Post-translational modifications of proteins can lead to degradation, subcellular translocation, or altered interaction with partner proteins. The small ubiquitin-like modifier SUMO (Pmt3 in Schizosaccharomyces pombe) is such a modification involved in numerous cellular processes. Pmt3 attachment to target proteins can be catalyzed by the SUMO E3 ligase Pli1. In this study we investigate the role of Pli1 and Pmt3 during meiotic differentiation and at repetitive DNA during mitotic growth. Target proteins for Pmt3 are many; however, Pli1 has a meiosis-specific function regulating meiotic recombination. We have found that meiotic recombination in euchromatic regions is stimulated by Pli1 and Pmt3 and that programmed double-strand breaks are formed and repaired with the same efficiency in pli1Δ- and wild type cells. Double-strand breaks can be repaired using either the sister chromatid or the homolog as template but only repair with the homolog produces an observable recombination event. We suggest that Pli1 stimulates meiotic recombination by inhibiting sister-chromatid recombination. Supporting this, we find that sister-chromatid recombination is altered in cells lacking Pli1. We propose a model that explains how Pli1 inhibits sister-chromatid recombination. This model accounts for the observation that Pli1 has the greatest effect on meiotic recombination in regions where double-strand break hotspots are scarce. Furthermore, we describe a role for Pli1 and Pmt3 in maintaining intact ribosomal DNA arrays during mitotic growth.