This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits distribution, and reproduction in any medium, provided the original author and source are credited. This license does not permit commercial exploitation without specific permission.Ran GTPase activates several target molecules to induce microtubule formation around the chromosomes and centrosomes. In fission yeast, in which the nuclear envelope does not break down during mitosis, Ran targets the centrosomal transforming acidic coiled-coil (TACC) protein Alp7 for spindle formation. Alp7 accumulates in the nucleus only during mitosis, although its underlying mechanism remains elusive. Here, we investigate the behaviour of Alp7 and its binding partner, Alp14/ TOG, throughout the cell cycle. Interestingly, Alp7 enters the nucleus during interphase but is subsequently exported to the cytoplasm by the Exportin-dependent nuclear export machinery. The continuous nuclear export of Alp7 during interphase is essential for maintaining the array-like cytoplasmic microtubule structure. The mitosis-specific nuclear accumulation of Alp7 seems to be under the control of cyclin-dependent kinase (CDK). These results indicate that the spatiotemporal regulation of microtubule formation is established by the Alp7/TACC-Alp14/ TOG complex through the coordinated interplay of Ran and CDK.

Tethering kinetochores at spindle poles facilitates their efficient capture and segregation by microtubules at mitotic onset in yeast. During meiotic prophase of fission yeast, however, kinetochores are detached from the poles, which facilitates meiotic recombination but may cause a risk of chromosome mis-segregation during meiosis. How cells circumvent this dilemma remains unclear. Here we show that an extensive microtubule array assembles from the poles at meiosis I onset and retrieves scattered kinetochores towards the poles to prevent chromosome drift. Moreover, the microtubule-associated protein complex Alp7-Alp14 (the fission yeast orthologues of mammalian TACC-TOG) is phosphorylated by Polo kinase, which promotes its meiosis-specific association to the outer kinetochore complex Nuf2-Ndc80 of scattered kinetochores, thereby assisting in capturing remote kinetochores. Although TOG was recently characterized as a microtubule polymerase, Dis1 (the other TOG orthologue in fission yeast), together with the Dam1 complex, plays a role in microtubule shortening to pull kinetochores polewards. Thus, microtubules and their binding proteins uniquely reconstitute chromosome configuration during meiosis.

HighlightsFission yeast Alp7 is a member of the conserved TACC protein family.Amino acid residues within the TACC domain required for SPB targeting are identified.SPB localisation of Alp7 is essential for proper spindle assembly.Pericentrin-related Pcp1 acts as one of the platforms for Alp7 recruitment during mitosis.