Divergence of cytokinesis and dimorphism control by myosin II regulatory light chain in fission yeasts

Non-muscle myosin II activation by regulatory light chain (Rlc1(Sp)) phosphorylation at Ser35 is crucial for cytokinesis during respiration in the fission yeast Schizosaccharomyces pombe. We show that in the early divergent and dimorphic fission yeast S. japonicus non-phosphorylated Rlc1(Sj) regulates the activity of Myo2(Sj) and Myp2(Sj) heavy chains during cytokinesis. Intriguingly, Rlc1(Sj)-Myo2(Sj) nodes delay yeast to hyphae onset but are essential for mycelial development. Structure-function analysis revealed that phosphorylation-induced folding of Rlc1(Sp) α1 helix into an open conformation allows precise regulation of Myo2(Sp) during cytokinesis. Consistently, inclusion of bulky tryptophan residues in the adjacent α5 helix triggered Rlc1(Sp) shift and supported cytokinesis in absence of Ser35 phosphorylation. Remarkably, unphosphorylated Rlc1(Sj) lacking the α1 helix was competent to regulate S. pombe cytokinesis during respiration. Hence, early diversification resulted in two efficient phosphorylation-independent and -dependent modes of Rlc1 regulation of myosin II activity in fission yeasts, the latter being conserved through evolution.