Phased small RNA-mediated systemic signaling in plants.

Shine, M B; Zhang, Kai; Liu, Huazhen; Lim, Gah-Hyun; Xia, Fan; Yu, Keshun; Hunt, Arthur G; Kachroo, Aardra et al. · Sci Adv · 2022

basic_science · Level V

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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) <i>trans-acting small interfering RNA3a</i> RNAs (tasi-RNA) derived from <i>TAS3a</i> and synthesized within 3 hours of pathogen infection are the early mobile signal in SAR. <i>TAS3a</i> 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 <i>Auxin response factors</i> (<i>ARF</i>) <i>2</i>, <i>3</i>, and <i>4</i> to induce SAR. Conversely, increased expression of <i>ARF3</i> represses SAR. Knockout mutations in <i>TAS3a</i> 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.