Summary Faithful genome propagation requires coordination between nuclear envelope (NE) breakdown, spindle formation and chromosomal events. The conserved ‘linker of nucleoskeleton and cytoskeleton’ (LINC) complex connects fission yeast centromeres and the centrosome, across the NE, during interphase. During meiosis, LINC connects the centrosome with telomeres rather than centromeres. We previously showed that loss of telomere-LINC contacts compromises meiotic spindle formation. Here, we define the precise events regulated by telomere-LINC contacts and address the analogous possibility, that centromeres regulate mitotic spindle formation. We develop conditionally inactivated LINC complexes in which the conserved SUN-domain protein Sad1 remains stable but severs interphase centromere-LINC contacts. Strikingly, the loss of such contacts abolishes spindle formation. We pinpoint the defect to a failure in the partial NE breakdown required for centrosome insertion into the NE, a step analogous to mammalian NE breakdown. Thus, interphase chromosome-LINC contacts constitute a cell cycle control device linking nucleoplasmic and cytoplasmic events.

Contact between telomeres and the fission yeast spindle pole body during meiotic prophase is crucial for subsequent spindle assembly, but the feature of telomeres that confers their ability to promote spindle formation remains mysterious. Here we show that while strains harbouring circular chromosomes devoid of telomere repeat tracts undergo aberrant meiosis with defective spindles, the insertion of a single internal telomere repeat stretch rescues the spindle defects. Moreover, the telomeric overhangbinding protein Pot1 is dispensable for rescue of spindle formation. Hence, an inherent feature of the double-strand telomeric region endows telomeres with the capacity to promote spindle formation.

While telomeres have well‐studied roles in preserving the integrity of chromosome ends, they play radically different and fundamentally important roles in meiosis; understanding these roles will not only shed light on mechanisms ensuring successful sexual reproduction but also on mitotic growth. During meiotic prophase, all the telomeres in the cell cluster at the nuclear periphery to form the highly conserved ‘bouquet’ structure. The fission yeast bouquet associates with the spindle pole body (SPB; the fission yeast centrosome equivalent) and can be specifically disrupted by mutating telomere proteins or meiosis‐specific proteins that connect the telomere complex with the SPB, allowing functional analysis. We have shown that the bouquet is required for proper meiotic spindle formation (Tomita & Cooper, Cell 2007). We find that while the SPB duplicates properly in the absence of the bouquet, the duplicated SPBs often fail to separate and show defects γ‐tubulin complex (γ‐TUC) localization to the spindle poles, suggesting that the bouquet modifies an SPB protein that controls γ‐TUC recruitment. Bouquet‐defective cells can overcome these challenges and form proper meiotic spindles if their SPBs become transiently associated with nontelomeric heterochromatin during meiotic prophase, highlighting the importance of chromatin‐SPB interactions for promoting spindle formation. Finally, we present data leading to the provocative idea that the bouquet influences meiotic kinetochore assembly and centromere‐spindle attachment.