Phased small RNA–mediated systemic signaling in plants

M. B. Shine, Kai Zhang, Huazhen Liu, Gah Hyun Lim, Fan Xia, Keshun Yu, Arthur G. Hunt, Aardra Kachroo, Pradeep Kachroo

Research output: Contribution to journalArticlepeer-review

Abstract

Systemic acquired resistance (SAR) involves the generation of systemically transported signal that arms distal plant parts against secondary infections. We show that two phased 21–nucleotide (nt) trans-acting small interfering RNA3a RNAs (tasi-RNA) derived from TAS3a and synthesized within 3 hours of pathogen infection are the early mobile signal in SAR. TAS3a undergoes alternate polyadenylation, resulting in the generation of 555- and 367-nt transcripts. The 555-nt transcripts likely serves as the sole precursor for tasi-RNAs D7 and D8, which cleave Auxin response factors (ARF) 2, 3, and 4 to induce SAR. Conversely, increased expression of ARF3 represses SAR. Knockout mutations in TAS3a or RNA silencing components required for tasi-RNA biogenesis compromise SAR without altering levels of known SAR-inducing chemicals. Both tasi-ARFs and the 367-nt transcripts are mobile and transported via plasmodesmata. Together, we show that tasi-ARFs are the early mobile signal in SAR.

Original languageEnglish
Article numbereabm8791
JournalScience advances
Volume8
Issue number25
DOIs
StatePublished - Jun 2022

Bibliographical note

Funding Information:
We thank H. Vaucheret for ago1 and tas3a; X. Chen for tas3b; A. Maizel for mir390a and 35S-miR-ARF construct; and ABRC for ARF-GUS, tas2, ago7, rdr6, and sgs3 seeds. We thank J. Johnson for help with analytical analysis, S. W. Yang for advise on sRNA analysis, R. Liu for help with SAR assays, and W. Havens and A. Crume for technical help. Chemical analysis reported in this study was carried out at the Center for Agricultural and Life Sciences Metabolomics (CALM; https://plantpathology.ca.uky.edu/lab/Analytical-CORE).This work was supported by grants from National Science Foundation (MCB no. 0421914, IOS no. 051909, and IOS no. 0817818), Kentucky Soybean Board (3084113467), United Soybean Board (2220-172-0141) and USDA National Institute of Food and Agriculture (Hatch project 1014539).

Publisher Copyright:
Copyright © 2022 The Authors, some rights reserved

ASJC Scopus subject areas

  • General

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