nMAT1, a nuclear‐encoded maturase involved in the trans‐splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function

Abstract

SUMMARYMitochondrial genomes (mtDNAs) in angiosperms contain numerous group II-type introns that reside mainly within protein-coding genes that are required for organellar genome expression and respiration. While splicing of group II introns in non-plant systems is facilitated by proteins encoded within the introns themselves (maturases), the mitochondrial introns in plants have diverged and have lost the vast majority of their intronencoded ORFs. Only a single maturase gene (matR) is retained in plant mtDNAs, but its role(s) in the splicing of mitochondrial introns is currently unknown. In addition to matR, plants also harbor four nuclear maturase genes (nMat 1 to 4) encoding mitochondrial proteins that are expected to act in the splicing of group II introns. Recently, we established the role of one of these proteins, nMAT2, in the splicing of several mitochondrial introns in Arabidopsis. Here, we show that nMAT1 is required for trans-splicing of nad1 intron 1 and also functions in cis-splicing of nad2 intron 1 and nad4 intron 2. Homozygous nMat1 plants show retarded growth and developmental phenotypes, modified respiration activities and altered stress responses that are tightly correlated with mitochondrial complex I defects.

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.…”

The γ-Carbonic Anhydrase Subcomplex of Mitochondrial Complex I Is Essential for Development and Important for Photomorphogenesis of Arabidopsis

“…Therefore, it was proposed that the gCA subcomplex may play a role in the light-dependent life style of plants (Brauna and Zabaleta, 2007). Several Arabidopsis mutants have been reported that affect proteins of complex I; these mutants showed growth retardation, abnormal leaf morphology, and poor germination (de Longevialle et al, 2007;Keren et al, 2012). A tobacco (Nicotiana tabacum) complex I-specific mutant, CMSII, exhibits decreased photosynthesis at atmospheric Figure 1.…”

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.…”