Plants have evolved sophisticated immune mechanisms involving cell surface-resident pattern recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat (NLR) proteins to detect infections. Disruption of a PRR-activated MEKK1-MKK1/2-MPK4 MAP kinase cascade leads to the activation of NLR SUMM2-mediated autoimmunity. To unravel the intricate regulation of PRR and NLR activation, we conducted an RNAi-based genetic screen for mekk1 autoimmune suppressors, identifying a set of genes termed Lethality suppressor of mekk1 (LET). Among these, LET1 and LET2 encode malectin-like receptor-like kinases, collaborating with the GPI-anchored protein LLG1 to activate SUMM2. LET3/LET7, a pair of closely related E3 ubiquitin ligases, antagonistically modulate the stability of calmodulin-binding receptor-like cytoplasmic kinase CRCK3, guarded by SUMM2 for immune activation. Notably, LET3, unlike conventional E3 ligases, stabilizes CRCK3 independently of its ligase activity, while LET7 counteracts LET3 by inducing CRCK3 degradation through monoubiquitylation and internalization. Intriguingly, the expression of LET3-GFP in Arabidopsis transgenic plants results in the formation of large intracellular puncta resembling protein condensates, termed LET3 bodies. These LET3 bodies undergo dynamic regulation through the LET2-LET1-CRCK3-LET3 phosphorylation cascade, suggesting that phosphorylation status dictates LET3 body formation. Moreover, both CRCK3 and LET3, expressed abundantly in roots and conserved across plant species, confer resistance to Fusarium oxysporum, a destructive soil-borne fungal pathogen, in Arabidopsis and cotton. These findings unveil the antagonistic role of an E3 ligase pair in fine-tuning kinase proteostasis for NLR activation and shed light on a previously unexplored function of autoimmune activators in governing plant root immunity against fungal pathogens.