During meiosis, homologous chromosomes synapse and recombine at sites marked by the binding of the mismatch repair protein MLH1. In hexaploid wheat, the Ph1 locus has a major effect on whether crossover occurs between homologues or between related homoeologues. Here we report that—in wheat–rye hybrids where homologues are absent—Ph1 affects neither the level of synapsis nor the number of MLH1. Thus in the case of wheat–wild relative hybrids, Ph1 must affect whether MLH1 sites are able to progress to crossover. The observed level of synapsis implies that Ph1 functions to promote homologue pairing rather than suppress homoeologue pairing in wheat. Therefore, Ph1 stabilises polyploidy in wheat by both promoting homologue pairing and preventing MLH1 sites from becoming crossovers on paired homoeologues during meiosis.

Significance: Homologous chromosome pairing ensures that each product of meiosis contains a full haploid genome complement and is particularly important in allopolyploid plants which contain multiple, genetically related sets of chromosomes. In domesticated allohexaploid wheat, the Ph1 locus drives homologous bivalent formation and is required to maintain genome stability and disomic inheritance. In this study, we show that the most closely related gene in Arabidopsis , the cyclin-dependent protein kinase CDKG1, also functions in chromosome pairing and is required for the completion of synapsis in male meiocytes at high ambient temperature. This class of CDK has been previously implicated in RNA splicing and may be responsible for the intrinsic temperature sensitivity of meiosis in males.

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).