AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria

Abstract

Mitochondria (mt) in plants house about 20 group-II introns, which lie within protein-coding genes required in both organellar genome expression and respiration activities. While in nonplant systems the splicing of group-II introns is mediated by proteins encoded within the introns themselves (known as ''maturases''), only a single maturase ORF (matR) has retained in the mitochondrial genomes in plants; however, its putative role(s) in the splicing of organellar introns is yet to be established. Clues to other proteins are scarce, but these are likely encoded within the nucleus as there are no obvious candidates among the remaining ORFs within the mtDNA. Intriguingly, higher plants genomes contain four maturase-related genes, which exist in the nucleus as self-standing ORFs, out of the context of their evolutionary-related group-II introns ''hosts.'' These are all predicted to reside within mitochondria and may therefore act ''in-trans'' in the splicing of organellar-encoded introns. Here, we analyzed the intracellular locations of the four nuclear-encoded maturases in Arabidopsis and established the roles of one of these genes, At5g46920 (AtnMat2), in the splicing of several mitochondrial introns, including the single intron within cox2, nad1 intron2, and nad7 intron2.

The Pentatricopeptide Repeat Proteins TANG2 and ORGANELLE TRANSCRIPT PROCESSING439 Are Involved in the Splicing of the Multipartite nad5 Transcript Encoding a Subunit of Mitochondrial Complex I

“…This phenomenon has been reported for other mutants, such as otp43 (Falcon de Longevialle et al, 2007), bir6 (Koprivova et al, 2010), mtsf1 (Haïli et al, 2013), nMat1 (Keren et al, 2012), nMat2 (Keren et al, 2009), nMat4 (Cohen et al, 2014), mcsf1 (Zmudjak et al, 2013), and indh (Wydro et al, 2013), as well as the Nicotiana sylvestris mutant cms2 (Gutierres et al, 1997) and the maize (Zea mays) nonchromosomal stripe1 (Karpova and Newton, 1999). The molecular defect in tang2 is much stronger than that of otp439, and this is reflected by the quantity of the assembled complex I in the mutants, which is very likely the reason behind the discrepancy between their phenotypes.…”

“…and M. polymorpha also contain several group I introns, the vast majority of the introns in flowering plants (with the exception of the cox1 intron in some species) belong to group II, with 23 in Arabidopsis and rice (Oryza sativa; Bonen, 2008). These introns seem to have lost their self-splicing ability, thus necessitating the help of maturases such as the nuclearly encoded nMAT1, nMAT2, nMAT3, and nMAT4 and possibly the mitochondrial MatR, whose function is still elusive (Keren et al, 2009(Keren et al, , 2012Brown et al, 2014;Cohen et al, 2014). Plant mitochondrial DNA is renowned for its high recombination rates and its ability to integrate foreign DNA sequences, explaining the difficulty of retracing the evolutionary story of group II introns (Bonen, 2008).…”

“…The expression of the nad genes involves a combination of cis-and trans-splicing events that remove group II introns from the transcripts (Bonen, 2008). Several RNA-binding proteins are known to be involved in mitochondrial splicing events in nad transcripts: ORGANELLE TRANSCRIPT PROCESS-ING43 (OTP43; trans-splicing of nad1 intron 1; Falcon de Longevialle et al, 2007), ABSCISIC ACID OVERLY SENSITIVE5 (cis-splicing of nad2 intron 3; Liu et al, 2010), RCC1/UV-B RESISTANCE8/GUANINE NUCLEOTIDE EXCHANGE FACTOR3 (RUG3; (trans-splicing of nad2 intron 2 and cis-splicing of intron 3; Kühn et al, 2011), NUCLEAR MALE STERILE1 (cis-splicing of nad4 intron 1; Brangeon et al, 2000), BUTHIONINE SULFOMIXINE-INSENSITIVE ROOTS6 (BIR6; cis-splicing of nad7 intron 1; Koprivova et al, 2010), and other less-specific factors such as PUTATIVE MITOCHONDRIAL RNA HELI-CASE2 (PMH2; Köhler et al, 2010), maturases (nMAT1, nMAT2, and nMAT4; Keren et al, 2009Keren et al, , 2012Brown et al, 2014;Cohen et al, 2014), and the MITOCHONDRIAL CHLOROPLAST RNA SPLICING ASSOCIATED FACTORlike SPLICING FACTOR1 (mCSF1; Zmudjak et al, 2013) affecting numerous introns.…”

In-Depth Temporal Transcriptome Profiling Reveals a Crucial Developmental Switch with Roles for RNA Processing and Organelle Metabolism That Are Essential for Germination in Arabidopsis

“…S5). Notably, a number of recent studies have also confirmed the observed localization for four of these proteins, At5g46920 (Keren et al, 2009), At1g80270 (Doniwa et al, 2010), At5g60960 (Hammani et al, 2011), and At4g36040 (Chen et al, 2010).…”

Post-transcriptional Regulation in Mitochondria of Rice and Wheat at Low Temperatures

“…To date, there has been little information regarding their changes to explain regulation under different environments because PPR genes are expressed at low levels 47 . Furthermore, group II intron splicing factors besides PPR proteins have been found: MRS2, a homologue of the yeast splicing factor 68,69 , maturases, Marchantia or yeast group II intronic ORF homologs in higher plants 31,32,53,55 , PMH2, a DEAD-box protein 33 , and so on. Information on these genes will help develop environmental tolerances of crops.…”