A nuclear tRNA-derived fragment triggers immunity in Arabidopsis

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 (tRF^31Asp2). Several tRFs, including tRF^31Asp2, are induced at early stages of infection and associate with AGO2 in the nucleus. Infiltrating Arabidopsis leaves with synthetic tRF^31Asp2 induces over 500 defense-associated genes, conferring immunity against virulent and avirulent Pst as well as aphids, while tRF^31Asp2 depletion compromises resistance to avirulent Pst. The biological activity of tRF^31Asp2 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 tRF^31Asp2 binds specific sequences in defense genes and the Gypsy superfamily of LTR retrotransposons, particularly at their primer binding sites (PBS). tRF^31Asp2 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, tRF^31Asp2 may exploit a similar mechanism to coordinate defense responses. Together, these findings reveal a role for DCL1 and tRF^31Asp2 in regulating plant immunity and transcriptional dynamics at defense-associated loci and retrotransposons.