The dmf1/mid1 gene is essential for correct positioning of the division septum in fission yeast.

Abstract

Little is known about the mechanisms that establish the position of the division plane in eukaryotic cells.Wild-type fission yeast cells divide by forming a septum in the middle of the cell at the end of mitosis. Dmfl mutants complete mitosis and initiate septum formation, but the septa that form are positioned at random locations and angles in the cell, rather than in the middle. We have cloned the dmfl gene as a suppressor of the cdc7-24 mutant. The dmfl mutant is allelic with mid1. The gene encodes a novel protein containing a putative nuclear localization signal, and a carboxy-terminal PH domain. In wild-type cells, Dmflp is nuclear during interphase, and relocates to form a medial ring at the cell cortex coincident with the onset of mitosis. This relocalization occurs before formation of the actin ring and is associated with increased phosphorylation of Dmflp. The Dmflp ring can be formed in the absence of an actin ring, but depends on some of the genes required for actin ring formation. When the septum is completed and the cells separate, Dmflp staining is once again nuclear. These data implicate Dmflp as an important element in assuring correct placement of the division septum in Schizosaccharomyces pombe cells. [Key Words: dmfl/midl; S. pombe; cytokinesis]Received April 10, 1996; revised version accepted August 22, 1996.Cells must assure correct spatial and temporal coordination of mitosis with cytokinesis so that each daughter cell will receive a nucleus and an appropriate complement of cytoplasmic material following cell division. A number of studies indicate that the position of the cleavage plane is determined during mitosis, but in most systems very little is known about the nature of the signal or the proteins involved (for review, see Strome 1993). Cytokinesis requires assembly of the division apparatus at an appropriate site on the cell cortex. In higher eukaryotes, a contractile ring forms around the equator of the parent cell at the end of mitosis. The sliding of actin and myosin filaments generates a force that pulls the plasma membrane inward to create the cleavage furrow, which narrows to form the midbody as division is completed (for review, see Satterwhite and Pollard 1992;Fishkind and Wang 1995). A structure called the telophase disc, which forms prior to the appearance of the contractile ring, has been proposed to organize contractile ring formation (Margolis and Andreassen 1993).The mitotic apparatus plays a critical role in determining where cell cleavage will occur. The site of cell division is defined by the plane of the metaphase plate, and is at right angles to the long axis of the mitotic spindle.

Mid1/anillin and the spatial regulation of cytokinesis in fission yeast

“…The absence of Mid1 gives rise to aberrant contractile rings and septa with very strong morphological defectsmost cells actually assemble disorganized actomyosin strands instead of real rings-located at random positions and angles inside the cell Sohrmann et al, 1996] except at the very cell tips [Huang et al, 2007].…”

“…As mitosis progresses through anaphase, Mid1 cortical nodes compact into a tight ring together with other contractile ring components. Mid1 eventually dissociates from the contractile ring as it starts to constrict [Sohrmann et al, 1996;Paoletti and Chang, 2000] (see Fig. 1).…”

“…Although Mid1 is a major spatial cue for contractile ring assembly, fission yeast cells can assemble a functional contractile ring in the absence of Mid1, though inefficiently and at random locations Sohrmann et al, 1996]. In this case, the contractile ring is formed from actomyosin filaments assembled randomly on the cortex, which eventually converge to assemble a contractile ring [Huang et al, 2008].…”

“…Cdc15 localization at the cell tips during interphase is not represented. mutants defective in division plane positioning Sohrmann et al, 1996;]. Lessons learnt from their analysis identified the anillin-like protein Mid1/Dmf1 as a central player in the definition of the division plane in fission yeast.…”

“…The alternate Cdc12 Spot-Leading Cable model proposes that a major Cdc12 spot moves toward the cell middle and nucleates an actin leading cable beneath the plasma membrane and perpendicular to the long axis of the cell, which eventually gives rise to the contractile ring [Chang, 1999;Kamasaki et al, 2007]. The facts that Cdc12 spot is not essential for Cdc12 function [Yonetani et al, 2008] and does not seem to nucleate actin filaments and that Myo2 activity is necessary for ring compaction [Coffman et al, 2009] rather favor the SCPR over the Cdc12 Spot-Leading Cable model at this stage.Although Mid1 is a major spatial cue for contractile ring assembly, fission yeast cells can assemble a functional contractile ring in the absence of Mid1, though inefficiently and at random locations Sohrmann et al, 1996]. In this case, the contractile ring is formed from actomyosin filaments assembled randomly on the cortex, which eventually converge to assemble a contractile ring [Huang et al, 2008].…”