The SUMO E3 Ligase-Like Proteins PIAL1 and PIAL2 Interact with MOM1 and Form a Novel Complex Required for Transcriptional Silencing

Abstract

The mechanism by which MORPHEUS' MOLECULE1 (MOM1) contributes to transcriptional gene silencing has remained elusive since the gene was first identified and characterized. Here, we report that two Arabidopsis thaliana PIAS (PROTEIN INHIBITOR OF ACTIVATED STAT)-type SUMO E3 ligase-like proteins, PIAL1 and PIAL2, function redundantly to mediate transcriptional silencing at MOM1 target loci. PIAL1 and PIAL2 physically interact with each other and with MOM1 to form a high molecular mass complex. In the absence of either PIAL2 or MOM1, the formation of the high molecular mass complex is disrupted. We identified a previously uncharacterized IND (interacting domain) in PIAL1 and PIAL2 and demonstrated that IND directly interacts with MOM1. The CMM2 (conserved MOM1 motif 2) domain of MOM1 was previously shown to be required for the dimerization of MOM1. We demonstrated that the CMM2 domain is also required for the interaction of MOM1 with PIAL1 and PIAL2. We found that although PIAL2 has SUMO E3 ligase activity, the activity is dispensable for PIAL2's function in transcriptional silencing. This study suggests that PIAL1 and PIAl2 act as components of the MOM1-containing complex to mediate transcriptional silencing at heterochromatin regions.

Protein sumoylation and phosphorylation intersect in Arabidopsis signaling

“…It should be noted that PIAL1 and PIAL2 have recently been ascribed a function as (alternative) subunits of a gene silencing complex that affects mainly transposable elements (Han et al, 2016). Analysis of the transcriptome of pial1 pial2 mutants as published by Han et al (2016) indicated only five genes upregulated at the transcriptional level among our set of 56 significantly upregulated proteins (AT1G26380, AT2G14610, AT2G20560, AT4G04180, AT5G27850). In the other cases, post-transcriptional steps such as increased protein stability may be responsible for the upregulation.…”

“…It should be noted that PIAL1 and PIAL2 have recently been ascribed a function as (alternative) subunits of a gene silencing complex that affects mainly transposable elements (Han et al ., ). Analysis of the transcriptome of pial1 pial2 mutants as published by Han et al .…”

“…Analysis of the transcriptome of pial1 pial2 mutants as published by Han et al . () indicated only five genes upregulated at the transcriptional level among our set of 56 significantly upregulated proteins (AT1G26380, AT2G14610, AT2G20560, AT4G04180, AT5G27850). In the other cases, post‐transcriptional steps such as increased protein stability may be responsible for the upregulation.…”

“…For this reason, it is currently unclear how PIAL1/2 are integrated into cellular sumoylation processes. PIAL1/2 have been analyzed for their ability to form SUMO chains, but recent work also showed a function in transcriptional repression of transposable elements, in a complex that contains the MOM1 protein (Han et al, 2016). One of the goals of this work was to better understand how PIAL1/2 intersect with SIZ1, a SUMO ligase with mono-sumoylation activity.…”

Comparative RNA‐seq analysis of nickel hyperaccumulating and non‐accumulating populations of Senecio coronatus (Asteraceae)

“…These included RTEL1, which is involved in telomere maintenance (Recker et al, 2014), and RecA2, which is required for DNA repair in organelles (Miller-Messmer et al, 2012;Recker et al, 2014). Three genes required for the maintenance of epigenetic silencing of gene expression, MOM1, STRS1 and ICU2 (Hyun et al, 2013;Khan et al, 2014;Han et al, 2016), as well as several chromatin remodellers and a histone deacetylase, also showed elevated expression levels in the hyperaccumulators (Table S6); this finding is line with the recent suggestion that chromatin compaction may increase genome stability in hyperaccumulators (Gull ı et al, 2018). (Merlot et al, 2014;Sobczyk et al, 2017).…”