A potential tension-sensing mechanism that ensures timely anaphase onset upon metaphase spindle orientation

The spindle orientation checkpoint (SOC) in fission yeast has been proposed to delay metaphase-to-anaphase transition when the spindle poles are misaligned with respect to the long axis of the cell. This checkpoint is activated in the absence of either an actomyosin division ring [1] or astral microtubules [2]. Although the SOC could be overridden in the absence of the transcription factor Atf1p, its mechanistic nature remained unclear. Here, we show that the SOC-triggered metaphase delay depends on a subset of the spindle assembly checkpoint (SAC) components Mph1p and Bub1p. Based on this finding and a detailed imaging of the spindle orientation process, we hypothesized that the spindle pole might contain proteins capable of sensing the achievement of spindle alignment. We identified the kendrin-like spindle pole body resident Pcp1p as a candidate molecule. A targeted mutation in its central domain specifically triggered the SOC in spite of the presence of oriented spindles, causing a metaphase delay that could be relieved in the absence of Mph1p, Bub1p, and Atf1p. Thus, Pcp1p might provide a link between the mechanical process of spindle alignment and the signal transduction that initiates anaphase.