Group II Intron-Encoded Proteins (IEPs/Maturases) as Key Regulators of Nad1 Expression and Complex I Biogenesis in Land Plant Mitochondria

Abstract

Mitochondria are semi-autonomous organelles that produce much of the energy required for cellular metabolism. As descendants of a bacterial symbiont, most mitochondria harbor their own genetic system (mtDNA/mitogenome), with intrinsic machineries for transcription and protein translation. A notable feature of plant mitochondria involves the presence of introns (mostly group II-type) that reside in many organellar genes. The splicing of the mtRNAs relies on the activities of various protein cofactors, which may also link organellar functions with cellular or environmental signals. The splicing of canonical group II introns is aided by an ancient class of RT-like enzymes (IEPs/maturases, MATs) that are encoded by the introns themselves and act specifically on their host introns. The plant organellar introns are degenerated in structure and are generally also missing their cognate intron-encoded proteins. The factors required for plant mtRNA processing are mostly nuclearly-encoded, with the exception of a few degenerated MATs. These are in particular pivotal for the maturation of NADH-dehydrogenase transcripts. In the following review we provide an update on the non-canonical MAT factors in angiosperm mitochondria and summarize the current knowledge of their essential roles in regulating Nad1 expression and complex I (CI) biogenesis during embryogenesis and early plant life.

MSP1 encodes an essential RNA‐binding pentatricopeptide repeat factor required for nad1 maturation and complex I biogenesis in Arabidopsis mitochondria

“…Group II introns are characterized by six domains (D1–D6) based on secondary structure, which adopt a complex tertiary structure mediated by long‐range tertiary interactions (Zhao & Pyle, 2017). Canonical introns in this class are able to catalyze their own excision in vitro , but their activities in vivo rely on intron‐encoded proteins (maturases, MATs), which assist in the folding of their cognate introns into the catalytically active form (Zhao & Pyle, 2017; Mizrahi et al ., 2022). The mitochondrial introns in angiosperms have diverged considerably in sequence, and most have also lost their cognate maturase‐ORFs (Guo & Mower, 2013; Schmitz‐Linneweber et al ., 2015).…”

MSP1encodes an essential RNA-binding PPR factor required fornad1maturation and complex I biogenesis inArabidopsismitochondria

“…The copyright holder for this preprint this version posted November 13, 2022. ; https://doi.org/10.1101/2022.11.12.516219 doi: bioRxiv preprint in the folding of their cognate introns into the catalytically-active form (Mizrahi et al, 2022;Zhao and Pyle, 2017). The mitochondrial introns in angiosperms have diverged considerably in sequence and have usually also lost their cognate maturase-ORFs (Guo and Mower, 2013;Schmitz-Linneweber et al, 2015).…”

“…Group II introns are characterized by six domains (D1-D6) based on secondary structure, which adopt a complex tertiary structure mediated by long-range tertiary interactions (Zhao and Pyle, 2017). Canonical introns in this class are able to catalyze their own excision in-vitro, but their activities in-vivo rely on intron-encoded proteins ( i.e ., maturase, Pfam-01348), which assist in the folding of their cognate introns into the catalytically-active form (Mizrahi et al, 2022; Zhao and Pyle, 2017). The mitochondrial introns in angiosperms have diverged considerably in sequence and have usually also lost their cognate maturase-ORFs (Guo and Mower, 2013; Schmitz-Linneweber et al, 2015).…”

“…During evolution, land plants have acquired many host factors to assist in the splicing of their highly derived organellar introns (Brown et al, 2014; Zmudjak and Ostersetzer-Biran, 2017). A few are related to maturases (Pfam-01348)(Mizrahi et al ., 2022), but most belong to a diverse set of RNA-binding protein families, such as RNA-helicases (pfam-00270), mitochondrial transcription termination factors (mTERFs, Pfam-02536), plant organelle RNA recognition (PORR, Pfam-11955), and pentatricopeptide repeat (PPR, Pfam-13812) proteins (Zmudjak and Ostersetzer-Biran, 2017). Currently there is very little mechanistic information about the molecular functions of these factors, specifically how they facilitate the processing of their mtRNA targets.…”

“…During evolution, land plants have acquired many host factors to assist in the splicing of their highly derived organellar introns (Brown et al, 2014;Zmudjak & Ostersetzer-Biran, 2017). A few are related to maturases (Pfam-01348) (Mizrahi et al, 2022), but most belong to different protein families, such as RNAhelicases (pfam-00270), mTERFs (Pfam-02536), PORR (Pfam-11955), or PPR (Pfam-13812) proteins (see e.g., (Colas des Francs- Zmudjak & Ostersetzer-Biran, 2017).…”