Plant immune responses are tightly regulated to ensure their appropriate deployment. The overexpression of TOPLESS-RELATED 1 (TPR1), a SUPPRESSOR OF npr1-1, CONSTITUTIVE 1 (SNC1)-interacting protein, results in autoimmunity, which reduces plant growth and development. However, how TPR1 activity is regulated remains unknown. Loss-of-function of SIZ1, a (SUMO) E3 ligase, induces an autoimmune response, partially due to elevated SNC1 levels. Here we show that SNC1 expression is upregulated in Arabidopsis thaliana siz1-2 due to the positive feedback effect of salicylic acid. SIZ1 physically interacts with TPR1 and facilitates its SUMO modification. The K282 and K721 residues in TPR1 serve as critical SUMO attachment sites. Simultaneous K282R and K721R substitutions in TPR1 blocked its SUMOylation, enhanced its transcriptional co-repressor activity and increased its association with HISTONE DEACETYLASE 19 (HDA19), suggesting that SUMOylation of TPR1 represses its transcriptional co-repressor activity and inhibits its interaction with HDA19. In agreement with this finding, simultaneous K282R and K721R substitutions enhanced the TPR1-mediated immunity, and the tpr1 mutation partially suppressed the autoimmunity of siz1-2. These results demonstrate that SIZ1-mediated SUMOylation of TPR1 represses plant immunity, which at least partly contribute to the suppression of autoimmunity under non-pathogenic conditions to ensure proper plant development.