an asymmetric cell division,
and the small germ cell subsequently becomes engulfed within
the cytoplasm of the larger vegetative cell. The vegetative cell
has dispersed nuclear chromatin and exits the cell cycle in G1 phase, whereas the germ cell has condensed nuclear chromatin
and continues through a further round of mitosis to produce
twin sperm cells.
Male gametophyte patterning mutants
Asymmetric division of the microspore is a vital process
during male gametogenesis since it marks the stage at which
the germline is set aside during pollen development. The
resulting germ cell will then undergo a further mitotic division
along with cell specification to produce twin sperm cells
(Figure 1). The haploid nature of the gametophyte genome
makes it a powerful model to test genetics-led hypotheses,
and many studies have exploited gametophytic genetics to
discover genes that are important for male gametophyte
development (Figure 1).
Genes regulating asymmetric division
The asymmetry of microspore division is critical for the
formation of the male germline, as induced symmetric
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Authors Journal compilation division results in two daughter cells that both follow
a default vegetative cell fate programme [14]. Very few
mutants and their corresponding genes have been isolated
that affect asymmetric microspore division, and, perhaps
unsurprisingly, most of these genes have important general
cellular functions. Nevertheless, these are essential in
establishing and maintaining the cell polarity required for
asymmetric division and germ cell fate.
MOR1 (MICROTUBULE ORGANIZATION 1)/
GEM1 (GEMINI 1) is a member of the MAP215 family
of microtubule-associated proteins and plays a vital role
in microspore polarity and cytokinesis by stimulating the
growth and stability of interphase, spindle and phragmoplast
microtubule arrays [15–17]. Similarly, the two functionally
redundant γ -tubulin genes, TUBG1 and TUBG2, demonstrate further the importance of microtubules in establishing
correct microspore division asymmetry [18].
In contrast with the above mutants, two-in-one (tio)
microspores complete asymmetric nuclear division, but fail
to complete cytokinesis, resulting in binucleate pollen grains.
TIO is the plant homologue of the serine/threonine protein
kinase FUSED [19] and localizes to the phragmoplast
midline to play an essential role in centrifugal cell plate
expansion. This could operate through the canonical
NACK-PQR MAPK (mitogen-activated protein kinase)
pathway [20] at the cell plate, since HINKEL (AtNACK1 in Arabidopsis) and TETRASPORE (AtNACK2 in
Cell–Cell Communication in Plant Reproduction
Figure 2 A model of the regulatory events that distinguish male germ cell and vegetative cell fate
Following asymmetric division of the microspore, the cell-cycle inhibitors KRP6 and KRP7 are present in both the germ cell and
vegetative cell. Transient expression of FBL17 specifically in the germ cell leads to the degradation of these KRPs, allowing
CDKA to complex with cyclin D and subsequently phosphorylate RBR. Upon phosphorylation, RBR-mediated repression of the
E2F/DP pathway is relieved and allows progression of the germ cell through S-phase. FBL17 is not expressed in the vegetative
cell, and so CDKA inhibition by high levels of KRP6 and KRP7 is maintained, resulting in continued repression of the E2F/DP
pathway by unphosphorylated RBR. Together, these two pathways serve to enforce vegetative cell fate by preventing entry
into the cell cycle. Gamete specification begins shortly after germ cell division, where the expression of DUO1 and DUO3 in the
germ cell leads to the activation of common and distinct germline differentiation genes. Once S-phase has been completed,
the DUO1-dependent activation of the G2 /M-phase regulator CYCB1;1 promotes germ cell-cycle progression and entry into
mitosis. In parallel, DUO3 also controls G2 /M-phase transition, independent of CYCB1;1, but involving unknown mechanisms.
DUO1 and DUO3 therefore integrate germline differentiation with cell-cycle progression. Ultimately, the co-operation of
these parallel pathways results in a pair of fully differentiated sperm cells equipped with a complement of essential germline
factors such as GCS1 that are required for successful gamete fusion.
Arabidopsis) double-mutant microspores show cell plate
expansion and cytokinesis defects similar to tio microspores
[21]. Two functionally redundant microtubule motor kinesins, PAKRP1 (phragmoplast-associated kinesin-related protein 1)/kinesin-12A and PAKRP1L (PAKRP1-like)/kinesin12B, also localize to the midline of the phragmoplast, and
double-mutant microspores fail to form a well-organized
antiparallel microtubule array between reforming nuclei [22].
It is evident that symmetrical cell division leads to failure
of germline formation. These observations strengthen the
hypothesis that correct differentiation of the germ cell lineage
depends on persistent cell fate determinants being correctly
segregated during asymmetric division [14]. Furthermore,
the failure to clearly establish germ cell fate in gem1 [15]
and tio [19] mutants, which arise from failure of cytokinesis,
indicates that the confinement of such cell fate determinants
by a new cell wall is critical to ‘seal in’ germ cell fate. Basic
components of cellular machinery are thus important for
patterning the male gametophyte and demonstrate how the
orderly completion of cell-cycle events is intricately linked
with cellular differentiation. The major outstanding challenge
is not only to identify additional components involved in establishing microspore polarity, but also to discover the linked
cell fate determinants responsible for specifying the differing fates of the vegetative and germ cells.
Genes required for germ cell division
The differential control of cell-cycle progression in the
vegetative and germ cells is paramount in ensuring that twin
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sperm cells are produced for double fertilization. A number
of mutants have been described in Arabidopsis that produce
bicellular pollen (a single germ cell within the vegetative cell)
due to failure of germ cell division.
Components of the canonical cell-cycle machinery are
expected to play essential roles in germ cell division, and
the analysis of CDKA;1 (A-type cyclin-dependent kinase) in
Arabidopsis has revealed an essential role in germ cell division
[23,24]. Germ cell division fails in cdka;1 mutants, whereas
the DNA synthesis (S-) phase is delayed. A very similar
phenotype to the cdka;1 mutant is observed when the FBL17
(F-box-like 17) gene is disrupted [25,25a]. Substrate-specific
F-box proteins associate with Skp1 and CUL1 to form SCF
(Skp1/Cullin/F-box) E3 ubiquitin protein ligase complexes
[26,27]. FBL17 is transiently expressed only in the male
germ cell after asymmetric microspore division and targets
the CDK (cyclin-dependent kinase) inhibitors KRP6 and
KRP7 for proteasome-dependent degradation, enabling the
germ cell to progress through S-phase [25]. Conversely,
the persistence of KRP6/KRP7 in the vegetative cell
is proposed to maintain inhibition of CDKA activity
and vegetative cell-cycle progression. Germline-specific
expression of FBL17 thus enables differential control of the
cell cycle in the germ and vegetative cells, effectively licensing
germ cells for progression through S-phase (Figure 2).
Similarly, proteasome-mediated degradation of KRP6 in
microspores by two RING-finger E3 ligases, RHF1a and
RHF2a, allows regular progression through microspore
and subsequent germ cell mitotic cell cycles during male
gametophyte development [28].
It is well established that the Rb (retinoblastoma)-E2F
pathway controls cell-cycle progression in a variety of organisms [29], including plants [30,31]. Once phosphorylated by
CDKs during the latter stages of G1 -phase, Rb repression of
E2F/DP family transcription factors is alleviated, activating
downstream cell-cycle genes that commit cells to S-phase
[32]. A recent study has demonstrated that the plant
homologue RBR (Rb-related) plays a pivotal role in male
gametophyte patterning [33].
Loss of RBR does not have a major impact on microspore
division, but does result in a complex array of phenotypes
characterized by the limited hyperproliferation of the
vegetative cell and, to a lesser extent, the germline [33].
Hyperproliferation in the absence of RBR is caused by
CDKA;1 activity, since introduction of a cdka;1 mutant allele
prevents cell proliferation in rbr pollen [33]. Cell fate is
also incorrectly specified in a fraction of rbr vegetative cells.
These rbr vegetative cells appear to retain the progenitorlike character of the microspore and attempt to imperfectly
reiterate asymmetric division to produce an additional cell
with a range of fate identities. These findings point to RBR
primarily controlling cell-cycle progression, while having a
secondary impact on cell fate commitment. This places RBR
repression of the E2F/DP pathway downstream of KRPdependent CDKA;1 inhibition, thus both mechanisms cooperate to ensure commitment to vegetative cell fate by
enforcing cell-cycle exit.
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Authors Journal compilation Integrating germ cell division with cell
fate determination
Single germ cell phenotypes are also characteristic of duo
pollen (duo) mutants. Asymmetric microspore division is
completed in these mutants; however, the resulting germ
cell fails to undergo cell division [34]. In the duo1 mutant,
germ cells complete S-phase, but fail to enter mitosis. DUO1
encodes a novel conserved R2R3 Myb protein specifically
expressed in the male germline [35]. We have demonstrated
recently that failure of mitotic entry in duo1 germ cells is
caused by the lack of germline activation of the G2 /M-phase
regulator cyclin B1;1 (CYCB1;1) [36].
Unlike fbl17 and cdka;1 mutant germ cells, which are
able to exclusively fertilize the egg cell [24,25], duo1 pollen
is unable to fertilize. This suggests that, in addition to
cell-cycle defects, key features of gamete differentiation
are incomplete in duo1. By monitoring the expression
of genes associated with germ cell specification, we have
demonstrated that, in addition to controlling germline
expression of CYCB1;1, DUO1 also dictates correct
differentiation of the male germline (Figure 2). The three
molecular markers that are suppressed in duo1 pollen
reported the expression of three germline-expressed genes:
MGH3 (MALE GAMETE-SPECIFIC HISTONE H3), a
male germline-specific histone H3.3 variant [37], GEX2
(GAMETE-EXPRESSED2), encoding a putative membraneassociated protein [38,39], and GCS1 (GENERATIVE CELL
SPECIFIC 1) (HAP2), encoding a sperm cell-surface protein
required for fertilization [40,41]. Thus the lack of GCS1
expression in the absence of DUO1 is sufficient to explain
why duo1 pollen is infertile.
In addition to the suppressed expression of these normally
germline-specific markers in duo1 germ cells, ectopic
expression of DUO1 is sufficient to activate their expression
in a range of non-germline cells [36]. When DUO1 is
ectopically expressed in seedlings, transcripts of MGH3,
GEX2 and GCS1 are detected only in response to DUO1.
Whereas these germline differentiation genes are activated in
response to ectopic DUO1 expression, this is not sufficient
to induce CYCB1;1 transcripts. Thus DUO1-dependent
expression of CYCB1;1 in the germline may involve
indirect transcriptional mechanisms or post-transcriptional
controls.
The recent discovery of DUO3 adds a further node to
an emerging germline regulatory network (Figure 2). Like
DUO1, DUO3 is a key regulatory protein that is required
for germ cell division and correct gamete specification [42].
DUO3 is a conserved nuclear protein in land plants and
contains domains related to GON-4, a cell lineage regulator of
gonadogenesis in Caenorhabditis elegans and haemopoeisis in
zebrafish [43,44]. duo3 germ cells either fail to divide or show
a delay in division, and, unlike DUO1, DUO3 promotes
entry into mitosis independently of CYCB1;1. A proportion
of duo3 germ cells show persistent expression of CYCB1;1,
indicating that failure of division in duo3 could be due
to incomplete activation of the APC (anaphase-promoting
Cell–Cell Communication in Plant Reproduction
complex), which normally degrades CYCB1;1 to promote
exit from mitosis [45].
Use of the same molecular markers that are suppressed
in the duo1 mutant has identified distinct yet overlapping
control of germline differentiation genes by DUO1 and
DUO3. Complete expression of GCS1 and GEX2 requires
both DUO1 and DUO3, whereas expression of MGH3
depends solely upon DUO1. The mechanism by which
DUO1 and DUO3 activate the expression of common targets
remains unknown, yet it has been proposed that they interact
in a transcriptional complex or that they may act in tandem
through a DUO3-dependent chromatin-remodelling route
[42].
Whereas DUO1 expression is restricted to the male
germline, DUO3 is widely expressed in sporophytic tissues,
particularly at sites of cell division, as well as in both
the vegetative cell and germ cell in developing pollen.
Consistent with its wide expression pattern, analysis of duo3
homozygous plants revealed embryo developmental defects
associated with a reduced rate and co-ordination of cell
division [42]. Thus, like DUO1 in the male gametophyte,
DUO3 has an essential developmental role in cell-cycle
progression and cell specification, but DUO3 may function
as a general regulator in both gametophytic and sporophytic
tissues.
Perspectives
The wealth of genetic and genomic resources for various plant
species now available makes this an exciting time for male
gametophyte biology [8]. Comprehensive transcriptomic
studies have massively increased our knowledge base of
the complexity and dynamics of haploid gene expression
in the developing gametophyte and sperm cells [5,7].
These transcriptomic datasets have already been exploited
to discover a network level response of MIKC* MADS
box transcription factors involved in pollen maturation
[46,47]. Moreover, the recent application of novel proteomic
technologies has further widened our perspective of pollen
biochemistry [48,49]. Recent evidence has emerged for the
expression and function of critical components of small RNA
pathways in the developing male gametophyte [50,51]. These
small RNA pathways add another layer to an already complex
and diverse gametophytic gene expression programme [8].
The discovery of DUO1 and DUO3 provides compelling
insights into how the processes of cell proliferation and
cell differentiation are integrated during male germline
development. Many challenges lay ahead if we are to
fully understand the complexity and architecture of these
overlapping regulatory networks. In addition to uncovering
the plethora of downstream target genes and the nature of
their activation, an unresolved issue is the regulation of these
germline determinants and how their activation is linked
with asymmetric division of the microspore. Analysis of
the DUO1 promoter has provided encouraging evidence
of upstream regulators, since its regulation is dependent
on positive elements in its minimal promoter [36] and
not on a proposed derepression mechanism involving the
lily repressor protein GRSF (germline restrictive silencing
factor) [36,52]. Furthermore, the pathways by which DUO1
and DUO3 co-ordinate germ cell division remain largely
unknown. Analysing these mechanisms not only will provide
further insights into male gametogenesis, but also will have
an impact on our understanding of how cell-specific modules
are recruited to co-ordinate cell-cycle progression using basic
cell-cycle components.
The future therefore promises to deliver some exciting and
novel discoveries in male gametophyte biology. Exploitation
of the male gametophyte as an experimental system has
already had a major impact on our knowledge of fundamental
cellular processes and the machinery that drives them. Much
of this knowledge has been gained through transcriptomic
analyses [8] and the genetic approaches discussed in the
present review. The future challenge is to apply systematic
approaches and to exploit new knowledge of gametophytic
gene expression to formulate new hypotheses. Concerted
efforts are thus expected to not only deliver a corroborated
and system level perspective of the mechanisms controlling
male gametogenesis and gamete function, but also provide
insight into the complex interplay between cell proliferation
and differentiation in plants.
Funding
Work in the Twell laboratory is supported by research grants from
Biotechnology and the Biological Sciences Research Council (BBSRC).
M.B. is supported by a BBSRC-funded studentship.
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Received 21 August 2009
doi:10.1042/BST0380577