The Meiotic SUN Belt of Maize Is Disrupted By Mutants Defective in Chromosome Segregation

The nuclear envelope (NE) is increasingly recognized as not just a partition, but an active link transducing forces between the cytoplasm and the sucleoplasm.  During the prophase of meiosis I, the NE carries out the specialized functions associated with the vital processes of meiotic chromosome pairing and recombination.  Resident NE proteins such as SUN or KASH connect the cytoskeleton and chromosomes through telemeres or chromosome pairing centers.  Although plant SUN proteins have been identified in several species, their precise role remains to be fully defined.  We found by 3D fluorescence microscopy that peptide antibodies raised against ZmSUN2, a C-terminal SUN domain proteins of maize, stained a novel banded belt-like structure that encircled the entire nucleus during most of meiotic prophase.  Interestingly, at the zygotene stage, the staining pattern changed to a partial band that included the NE-associated telomere cluster known as the bouquet.  This meiotic SUN belt did not show obvious colocalization with microtubules or microfilaments, although early prophase nuclei exhibited a typical pattern tubulin staining enriched around large areas of the entire nucleus.  We took a genetic approach to investigate the functional significance this SUN structure.  We found that three different meiosis-specific mutants, desynaptic (dy1), asynaptic1 (as1), and divergent spindle1 (dv1), disrupted the 3D SUN staining patterns and nuclear morphology.  These results suggest the possibility of multiple functions for the meiotic SUN belt in telomere dynamics, chromosome synapsis, and integrating signals and forces across the nuclear envelope during meiotic prophase.