Organellar maturases: A window into the evolution of the spliceosome

Abstract

During the evolution of eukaryotic genomes, many genes have been interrupted by intervening sequences (introns) that must be removed post-transcriptionally from RNA precursors to form mRNAs ready for translation. The origin of nuclear introns is still under debate, but one hypothesis is that the spliceosome and the intron-exon structure of genes have evolved from bacterial-type group II introns that invaded the eukaryotic genomes. The group II introns were most likely introduced into the eukaryotic genome from an α-proteobacterial predecessor of mitochondria early during the endosymbiosis event. These self-splicing and mobile introns spread through the eukaryotic genome and later degenerated. Pieces of introns became part of the general splicing machinery we know today as the spliceosome. In addition, group II introns likely brought intron maturases with them to the nucleus. Maturases are found in most bacterial introns, where they act as highly specific splicing factors for group II introns. In the spliceosome, the core protein Prp8 shows homology to group II intron-encoded maturases. While maturases are entirely intron specific, their descendant of the spliceosomal machinery, the Prp8 protein, is an extremely versatile splicing factor with multiple interacting proteins and RNAs. How could such a general player in spliceosomal splicing evolve from the monospecific bacterial maturases? Analysis of the organellar splicing machinery in plants may give clues on the evolution of nuclear splicing. Plants encode various proteins which are closely related to bacterial maturases. The organellar genomes contain one maturase each, named MatK in chloroplasts and MatR in mitochondria. In addition, several maturase genes have been found in the nucleus as well, which are acting on mitochondrial pre-RNAs. All plant maturases show sequence deviation from their progenitor bacterial maturases, and interestingly are all acting on multiple organellar group II intron targets. Moreover, they seem to function in the splicing of group II introns together with a number of additional nuclear-encoded splicing factors, possibly acting as an organellar proto-spliceosome. Together, this makes them interesting models for the early evolution of nuclear spliceosomal splicing. In this review, we summarize recent advances in our understanding of the role of plant maturases and their accessory factors in plants. This article is part of a Special Issue entitled: Chloroplast Biogenesis.

A Member of the Arabidopsis Mitochondrial Transcription Termination Factor Family Is Required for Maturation of Chloroplast Transfer RNAIle(GAU)

“…Although chloroplasts preserve features of prokaryotic genome organization, their gene expression system is far more complex than that of its cyanobacterial progenitor (for review, see Liere et al, 2011), as the maturation of chloroplast RNAs and their translation into proteins require a plethora of nucleus-encoded proteins. This machinery now includes additional RNA polymerases and s-factors as well as monospecific or merospecific RNA maturation factors that promote RNA transcription, splicing, editing, end formation, or translation (for review, see Stern et al, 2010;Lerbs-Mache, 2011;Tiller and Bock, 2014;Börner et al, 2015;Schmitz-Linneweber et al, 2015;Shikanai, 2015).…”

Mobile Group II Introns as Ancestral Eukaryotic Elements

“…They are particularly prevalent in the mtDNA of higher plants [5, 50]. Both cpDNA and mtDNA are highly dynamic and exhibit substantial variation in content and organization even among closely related species.…”

“…MatK and MatR work in combination with nuclear RNA processing factors and represent “a model for an early proto-spliceosomal activity” [58, 60], possibly providing insight into spliceosome evolution in early eukaryotes [50]. These organellar “proto-spliceosomes” are quite complex, facilitating splicing of different introns, and involving multiple proteins with diverse properties.…”

“…These organellar “proto-spliceosomes” are quite complex, facilitating splicing of different introns, and involving multiple proteins with diverse properties. Among the protein factors identified so far are nuclear-encoded maturases (nMATs), RNA chaperones, RNA stabilizing proteins, and RNA helicases [50, 61]. Recently, a multimolecular RNP supercomplex was characterized for trans -splicing group II introns from cpDNA of the green alga Chlamydomonas reinhardtii , revealing striking similarity to the nuclear spliceosome, such as dynamic association of trans -acting RNAs with a set of protein splicing factors [62].…”

“…More specifically, studying organellar group II introns and their splicing machinery might help us to resolve mysteries of spliceosomal intron emergence and the origin of the spliceosomal proteins. Keeping in mind that one of the key spliceosomal proteins, Prp8, displays homologies to group II intron IEPs and likely evolved from an ancestral maturase [2, 7, 23, 50, 64], understanding how organellar maturases act on multiple targets may help to answer the question of how maturase evolved into a core spliceosomal factor.…”