A nuclear tRNA-derived fragment triggers immunity in Arabidopsis

Authors: KIM, SUNG-II - Texas State University; LYU, HAOMIN - Texas A&M Agrilife; PUJARA, DINESH - Texas State University; BORDIYA, YOGENDRA - Texas State University; BHATT, PADAM - Texas State University; MAYORGA, JOSE - Texas State University; KUDJOE ZOGLI, PRINCE - University Of Nebraska; KUNDU, PRITHA - University Of Nebraska; CHUNG, HAEWON - University Of Texas; YAN, XINGXING - Texas A&M University; ZHANG, XIUREN - Texas A&M University; JONGHWAN, KIM - University Of Texas; LOUIS, JOE - University Of Nebraska; Yu, Qingyi; KANG, HONG-GI - Texas State University

Submitted to: Communications Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/13/2025
Publication Date: 4/1/2025
Citation: Kim, S., Lyu, H., Pujara, D.S., Bordiya, Y., Bhatt, P.S., Mayorga, J., Zogli, P.K., Kundu, P., Chung, H., Yan, X., Zhang, X., Kim, J., Louis, J., Yu, Q., Kang, H. 2025. A nuclear tRNA-derived fragment triggers immunity in Arabidopsis. Communications Biology. 8:533. https://doi.org/10.1038/s42003-025-07737-1.
DOI: https://doi.org/10.1038/s42003-025-07737-1

Interpretive Summary: Transfer RNAs (tRNAs) are molecules that have been known to play a role in protein synthesis. However, recent research has shown that tRNAs also have other functions beyond protein synthesis, such as organizing chromatin (DNA-protein complex), repairing DNA, and regulating immune responses. tRNA-derived small RNAs (tsRNAs) have been identified as important regulators in immune responses. In this study, we discovered a new function of a specific tsRNA called tRF31Asp2 in plant immunity against a bacterial pathogen. We found that tRF31Asp2 accumulates in the cell nucleus in response to the pathogen and activates defense-associated genes, leading to immunity against the pathogen as well as aphids. Further investigation revealed that tRF31Asp2 physically associates with specific target genes and a type of retrotransposons called Gypsy retrotransposons, which are known to be involved in immune responses. This suggests that tRF31Asp2 modulates the transcriptional reprogramming associated with plant immunity by binding to specific DNA sequences.

Technical 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.