Tissue-specific inhibition of protein sumoylation uncovers diverse SUMO functions during C. elegans vulval development

Abstract

The sumoylation (SUMO) pathway is involved in a variety of processes during C. elegans development, such as gonadal and vulval fate specification, cell cycle progression and maintenance of chromosome structure. The ubiquitous expression of the sumoylation machinery and its involvement in many essential processes has made it difficult to dissect the tissue-specific roles of protein sumoylation and identify the specific target proteins. To overcome these challenges, we have established tools to block protein sumoylation and degrade sumoylated target proteins in a tissue-specific and temporally controlled manner. We employed the auxin-inducible protein degradation system (AID) to down-regulate AID-tagged SUMO E3 ligase GEI-17 or the SUMO ortholog SMO-1, either in the vulval precursor cells (VPCs) or in the gonadal anchor cell (AC). Tissue-specific inhibition of GEI-17 and SMO-1 revealed diverse roles of the SUMO pathway during vulval development, such as AC positioning, basement membrane (BM) breaching, vulval cell fate specification and epithelial morphogenesis. Inhibition of sumoylation in the VPCs resulted in an abnormal shape of the vulval toroids and ectopic cell fusions. Sumoylation of the ETS transcription factor LIN-1 at K169 mediates a subset of these SUMO functions, especially the proper contraction of the ventral vulA toroids. Thus, the SUMO pathway plays diverse roles throughout vulval development.