Tetrahymena JanusA gene encodes a polo kinase whose loss triggers a dorsal/ventral intracellular homeosis

Homeotic mutations result in developmental abnormalities in which one body part is replaced by another. In flowering plants, ABC mutations result in transformations between petals, stamens, pistils, and sepals, 1 while in insects, HOX mutations replace antennae with legs and abdominal segments with those of the thorax. 2 Homeotic mutations can help to reveal the genetic architecture governing development while providing insights into the evolutionary origins of an organism's body plan. Here, we identify a gene whose loss of function transforms the dorsal surface of the unicellular ciliate, Tetrahymena thermophila , normally devoid of cortical organelles, into a mirror-image of the ventral surface, complete with supernumerary contractile vacuole pores (CVPs) and a secondary oral apparatus (OA) exhibiting reversed local left-right asymmetry. 3 Through next-generation sequencing (NGS), we discovered that JANA encodes a polo kinase that forms a circumferential cortical gradient, with a high point on the left-dorsal side of the cell. In Tetrahymena , polarized JanA/polo kinase localization appears to act in concert with other spatially restricted cortical morphogens to repress organelle assembly around most of the cell circumference, leaving a narrow wedge (a single ciliary row) to participate in oral assembly prior to cell division. Our study reveals a novel role for polo kinases in breaking the radial symmetry observed in early-divergent ciliates.