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In certain plant species, multiple forms of CMS are found. These forms can be distinguished by their associated novel mitochondrial ORFs and by the nuclear Rf genes that restore their fertility (3, 4). In such cases, the restorers for the different forms represent distinct genes that map to different chromosomal loci. In maize, for example, there are three forms of CMS: T, S, and C. Restoration of cms-T requires two genes, Rf1 and Rf2, that map to chromosomes 3 and 9, respectively (5, 6), whereas cms-S is restored by Rf3 on chromosome 3 (7, 8) and cms-C is restored by Rf4 on chromosome 8 (9). In rice, as well, restorer genes for three different forms of CMS have been found to map to different chromosomes (10). Even when linkage is observed between restorers for different forms of CMS, on close examination these have been found to segregate as distinct loci, as in the case of the wheat Rfv1 and Rf3 genes (11). Although a single type of CMS may be restored by genes mapping to different chromosomal positions (7, 12), the converse situation, in which more than one type of CMS can be restored by a gene or genes present at a single locus, has not been shown to occur.
In other plant species where more than one form of CMS is found, restorer genes for the different systems map to different nuclear genetic loci, and, in those cases where the locus is known to have effects on mitochondrial gene expression, these effects have been observed only on corresponding CMS-associated mitochondrial gene region. The Rf-Mmt locus therefore is novel in two respects: different forms of this single locus represent restorer genes for two distinct CMS systems, and one form of the locus, Rfn(Mmt), affects the transcripts of three different mitochondrial gene regions.
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In recent years, genes encoding RF proteins have been cloned from various plant species (reviewed in refs 5 and 11). The best studied cereal CMS/Rf systems are in the genus Oryza (Supplementary Table S1 and references therein). The Rf-1 locus located on chromosome 10 in rice has been isolated independently by several groups and shown to restore fertility in BT-type CMS (Supplementary Table S1)26,27,28. Rf-1 encodes a protein composed of 791 amino acids comprising 18 tandem PPR motifs26,27. Later it was discovered that in the elite restorer line Minghui63 (MH63), the locus on chromosome 10 encodes two Rf-1 genes, which were named Rf1a and Rf1b8. Rf1b orthologs in 6 restoring and 6 non-restoring lines differ by single amino acid substitutions8. RF1A was proposed to restore male fertility by blocking production of the suspected CMS-inducing protein ORF79 via endonucleolytic cleavage of the B-atp6/orf79 transcript. RF1B most likely also causes degradation of this dicistronic mRNA via an unknown mechanism8. RF1a has been demonstrated to be epistatic to RF1b8.
In CMS-WA rice, an interaction involving mitochondrially encoded, CMS-conferring Wild Abortive 352 (WA352) protein, nuclearly encoded COX11 protein and two RF genes has been described29. It was proposed that WA352 protein, produced exclusively in the tapetum of CMS-WA plants, interacts with COX11 and suppresses its function29. This suppression induces premature programmed tapetal cell death and leads to pollen abortion29. Two genes, Rf3 and Rf4, located on rice chromosomes 1 and 10 respectively, can restore CMS-WA30,31. PPR9-782-M and PPR782a, RF4 candidate proteins from the elite restorer line MH63 and cultivar IR24 respectively, are 86% identical to the RF1A restorer of CMS-BT rice and are encoded within the same chromosomal region32,33. Recently, two genes designated Rf5 and Rf6 were determined to restore fertility in Hong-Lian CMS rice12,13.
Apart from these examples from rice and sorghum, no RF genes encoding PPR proteins have been cloned and characterised from other cereal crops. Although CMS-based hybrid systems can be established without Rf sequence information, such knowledge will certainly accelerate marker-assisted selection and transfer of Rf alleles into elite breeding lines through traditional breeding. The obtained sequences could, however, also be directly introduced into desired lines by transgenic approaches. Intensive efforts are being made to identify restorer genes for msm1 and msm2 male-sterile cytoplasms in barley, and recently high-resolution genetic and physical mapping narrowed the region containing the Rfm1 locus in barley to the short arm of chromosome 6H37. Similarly, although several major restoring alleles in maize including Rf1 for CMS-Texas (CMS-T)38, Rf3 for CMS-USDA (CMS-S)39 and Rf4 for CMS-Charrua (CMS-C)40 have been mapped for decades, their sequences remain to be isolated.
With recent advances in sequencing technology, a whole plethora of fully or partially sequenced plant genomes and transcriptomes have become available. We took advantage of these large-scale data sets to systematically identify and characterise 158 RFL genes from 13 rice genomes and Brachypodium distachyon. We have compared several alternative methods for distinguishing RFL sequences from other P-class PPR proteins, resulting in a rapid but robust and effective pipeline. Subtle but characteristic features of PPR motifs in RFL proteins separate them from the remaining P-class PPR proteins in cereals. Only a few RFL genes are found as singlets with the vast majority organised into genomic clusters showing relatively low interspecific synteny. To explore mechanisms underlying the high sequence diversity we analysed an RFL cluster in nine rice species and were able to confirm recombination events as major factors driving evolution of this unusual subfamily of PPR proteins. We discuss the possible mode of action of RFL proteins and the implications for plant fertility. The catalogue of cereal RFL sequences gathered in this study will be a useful resource for experimental approaches and will help in identifying RFL sequences in newly mapped genetic regions predicted to contain a restorer-of-fertility gene.
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