TuMV infection alters miR168/AGO1 and miR403/AGO2 systems regulation in Arabidopsis

Abstract

Viral infections trigger a strong response of the plant RNA silencing machinery. The cargo protein AGO1 has a well-established role in siRNA loading. Several plant viruses have convergently evolved a molecular counter-attack reliant on inactivation of the AGO1-based plant defense by altering the regulatory loop that comprises miR168 and AGO1. Upon viral infections, another AGO protein, AGO2, is induced. AGO2 is in turn post-transcriptionally regulated by miR403. The simultaneous study of both regulatory systems working along an infection time-frame is lacking. Here it is shown the molecular response of Arabidopsis Turnip Mosaic Virus (TuMV) infection from early to late stages post-infection. Molecular analyses confirmed that TuMV induced mature miR168 accumulation in Arabidopsis, as reported also for other plant-virus interactions. However, differently from reported plant-virus interactions, miRNA precursors pre-miR168a and b were down-regulated and no significant transcriptional effect was detected on miR168a promoter. AGO1 mRNA was induced, but AGO1 protein levels were unchanged. Analyses of the miR403/AGO2 system showed a similar pattern, except for an induction of AGO2 protein levels. Additionally, low molecular weight forms of AGO1 and 2 proteins were detected and relatively overaccumulated under TuMV infections. Our results suggest that TuMV alters the biogenesis of miR168 and miR403 at the processing step. Whilst TuMV induces both miR168 and miR403 overaccumulation, it fails to prevent overaccumulation of the antiviral AGO2 at both mRNA and protein levels.

Argonaute 2 Controls Antiviral Activity against Sweet Potato Mild Mottle Virus in Nicotiana benthamiana

“…Another study revealed that upon TuMV infection, the mature form of miR403 was induced (and consistently the pri-miR403 level was reduced). Moreover, AGO2 mRNA was strongly induced suggesting that upregulation could escape AGO2 mRNA from AGO1-miR403 repression [28]. Indeed, gibberellic acid, UV irradiation and bacterial infection upregulated AGO2 mRNA revealing that AGO2 was regulated by a variety of biotic and abiotic stresses [20,29,30].…”

An atlas of small RNAs from potato

“…We also found that some miRNAs have a significantly different accumulation in both cultivars, these include miR397‐3p, miR530, miR7122, miR170, and miR403. These miRNAs, which were more abundant in Desiree compared with Eva, have been found to be involved in plant responses to stress (Dong & Pei, 2014 ; Kohli et al, 2014 ; Li et al, 2021 ; Manacorda et al, 2021 ; Xia et al, 2013 ). Future research efforts would determine whether these miRNAs are responsible for some of the stress responsive differences between Desiree and Eva.…”

“…We also found that some miRNAs have a significantly different accumulation in both cultivars, these include miR397-3p, miR530, miR7122, miR170, and miR403. These miRNAs, which were more abundant in Desiree compared with Eva, been found to be involved in plant responses to stress (Dong & Pei, 2014;Kohli et al, 2014;Manacorda et al, 2021;Xia et al, 2013).…”

Transcriptome Profiling Reveals a Petunia Transcription Factor, PhCOL4, Contributing to Antiviral RNA Silencing

“…AGO1 has been revealed to be involved in antiviral response to turnip crinkle virus ( Azevedo et al, 2010 ) and CMV ( Zhang et al, 2006 ). AGO2 plays an essential role in resisting CMV ( Harvey et al, 2011 ), PVX ( Jaubert et al, 2011 ), and TuMV ( Manacorda et al, 2021 ). AGO1 and AGO7 function cooperatively to ensure the removal of viral RNAs with different secondary structures ( Qu et al, 2008 ).…”