The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes

Dahan, Jennifer; Mireau, Hakim

doi:10.4161/rna.25568

Cited by 130 publications

(122 citation statements)

References 76 publications

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“…Both Rf loci occur within a cluster of tandemly repeated PPR genes, and LG7 contains the highest concentration of restorer-like PPRs in the M. guttatus genome [33]. Thus, the molecular basis of the CMS-Rf system in Mimulus resembles the cryptic CMS seen in diverse crop hybrids [30], and is probably representative of evolutionary processes commonly occurring throughout flowering plants [31,34].…”

Section: Introductionmentioning

confidence: 96%

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

et al. 2016

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Intraspecific coevolution between selfish elements and suppressors may promote interspecific hybrid incompatibility, but evidence of this process is rare. Here, we use genomic data to test alternative models for the evolution of cytonuclear hybrid male sterility in Mimulus. In hybrids between Iron Mountain (IM) Mimulus guttatus Â Mimulus nasutus, two tightly linked M. guttatus alleles (Rf1/Rf2) each restore male fertility by suppressing a local mitochondrial male-sterility gene (IM-CMS). Unlike neutral models for the evolution of hybrid incompatibility loci, selfish evolution predicts that the Rf alleles experienced strong selection in the presence of IM-CMS. Using whole-genome sequences, we compared patterns of population-genetic variation in Rf at IM to a neighbouring population that lacks IM-CMS. Consistent with local selection in the presence of IM-CMS, the Rf region shows elevated F ST , high local linkage disequilibrium and a distinct haplotype structure at IM, but not at Cone Peak (CP), suggesting a recent sweep in the presence of IM-CMS. In both populations, Rf2 exhibited lower polymorphism than other regions, but the low-diversity outliers were different between CP and IM. Our results confirm theoretical predictions of ubiquitous cytonuclear conflict in plants and provide a population-genetic mechanism for the evolution of a common form of hybrid incompatibility.

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Section: Introductionmentioning

confidence: 96%

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

et al. 2016

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“…Plant CMS results from genomic incompatibility between mitochondria and nuclei and is typically associated with an aberrant chimeric gene in the mitochondria (3)(4)(5)(6). A specific set of nuclear genes called restorer-of-fertility (Rf) genes, which primarily belong to the pentatricopeptide repeat (PPR) family, repress CMS through the promotion of the cleavage, degradation, or editing of CMS-associated aberrant transcripts or the inhibition of the translation of these genes (7)(8)(9). PPR proteins regulate RNA metabolism at multiple levels, from RNA editing, stability, processing, and splicing to translation (10,11).…”

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confidence: 99%

Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility

Huang

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

139

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Cytoplasmic male sterility (CMS) has been extensively used for hybrid seed production in many major crops. Honglian CMS (HL-CMS) is one of the three major types of CMS in rice and has contributed greatly to food security worldwide. The HL-CMS trait is associated with an aberrant chimeric mitochondrial transcript, atp6-orfH79, which causes pollen sterility and can be rescued by two nonallelic restorer-offertility (Rf) genes, Rf5 or Rf6. Here, we report the identification of Rf6, which encodes a novel pentatricopeptide repeat (PPR) family protein with a characteristic duplication of PPR motifs 3-5. RF6 is targeted to mitochondria, where it physically associates with hexokinase 6 (OsHXK6) and promotes the processing of the aberrant CMSassociated transcript atp6-orfH79 at nucleotide 1238, which ensures normal pollen development and restores fertility. The duplicated motif 3 of RF6 is essential for RF6-OsHXK6 interactions, processing of the aberrant transcript, and restoration of fertility. Furthermore, reductions in the level of OsHXK6 result in atp6-orfH79 transcript accumulation and male sterility. Together these results reveal a novel mechanism for CMS restoration by which RF6 functions with OsHXK6 to restore HL-CMS fertility. The present study also provides insight into the function of hexokinase 6 in regulating mitochondrial RNA metabolism and may facilitate further exploitation of heterosis in rice.cytoplasmic male sterility | pentatricopeptide repeat | restorer-of-fertility | RF6 | hexokinase 6 P lant cytoplasmic male sterility (CMS) is a trait characterized by a lack of functional pollen grains in plants, although female gametes are still viable (1). CMS has been widely used to produce hybrid seeds to improve plant yield, improve resistance to diseases or stresses, or enhance taste (2). Plant CMS results from genomic incompatibility between mitochondria and nuclei and is typically associated with an aberrant chimeric gene in the mitochondria (3-6). A specific set of nuclear genes called restorer-of-fertility (Rf) genes, which primarily belong to the pentatricopeptide repeat (PPR) family, repress CMS through the promotion of the cleavage, degradation, or editing of CMS-associated aberrant transcripts or the inhibition of the translation of these genes (7-9). PPR proteins regulate RNA metabolism at multiple levels, from RNA editing, stability, processing, and splicing to translation (10, 11). PPR proteins can be classified into PLS and P families based on the structure of PPR motifs (11). PLS family members generally exhibit direct RNA binding (12)(13)(14) or editing activity (15-17), whereas P-family proteins often lack sites for binding to RNA, particularly mitochondrial CMS-related RNA (18,19). Most of the known PPR proteins implicated in restoration of fertility (RF) are P-family members. Thus, RF-related PPR proteins may require additional partners, such as RNA-binding or splicing factors to process CMSrelated transcripts.Rice CMS is categorized into three major types: Wild Abortive (WA), originating from...

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“…Till date, only few Rf genes have been cloned, majority of which are known to encode for PPR proteins. Almost all plant genomes contain 10-30 Rf like proteins [59,60] that share significant sequence similarity with the Rf-PPRs from other plant species and thus cross species comparison of PPR proteins with known Rf genes can be used to identify a subset of Rf proteins known as RFL PPRs [39,47,61,62]. A microsynteny analysis was conducted between Arabidopsis and radish and was used to clone the PPR encoding Rfo locus in radish [28].…”

Section: Rfls Prediction In Legumesmentioning

confidence: 99%

“…These regions where RFL genes are clustered together could be considered as candidate regions to identify Rf genes in these species. For eg., 26 Rf like PPRs were identified in Arabidopsis in two clusters on chromosome 1 [28,60], chromosome 10 of rice possess 9 PPRs, out of which 3 were Rf PPRs [62]. Small cluster of RFL PPRs were identified on genome of Glycine, Vigna, Cicer and Phaseolus and allowed us to narrow down the list to 15 potential Rf genes in 4 legumes ( Table 2).…”

Section: Rfls Prediction In Legumesmentioning

confidence: 99%

Insights into PPR Gene Family in Cajanus Cajan and Other Legume Species

Kaur¹,

Verma²

2016

J Data Mining Genomics Proteomics

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PPR proteins comprises of several hundred members among land plants and govern a fascinating array of functions in organeller genomes that ranges from participation in stabilization of organeller transcripts, RNA editing to fertility restoration of CMS lines. Despite the availability of genome sequences of several legume species, comprehensive cataloguing of members of PPR gene family has not been carried out. In the current study, we identified 523, 830, 534, 816, 441 and 677 PPR proteins in Cajanus, Glycine, Phaseolus, Medicago, Vigna and Cicer genomes, respectively and their complete in silico categorization was undertaken to classify them into various sub-classes and their localization prediction. Chromosomal coordinates of 271 Cajanus PPR genes were predicted and their homologues were identified in 5 other legumes revealing extensive genome conservation. PPR genes of all 6 legume species were further probed to identify restorer of fertility-like PPRs (RFLs) on the basis of protein clustering and followed by homology searches to already known Rf-PPR genes. Seventy RFL PPR genes (P sub-class) were identified and were scrutinized by phylogenetic analysis which revealed extended similarity and common features shared by these RFLs across the species. Some of these RFL PPRs were present as small clusters in Glycine, Phaseolus, Vigna and Cicer genomes. This study has generated a knowledge base about PPR gene family in legumes and opens several avenues for future investigations into their molecular functions, evolutionary relationships and their potential in identifying markers to enable cloning of Rf genes.Citation: Kaur P, Verma M, Chaduvula PK, Saxena S, Baliyan N, et al. (2016) Due to certain limitations of demarking PPR motifs by classical system of categorization, PPR motifs has been redefined by Cheng et al. [15] whereby 10 PPR motif variants have been described and used to annotate PPR sequences in 109 genomes. Newly identified motif variants in PLS sub-class includes P1 and P2 motifs that differ from classical P motif in first helix; S2 (32 amino acid), SS (31 amino acid), E1 (34 amino acid) and E2 (34 amino acid) motif. This revision of PPR classification has provided a clearer picture of PPR structure and thus will provide new insights into their role in molecular and structural evolution.Most of these nuclear encoded PPRs carry N-terminal mitochondrial or chloroplast targeting sequence and are important contributors of various organellar post-transcriptional processes by virtue of their sequence specific RNA binding activity. Considering the array of functions governed by PPR proteins, identification and characterization of homologous and species specific PPR proteins in other plant species is critical for understanding the dynamics of nuclear cytoplasmic interactions.Cytoplasmic male sterility system is widely exploited/ phenomenon for hybrid seed production and has been extensively studied at molecular and biochemical level in various crops. Fertility restorers are an important component o...

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The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes

Cited by 130 publications

References 76 publications

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

Selfish evolution of cytonuclear hybrid incompatibility inMimulus

Pentatricopeptide-repeat family protein RF6 functions with hexokinase 6 to rescue rice cytoplasmic male sterility

Insights into PPR Gene Family in Cajanus Cajan and Other Legume Species

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