Meiotic and Mitotic Cell Cycle Mutants Involved in Gametophyte Development in Arabidopsis
National Laboratory of Protein Engineering and Plant Genetic Engineering, College of Life Sciences, Peking University, Beijing 100871, P.R. China
1 To whom correspondence should be addressed. E-mail qulj{at}pku.edu.cn, Fax: 86-10-62753339, Tel: 86-10-62753018.
 |
Abstract |
|---|
 TOP Abstract INTRODUCTION |
|---|
The alternation between diploid and haploid generations is fundamental in the life cycles of both animals and plants. The meiotic cell cycle is common to both animals and plants gamete formation, but in animals the products of meiosis are gametes, whereas for most plants, subsequent mitotic cell cycles are needed for their formation. Clarifying the regulatory mechanisms of mitotic cell cycle progression during gametophyte development will help understanding of sexual reproduction in plants. Many mutants defective in gametophyte development and, in particular, many meiotic and mitotic cell cycle mutants in Arabidopsis male and female gametophyte development were identified through both forward and reverse genetics approaches.
Received for publication April 14, 2008. Accepted for publication April 17, 2008.
|
INTRODUCTION |
|---|
|
TOPAbstractINTRODUCTION |
|---|
Life cycles alternate between diploid and haploid generations in both animals and plants. In animals, haploid sperm and eggs are produced directly after meiosis, but, in plants, the mitosis products undergo two or three rounds of mitosis, producing multi-cellular haploid gametophytes (Drews and Yadegari, 2002). Both animals and plants share the conserved meiotic cell cycle.
With the completion of the Arabidopsis thaliana genome sequence in 2000 and the availability of SALK mutants, Arabidopsis is being more and more widely used as a model system to study various biological pathways and processes, including gametophyte development. Cytological observations of gametophyte development have been extensively conducted over the last decades (McCormick, 1993; Preuss, 1995). In Arabidopsis, the diploid sporogenous initial cells, also called microspore mother cells or megaspore mother cells, undergo meiosis to produce a tetrad of microspores in the anther, or four megaspores in the ovule. The microspores, freed from the tetrad by the action of callase, further undergo an asymmetric mitosis (pollen mitosis I, PM I) to form bi-cellular pollen composed of two cells with distinct fates. The larger cell, the vegetative cell, does not divide again and later forms a pollen tube. The smaller cell, the generative cell, undergoes a symmetric mitosis (pollen mitosis II, PM II) to produce two sperm cells (McCormick, 1993, 2004). The three-celled pollen grain is called the male gametophyte. For female gametophyte development, only one functional megaspore out of the four megaspores survives, and it undergoes three rounds of mitotic divisions and subsequent cellularizations to produce a seven-celled mature embryo sac, also termed the female gametophyte (Yang and Sundaresan, 2000; Drews and Yadegari, 2002).
Meiotic Mutants in Arabidopsis
Meiosis is a conserved cell division that produces haploid cells from diploid parental cells, which is essential for eukaryotic sexual reproduction. During the development of male reproductive structure, archesporial cells, differentiated from a group of cells in developing anthers, produce primary sporogenous cells, which then differentiate into the pollen mother cells (PMCs) that undergo meiosis, and the primary parietal cells (PPCs), which give rise to the tapetum, endothecium, and the middle layer of the anthers (Yang et al., 1999b). Notably, the occurrence of meiosis is highly synchronized in the PMCs (Armstrong et al., 2001). In the development of the female reproductive structure, the archesporial cell, differentiated from a single hypodermal cell, directly differentiates into the megaspore mother cell (MMC), which then undergoes meiosis to give four megaspores. Only the chalazal megaspore is functional and develops into the female gametophyte, whereas the other three micropylar megaspores are degraded quickly (Yang and Sundaresan, 2000). Interestingly, in many angiosperms, meiosis in the male is not synchronized with meiosis in the female. In Arabidopsis, for example, male meiosis is completed while female meiosis is still at prophase I (Caryl et al., 2003).
A detailed cytological description of meiosis, especially chromosome behavior, has been established through cytological and genetic studies. After a single round of DNA replication, two rounds of nuclear divisions occur: meiosis I, which involves the segregation of homologous chromosomes, and meiosis II, which is similar to mitosis and leads to the segregation of sister chromatids. After meiosis II, four haploid spores are formed upon cytokinesis. The recognition between homologs in prophase I (meiosis I), achieved through homolog pairing and stabilized by synapsis, are critical for proper homolog chromosome segregation at anaphase I (Roeder, 1990). Prophase I is divided into five stages: leptotene, zygotene, pachytene, diplotene, and diakinesis. Detailed reviews of chromosomal behaviors during meiosis are available (Ross et al., 1996, 1997; Caryl et al., 2003; Ma, 2005).
To characterize important components involved in meiosis, many mutants defective during meiosis were identified some decades ago (Baker et al., 1976; Golubovskaya, 1979). Unfortunately, only a few responsible genes were characterized from these meiotic mutants. In recent years, with more Arabidopsis meiotic mutants identified and the cytogenetic and immunological techniques improved, the regulation mechanism of meiosis in Arabidopsis is better understood. Many Arabidopsis meiotic mutants were identified by screening mutagenized populations that had been generated by EMS, T-DNA or transposons, using reduced fertility or sterility of plants as the screening criteria (Ross et al., 1997; Bhatt et al., 1999; Siddiqi et al., 2000; Mercier et al., 2001). Those putative meiotic mutants identified were then confirmed through cytological and genetic examination. However, a reduced fertility phenotype will identify not only meiotic mutants, but also mutants defective in various aspects of reproductive development. Some meiotic genes were identified because of sequence similarity to genes already known to be involved in meiotic events in other organisms, such as yeast DMC1 (Klimyuk and Jones, 1997; Doutriaux et al., 1998), RAD51 (Doutriaux et al., 1998), and SPO11 (Hartung and Puchta, 2000; Grelon et al., 2001). However, in many cases, homologues could not always be identified in Arabidopsis due to the evolutionary divergence between different organisms. These identified meiotic mutants were categorized based on the meiotic mutant phenotypes or by the steps affected in meiosis.
Sister Chromatid Cohesion
Sister chromatid cohesion is a prerequisite for meiosis. From DNA replication in S phase, sister chromatids are associated until anaphase II; this association is maintained by sister chromatid cohesion (van Heemst and Heyting, 2000; Lee and Orr-Weaver, 2001). Sister chromatid cohesion requires the cohesion complex. Arabidopsis SYN1/DIF1 is a homolog to the yeast RAD21/REC8 gene, which encodes a meiosis-specific cohesion subunit (Stoop-Myer and Amon, 1999). A mutation of SYN1/DIF1 results in multiple meiotic defects, which affect both male and female fertility. For example, chromosome condensation and pairing in syn1/dif1 is abnormal, shown by the presence of univalent chromosomes and chromosome fragmentation at metaphase I, and acentric fragments and chromatin bridges in meiosis I and II. Consequently, chromosome segregation is severely affected, resulting in meiotic products of uneven size and shape, and of variable ploidy (Bai et al., 1999; Bhatt et al., 1999). In female meiosis of syn1/dif1, the ovules do not contain an obvious embryo sac (Bhatt et al., 1999).
Another important gene is SWITCH1/DYAD, which is also essential for sister chromatid cohesion in both male and female meioses (Mercier et al., 2001; Agashe et al., 2002). In female meiosis, swi1/dyad undergoes a mitosis-like division rather than a meiosis, and no embryo sac forms (Siddiqi et al., 2000). In male meiosis of swi1/dyad, uneven segregation of the chromatids during the first and second meiotic divisions results in the production of up to 10 nuclei, which degenerate later (Mercier et al., 2001).
Homologous Chromosome Synapsis and Recombination
Chromosome pairing and synapsis in prophase I ensure proper separation of homologs at anaphase I. In most eukaryotes, synapsis is mediated by the synaptonemal complex (SC), the function of which is evolutionarily conserved among plants and animals.
The synapsis-defective mutants are either asynaptic mutants, which fail to complete synapsis, or desynaptic mutants, in which chromosome synapsis occurs but is not maintained until anaphase I. The common features of both asynaptic and desynaptic mutants are of univalents instead of bivalents during prophase I. By forward genetics approaches, a few mutants were found to be synapsis defective, namely asynaptic1 (asy1), ahp2, solo dancers (sds), dsynaptic1 (dsy1), and dsynaptic10 (dsy10). These mutants all exhibited reduced fertility phenotypes in both male and female, and dsy10 was sterile (Hollingsworth et al., 1990; Peirson et al., 1996; Ross et al., 1997; Armstrong et al., 2002; Azumi et al., 2002). The homologous chromosomes of asy1 fail to undergo synapsis at prophase I, ahp2 is defective in pairing and bivalent formation, whereas sds is defective in homolog synapsis, recombination and bivalent formation. ASY1 encodes a protein that is homologous to the HOP1 protein—a protein that plays an important role in SC assembly in yeast (Hollingsworth et al., 1990). AHP2 gene encodes a protein showing high sequence similarity with two yeast proteins that were demonstrated to be involved in homolog paring, namely Meu13p from S. pombe and the HOP2 protein from S. cerevisiae. The similar synapsis defective phenotypes of these mutants suggest that Arabidopsis ASY1 and AHP2 may share conserved functions with yeast HOP1, and with Mer13p and HOP2, respectively, during synapsis, and that meiosis in yeast and plants share a similar machinery for homologous chromosome synapsis and recombination (Hollingsworth et al., 1990; Schommer et al., 2003). Interestingly, the SDS gene encodes a protein containing a conserved cyclin-like domain. Cyclins are known to function in the mitotic cell cycle in both animals and in plants. Because meiosis II is reported to be more like mitosis, it is possible that the SDS protein represents a novel type of cyclin, functioning specifically in the meiotic cell cycle, most likely in meiosis II (Azumi et al., 2002). Although genetic and cytological analyses for dsy1 and dsy10 were conducted almost a decade ago (Peirson et al., 1996; Ross et al., 1997), the molecular lesions for these two mutants have not been characterized.
In addition to forward genetics approaches, reverse genetics was also widely adopted to identify those meiosis-involved genes in Arabidopsis that are homologous to their counterparts in yeast. In yeast, many genes involved in meiotic recombination have been identified and well characterized (Zickler and Kleckner, 1999). For example, the yeast SPO11 protein was essential for double-strand break formation (DSB), which is followed by meiotic recombination (Keeney et al., 1997). SPO11 homologs were then identified in other organisms such as human, mouse, and Drosophila. The Arabidopsis mutant spo11–1 is defective in homologous chromosome pairing, recombination and bivalent formation, leading to polyads during male meiosis and no differentiation of the embryo sac in female meiosis (Grelon et al., 2001).
Other yeast proteins are involved in meiosis. For example, RAD50 and MRE11 are required for recombination and DSB repair following SPO11-mediated DSB, whereas Rad51 and Dmc1 participate in homologous chromosome recombination and bivalent formation. Mutants in the Arabidopsis homologs of these genes all have meiotic defects. For example, loss of function of AtRAD50 or AtMRE11 resulted in chromosome fragmentation and hypersensitivity to DNA damage (Gallego et al., 2001; Puizina et al., 2004). Mutants of AtDMC1 had defects in bivalent formation, and the atrad51 mutant showed meiotic defects in chromosome pairing, synapsis and DSB repair (Couteau et al., 1999); both mutants had very low male and female fertilities. These studies also support the conclusion that the machinery used in meiosis, such as those involved in SPO11-mediated DSB, DSB repair, homologous chromosome recombination and bivalent formation, is conserved among eukaryotes.
Chromosome Separation and Segregation
Throughout meiosis, chromosome segregation occurs twice—homolog separation in anaphase I and sister chromatid segregation in anaphase II. Despite the great importance of chromosome segregation, little is known about the genes involved in these two segregation events in Arabidopsis. A male sterile Ds transposon line, ask1, was identified, in which both homologous chromosome separation in anaphase I and sister chromatid segregation in anaphase II during male meiosis were affected (Yang et al., 1999a). Therefore, ask1 produces polyads with variable size and content. ASK1 encodes a protein homologous to yeast SKP1, which is an essential subunit of the SCF complex. This result suggests that the SCF complex might be involved in the chromosome segregation events.
Another mutant isolated from Ds transposon lines is kata/atk1, which also exhibits reduced male fertility (Chen et al., 2002). At metaphase I in kata/atk1 male meiocytes, the chromosomes fail to align correctly at the equator of the cell, leading to the failure of segregation at anaphase I. The ATK1 gene encodes a kinesin-like protein, and kinesin is known to be involved in meiotic spindle formation (Endow et al., 1994). Therefore, the meiotic defect in atk1 could be due to abnormal spindle formation.
Mutants Involved in Meiotic Cell Cycle Progression and Regulation
In addition to the mutants that exhibited abnormal chromosomal behavior during meiosis, there are some other meiotic mutants in which cell cycle progression and regulation are affected.
For example, the temperature-sensitive mutant tam1 (tardy asynchronous meiosis) displayed an asynchronous PMC meiosis, especially on entering the metaphase I and metaphase II, and produced abnormal dyad meiotic products (Magnard et al., 2001). TAM1 encodes an A-type cyclin, CYCA1;2, playing an essential role in regulating entry into metaphase in meiosis (Wang et al., 2004).
Other defects in meiotic cell cycle progression also lead to abnormal meiosis. In the ms5/tdm1 (three-division mutant), a third division occurs after meiosis II without further DNA/chromosome replication. Microsporocytes in ms5 appeared normal, but became polyads after meiosis II and soon degenerated. The MS5 gene encodes a 434-aa protein that has limited similarity with the SC (synaptonemal complex) protein from rat and the regulatory subunit of a cyclin-dependent kinase (CDK) from Xenopus (Glover et al., 1998; Sanders et al., 1999). In another mutant, the meiocytes of the male sterile mutant mmd1/duet showed normal early chromosomal behaviors, including chromosome condensation, pairing, and homolog synapsis up to diakinesis. From diakinesis on, mmd1/duet exhibits cytoplasmic shrinkage and chromosome fragmentation, and cell death occurred before cytokinesis in telophase II. Since mmd1/duet has normal chromosome events, it was proposed that MMD1/DUET was involved in regulating meiotic cell cycle progression (Reddy et al., 2003; Yang et al., 2003b). Reverse genetic studies also identifed genes regulating meiotic cell cycle progression. The yeast cell cycle regulator gene CDC45 plays an important role in regulating DNA synthesis in mitosis (Zou and Stillman, 2000). Plants in which RNAi was used to down-regulate the expression of the Arabidopsis CDC45 homolog, AtCDC45, exhibited reduced male and female fertilities, and produced polyads rather than tetrads, suggesting that DNA synthesis machinery is conserved in Arabidopsis (Stevens et al., 2004).
Cytokinesis is also very important in meiosis. In the mutant stud/tes, cytokinesis failed to occur in male meiosis, producing large tetraspores containing four nuclei. During subsequent pollen development, these nuclei of these large tetraspores underwent PM I and PM II separately and eventually give rise to multiple gametes (up to eight sperm) in a giant pollen grain (Hulskamp et al., 1997; Spielman et al., 1997). STUD/TES encodes a kinesin, which is believed to serve as a microtubule-associated motor. Apparently, STUD/TES affects the normal function of microtubules associated with male meiosis (Yang et al., 2003a). It is not yet clear whether other kinesin family members, in addition to ATK1 and STUD/TES, are involved in the cellular events during male meiosis.
Gametophytic Mutants Involved in Mitotic Cell Cycle Regulation
The screening criteria for gametophytic mutants are different from the screening for meiotic mutants. Meiotic mutants are sporophytic mutants that are usually recessive and exhibit the expected 1:2:1 segregation patterns. Only homozygous meiotic mutants exhibit reductions in male and/or female fertility, which is reflected in their reduced seed set. In contrast to meiotic mutants, gametophytic mutants affect male and/or female gametophyte development and exhibit altered segregation patterns. Gametophytic mutations can be transmitted from generation to generation as heterozygotes. Female or male gametophyte-specific mutations with complete penetrance are not transmitted by the respective gametophytes and thus the segregation ratio is 1:1. Generally speaking, in gametophytic mutants affecting both male and female transmission, the penetrance is incomplete and thus mutations can be transmitted to subsequent generations.
Female gametophytic mutants with complete penetrance exhibit 50% aborted ovules, which are easy to distinguish, as they are tiny, undeveloped and white. By contrast, defective seeds are either white developed seeds (embryo development abnormality) or brown shrunken seeds (endosperm development abnormality). For gametophytic maternal mutants, distinguishing aborted ovules from defective seeds is important, because gametophytic maternal mutations have 50% aborted seed development as well as 1:1 segregation ratios. Gametophytic maternal mutants can be confused with haplo-insufficient mutants and paternal imprinting mutants. Therefore, molecular and genetic analyses are very important for the genotypic confirmation. As good examples, the functional and genetic analysis for the mutants mea, fie, and fis2 are discussed in detail (Ohad et al., 1996; Chaudhury et al., 1997; Grossniklaus et al., 1998).
Male gametophytic mutants can be defective in different stages of pollen development, such as gametogenesis, pollen tube germination, proper pollen tube guidance by ovules, and fertilization. In most cases, male gametophytic mutants with complete penetrance have normal seed set, except for mutants defective in fertilization/pollen tube reception. Because the seed set is normal, these mutants can only be screened and identified via segregation distortion and reciprocal crosses with wild-type plants. Further cytological observation is also needed to help confirm the male gametophytic mutations. For fertilization/pollen tube reception mutants in which the pollen tube guidance is normal, the sperm cannot be released. Some fertilization-affected male or female gametophytic mutants have been characterized (von Besser et al., 2006; Escobar-Restrepo et al., 2007). As an example of fertilization-affected male gametophytic mutants in Arabidopsis, hap2 is completely blocked in its fertilization, whereas half of the hap2 pollen tube guidance is disrupted, although hap2 pollen tube length is not affected. HAP2/GCS1 encodes a hypothetical protein with unknown function, which is specifically expressed in sperm cells (von Besser et al., 2006). In terms of the female gametophytic mutants, the feronia mutant, in which a receptor-like kinase localized in the filiform apparatus was mutated, showed disturbance in fertilization/pollen tube reception (Escobar-Restrepo et al., 2007). The receptor-like kinase, FERONIA, may bind to a ligand on the approaching pollen tube so that the pollen tube bursts for the release of the sperm. It will be an interesting question to examine whether there is a functional link between HAP2 and FERONIA. Identification and characterization of more male gametophytic mutants affecting the pollen tube reception might help unveil putative ligands on the pollen tube.
A number of gametophytic mutants have been identified, using reduced seed set and segregation distortion as the criteria (Christensen et al., 2002; Drews and Yadegari, 2002; McCormick, 2004). Here, we will mainly focus on those mutants defective in cell cycle progression during gametophyte development.
Female Gametophytic Mutants Affecting Cell Cycle Progression
Several of the identified female gametophytic mutants in Arabidopsis are defective in cell cycle progression, such as mutations affecting division initiation and regulation during the three rounds of mitotic nuclear divisions from FG1 (Female Gametophyte 1) to FG5 (Female Gametophyte 5) (Moore et al., 1997; Christensen et al., 1998, 2002; Pagnussat et al., 2005).
In the mutants female gametophyte 2 (fem2), fem3, gametophyte factor (gf), gfa4, and gfa5, the embryo sac is arrested in the FG1 stage (Christensen et al., 1997; Feldmann et al., 1997; Christensen et al., 1998), suggesting that these genes are necessary for the early development of the female gametophyte. However, the genes responsible for these phenotypes have not been identified. In the nomega and prl mutants, the embryo sac is arrested at the two-nucleate stage (FG2) and four-nucleate stage (FG4), respectively, suggesting that NOMEGA and PRL are required for the second and the third nuclear divisions, respectively (Springer et al., 2000; Kwee and Sundaresan, 2003). The NOMEGA gene encodes a protein with high sequence similarity to the APC6/CDC16 (cell division cycle) subunit of the Anaphase Promoting Complex/Cyclosome (APC/C). The APC/C complex functions as an E3 ligase in the ubiquitin-mediated proteolysis pathway, which controls several key steps in cell cycle. The APC/C was initially found to be involved in the targeted proteolysis of A- and B-type cyclins in clams and Xenopus (Hershko et al., 1991), thus facilitating exit from mitosis (Zachariae and Nasmyth, 1999). Molecular analysis showed that in nomega, cyclin B, a critical substrate for APC/C, is not degraded in the embryo sacs, further supporting that NOMEGA and APC/C complex play important roles in cell cycle progression during female gametophyte development (Kwee and Sundaresan, 2003). PROLIFERA (PRL) is the homologue of the DNA replication licensing factor Mcm7, which is highly conserved in all eukaryotes (Springer et al., 1995). The level of the PRL protein is also precisely regulated during cell cycle progression. Mutation of PRL results in the reduced transmission; 50% of the embryo sacs arrest at the four-nucleate stage, and the prl homozygous lines are never identified due to the maternally embryo lethality (Springer et al., 2000). This suggests that maintenance of PRL level above a certain threshold is essential for megagametogenesis and embryo development, and that PRL might be a DNA replication licensing factor required at the S phase of the mitotic cell cycle. hdd (hadad) is another female gametophytic mutant, in which the embryo sacs are arrested at the one-, two-, or four-nucleate stage (Moore et al., 1997), suggesting that HDD is required for nuclear divisions in megagametogenesis.
Among all the female gametophytic mutants, slow walker1 (swa1) is especially interesting (Shi et al., 2005). Megagametophyte development in the swa1 mutants was not synchronized, with the embryo sacs variably arrested at the two-, four-, or eight-nucleate stage, in the same pistil. Different from the mutants above that are arrested at precise stages, nuclear divisions in swa1 megagametophyte could eventually be achieved, but the cell cycle is prolonged and postponed, because delayed pollination experiments could partially rescue the swa1 embryo sacs and form functional embryos (Shi et al., 2005). SWA1 encodes a nucleolus-localized protein with six WD40 repeats, which possibly plays a role in rRNA biogenesis required for mitotic divisions in female gametogenesis (Shi et al., 2005). It will be interesting to further investigate why the alteration of a general process (rRNA biogenesis) affects a specific developmental event, gametogenesis, but not the sporophytic cells.
Although most of the mutants affecting megagametophyte development were identified by examining the stage at which the mitotic divisions are arrested during megagametophyte development, the rbr1 (retinoblastoma-related) mutant is an exception. It was identified as a mutation in which mitotic divisions failed to arrest properly during megagametophyte development (Huang and Sheridan, 1996; Ebel et al., 2004; Evans, 2007). In metazoans, pRB is a key negative regulator of cell division, and, by repressing E2F transcription factors, it controls the G1/S transition. The rbr1 mutation in Arabidopsis resulted in excessive nuclear proliferation in embryo sacs in unfertilized pistils. In rbr1, supernumerary nuclei were present at the micropylar end of the megagametophyte and the central cell nucleus initiates autonomous endosperm development, suggesting that RBR1 has a novel function in cell cycle control during gametogenesis and in the repression of autonomous endosperm development (Ebel et al., 2004). The ig1 (indeterminate gametophyte1) mutation from maize exhibited a similar phenotype to rbr1 in Arabidopsis, producing excessive nuclei in embryo sacs during megagametogenesis (Evans, 2007).
Male Gametophytic Mutants Affecting Cell Cycle Progression
Male gametogenesis in angiosperms depends on a determinative asymmetric mitotic cell division at PM I, which gives rise to a larger vegetative cell (VC) and a smaller generative cell (GC). The GC has a condensed nucleus and a reduced amount of cytoplasm, which lacks metabolic reserves and contains fewer organelles compared to the VC. In most angiosperms (about 70%), such as Solanaceae and Liliaceae, pollen grains are released from the anther when they contain the two cells (VC and GC), and the second symmetric mitotic cell division (PM II) of GC, to produce two sperm cells, occurs when the pollen tube grows through the female pistil. In other angiosperms such as Arabidopsis and rice, the PMII occurs in the anther locule before pollen is released (McCormick, 1993). Each mature Arabidopsis pollen grain therefore contains three cells—one vegetative cell and two sperm cells enclosed within the cytoplasm of the vegetative cell. The two sequential mitotic cell divisions are critical to produce viable sperm for fertilization. Gametophytic mutants affecting various aspects of pollen development and function have been identified in Arabidopsis through genetic screening for segregation distortion and phenotypical screening for abnormal pollen morphology (Chen and McCormick, 1996; Bonhomme et al., 1998; Howden et al., 1998; Grini et al., 1999; Johnson and McCormick, 2001; Lalanne and Twell, 2002; Twell et al., 2002; Lalanne et al., 2004). Out of those mutants, some male gametophytic mutations affecting PM I and PM II have been characterized, such as sidecar pollen, duo1 (duo pollen1), duo2 (duo pollen2), gem1 (gemini pllen1), and gem2 (gemini pllen2) (Chen and McCormick, 1996; Park et al., 1998; Park and Twell, 2001; Park et al., 2004; Durbarry et al., 2005).
SIDECAR POLLEN is the first male gametophytic mutation described in Arabidopsis (Chen and McCormick, 1996). sidecar pollen heterozygotes produce about 45% of the wild-type pollen, 48% of the aborted pollen, and 7% of the abnormal pollen, each with an extra cell. Cytological analyses of sidecar pollen showed that the mutated microspores underwent a premature and symmetric cell division prior to the normal asymmetric division, despite the differential incomplete gametophytic penetrance. Since the sidecar pollen mutant was identified from fast neutron-generated mutant seeds, the corresponding gene has not been cloned yet (Chen and McCormick, 1996).
The mutants duo pollen1 (duo1), duo pollen2 (duo2), gemini pollen1 (gem1), and gemini pollen2 (gem2) were all screened from ethyl methanesulfonate (EMS) mutagenized populations (Park et al., 1998; Park and Twell, 2001; Twell et al., 2002; Park et al., 2004; Durbarry et al., 2005). Both duo1 and duo2 mutants underwent normal pollen mitosis I, while the subsequent generative cell division was blocked, producing bicellular pollen grains containing only one sperm cell at anthesis. duo1 and duo2 were defective at distinct stages of PM II. The generative cells in duo1 pollen failed to enter pollen mitosis II at G2-M transition, whereas the generative cells in duo2 entered PM II but arrested at prometaphase (Durbarry et al., 2005). DUO1 encodes a novel R2R3 MYB transcription factor that is specific to the male germline and accumulates in generative and sperm cell nuclei. The identification of the DUO1 protein suggests that distinct members of the MYB gene family have been recruited during evolution as specific regulators of gametophytic development (Rotman et al., 2005). The molecular lesion in duo2 is not clear yet.
Both gemini pollen1 (gem1) and gemini pollen2 (gem2) were defective in gametophytic cytokinesis of PM I (Park et al., 1998; Park and Twell, 2001; Twell et al., 2002; Park et al., 2004). gemini pollen1 displayed, with incomplete penetrance, altered cell division symmetry and cell fate at PM I. At the mature pollen stage, the gem1 pollen grains have two cells, each with decondensed chromatin and with the capacity to express a vegetative cell-specific marker gene (Park and Twell, 2001). GEM1 encodes the MOR1 protein, which is a member of the XMAP215/chTOG family of microtubule-associated proteins (Twell et al., 2002). MOR1 was reported to bind microtubules and was localized to the areas of overlapping microtubules in the phragmoplast (Twell et al., 2002). Notably, different microtubule-associated proteins are utilized in different cell cycles, namely STUD/TES in meiosis (Yang et al., 2003a) and GEM1 in PM I. This adds additional complexity to the regulation of cytokinesis during gametophyte development. Similar to gem1, gem2 is defective with PMI. gem2 did not affect karyokinesis at PM I, but resulted in repositioning of the cell plate and partial or complete failure of cytokinesis. Therefore, gem2 had both sister cells with vegetative cell fate or binucleate pollen grains. Furthermore, gem2 had defective cellularization of the embryo sac during megagametogenesis. gem2 maps to a different locus from gem1, but the corresponding gene is not yet known (Park et al., 2004).
In 2006, two independent groups identified the role of an Arabidopsis A-type cyclin-dependent kinase (CDKA;1, also called CDC2A) in pollen development using reverse genetics approach (Iwakawa et al., 2006; Nowack et al., 2006). In pollen of the cdc2a mutants, only one generative cell-like gamete, instead of two sperm cells, was produced due to the PM II failure. The single gamete was more like a generative cell, yet it contains 2C DNA content mirroring the wild-type sperm cell prior to fertilization. The cdc2a pollen were viable and the sperm within could exclusively fertilize the egg cell in the embryo sac rather than central cell, although the development of the fertilized embryo was arrested before the globular stage, possibly due to endosperm defects (Nowack et al., 2006). Interestingly, autonomous endosperm cell development was observed in cdc2a ovules, despite the exclusive fertilization to egg cell. These data suggest that the cell fate of sperm cells is possibly determined before the second mitosis and that there might be a positive signal from the fertilization of the egg cell to promote the onset of the endosperm cell development (Nowack et al., 2006).
Two homologous RING-finger proteins, RHF1a and RHF2a, were shown to be critical for male and female gametophyte development (Liu et al., 2008). Unlike many gametophytic mutants which affect either the male or female, the rhf1a rhf2a double mutants are defective in the formation of both male and female gametophytes: interphase arrest of the mitotic cell cycle at the microspore stage of pollen development and at the female gametophyte stage 1 (FG1) of embryo sac development. ICK4/KRP6, a CDK inhibitor, was shown to be the substrate of the RHF1a and RHF2a E3 ligases, suggesting that protein degradation machinery was adopted by plants to regulate mitotic cell cycle progression during both male and female gametogenesis.
Perspectives
Gametophyte development is a complicated developmental scenario that comprises many cellular processes. Over the past decades, much information has been gained on the cytological description of gametophyte development in Arabidopsis. However, the molecular mechanisms of this process are largely unknown. Cell divisions are fundamental biological events for gametophyte formation. Whether cell cycle regulation in gametophyte development (including male/female meiosis and mitosis) shares the same machinery with the cell cycle progression in sporophytic cells is an intriguing and interesting question. Some cell cycle regulators, involved in the sporophytic cell cycle progression or regulation such as CDC45, APC6, RBR1, and CDKA;1, are also shown to be critical for gametophyte development. These data suggest that the components used for sporophytic cell cycle regulation might also be involved in the cell division process in gametophyte development. However, the identification of SDS revealed that there are also novel and meiosis-specific components. Taken together with the phenomena that those identified cell cycle regulator genes only affect a certain round of cell division or a certain sex, it is reasonable to predict that there should be some cell cycle regulators specifically functioning in gametophyte development, not in sporophytic cell cycle processes. With the rapid progress in genetic and molecular analysis of more gametophytic mutants (Table 1 and Figure 1), and with the availability of whole genome sequences, genome-wide expression profiling, tissue-specific cDNA libraries as well as new proteomics technology, our understanding of the regulation of the meiotic and mitotic cell cycle progression during gametophyte development will be largely enlarged and deepened.
|
|
|
Acknowledgements |
|---|
The authors apologize to those whose work could not be included because of space constraints. The authors would like to thank Sheila McCormick for comments. Research in Qu laboratory is supported by the National Natural Science Foundation of China (Grant No. 30625002 to LJQ) and the 111 Project.
-
Agashe B, Prasad CK, Siddiqi I. Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development (2002) 129:3935–3943.[Web of Science][Medline]
Armstrong SJ, Caryl AP, Jones GH, Franklin FC. Asy1, a protein required for meiotic chromosome synapsis, localizes to axis-associated chromatin in Arabidopsis and Brassica. J. Cell Sci. (2002) 115:3645–3655.
Armstrong SJ, Franklin FC, Jones GH. Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J. Cell Sci. (2001) 114:4207–4217.
Azumi Y, Liu D, Zhao D, Li W, Wang G, Hu Y, Ma H. Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J. (2002) 21:3081–3095.[CrossRef][Web of Science][Medline]
Bai X, Peirson BN, Dong F, Xue C, Makaroff CA. Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell (1999) 11:417–430.
Baker BS, Carpenter AT, Esposito MS, Esposito RE, Sandler L. The genetic control of meiosis. Annu. Rev. Genet. (1976) 10:53–134.[CrossRef][Web of Science][Medline]
Bhatt AM, Lister C, Page T, Fransz P, Findlay K, Jones GH, Dickinson HG, Dean C. The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. Plant J. (1999) 19:463–472.[CrossRef][Web of Science][Medline]
Bonhomme S, Horlow C, Vezon D, de Laissardiere S, Guyon A, Ferault M, Marchand M, Bechtold N, Pelletier G. T-DNA mediated disruption of essential gametophytic genes in Arabidopsis is unexpectedly rare and cannot be inferred from segregation distortion alone. Mol. Gen. Genet. (1998) 260:444–452.[CrossRef][Web of Science][Medline]
Caryl AP, Jones GH, Franklin FC. Dissecting plant meiosis using Arabidopsis thaliana mutants. J. Exp. Bot. (2003) 54:25–38.
Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, Peacock WJ. Fertilization-independent seed development in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A (1997) 94:4223–4228.
Chen C, Marcus A, Li W, Hu Y, Calzada JP, Grossniklaus U, Cyr RJ, Ma H. The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development (2002) 129:2401–2409.[Web of Science][Medline]
Chen YC, McCormick S. sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development (1996) 122:3243–3253.[Abstract]
Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J, Shaw JM, Drews GN. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell (2002) 14:2215–2232.
Christensen CA, King E, Jordan JR, Drews GN. Megagametogenesis in Arabdopsis wild type and the Gf mutant. Sex. Plant Reprod. (1997) 10:49–64.[CrossRef]
Christensen CA, Subramanian S, Drews GN. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev. Biol. (1998) 202:136–151.[CrossRef][Web of Science][Medline]
Couteau F, Belzile F, Horlow C, Grandjean O, Vezon D, Doutriaux MP. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmc1 mutant of Arabidopsis. Plant Cell (1999) 11:1623–1634.
Doutriaux MP, Couteau F, Bergounioux C, White C. Isolation and characterisation of the RAD51 and DMC1 homologs from Arabidopsis thaliana. Mol. Gen. Genet. (1998) 257:283–291.[CrossRef][Web of Science][Medline]
Drews GN, Yadegari R. Development and function of the angiosperm female gametophyte. Annu. Rev. Genet. (2002) 36:99–124.[CrossRef][Web of Science][Medline]
Durbarry A, Vizir I, Twell D. Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol. (2005) 137:297–307.
Ebel C, Mariconti L, Gruissem W. Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature (2004) 429:776–780.[CrossRef][Web of Science][Medline]
Endow SA, Chandra R, Komma DJ, Yamamoto AH, Salmon ED. Mutants of the Drosophila ncd microtubule motor protein cause centrosomal and spindle pole defects in mitosis. J. Cell Sci. (1994) 107(Pt 4):859–867.[Abstract]
Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science (2007) 317:656–660.
Evans MM. The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo Sac and leaf development. Plant Cell (2007) 19:46–62.
Feldmann KA, Coury DA, Christianson ML. Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics (1997) 147:1411–1422.[Abstract]
Gallego ME, Jeanneau M, Granier F, Bouchez D, Bechtold N, White CI. Disruption of the Arabidopsis RAD50 gene leads to plant sterility and MMS sensitivity. Plant J (2001) 25:31–41.[CrossRef][Web of Science][Medline]
Glover J, Grelon M, Craig S, Chaudhury A, Dennis E. Cloning and characterization of MS5 from Arabidopsis: a gene critical in male meiosis. Plant J (1998) 15:345–356.[CrossRef][Web of Science][Medline]
Golubovskaya IN. Genetic control of meiosis. Int. Rev. Cytol. (1979) 58:247–290.[Medline]
Grelon M, Vezon D, Gendrot G, Pelletier G. AtSPO11–1 is necessary for efficient meiotic recombination in plants. EMBO J (2001) 20:589–600.[CrossRef][Web of Science][Medline]
Grini PE, Schnittger A, Schwarz H, Zimmermann I, Schwab B, Jurgens G, Hulskamp M. Isolation of ethyl methanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1. Genetics (1999) 151:849–863.
Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science (1998) 280:446–450.
Hartung F, Puchta H. Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res. (2000) 28:1548–1554.
Hershko A, Ganoth D, Pehrson J, Palazzo RE, Cohen LH. Methylated ubiquitin inhibits cyclin degradation in clam embryo extracts. J. Biol. Chem. (1991) 266:16376–16379.
Hollingsworth NM, Goetsch L, Byers B. The HOP1 gene encodes a meiosis-specific component of yeast chromosomes. Cell (1990) 61:73–84.[CrossRef][Web of Science][Medline]
Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics (1998) 149:621–631.
Huang BQ, Sheridan WF. Embryo sac development in the Maize indeterminate gametophyte1 mutant: abnormal nuclear behavior and defective microtubule organization. Plant Cell (1996) 8:1391–1407.[Abstract]
Hulskamp M, Parekh NS, Grini P, Schneitz K, Zimmermann I, Lolle SJ, Pruitt RE. The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev. Biol. (1997) 187:114–124.[CrossRef][Web of Science][Medline]
Iwakawa H, Shinmyo A, Sekine M. Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J (2006) 45:819–831.[CrossRef][Web of Science][Medline]
Johnson SA, McCormick S. Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol. (2001) 126:685–695.
Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell (1997) 88:375–384.[CrossRef][Web of Science][Medline]
Klimyuk VI, Jones JD. AtDMC1, the Arabidopsis homologue of the yeast DMC1 gene: characterization, transposon-induced allelic variation and meiosis-associated expression. Plant J (1997) 11:1–14.[CrossRef][Web of Science][Medline]
Kwee HS, Sundaresan V. The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the Anaphase Promoting Complex in Arabidopsis. Plant J (2003) 36:853–866.[CrossRef][Web of Science][Medline]
Lalanne E, Twell D. Genetic control of male germ unit organization in Arabidopsis. Plant Physiol. (2002) 129:865–875.
Lalanne E, Michaelidis C, Moore JM, Gagliano W, Johnson A, Patel R, Howden R, Vielle-Calzada JP, Grossniklaus U, Twell D. Analysis of transposon insertion mutants highlights the diversity of mechanisms underlying male progamic development in Arabidopsis. Genetics (2004) 167:1975–1986.
Lee JY, Orr-Weaver TL. The molecular basis of sister-chromatid cohesion. Annu. Rev. Cell Dev. Biol. (2001) 17:753–777.[CrossRef][Web of Science][Medline]
Li W, Chen C, Markmann-Mulisch U, Timofejeva L, Schmelzer E, Ma H, Reiss B. The Arabidopsis AtRAD51 gene is dispensable for vegetative development but required for meiosis. Proc. Natl Acad. Sci. U S A (2004) 101:10596–10601.
Liu J, Zhang Y, Qin G, Tsuge T, Sakaguchi N, Luo G, Sun K, Shi D, Aki S, Zheng N, Aoyama T, Oka A, Yang W, Umeda M, Xie Q, Gu H, Qu L-J. (2008). Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell (on-line published, www.plantcell.org/cgi/doi/10.1105/tpc.108.059741).
Ma H. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu. Rev. Plant Biol. (2005) 56:393–434.[CrossRef][Medline]
Magnard JL, Yang M, Chen YC, Leary M, McCormick S. The Arabidopsis gene tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiol. (2001) 127:1157–1166.
McCormick S. Male gametophyte development. Plant Cell (1993) 5:1265–1275.
McCormick S. Control of male gametophyte development. Plant Cell (2004) (16 Suppl):S142–S153.
Mercier R, Vezon D, Bullier E, Motamayor JC, Sellier A, Lefevre F, Pelletier G, Horlow C. SWITCH1 (SWI1): a novel protein required for the establishment of sister chromatid cohesion and for bivalent formation at meiosis. Genes Dev. (2001) 15:1859–1871.
Moore JM, Calzada JP, Gagliano W, Grossniklaus U. Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harb. Symp. Quant. Biol. (1997) 62:35–47.
Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A. A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat. Genet. (2006) 38:63–67.[Web of Science][Medline]
Ohad N, Margossian L, Hsu YC, Williams C, Repetti P, Fischer RL. A mutation that allows endosperm development without fertilization. Proc. Natl Acad. Sci. U S A (1996) 93:5319–5324.
Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie LF, Ye D, Sundaresan V. Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development (2005) 132:603–614.
Park SK, Twell D. Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen1 mutant. Plant Physiol. (2001) 126:899–909.
Park SK, Howden R, Twell D. The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development (1998) 125:3789–3799.[Abstract]
Park SK, Rahman D, Oh SA, Twell D. gemini pollen 2, a male and female gametophytic cytokinesis defective mutation. Sex. Plant Reprod. (2004) 17:63–70.
Peirson BN, Owen HA, Feldmann KA, Makaroff CA. Characterization of three male-sterile mutants of Arabidopsis thaliana exhibiting alterations in meiosis. Sex. Plant Reprod. (1996) 9:1–16.
Preuss D. Being fruitful: genetics of reproduction in Arabidopsis. Trends Genet. (1995) 11:147–153.[CrossRef][Web of Science][Medline]
Puizina J, Siroky J, Mokros P, Schweizer D, Riha K. Mre11 deficiency in Arabidopsis is associated with chromosomal instability in somatic cells and Spo11-dependent genome fragmentation during meiosis. Plant Cell (2004) 16:1968–1978.
Reddy TV, Kaur J, Agashe B, Sundaresan V, Siddiqi I. The DUET gene is necessary for chromosome organization and progression during male meiosis in Arabidopsis and encodes a PHD finger protein. Development (2003) 130:5975–5987.
Roeder GS. Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends Genet. (1990) 6:385–389.[CrossRef][Web of Science][Medline]
Ross KJ, Fransz P, Jones GH. A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res. (1996) 4:507–516.[CrossRef][Web of Science][Medline]
Ross KJ, Fransz P, Armstrong SJ, Vizir I, Mulligan B, Franklin FC, Jones GH. Cytological characterization of four meiotic mutants of Arabidopsis isolated from T-DNA-transformed lines. Chromosome Res. (1997) 5:551–559.[CrossRef][Web of Science][Medline]
Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D. A novel class of MYB factors controls sperm-cell formation in plants. Curr. Biol. (2005) 15:244–248.[CrossRef][Web of Science][Medline]
Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, LEE PY, Truong MT, Beals TP, Goldberg RB. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. (1999) 11:297–322.[CrossRef]
Schommer C, Beven A, Lawrenson T, Shaw P, Sablowski R. AHP2 is required for bivalent formation and for segregation of homologous chromosomes in Arabidopsis meiosis. Plant J (2003) 36:1–11.[CrossRef][Web of Science][Medline]
Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC. SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell (2005) 17:2340–2354.
Siddiqi I, Ganesh G, Grossniklaus U, Subbiah V. The dyad gene is required for progression through female meiosis in Arabidopsis. Development (2000) 127:197–207.[Abstract]
Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development (1997) 124:2645–2657.[Abstract]
Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA. The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development (2000) 127:1815–1822.[Abstract]
Springer PS, McCombie WR, Sundaresan V, Martienssen RA. Gene trap tagging of PROLIFERA, an essential MCM2–3–5-like gene in Arabidopsis. Science (1995) 268:877–880.
Stevens R, Grelon M, Vezon D, Oh J, Meyer P, Perennes C, Domenichini S, Bergounioux C. A CDC45 homolog in Arabidopsis is essential for meiosis, as shown by RNA interference-induced gene silencing. Plant Cell (2004) 16:99–113.
Stoop-Myer C, Amon A. Meiosis: Rec8 is the reason for cohesion. Nat. Cell Biol. (1999) 1:E125–E127.[CrossRef][Web of Science][Medline]
Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat. Cell Biol. (2002) 4:711–714.[CrossRef][Web of Science][Medline]
van Heemst D, Heyting C. Sister chromatid cohesion and recombination in meiosis. Chromosoma (2000) 109:10–26.[CrossRef][Web of Science][Medline]
von Besser K, Frank AC, Johnson MA, Preuss D. Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development (2006) 133:4761–4769.
Wang Y, Magnard JL, McCormick S, Yang M. Progression through meiosis I and meiosis II in Arabidopsis anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiol. (2004) 136:4127–4135.
Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J (2003a) 34:229–240.[CrossRef][Web of Science][Medline]
Yang M, Hu Y, Lodhi M, McCombie WR, Ma H. The Arabidopsis SKP1-LIKE1 gene is essential for male meiosis and may control homologue separation. Proc. Natl Acad. Sci. U S A (1999a) 96:11416–11421.
Yang WC, Sundaresan V. Genetics of gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. (2000) 3:53–57.
Yang WC, Ye D, Xu J, Sundaresan V. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes Dev. (1999b) 13:2108–2117.
Yang X, Makaroff CA, Ma H. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell (2003b) 15:1281–1295.
Zachariae W, Nasmyth K. Whose end is destruction: cell division and the anaphase-promoting complex. Genes Dev. (1999) 13:2039–2058.
Zickler D, Kleckner N. Meiotic chromosomes: integrating structure and function. Annu. Rev. Genet. (1999) 33:603–754.[CrossRef][Web of Science][Medline]
Zou L, Stillman B. Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol. Cell Biol. (2000) 20:3086–3096.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||