Abstract
ABSTRACTChromosome segregation in female meiosis in many metazoans is mediated by acentrosomal spindles, the existence of which implies that microtubule spindles self-assemble without the participation of the centrosomes. Although it is thought that acentrosomal meiosis is not conserved in fungi, we recently reported the formation of self-assembled microtubule arrays, which were able to segregate chromosomes, in fission yeast mutants, in which the contribution of the spindle pole body (SPB; the centrosome equivalent in yeast) was specifically blocked during meiosis. Here, we demonstrate that this unexpected microtubule formation represents a bona fide type of acentrosomal spindle. Moreover, a comparative analysis of these self-assembled spindles and the canonical SPB-dependent spindle reveals similarities and differences; for example, both spindles have a similar polarity, but the location of the γ-tubulin complex differs. We also show that the robustness of self-assembled spindles can be reinforced by eliminating kinesin-8 family members, whereas kinesin-8 mutants have an adverse impact on SPB-dependent spindles. Hence, we consider that reinforced self-assembled spindles in yeast will help to clarify the molecular mechanisms behind acentrosomal meiosis, a crucial step towards better understanding gametogenesis.
Highlights
Meiosis is a specialized type of cell division in which a diploid progenitor cell undergoes two reductional divisions, namely meiosis I (MI) and meiosis II (MII), to produce haploid cells (Griswold and Hunt, 2013)
This phenotype, together with the fact that the formation of microtubule arrangements occurs in the nuclear environment while the spindle pole body (SPB) localizes far from the nucleus (PinedaSantaella and Fernández-Álvarez, 2019), strongly suggests that the array of microtubules observed in bqt1Δ sad1.2 meiocytes is assembled without the participation of the SPB
To further confirm the self-assembly of the microtubule array, we explored whether the linker of nucleoskeleton and cytoskeleton (LINC) complex, which is permanently associated with the inner part of the SPB in fission yeast mitosis and meiosis at the nuclear envelope (NE) (Hagan and Yanagida, 1995; Rothballer et al, 2013), might contribute to the formation of the microtubule array
Summary
Meiosis is a specialized type of cell division in which a diploid progenitor cell undergoes two reductional divisions, namely meiosis I (MI) and meiosis II (MII), to produce haploid cells (Griswold and Hunt, 2013). Chromosome segregation during meiotic divisions is mediated by the spindle, which consists of microtubules together with a vast cohort of structural and regulatory proteins. In mitosis and male meiosis, spindle formation is mediated by the centrosomes, the major microtubule-organizing centres in the cell, which localize to the spindle poles (Walczak and Heald, 2008). Andalusian Centre for Developmental Biology (CABD), Universidad Pablo de Olavide – Consejo Superior de Investigaciones Cientıficas (CSIC), Junta de Andalucıá , Ctra. A.P., 0000-0003-1156-8104; N.F., 0000-0001-9381-0296; A.J., 0000-00017628-1273; M.C.M., 0000-0002-9513-572X; Á.S., 0000-0001-7685-6444; A.F., 0000-0002-7455-1425
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