Research Progress in the Molecular Functions of Plant mTERF Proteins

Abstract

Present-day chloroplast and mitochondrial genomes contain only a few dozen genes involved in ATP synthesis, photosynthesis, and gene expression. The proteins encoded by these genes are only a small fraction of the many hundreds of proteins that act in chloroplasts and mitochondria. Hence, the vast majority, including components of organellar gene expression (OGE) machineries, are encoded by nuclear genes, translated into the cytosol and imported to these organelles. Consequently, the expression of nuclear and organellar genomes has to be very precisely coordinated. Furthermore, OGE regulation is crucial to chloroplast and mitochondria biogenesis, and hence, to plant growth and development. Notwithstanding, the molecular mechanisms governing OGE are still poorly understood. Recent results have revealed the increasing importance of nuclear-encoded modular proteins capable of binding nucleic acids and regulating OGE. Mitochondrial transcription termination factor (mTERF) proteins are a good example of this category of OGE regulators. Plant mTERFs are located in chloroplasts and/or mitochondria, and have been characterized mainly from the isolation and analyses of Arabidopsis and maize mutants. These studies have revealed their fundamental roles in different plant development aspects and responses to abiotic stress. Fourteen mTERFs have been hitherto characterized in land plants, albeit to a different extent. These numbers are limited if we consider that 31 and 35 mTERFs have been, respectively, identified in maize and Arabidopsis. Notwithstanding, remarkable progress has been made in recent years to elucidate the molecular mechanisms by which mTERFs regulate OGE. Consequently, it has been experimentally demonstrated that plant mTERFs are required for the transcription termination of chloroplast genes (mTERF6 and mTERF8), transcriptional pausing and the stabilization of chloroplast transcripts (MDA1/mTERF5), intron splicing in chloroplasts (BSM/RUG2/mTERF4 and Zm-mTERF4) and mitochondria (mTERF15 and ZmSMK3) and very recently, also in the assembly of chloroplast ribosomes and translation (mTERF9). This review aims to provide a detailed update of current knowledge about the molecular functions of plant mTERF proteins. It principally focuses on new research that has made an outstanding contribution to unravel the molecular mechanisms by which plant mTERFs regulate the expression of chloroplast and mitochondrial genomes.

Identification, Characterization, and Expression Profile Analysis of the mTERF Gene Family and Its Role in the Response to Abiotic Stress in Barley (Hordeum vulgare L.)

“…Due to endosymbiotic evolution from their cyanobacterial ancestors, most of the organellar genes within chloroplasts and mitochondria have been either lost or transferred to the nucleus (Gray, 2012). Current chloroplast and mitochondrial genomes retain only a tiny fraction of the genes, which are required for photosynthesis, gene expression, and electron transport chains (Lang et al, 1999;Yagi and Shiina, 2012;Robles and Quesada, 2021). Nevertheless, thousands of proteins have been predicted to be localized in plant mitochondria and chloroplasts according to bioinformatics analysis, most of which are encoded by the nuclear genome (Binder and Brennicke, 2003;Huang et al, 2013;Lee et al, 2013).…”

Transcriptomic and Physiological Response of Durum Wheat Grain to Short-Term Heat Stress during Early Grain Filling

“…In this manner, we identified seven members of the mTERF family as the most relevant nodes of this network (Figure 6a). Plant mTERFs are nuclear-encoded proteins capable of binding nucleic acids and regulating organellar gene expression and therefore are located in chloroplasts and/or mitochondria [85]. Several studies based on the phenotype of mTERF mutants suggested that these genes are essential for the functional acclimation to diverse abiotic stresses, including heat stress [86].…”

mTERF18 and ATAD3 are required for mitochondrial nucleoid structure and their disruption confers heat tolerance in Arabidopsis thaliana

“…30 amino acid motif (Hammani et al ., 2014), were first discovered in human mitochondria and are unique to multicellular eukaryotes (Kruse et al ., 1989). All mTERFs studied to date bind either DNA or RNA in organelles and control DNA replication or organelle gene expression at different levels (Roberti et al ., 2009; Hammani & Giegé, 2014; Kleine & Leister, 2015; Quesada, 2016; Jiang et al ., 2020; Robles & Quesada, 2021). While humans express only four mTERFs, in Arabidopsis there are 35 mTERFs, most of which are localized to chloroplasts and/or mitochondria (Babiychuk et al ., 2011; Kleine, 2012).…”

“…mTERF2 associates with ycf3 and rps12 RNAs to promote splicing of group IIB introns (Lee et al ., 2021). For many other plant mTERFs, their nucleic acid targets and interacting proteins remain to be identified (Robles & Quesada, 2021).…”