A Mitochondria-Targeted PPR Protein Restores pol Cytoplasmic Male Sterility by Reducing orf224 Transcript Levels in Oilseed Rape

Abstract

Cytoplasmic male sterility (CMS) in plants is a maternally inherited inability to produce functional pollen. CMS is generally caused by aberrant mitochondrial genes that are often chimeric in structure and frequently co-transcribed with conventional mitochondrial genes (Hanson and Bentolila, 2004). In many instances, male sterility can be recovered by nuclear-encoded restorer of fertility (Rf) genes. CMS/Rf systems serve as an excellent model to study mitochondrial-nuclear coevolution and interaction in plants as well as as a useful genetic tool for breeding to exploit hybrid vigor in crops (Chen and Liu, 2014). Polima (pol) CMS, initially reported in China, was the first CMS system used for commercial F 1 hybrid seed production in Brassica napus (Witt et al., 1991). The pol CMS system is associated with the presence of a chimeric open reading frame (ORF), orf224, located upstream of atp6, which encodes subunit 6 of mitochondrial ATPase (Singh and Brown, 1991;L'Homme and Brown, 1993). In the presence of the nuclear restorer gene, Rfp, processing of orf224/atp6 RNA is affected and its transcripts are specifically altered, which suggests that orf224 is the causal gene of pol CMS (Singh and Brown, 1991). A previous comparison of RNA-seq data between fertile and sterile young flower buds with pol CMS suggested that energy deficiency caused by orf224/atp6 may inhibit a series of genes that regulate pollen development via nuclear-mitochondrial interactions (An et al., 2014). However, how orf224/atp6 causes male sterility and how Rfp conditions orf224/atp6 transcription remain unclear. Answering both questions would represent an important step in characterizing Rfp.

PPR proteins – orchestrators of organelle RNA metabolism

“…There are also reports on agriculturally relevant species such as Zea mays (maize) or Oryza sativa (rice), which combined represent 25% of the total (Table ). For those from ‘other plant species’ the majority did not characterise the PPR function directly but instead linked it to an observed phenotype, most commonly cytoplasmic male sterility (CMS) (Gillman et al , Uyttewaal et al , Liu et al ). This is where ordinarily monoecious plants are converted to females because of pollen abortion, a desirable agronomic trait for ease of production of hybrid lines (reviewed in Budar et al ).…”

The RNA editing factor DUA1 is crucial to chloroplast development at low temperature in rice

“…However, little or no functional redundancy among PPR proteins has been found in higher plants, this situation indicates that the functions of PPR proteins are highly diversified in these plants. Accumulating evidence has revealed that PPR proteins are involved in a wide range of biological processes, such as cytoplasmic male sterility (CMS; Gaborieau et al ., ; Igarashi et al ., ; Liu et al ., , ), embryogenesis (Cai et al ., ; Li et al ., ; Tadini et al ., ), retrograde signaling (Sun et al ., ), and low temperature stress (Wu et al ., ; Wang et al ., ). However, the molecular mechanisms underlying the roles of PPR proteins in low temperature stress remain largely unknown.…”

“…Accumulating evidence has revealed that PPR proteins are involved in a wide range of biological processes, such as cytoplasmic male sterility (CMS; Gaborieau et al, *These authors contributed equally to this work. 2016; Igarashi et al, 2016;Liu et al, 2016Liu et al, , 2017, embryogenesis Li et al, 2018;Tadini et al, 2018), retrograde signaling (Sun et al, 2016), and low temperature stress (Wu et al, 2016b;Wang et al, 2017). However, the molecular mechanisms underlying the roles of PPR proteins in low temperature stress remain largely unknown.…”

Plant Mitochondrial Genome Evolution and Cytoplasmic Male Sterility

“…These are encoded not by the mitochondria, but by sequences in the nuclear genome. That is, sterility is reversed through synergistic cytonuclear interactions and antero/retrograde signaling between the mitochondrial and nuclear genomes (Rhoads and Subbaiah, 2007;Chen and Liu, 2014;Kitazaki et al, 2015;Liu et al, 2016). The exact nature of many of these RF loci, however, remains unknown.…”

“…Remarkably, many of the properties of the RF loci remain unknown. However, the coding capacity for those that are known (or can be predicted) are quite diverse, from an aldehyde dehydrogenase in maize (the first isolated plant restorer gene, Cui et al, 1996;Liu et al, 2001) to a putative peptidase in sugar beet (Matsuhira et al, 2012) to a suite of PPR proteins in diverse species (Brown et al, 2003;Kazama and Toriyama, 2003;Koizuka et al, 2003;Akagi et al, 2004;Komori et al, 2004;Klein et al, 2005;Wang et al, 2006;Uyttewaal et al, 2008;Jordan et al, 2010;Hu et al, 2012;Wang et al, 2013c;Kitazaki et al, 2015;Liu et al, 2016).…”