NatA complex is a leaf-intrinsic brake on systemic responses induced by root endophytic fungi.

Abstract

Root-associated beneficial microbes prime host plants for induced systemic resistance (ISR) in leaves. Although continuous immune activation triggered by root endophytic fungi would impair leaf growth, how host plants avoid autoimmunity during endophytic fungi-mediated ISR priming is unknown. Here, we show that the <i>Arabidopsis</i> NatA N-terminal-acetyltransferase complex acts as a leaf-intrinsic brake on these root-to-leaf systemic responses. Impairment of the NatA subunit SUF1 (also named HYPK) or NAA15 unleashed chronic N-hydroxy-pipecolic-acid (NHP)/salicylic-acid (SA) signaling activation, converting beneficial ISR priming into growth-inhibitory leaf senescence. Transcriptome and quantitative proteomic analysis revealed the selective activation of defense and SA signaling pathways in the leaves of NatA mutants. Crossing <i>suf1</i> or <i>naa15</i> with <i>fmo1</i> and <i>eds5</i> abolished autoimmunity, confirming that the phenotype requires FMO1-dependent NHP and downstream SA synthesis and signaling activation. Thus, by destabilizing defense proteins, NatA enables plants to sustain lifelong ISR priming without growth penalty, guiding breeders to consider ISR control traits.