Structural-functional dynamics of group II introns in plant mitochondria: splicing diversity-driven genome plasticity and regulatory adaptation

Introns, fundamental components of eukaryotic genomes, perform critical functions in regulating gene expression through splicing mechanisms. In addition to their primary role in RNA processing, other functional aspects of introns include the enhancement of neighboring gene expression by intronic enhancers, the regulation of alternative splicing by cis-acting elements, and participation in mRNA trafficking and chromatin organization through interactions with nuclear speckles and chromatin-modifying complexes. Introns are classified into four main groups based on their structural characteristics and splicing mechanisms: (1) nuclear mRNA introns processed by spliceosomes composed of small nuclear ribonucleoproteins; (2) tRNA introns removed by specific endonucleases that cleave at conserved sequences; (3) self-splicing group I introns that use guanosine cofactors to initiate transesterification reactions; and (4) ribozyme-containing group II introns with reverse transcriptase-associated mobility. Although plant mitochondria contain both group I and group II introns, group II introns demonstrate greater prevalence and functional significance across most examined species, constituting over 80% of mitochondrial introns in angiosperms.Group II introns represent a distinct class of ribozyme–protein complexes, consisting of catalytic RNA components with six conserved domains (DI–DVI) and intron-encoded proteins performing maturase, reverse transcriptase, and endonuclease activities. These introns are characterized by their conserved secondary structure, where DI forms the scaffold, DV contains the catalytic AGC triad, and DVI harbors the branch point adenosine. They also function as mobile genetic elements with splicing mechanisms analogous to nuclear spliceosomes, suggesting evolutionary convergence in eukaryotic gene regulation. In plant mitochondria, which are organelles of α-proteobacterial origin, group II introns exhibit dynamic genomic behavior through horizontal transfer events, facilitated by intron-encoded protein-driven reverse splicing, resulting in their acquisition or loss across plant lineages. These introns primarily occur in genes encoding respiratory chain components, including nad for NADH dehydrogenase, sdh for succinate dehydrogenase, and cob for cytochrome c reductase, where their splicing is integrally linked to mitochondrial transcript maturation. This maturation process includes two critical post-transcriptional modifications: (1) intron splicing, which not only ensures proper mRNA processing but also generates trans-acting protein factors affecting RNA metabolism; and (2) C-to-U RNA editing, which corrects nucleotide mismatches to maintain functional conservation. Group II introns display structural diversity, including simplified forms produced by trans-splicing and nested intron arrangements forming twintrons, where outer intron splicing requires prior internal intron in ORF removal. This structural plasticity highlights their dual role as regulators of respiratory gene expression and drivers of mitogenome evolution.This review discusses recent developments in plant mitochondrial group II introns, focusing on their structure, splicing diversity, such as hydrolytic and circularization pathways, and interaction with RNA editing factors. Through examination of the “splicing–editing” relationship and evolutionary pathways of these elements, this study provides new perspectives on the adaptive mechanisms influencing mitogenome dynamics and energy metabolism in plants.