Meiotic Crossover Control is Related to Cohesin Proteins in Tomato

In most multicellular eukaryotes, synaptonemal complex (SC) formation between pairs of homologous chromosomes (bivalents) during prophase I of meiosis is closely linked with crossing over.  Asynaptic mutants reduce the amount of SC formation (synapsis), which, in plants, is often associated with the presence of univalents.  Univalents arise when no crossover occurs between bivalents, and univalents segregate randomly at anaphase I, resulting in genetically unbalanced gametes and reduced fertility.  Offspring recovered from some asynaptic plant mutants showed the expected reduced levels of crossing over, while other mutants showed higher crossover frequencies.  Both types of mutants often had elevated frequencies of double crossovers.  To investigate the unexpectedly high level of crossing over associated with reduced synapsis, we examined spreads of SCs from the as1 mutant of tomato using both light and electron microscopic immunolocalization.  The as1 mutation is a monogenic, recessive, meiosis-specific mutation that causes incomplete synapsis and frequent univalent formation with little or no effect on crossover frequency except for a higher rate of double crossovers.  We found that spreads of SCs from homozygous as1 microsporocytes have increased numbers of MLH1 foci (a crossover marker) per unit length of SC compared to wild-type.  These changes are associated with reduced levels of detectable cohesin proteins in the axial and lateral elements (AE/LEs) of SCs, and the AE/LEs of as1 mutants are also significantly longer than those of wild-type or another asynaptic tomato mutant.  These results indicate that chromosome axis structure, synapsis, and crossover control are all closely linked in plants.