Journal of Genetics and Genomics

Meiosis: Recent Progress and New Opportunities

Hong Ma, Howard J. Cooke, Qinghua Shi

2014, 41(3): 83-85. doi: 10.1016/j.jgg.2014.01.004

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Reconstitution of Gametogenesis In Vitro: Meiosis Is the Biggest Obstacle

Yuan-Chao Sun, Shun-Feng Cheng, Rui Sun, Yong Zhao, Wei Shen

2014, 41(3): 87-95. doi: 10.1016/j.jgg.2013.12.008

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Germ-line cells are responsible for transmitting genetic and epigenetic information across generations, and ensuring the creation of new individuals from one generation to the next. Gametogenesis process requires several rigorous steps, including primordial germ cell (PGC) specification, proliferation, migration to the gonadal ridges and differentiation into mature gametes such as sperms and oocytes. But this process is not clearly explored because a small number of PGCs are deeply embedded in the developing embryo. In the attempt to establish an in vitro model for understanding gametogenesis process well, several groups have made considerable progress in differentiating embryonic stem cells (ESCs) and adult stem cells (ASCs) into germ-like cells over the past ten years. These stem cell-derived germ cells appear to be capable of undergoing meiosis and generating both male and female gametes. But most of gametes turn out to be not fully functional due to their abnormal meiosis process compared to endogenous germ cells. Therefore, a robust system of differentiating stem cells into germ cells would enable us to investigate the genetic, epigenetic and environmental factors associated with germ cell development. Here, we review the stem cell-derived germ cell development, and discuss the potential and challenges in the differentiation of functional germ cells from stem cells.

The Role of Chromatin Modifications in Progression through Mouse Meiotic Prophase

James H. Crichton, Christopher J. Playfoot, Ian R. Adams

2014, 41(3): 97-106. doi: 10.1016/j.jgg.2014.01.003

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Meiosis is a key event in gametogenesis that generates new combinations of genetic information and is required to reduce the chromosome content of the gametes. Meiotic chromosomes undergo a number of specialised events during prophase to allow meiotic recombination, homologous chromosome synapsis and reductional chromosome segregation to occur. In mammalian cells, DNA physically associates with histones to form chromatin, which can be modified by methylation, phosphorylation, ubiquitination and acetylation to help regulate higher order chromatin structure, gene expression, and chromosome organisation. Recent studies have identified some of the enzymes responsible for generating chromatin modifications in meiotic mammalian cells, and shown that these chromatin modifying enzymes are required for key meiosis-specific events that occur during meiotic prophase. This review will discuss the role of chromatin modifications in meiotic recombination, homologous chromosome synapsis and regulation of meiotic gene expression in mammals.

The Synaptonemal Complex of Basal Metazoan Hydra: More Similarities to Vertebrate than Invertebrate Meiosis Model Organisms

Johanna Fraune, Miriam Wiesner, Ricardo Benavente

2014, 41(3): 107-115. doi: 10.1016/j.jgg.2014.01.009

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The synaptonemal complex (SC) is an evolutionarily well-conserved structure that mediates chromosome synapsis during prophase of the first meiotic division. Although its structure is conserved, the characterized protein components in the current metazoan meiosis model systems (Drosophila melanogaster, Caenorhabditis elegans, and Mus musculus) show no sequence homology, challenging the question of a single evolutionary origin of the SC. However, our recent studies revealed the monophyletic origin of the mammalian SC protein components. Many of them being ancient in Metazoa and already present in the cnidarian Hydra. Remarkably, a comparison between different model systems disclosed a great similarity between the SC components of Hydra and mammals while the proteins of the ecdysozoan systems (D. melanogaster and C. elegans) differ significantly. In this review, we introduce the basal-branching metazoan species Hydra as a potential novel invertebrate model system for meiosis research and particularly for the investigation of SC evolution, function and assembly. Also, available methods for SC research in Hydra are summarized.

Molecular Mechanisms of Homologous Chromosome Pairing and Segregation in Plants

Jing Zhang, Bing Zhang, Handong Su, James A. Birchler, Fangpu Han

2014, 41(3): 117-123. doi: 10.1016/j.jgg.2013.12.003

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In most eukaryotic species, three basic steps of pairing, recombination and synapsis occur during prophase of meiosis I. Homologous chromosomal pairing and recombination are essential for accurate segregation of chromosomes. In contrast to the well-studied processes such as recombination and synapsis, many aspects of chromosome pairing are still obscure. Recent progress in several species indicates that the telomere bouquet formation can facilitate homologous chromosome pairing by bringing chromosome ends into close proximity, but the sole presence of telomere clustering is not sufficient for recognizing homologous pairs. On the other hand, accurate segregation of the genetic material from parent to offspring during meiosis is dependent on the segregation of homologs in the reductional meiotic division (MI) with sister kinetochores exhibiting mono-orientation from the same pole, and the segregation of sister chromatids during the equational meiotic division (MII) with kinetochores showing bi-orientation from the two poles. The underlying mechanism of orientation and segregation is still unclear. Here we focus on recent studies in plants and other species that provide insight into how chromosomes find their partners and mechanisms mediating chromosomal segregation.

Ten Years of Gene Discovery for Meiotic Event Control in Rice

Qiong Luo, Yafei Li, Yi Shen, Zhukuan Cheng

2014, 41(3): 125-137. doi: 10.1016/j.jgg.2014.02.002

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Meiosis is the crucial process by which sexually propagating eukaryotes give rise to haploid gametes from diploid cells. Several key processes, like homologous chromosomes pairing, synapsis, recombination, and segregation, sequentially take place in meiosis. Although these widely conserved events are under both genetic and epigenetic control, the accurate details of molecular mechanisms are continuing to investigate. Rice is a good model organism for exploring the molecular mechanisms of meiosis in higher plants. So far, 28 rice meiotic genes have been characterized. In this review, we give an overview of the discovery of rice meiotic genes in the last ten years, with a particular focus on their functions in meiosis.

Comparative Transcriptomics of Early Meiosis in Arabidopsis and Maize

Stefanie Dukowic-Schulze, Anthony Harris, Junhua Li, Anitha Sundararajan, Joann Mudge, Ernest F. Retzel, Wojciech P. Pawlowski, Changbin Chen

2014, 41(3): 139-152. doi: 10.1016/j.jgg.2013.11.007

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Though sexually reproductive plants share the same principle and most processes in meiosis, there are distinct features detectable. To address the similarities and differences of early meiosis transcriptomes from the dicot model system Arabidopsis and monocot model system maize, we performed comparative analyses of RNA-seq data of isolated meiocytes, anthers and seedlings from both species separately and via orthologous genes. Overall gene expression showed similarities, such as an increased number of reads mapping to unannotated features, and differences, such as the amount of differentially expressed genes. We detected major similarities and differences in functional annotations of genes up-regulated in meiocytes, which point to conserved features as well as unique features. Transcriptional regulation seems to be quite similar in Arabidopsis and maize, and we could reveal known and novel transcription factors and cis-regulatory elements acting in early meiosis. Taken together, meiosis between Arabidopsis and maize is conserved in many ways, but displays key distinctions that lie in the patterns of gene expression.

Expression of Epitope-Tagged SYN3 Cohesin Proteins Can Disrupt Meiosis in Arabidopsis

Li Yuan, Xiaohui Yang, Dirk Auman, Christopher A. Makaroff

2014, 41(3): 153-164. doi: 10.1016/j.jgg.2013.11.006

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α-kleisins are core components of meiotic and mitotic cohesin complexes. Arabidopsis contains genes encoding four α-kleisins. SYN1, a REC8 ortholog, is essential for meiosis, while SYN2 and SYN4 appear to be SCC1 orthologs and function in mitosis. SYN3 is enriched in the nucleolus of meiotic and mitotic cells and is essential for megagametogenesis. It was recently shown that expression of SYN3-RNAi constructs in buds cause changes in meiotic gene expression that result in meiotic alterations. In this report we show that expression of SYN3 from the 35S promoter with either a c-terminal Myc or FAST tag causes a reduction in SYN1 mRNA levels that results in alterations in sister chromatid cohesion, homologous chromosome synapsis and synaptonemal complex formation during both male and female meiosis.

Arabidopsis PTD Is Required for Type I Crossover Formation and Affects Recombination Frequency in Two Different Chromosomal Regions

Pingli Lu, Asela J. Wijeratne, Zhengjia Wang, Gregory P. Copenhaver, Hong Ma

2014, 41(3): 165-175. doi: 10.1016/j.jgg.2014.02.001

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In eukaryotes, crossovers together with sister chromatid cohesion maintain physical association between homologous chromosomes, ensuring accurate chromosome segregation during meiosis I and resulting in exchange of genetic information between homologues. The Arabidopsis PTD (Parting Dancers) gene affects the level of meiotic crossover formation, but its functional relationships with other core meiotic genes, such as AtSPO11-1, AtRAD51, and AtMSH4, are unclear; whether PTD has other functions in meiosis is also unknown. To further analyze PTD function and to test for epistatic relationships, we compared the meiotic chromosome behaviors of Atspo11-1 ptd and Atrad51 ptd double mutants with the relevant single mutants. The results suggest that PTD functions downstream of AtSPO11-1 and AtRAD51 in the meiotic recombination pathway. Furthermore, we found that meiotic defects in rck ptd and Atmsh4 ptd double mutants showed similar meiotic phenotypes to those of the relevant single mutants, providing genetic evidences for roles of PTD and RCK in the type I crossovers pathway. Moreover, we employed a pollen tetrad-based fluorescence method and found that the meiotic crossover frequencies in two genetic intervals were significantly reduced from 6.63% and 22.26% in wild-type to 1.14% and 6.36%, respectively, in the ptd-2 mutant. These results revealed new aspects ofPTD function in meiotic crossover formation.

Meiotic Chromosome Behavior in a Human Male t(8;15) Carrier

Hanwei Jiang, Liu Wang, Yingxia Cui, Zhipeng Xu, Tonghang Guo, Dongkai Cheng, Peng Xu, Wen Yu, Qinghua Shi

2014, 41(3): 177-185. doi: 10.1016/j.jgg.2014.01.005

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Reciprocal translocation is one of the most common structural chromosomal rearrangements in human beings; it is widely recognized to be associated with male infertility. This association is mainly based on the abnormal chromosome behavior of the translocated chromosomes and sex chromosomes during meiosis prophase I in reciprocal translocation carriers. However, the underlying mechanisms are not completely known. Here we report a reciprocal translocation carrier of t(8;15), who is oligozoospermic due to apoptosis of primary spermatocytes and to premature germ cell desquamation from seminiferous tubules. Further analysis showed abnormal synapsis and recombination frequency in this patient, indicating a connection between chromosome behavior and apoptosis of primary spermatocytes. We also compared these observations with recently reported findings on spermatogenesis defects in reciprocal translocation carriers, and discuss the possible mechanisms underlying both common and unique phenotypes of reciprocal translocations involving different chromosomes with the aim of further understanding the regulation of human spermatogenesis.

2014 Vol. 41, No. 3