An understanding of the regulation of entry into meiosis and molecular mechanisms of apomictic pathway will provide vital insight into reproduction for plant breeding. However, the mechanism for the initiation of meiosis during sexual reproduction or for its omission in the apomictic pathway still remains largely unknown.
Here we review the current understanding of meiosis initiation and the apomictic pathway and raised several questions that are awaiting further investigation. Meiosis is an extremely important step in sexual reproduction.
It is widely accepted that it evolved from mitosis and shares certain features with mitosis Maynard Smith, Yet at least three meiosis-specific events make meiosis a specialized cell division: meiotic recombination and pairing between homologous chromosomes during prophase I, the suppression of sister-chromatid separation during the first meiotic division, and the absence of chromosome replication at the start of the second division Kleckner, While these meiosis-specific events have been studied extensively, the mechanisms that switch mitosis into meiosis are still puzzling.
In multicellular organisms, meiosis initiation takes place within multicellular organs; consequently, mechanisms that initiate meiosis must integrate developmental cues. In plants, the decision to start meiosis may also be connected with reproductive cell fate specification since plants do not have pre-determined germ lines.
Thus, the switch of somatic fate to germinal cell fate and the mitosis—meiosis cell cycle transition occur sequentially during the development of reproductive organs i.
Importantly, these sexual processes can be replaced by the asexual apomictic pathway in which meiosis is bypassed or a mitosis-like division occurs to produce unreduced daughter cells, followed by the development of an embryo without fertilization, apomictic plants can then produce diploid seeds with identical genetic content to their maternal genome. This phenomenon is called apomixis that occurs naturally in some flowering plants Barcaccia and Albertini, If apomixis is engineered into crops to produce clonal seeds, its application on agriculture will be broad and profound.
Here, we review the current understanding of the cell cycle transition that directs sporogenous cells to leave the mitotic cell cycle and enter the meiotic program in higher plants and additionally discuss advances in the apomictic pathway. The cellular events during meiosis are evolutionarily conserved among species; however, the mechanisms controlling the initiation of meiosis are diverse Pawlowski et al. The molecular controls elucidated to date involve signaling pathways, transcriptional and translational regulations of meiotic genes, and cyclin-dependent kinase CDK circuits.
Although different mechanisms are adopted, the final readout is likely the activation of a specific cyclin—CDK complex to initiate the meiotic S phase. It was also suggested from many studies that the decision to start meiosis is made before the onset of the pre-meiotic S phase Watanabe et al. Here, we first summarize the discoveries from several model species, and then discuss recent advances in plants. The meiosis decision in single-celled yeasts is often cued by environmental conditions.
In the budding yeast Saccharomyces cerevisiae , starvation induces expression of the Initiator of Meiosis I IME1 gene, which encodes a transcription factor responsible for activating early meiotic genes Chu et al. In fission yeast S. Under meiosis-inducing conditions, this repression of MEI2 is released, allowing binding to and stabilization of meiosis-specific mRNAs at the G1 phase Kitamura et al.
In addition, this process reinforces stabilization also by sequestrating MMI1 protein, which function is to eliminate these meiotic mRNAs Harigaya et al. Recently, protein S-palmitoylation, a lipid modification was also found to regulate the entry into meiosis Zhang et al. In mammals, meiosis is initiated at different stages of development in females and males Bowles and Koopman, Mouse studies have revealed that retinoic acid RA produced during embryonic development can induce meiosis in both sexes.
Stimulated by RA 8 Stra8 , a vertebrate-specific gene, is then induced by RA and is required for the transition to meiosis Anderson et al. Stra8 plays no role in the mitotic phases of embryonic germ-cell development, but in females it is required for pre-meiotic DNA replication and the subsequent events of meiotic prophase.
On the other hand, Dmrt1 represses Stra8 transcription in the mitotic phase, thereby preventing meiosis Matson et al. From these studies, the mechanisms that initiate meiosis are very different, and more importantly, the genes involved share no similarity. No doubt different strategies evolved because of the different reproductive requirements of diverse organisms.
In plants, meiosis is initiated in sporogenous cells that are differentiated in ovules and anthers Bhatt et al. In each ovule, only a single megaspore mother cell MMC surrounded by the somatic nucellar cells is differentiated and then undergoes meiosis Figure 1.
During anther development, after primary sporogenous cells i. Thus, the decision of mitosis—meiosis transition must coordinate with the developmental stages of anthers and ovules. For example, the signal that starts meiosis in an anther must be generated after complete development of the somatic layers of anthers Kelliher and Walbot, Interestingly, the signal can also establish the synchronization of the meiotic cell cycle in an anther.
On the other hand, only a single MMC in each ovule is specified to enter meiosis, which accompanies the development of ovule in parallel. Thus, the regulatory mechanism of meiosis initiation may be different between female and male in plants because of distinct development of sporogenesis.
Structure of plant reproductive organs in maize and sequence of events leading to spore or gametophyte formation in anthers and ovules. A Longitudinal section of an anther with numerous pollen mother cells PMCs, shown in gray that are proliferated from primary sporogenous cells by mitosis, which accompanies the development of surrounding 4 layers of somatic cells.
By the time when the development of surrounding somatic cells shown in A is complete, unknown meiosis initiation siganl is generated to start meisois synchronously in all PMCs of an anther.
Each PMC enters meiosis to produce four haploid spore cells. C Longitudinal section of an ovule with a single megaspore mother cell MMC, shown in gray. D Schematic illustration showing the sequential development of embryo sac through sexual reproduction or apomictic pathways. In sexual reproduction, the single MMC shown in gray is differentiated and then enters meiosis to produce a haploid functional megaspore FMS , and then develops into an embryo sac.
In apospory apomixis, somatic nucellar cells develop into embryo sac without meiosis. The first discovery about meiosis initiation was the isolation of the maize ameiotic1 am1 mutant by Rhoades The original am1 mutant allele does not undergo meiosis; instead mitosis-like divisions take place in well-developed meiocytes in both female and male organs Golubovskaya et al.
Am1 encodes a plant specific coiled-coil protein with unknown functions Pawlowski et al. All five null mutant alleles display identical phenotypes in male meiocytes in which mitosis replaces meiosis. However, female MMCs in the mutant may either undergo mitosis, or arrest at interphase. These results suggest that AM1 is required for meiosis initiation and may also regulate meiotic progression. These differences among species may indicate that the AM1-related genes have undergone species-specific diversification.
Using Agilent 44K microarrays, the authors compared transcriptomes in 1-mm and 1. In 1-mm anthers when meiosis is about to start in the wild-type, genes were missing and genes were ectopically expressed in am anthers. Both males and females use meiosis to produce their gametes, although there are some key differences between the sexes at certain stages. In females, the process of meiosis is called oogenesis, since it produces oocytes and ultimately yields mature ova eggs.
The male counterpart is spermatogenesis, the production of sperm. While they occur at different times and different locations depending on the sex, both processes begin meiosis in essentially the same way.
In preparation for meiosis , a germ cell goes through interphase, during which the entire cell including the genetic material contained in the nucleus undergoes replication. In order to undergo replication during interphase, the DNA deoxyribonucleic acid, the carrier of genetic information and developmental instructions is unraveled in the form of chromatin.
While replicating somatic cells follow interphase with mitosis , germ cells instead undergo meiosis. For clarity, the process is artificially divided into stages and steps; in reality, it is continuous and the steps generally overlap at transitions. The two-stage process of meiosis begins with meiosis I, also known as reduction division since it reduces the diploid number of chromosomes in each daughter cell by half. This first step is further subdivided into four main stages: prophase I, metaphase I, anaphase I, and telophase I.
Each stage is identified by the major characteristic events in its span which allow the dividing cell to progress toward the completion of meiosis. Prophase I takes up the greatest amount of time, especially in oogenesis.
The dividing cell may spend more than 90 percent of meiosis in Prophase I. Because this particular step includes so many events, it is further subdivided into six substages, the first of which is leptonema.
During leptonema, the diffuse chromatin starts condensing into chromosomes. Each of these chromosomes is double stranded, consisting of two identical sister chromatids which are held together by a centromere; this arrangement will later give each chromosome a variation on an X-like shape, depending on the positioning of the centromere. In the next substage, zygonema, there is further condensation of the chromosomes. As they come into closer contact, a protein compound called the synaptonemal complex forms between each pair of double-stranded chromosomes.
As Prophase I continues into its next substage, pachynema, the homologous chromosomes move even closer to each other as the synaptonemal complex becomes more intricate and developed. This process is called synapsis, and the synapsed chromosomes are called a tetrad.
The tetrad is composed of four chromatids which make up the two homologous chromosomes. Crossover between these homologous regions ensures that the sex chromosomes will segregate properly when the cell divides. Next, during anaphase I , the pairs of homologous chromosomes separate to different daughter cells.
Before the pairs can separate, however, the crossovers between chromosomes must be resolved and meiosis-specific cohesins must be released from the arms of the sister chromatids. Failure to separate the pairs of chromosomes to different daughter cells is referred to as nondisjunction , and it is a major source of aneuploidy. Overall, aneuploidy appears to be a relatively frequent event in humans. Meiosis II resembles a mitotic division, except that the chromosome number has been reduced by half.
Thus, the products of meiosis II are four haploid cells that contain a single copy of each chromosome. In mammals, the number of viable gametes obtained from meiosis differs between males and females.
In males, four haploid spermatids of similar size are produced from each spermatogonium. In females, however, the cytoplasmic divisions that occur during meiosis are very asymmetric.
Fully grown oocytes within the ovary are already much larger than sperm, and the future egg retains most of this volume as it passes through meiosis. As a consequence, only one functional oocyte is obtained from each female meiosis Figure 2.
The other three haploid cells are pinched off from the oocyte as polar bodies that contain very little cytoplasm. Prophase I is the longest and arguably most important segment of meiosis, because recombination occurs during this interval. For many years, cytologists have divided prophase I into multiple segments, based upon the appearance of the meiotic chromosomes. Thus, these scientists have described a leptotene from the Greek for "thin threads" phase, which is followed sequentially by the zygotene from the Greek for "paired threads" , pachytene from the Greek for "thick threads" , and diplotene from the Greek for "two threads" phases.
In recent years, cytology and genetics have come together so that researchers now understand some of the molecular events responsible for the stunning rearrangements of chromatin observed during these phases.
Recall that prophase I begins with the alignment of homologous chromosome pairs. Historically, alignment has been a difficult problem to approach experimentally, but new techniques for visualizing individual chromosomes with fluorescent probes are providing insights into the process. Recent experiments suggest that chromosomes from some species have specific sequences that act as pairing centers for alignment. In some cases, alignment appears to begin as early as interphase, when homologous chromosomes occupy the same territory within the interphase nucleus Figure 5.
The formation of DSBs is catalyzed by highly conserved proteins with topoisomerase activity that resemble the Spo11 protein from yeast. Genetic studies have shown that Spo11 activity is essential for meiosis in yeast, because spo11 mutants fail to sporulate.
As the invading strand is extended, a remarkable structure called synaptonemal complex SC develops around the paired homologues and holds them in close register, or synapsis. The stability of the SC increases as the invading strand first extends into the homologue and then is recaptured by the broken chromatid, forming double Holliday junctions. Investigators have been able to observe the process of SC formation with electron microscopy in meiocytes from the Allium plant Figure 6.
Bridges approximately nanometers long begin to form between the paired homologues following the DSB. Only a fraction of these bridges will mature into SC; moreover, not all Holliday junctions will mature into crossover sites. Gerton, J. Homologous chromosome interactions in meiosis: Diversity amidst conservation.
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Science , — Petes, T. Meiotic recombination hot spots and cold spots. Zickler, D. The meiotic spindle forms again. Metaphase II: In each of the two daughter cells the chromosomes pair of sister chromatids line up end-to-end along the equator of the cell. The centrioles are now at opposites poles in each of the daughter cells. Meiotic spindle fibres at each pole of the cell attach to each of the sister chromatids. Anaphase II: The sister chromatids are then pulled to opposite poles due to the action of the meiotic spindle.
The separated chromatids are now individual chromosomes. Telophase II and cytokinesis: The chromosomes complete their move to the opposite poles of the cell. A membrane forms around each set of chromosomes to create two new cell nuclei. This is the last phase of meiosis, however cell division is not complete without another round of cytokinesis.
Once cytokinesis is complete there are four granddaughter cells, each with half a set of chromosomes haploid : in males, these four cells are all sperm cells in females, one of the cells is an egg cell while the other three are polar bodies small cells that do not develop into eggs.
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