Organellar Introns in Fungi, Algae, and Plants

Abstract

Introns are ubiquitous in eukaryotic genomes and have long been considered as ‘junk RNA’ but the huge energy expenditure in their transcription, removal, and degradation indicate that they may have functional significance and can offer evolutionary advantages. In fungi, plants and algae introns make a significant contribution to the size of the organellar genomes. Organellar introns are classified as catalytic self-splicing introns that can be categorized as either Group I or Group II introns. There are some biases, with Group I introns being more frequently encountered in fungal mitochondrial genomes, whereas among plants Group II introns dominate within the mitochondrial and chloroplast genomes. Organellar introns can encode a variety of proteins, such as maturases, homing endonucleases, reverse transcriptases, and, in some cases, ribosomal proteins, along with other novel open reading frames. Although organellar introns are viewed to be ribozymes, they do interact with various intron- or nuclear genome-encoded protein factors that assist in the intron RNA to fold into competent splicing structures, or facilitate the turn-over of intron RNAs to prevent reverse splicing. Organellar introns are also known to be involved in non-canonical splicing, such as backsplicing and trans-splicing which can result in novel splicing products or, in some instances, compensate for the fragmentation of genes by recombination events. In organellar genomes, Group I and II introns may exist in nested intronic arrangements, such as introns within introns, referred to as twintrons, where splicing of the external intron may be dependent on splicing of the internal intron. These nested or complex introns, with two or three-component intron modules, are being explored as platforms for alternative splicing and their possible function as molecular switches for modulating gene expression which could be potentially applied towards heterologous gene expression. This review explores recent findings on organellar Group I and II introns, focusing on splicing and mobility mechanisms aided by associated intron/nuclear encoded proteins and their potential roles in organellar gene expression and cross talk between nuclear and organellar genomes. Potential application for these types of elements in biotechnology are also discussed.

From Genome Variation to Molecular Mechanisms: What we Have Learned From Yeast Mitochondrial Genomes?

“… Goddard and Burt (1999) provided a framework to explain the sporadic distribution of the ω intron; after invasion, the omega-HEGs undergo rapid degeneration and loss, followed by reinvasion. This process is coined as the Goddard–Burt life cycle by Mukhopadhyay and Hausner (2021) . The actual life cycle of introns is likely much more complex than cyclical invasion, degeneration, loss and then reinvasion.…”

The Pet127 protein is a mitochondrial 5′-to-3′ exoribonuclease from the PD-(D/E)XK superfamily involved in RNA maturation and intron degradation in yeasts

“…The results demonstrating the role of Pet127 in the degradation of intron-containing transcripts prompted us to investigate whether mitochondrial introns, particularly those belonging to Group I, could be linked to its biological function. Animal mitochondria are mostly intronless, with the exceptions mostly attributed to horizontal gene transfer events, and plant mitochondria are rich in Group II introns, but not in Group I ( Haugen et al 2005 ; Nielsen and Johansen 2009 ; Huchon et al 2015 ; Mukhopadhyay and Hausner 2021 ). There are, however, no Group I introns in the mitochondrial genomes of Rhodophyta, and ciliate mtDNAs generally lack introns, yet both groups contain Pet127 orthologs.…”

Mitochondrial Genomics of Six Cacao Pathogens From the Basidiomycete Family Marasmiaceae

“…roreri cob intronic ORF (orf357). The sequence and positional similarities and dissimilarities found for many of the Marasmiaceae intronic ORFs indicates a shared ancestral origin for many and varied histories of expansion and contraction dependent on the species, which is typical for mitogenomes (Megarioti and Kouvelis, 2020;Mukhopadhyay and Hausner, 2021). The intronic ORFs also share significant homologies with mitogenome intronic ORFs of unrelated fungal species (Supplementary Excel File 2), often outside the basidiomycetes, something commonly cited as evidence of introgression between diverse species.…”