Functional Diversification of Maize RNA Polymerase IV and V Subtypes via Alternative Catalytic Subunits

Abstract

Summary Unlike nuclear multisubunit RNA polymerases I, II and III, whose subunit compositions are conserved throughout eukaryotes, plant RNA Polymerases IV and V are non-essential, Pol II-related enzymes whose subunit compositions are still evolving. Whereas Arabidopsis Pols IV and V differ from Pol II in four or five of their twelve subunits, respectively, and differ from one another in three subunits, proteomic analyses show that maize Pols IV and V differ from Pol II in six subunits, but differ from each other only in their largest subunits. Use of alternative catalytic second-subunits, which are non-redundant for development and paramutation, yields at least two subtypes of Pol IV, and three subtypes of Pol V in maize. Pol IV/V associations with MOP1, RMR1, AGO121, Zm_DRD1/CHR127, SHH2a and SHH2b extend parallels between paramutation in maize and the RNA-directed DNA methylation pathway in Arabidopsis.

Nascent Transcription Affected by RNA Polymerase IV inZea mays

“…These additional RNAPs derive from duplications of specific Pol II subunits followed by subfunctionalization during plant evolution (Tucker et al 2011), yet the holoenzyme complexes still share some Pol II subunits (Ream et al 2009;Haag et al 2014).…”

“…Flowering plant genomes encode additional RNAP subunits comprising Pol IV and Pol V, which are central to a small interfering RNA (siRNA)-based silencing pathway primarily targeting repetitive sequences such as transposable elements (TEs) (Matzke and Mosher 2014;Matzke et al 2015). These additional RNAPs derive from duplications of specific Pol II subunits followed by subfunctionalization during plant evolution (Tucker et al 2011), yet the holoenzyme complexes still share some Pol II subunits (Ream et al 2009;Haag et al 2014).…”

“…Flowering plant genomes encode additional RNAP subunits comprising Pol IV and Pol V, which are central to a small interfering RNA (siRNA)-based silencing pathway primarily targeting repetitive sequences such as transposable elements (TEs) (Matzke and Mosher 2014;Matzke et al 2015). These additional RNAPs derive from duplications of specific Pol II subunits followed by subfunctionalization during plant evolution (Tucker et al 2011), yet the holoenzyme complexes still share some Pol II subunits (Ream et al 2009;Haag et al 2014).Zea mays (maize) has distinct largest subunits for Pol IV and V and, unlike Arabidopsis thaliana, three second-largest subunits Sidorenko et al 2009;Stonaker et al 2009) that in distinct combinations form two Pol IV and three Pol V isoforms (Haag et al 2014). Genetic analyses of rna polymerase d/e 2a (rpd/e2a) encoding one of the secondlargest subunits (Sidorenko et al 2009;Stonaker et al 2009) together with recent proteomic data showing association of a putative RNA-dependent RNA polymerase (RDR2) with only RPD/E2a-containing isoforms (Haag et al 2014) indicate that maize Pol IV isoforms have diverse functional roles in managing genome homeostasis.…”

“…Zea mays (maize) has distinct largest subunits for Pol IV and V and, unlike Arabidopsis thaliana, three second-largest subunits Sidorenko et al 2009;Stonaker et al 2009) that in distinct combinations form two Pol IV and three Pol V isoforms (Haag et al 2014). Genetic analyses of rna polymerase d/e 2a (rpd/e2a) encoding one of the secondlargest subunits (Sidorenko et al 2009;Stonaker et al 2009) together with recent proteomic data showing association of a putative RNA-dependent RNA polymerase (RDR2) with only RPD/E2a-containing isoforms (Haag et al 2014) indicate that maize Pol IV isoforms have diverse functional roles in managing genome homeostasis.…”

Subunits Common to RNA Polymerases

“…Meanwhile, RNA pol II produces all mRNAs and many non-coding RNAs [1,2]. Moreover, in plants, two additional polymerases, IV and V (or nuclear RNA polymerases D and E), reportedly synthesise small interfering RNAs (siRNAs), regulating methylation and participating in gene silencing, as well as long non-coding RNAs involved in development and response to environmental changes [3][4][5].…”