A small peptide inhibits siRNA amplification in plants by mediating autophagic degradation of SGS3/RDR6 bodies

Abstract

Selective autophagy mediates specific degradation of unwanted cytoplasmic components to maintain cellular homeostasis. The suppressor of gene silencing 3 (SGS3) and RNA‐dependent RNA polymerase 6 (RDR6)‐formed bodies (SGS3/RDR6 bodies) are essential for siRNA amplification in planta. However, whether autophagy receptors regulate selective turnover of SGS3/RDR6 bodies is unknown. By analyzing the transcriptomic response to virus infection in Arabidopsis, we identified a virus‐induced small peptide 1 (VISP1) composed of 71 amino acids, which harbor a ubiquitin‐interacting motif that mediates interaction with autophagy‐related protein 8. Overexpression of VISP1 induced selective autophagy and compromised antiviral immunity by inhibiting SGS3/RDR6‐dependent viral siRNA amplification, whereas visp1 mutants exhibited opposite effects. Biochemistry assays demonstrate that VISP1 interacted with SGS3 and mediated autophagic degradation of SGS3/RDR6 bodies. Further analyses revealed that overexpression of VISP1, mimicking the sgs3 mutant, impaired biogenesis of endogenous trans‐acting siRNAs and up‐regulated their targets. Collectively, we propose that VISP1 is a small peptide receptor functioning in the crosstalk between selective autophagy and RNA silencing.

Viral suppressors from members of the family Closteroviridae combating antiviral RNA silencing: a tale of a sophisticated arms race in host-pathogen interactions

“…To complete the effector phase of antiviral RNA silencing, RISCs target vsiRNA or miRNA complementary mRNAs and trigger their PTGS via endonucleolytic cleavage or translational inhibition (Waterhouse and Helliwell 2003;Brodersen et al 2008;Carbonell and Carrington 2015;Mengistu and Tenkegna 2021). For the amplification of antiviral RNA silencing, AGOsliced products serve as templates for RdRp (RDR for cellular RdRps) complexes using RNA-helicases (SGS3 and SDE5), the cofactors of RDR-mediated pathways (Vaucheret 2006;Jauvion et al 2010;Csorba et al 2015;Tong et al 2021).…”

Clearance or Hijack: Universal Interplay Mechanisms Between Viruses and Host Autophagy From Plants to Animals

“…Li and co-workers reported that geminiviruses appear to indirectly utilize the plant endogenous RNA silencing suppressor calmodulin-like protein (CaM) to inhibit the siRNA mechanism by promoting the autophagic degradation of SGS3 (Figure 2) Li et al, 2017). Recently, Tong et al (2021) identified a novel 71-amino acid virus-induced small peptide (VISP1) in plants that acts as an autophagy cargo receptor. VISP1 overexpression induces selective autophagy, which attenuates SGS3/ RDR6-dependent viral siRNA amplification and enhances viral infection; meanwhile, VISP1 mutants display the opposite effect.…”

“…Li and co-workers reported that geminiviruses appear to indirectly utilize the plant endogenous RNA silencing suppressor calmodulin-like protein (CaM) to inhibit the siRNA mechanism by promoting the autophagic degradation of SGS3 ( Figure 2 ) ( Li et al., 2014 ; Li et al., 2017 ). Recently, Tong et al. (2021) identified a novel 71-amino acid virus-induced small peptide (VISP1) in plants that acts as an autophagy cargo receptor.…”

Plant Autophagy: An Intricate Process Controlled by Various Signaling Pathways

“…In Arabidopsis , a small 71 amino acid peptide, VISP1, can be induced by Cucumber mosaic virus (CMV) infection and interacts with ATG8 through UIM (ubiquitin-interacting motif) motif. VISP1 functions as a selective autophagy receptor involved in degradation of SGS3 (suppressor of gene silencing 3)/RDR6 (RNA-dependent RNA polymerase 6)-bodies to negatively regulate siRNA amplification, resulting in suppression of antiviral immunity ( Tong et al, 2021 ).…”