In mammals, Samp1, a conserved inner nuclear membrane protein, encases mitotic spindles to ensure proper centrosome positioning. In C. elegans, loss of the homolog, SAMP-1, causes embryonic lethality. Whereas the maternally-rescued animals are sterile, hermaphrodite sterility was rescued with wild-type sperm suggesting a critical role of SAMP-1 in spermatogenesis. SAMP-1 undergoes dynamic localization during male meiosis. In the proliferative zone and early meiotic prophase SAMP-1 accumulated at the nuclear periphery as expected for a nuclear envelope protein in both hermaphrodite and male germ cells. In contrast to hermaphrodites, in late meiotic prophase SAMP-1 underwent dramatic movement in male germ cells. During diplotene and karyosome stage SAMP-1 was detected in the nucleoplasm and as paired homologs started congressing to the metaphase plate it formed a ring-like structure around the mid-bivalent. Although still detectable at the contact surfaces of segregating homologs during early anaphase I, SAMP-1 departed during late anaphase I and then reappeared between sister chromatids in metaphase II. SAMP-1 failed to accumulate on the unpaired X at metaphase I but was on X sisters at metaphase II. While we observed enrichment of SAMP-1 on the synapsed X chromosomes of tra-2
) XX males, accumulation was abrogated in the absence of HIM-8, which is required for X chromosome pairing and synapsis. Moreover, SAMP-1 failed to accumulate on asynapsed chromosome Vs in zim-2
) mutants. These results suggest that SAMP-1 binds specifically to the interface between bivalents at meiosis I. In metaphase I the area in between bivalents also contained the integral membrane ER signal peptidase subunit (SP12) homolog (C34B2.10), suggesting that there is a membranous domain between the bivalents. Depletion of SAMP-1 resulted in disorganized chromosomes and the formation of multipolar spindles as well as altered localization of the meiotic cohesin REC-8. In wild-type male germ lines, REC-8 localizes along both long and short arms of metaphase I chromosomes. Whereas in SAMP-1 depleted nuclei REC-8 was missing from the sister chromatid interface, it ectopically localized to the spindle poles. Similar REC-8 mislocalization was seen in mat-2
) (APC) mutants arrested in metaphase I suggesting that loss of SAMP-1 results in metaphase I arrest followed by multipolar spindle formation. Together, these results reveal a previously unrecognized role of the inner nuclear envelope protein SAMP-1 in the regulation of cohesion release at the metaphase-anaphase transition during meiosis.