A nuclear tRNA-derived fragment triggers immunity in Arabidopsis

Abstract

In Arabidopsis, effector-triggered immunity (ETI) against avirulent Pseudomonas syringae pv. tomato (Pst) correlates with the rapid, Dicer-Like 1 (DCL1)-dependent nuclear accumulation of a 31-nt 5'-tRNA fragment derived from Asp-tRNA (tRF31Asp2). Several tRFs, including tRF31Asp2, are induced at early stages of infection and associate with AGO2 in the nucleus. Infiltrating Arabidopsis leaves with synthetic tRF31Asp2 induces over 500 defense-associated genes, conferring immunity against virulent and avirulent Pst as well as aphids, while tRF31Asp2 depletion compromises resistance to avirulent Pst. The biological activity of tRF31Asp2 requires its 5' sequence and predicted stem-loop structure, and its loading into AGO2 or related clade members may contribute to activating defense responses. Chromatin affinity precipitation-sequencing revealed that tRF31Asp2 binds specific sequences in defense genes and the Gypsy superfamily of LTR retrotransposons, particularly at their primer binding sites (PBS). tRF31Asp2 binding appears to modulate transcriptional reprogramming, inducing neighboring tRF-responsive defense genes while suppressing active retrotransposons. Since Gypsy retrotransposon proliferation is primed by tRNA binding at PBS, tRF31Asp2 may exploit a similar mechanism to coordinate defense responses. Together, these findings reveal a role for DCL1 and tRF31Asp2 in regulating plant immunity and transcriptional dynamics at defense-associated loci and retrotransposons.