Abstract
Reciprocal crossing over and independent assortment of chromosomes during meiosis generate most of the genetic variation in sexually reproducing organisms. In barley, crossovers are confined primarily to distal regions of the chromosomes, which means that a substantial proportion of the genes of this crop rarely, if ever, engage in recombination events. There is potentially much to be gained by redistributing crossovers to more proximal regions, but our ability to achieve this is dependent upon a far better understanding of meiosis in this species. This study explores the meiotic process by describing with unprecedented resolution the early behaviour of chromosomal domains, the progression of synapsis and the structure of the synaptonemal complex (SC). Using a combination of molecular cytogenetics and advanced fluorescence imaging, we show for the first time in this species that non-homologous centromeres are coupled prior to synapsis. We demonstrate that at early meiotic prophase the loading of the SC-associated structural protein ASY1, the cluster of telomeres, and distal synaptic initiation sites occupy the same polarised region of the nucleus. Through the use of advanced 3D image analysis, we show that synapsis is driven predominantly from the telomeres, and that new synaptic initiation sites arise during zygotene. In addition, we identified two different SC configurations through the use of super-resolution 3D structured illumination microscopy (3D-SIM).
Highlights
Genetic variation in most sexually reproducing organisms is generated during meiosis by reciprocal crossing over between homologous chromosomes, and independent assortment of maternal and paternal chromosomes
We demonstrate by monitoring the molecular assembly of the synaptonemal complex (SC) that synapsis is driven from the telomeres, and that additional synaptic initiation sites are added throughout zygotene
In order to correlate centromere and telomere behaviour with the assembly of SC components, and to verify the identity of meiotic nuclei, FISH with centromere and telomere probes was combined with immunolocalisation of ASY1 in embedded meiocytes
Summary
Genetic variation in most sexually reproducing organisms is generated during meiosis by reciprocal crossing over between homologous chromosomes, and independent assortment of maternal and paternal chromosomes. Crossover interference in many organisms prevents the clustering of crossovers, and effectively caps the numbers of crossovers a bivalent may have. Superimposed on these constraints on crossover frequency and distribution is a phenomenon which confines crossovers to particular chromosome regions in some organisms. Mayer et al [5] have estimated that 3125 genes of barley map to regions classified as genetic centromeres, and one third (6788) of all genes of the barley genome fall within 10cM of these regions This corroborates the long-held view that a substantial proportion of the genes of the cereals and grasses are consigned to recombinationally cold regions of the genome, and rarely, if ever, recombines. There is potentially much to be gained by redistributing crossovers to more interstitial and proximal regions of chromosomes, which is dependent upon a detailed understanding of the process of meiosis and recombination in these crop species
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