Fibrillarin evolution through the Tree of Life: Comparative genomics and microsynteny network analyses provide new insights into the evolutionary history of Fibrillarin

Abstract

Fibrillarin (FIB), a methyltransferase essential for life in the vast majority of eukaryotes, is involved in methylation of rRNA required for proper ribosome assembly, as well as methylation of histone H2A of promoter regions of rRNA genes. RNA viral progression that affects both plants and animals requires FIB proteins. Despite the importance and high conservation of fibrillarins, there little is known about the evolutionary dynamics of this small gene family. We applied a phylogenomic microsynteny-network approach to elucidate the evolutionary history of FIB proteins across the Tree of Life. We identified 1063 non-redundant FIB sequences across 1049 completely sequenced genomes from Viruses, Bacteria, Archaea, and Eukarya. FIB is a highly conserved single-copy gene through Archaea and Eukarya lineages, except for plants, which have a gene family expansion due to paleopolyploidy and tandem duplications. We found a high conservation of the FIB genomic context during plant evolution. Surprisingly, FIB in mammals duplicated after the Eutheria split (e.g., ruminants, felines, primates) from therian mammals (e.g., marsupials) to form two main groups of sequences, the FIB and FIB-like groups. The FIB-like group transposed to another genomic context and remained syntenic in all the eutherian mammals. This transposition correlates with differences in the expression patterns of FIB-like proteins and with elevated Ks values potentially due to reduced evolutionary constraints of the duplicated copy. Our results point to a unique evolutionary event in mammals, between FIB and FIB-like genes, that led to non-redundant roles of the vital processes in which this protein is involved.

The Origin and Evolution of RNase T2 Family and Gametophytic Self-incompatibility System in Plants

“…Based on a phylogenetic analysis, the RNase T2 gene family was divided into three subgroups (Class I, II, and III), and the phylogenetic classification was supported by an analysis of conserved motifs ( Zhao et al 2017 ). Moreover, the phylogeny of RNase T2 family genes was verified by synteny network analysis ( Zhao and Schranz 2017 ), which was previously applied to infer the phylogeny of MADS-Box genes ( Zhao et al 2017 ), the TMBIM superfamily ( Gamboa-Tuz et al 2018 ), and fibrillarin (FIB) ( Pereira-Santana et al 2020 ). The number of RNase T2 genes was determined in each of the three classes of the 81 plant species.…”

Location, location, location: subcellular protein partitioning in proteostasis and aging

“…Ribosome assembly originates inside the nucleus in the membraneless nucleolus (Boisvert et al, 2007 ; Iarovaia et al 2019 ), where different ribosomal RNAs (rRNA) are transcribed by RNA polymerases (Paule and White 2000 ) and processed into the 40S (18S rRNA + 33 ribosomal proteins) and 60S (5S, 5.8S, and 28S rRNA + 46 ribosomal proteins) ribosomal subunits (Pena et al 2017 ). Processing of pre-rRNA is required for proper ribosomal subunit assembly and is promoted by the highly conserved rRNA 2’O-methyltransferase fibrillarin (FIB-1/FBL) (Pereira-Santana et al 2020 ). The nucleolus can expand or retract to address cellular needs for ribosomal biogenesis, and fibrillarin levels have been correlated with nucleolar expansion (Weber and Brangwynne 2015 ), which stimulates the rate of ribosome assembly (Tollervey et al 1993 ).…”

Fibrillarin-1 and Fibrillarin-2 are required for divergent cell lineage development in planarian homeostasis and regeneration

“…Fibrillarin (FBL) is an essential nucleolar protein that is conserved in organisms ranging from yeast to humans. The main structure of FBL contains two functional domains: a glycine/arginine-rich (GAR) region with nuclear localization signals and an RNA binding domain with methyltransferase (MTase) activity (Pereira-Santana et al , 2020; Rodriguez-Corona et al , 2015). Depending on its functional domain, FBL catalyzes the 2’-O-methylation of rRNA to process pre-rRNA into 18S rRNA and 28S rRNA.…”