Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection
© Geddy and Brown; licensee BioMed Central Ltd. 2007
Received: 14 November 2006
Accepted: 23 May 2007
Published: 23 May 2007
The pentatricopeptide repeat (PPR) is a degenerate 35 amino acid motif that occurs in multiple tandem copies in members of a recently recognized eukaryotic gene family. Most analyzed eukaryotic genomes contain only a small number of PPR genes, but in plants the family is greatly expanded. The factors that underlie the expansion of this gene family in plants are not as yet understood.
We show that the location of PPR genes is highly variable in comparisons between orthologous, closely related, and otherwise co-linear chromosomal regions of the Brassica rapa or radish and Arabidopsis thaliana. This observation also pertains to paralogous duplicated segments of the genomes of Arabidopsis thaliana and Brassica rapa. In addition, we show that PPR genes that seem closely linearly aligned in these comparisons are not generally found to be closely related to one another at the nucleotide and amino acid sequence level. We observe a relatively high level of non-synonomous vs synonomous changes among a group tandemly repeated radish PPR genes, suggesting that these, and possibly other PPR genes, are subject to diversifying selection. We also show that a duplicated region of the Arabidopsis genome possesses a relatively high density of PPR genes showing high similarity to restorers of fertility of cytoplasmic male sterile (CMS) systems of petunia, radish and rice. The PPR genes in these regions, together with the restorer genes, are more highly similar to one another, in sequence as well as in structure, than to other PPR genes, even within the same sub-family.
Our results suggest are consistent with a model in which at least some PPR genes undergo a "birth and death" process that involves transposition to unrelated chromosomal sites. PPR genes hold certain features in common with disease resistance genes (R genes), and their "nomadic" character suggests that their evolutionary expansion in plants may have involved novel molecular processes and selective pressures.
The pentatricopeptide repeat (PPR) peptide motif, first described by Small and Peeters , is a degenerate 35 amino acid sequence, closely related to the 34 amino acid tetratricopeptide repeat (TPR) motif. TPRs occur as tandem repeats in a widespread protein family of both prokaryotes and eukaryotes. PPRs also occur in multiple tandem repeats, but have thus far been found to be exclusively eukaryotic in their distribution. On the basis of the solved structure of a TPR domain  as well as modelling approaches , each PPR domain is though to be configured as two distinct anti-parallel alpha-helices, helices A and B. In PPR proteins, tandem repeats of these alpha-helical pairs are predicted to form a superhelix that encloses a central spiral groove with a positively charged ligand-binding surface . PPR proteins are known to mediate specific RNA processing events including RNA editing , transcript processing , and translation initiation , and are thus thought to be capable of specific binding to both protein and RNA molecules.
Although all sequenced eukaryotic genomes have been found to encode PPR proteins, the numbers of PPR genes in both animal and fungal genomes is relatively small. In plants, however, the size of this gene family is greatly expanded. In Arabidopsis thaliana there are 441 identified PPR genes and more than 655 PPR proteins have been predicted to occur in the rice genome .
Analysis of the PPR gene content of the Arabidopsis genome by Lurin et al.  elucidated several categories and subcategories of PPR genes. The largest category encodes proteins that are composed of tandem repeats of the "classical" 35 amino acid PPR motif initially described by Small and Peeters , and now referred to as the P-type repeat. Lurin et al.  were able to differentiate three additional PPR-related motifs found in PPR-encoding genes. Two of these motifs, S and L1, are tandemly arrayed with the classical P-type motif in a repeated P-L1-S (PLS) pattern, with the third motif, L2, replacing L1 in the last repeat pattern at the C-terminal end of the protein. Their analyses also showed that the PLS subfamily of PPR-encoding genes is unique to plants and not found in other systems. Four subgroups of PPR proteins from the PLS subfamily differ in the structure of their C-terminal domains. Although two of the subgroups, E and E+, are highly degenerate in their C-terminal sequences, the DYW subgroup shows some conservation of amino acid residues. It has been suggested that this C-terminal domain may function as a catalytic domain for these PPR proteins . One PPR gene belonging to the PLS subfamily is Emb175, a gene essential for plant embryogenesis. EMB175, like many PPR proteins, is targeted to the plastid .
Another major group of plant-specific PPR genes are the restorer of fertility (Rf) genes. These nuclear-encoded genes act to suppress male sterility associated with cytoplasmic male sterility (CMS), a phenomenon related to the expression of mitochondrially-encoded sterility-associated genes. Rf genes identified thus far in petunia, rice and radish belong to the P subfamily of PPR genes [8–10].
Expansion of the complement of PPR genes within plant genomes may have occurred through gene duplication. In Arabidopsis, ancient large-scale genome duplication events have resulted in multiplication of loci and regions of synteny, where gene number and location are conserved as paralogous copies. Gene duplication can also arise from tandem and segmental gene duplication, creating clusters of identical genes that diverge over time [11, 12]. With the exception of one location on chromosome 1, no clustering of PPR genes has been reported for Arabidopsis . However, tandem clusters of PPR genes have been observed in petunia  radish  and rice [9, 13, 14].
The synteny observed in duplicated genomic regions within a genome or between orthologous copies in related genomes can be exploited in gene mapping. However, disruptions of synteny can occur due to gene loss, rearrangement, acquisition or duplication. The source of these structural changes can be due to tandem and segmental duplication, as discussed above, but could also be attributed to aberrant homologous recombination, selection, or changes introduced by transposition events.
The radish restorer of fertility, Rfo, is found in a cluster of PPR genes at a genomic site where no corresponding PPR gene is found in the syntenic region of Arabidopsis . We report here that other PPR genes display a characteristic lack of synteny in comparisons of both orthologous and paralogous plant genomic regions. We show that while non-PPR genes are largely co-linear in arrangement and identical in orientation between different related regions, PPR genes are rarely maintained in the same position or orientation when two related regions are compared. We show that PPR gene family members share characteristics with plant disease resistance genes (R genes); in particular we present evidence that at least some PPR genes, as per R genes, are subject to diversifying selection, i.e. an evolutionary process that selects for, rather than against, mutations that lead to amino acid replacements in the encoded proteins. Such diversifying selection processes may also act to multiply and distribute copies of the genes. Our results also suggest that the Birth-and-Death process initially described for immunoglobulin genes , and adapted by Michelmore and Meyers  for R genes, may apply as well to the duplication and divergence of PPR genes.
Locations of PPR genes are highly variable between co-linear regions of Arabidopsis and Brassica or Raphanus genomes
The syntenic region of the Arabidopsis genome also contains a predicted gene (At1g13040) that could potentially specify a protein with six PPR domains. In contrast with At1g13020, At1g13030 and At1g13060, this protein, has little similarity with PPR protein encoded by the PPR gene in the co-linear Brassica rapa region (26% identity [I], 46% similarity [+]). Moreover, its location, between At1g13030 and At1g13050, is different from that of the Brassica rapa PPR gene, which is positioned between orthologs of At1g13020 and At1g13030; its transcriptional orientation, with respect to the co-linear genes of the region, also differs. Interestingly, this Brassica PPR protein does show a high degree of sequence similarity with Arabidopsis PPR genes present at distinct sites on chromosome one. In particular, it possesses 69% identity and 81% similarity with the protein encoded by At1g12300, a PPR gene located in a cluster of such genes near the 4.3 megabase (Mb) mark of chromosome one. Thus, we observe a preservation of synteny for most genes between these Arabidopsis and Brassica genomic regions but an apparent lack of synteny for the PPR genes. This suggests that the function and order of the non-PPR genes in the region has been conserved during the evolution of the Brassicaceae, but that one, and possibly both of the PPR genes in these two related chromosome regions has descended from a progenitor located at a distinct, non-syntenic chromosomal site.
IJC2 and P2-9 both show extensive similarity to a region of Arabidopsis chromosome I spanning the nine genes flanked by At1g12760 and At1g12820 (Figure 2); one of these Arabidopsis genes, At1g12775, encodes a PPR domain protein. The nucleotide sequence identity between the Arabidopsis and Brassica coding sequences in this region is 85–90%. Gene order is maintained between Arabidopsis and the two Brassica rapa sequences, with a few exceptions. No counterpart of At1g12790, and only a portion of At1g12800, are found in the Brassica cosmids.
The Brassica rapa gene P2-9-3 is similar in both sequence and orientation to the Arabidopsis PPR gene At1g12775. P2-9-1 is a duplication of the 3' end of P2-9-3. In addition, P2-9-1 and P2-9-2 are represented in IJC2 as IJC2-4 and IJC2-3, respectively, and are inverted in orientation with respect to their P2-9 counterparts. It is likely that after the genomic duplication leading to the formation of these paralogous regions, a local rearrangement occurred. This rearrangement may have excised the P2-9-1/P2-9-2//IJC2-4/IJC2-3 fragment and reinserted it into the genome, knocking out the 3' end of IJC2-2 and replacing it with the inverted fragment. This may have occurred through the homologous recombination of P2-9-1 and the 3' end of P2-9-3//IJC2-2.
The Brassica rapa PPR-encoding open reading frame (ORF) P2-9-1 is found in a genomic region that corresponds to sequences flanking At1g12760; no PPR domain-encoding regions occur in this location in the Arabidopsis sequence. As explained above, the duplication of the Brassica rapa ortholog of At1g12775, P2-9-3, likely resulted in the presence of multiple PPR sequences. The positioning of P2-9-1 to the left of the At1g12760 ortholog P2-9-2 suggests that a genome rearrangement occurred at this location after the split between Arabidopsis and Brassica which resulted in the movement of At1g12760/P2-9-2 sequences. Thus, as in other genomic comparisons, PPR encoding regions in P2-9, IJC2 and the corresponding Arabidopsis chromosome I segment are more highly rearranged than flanking regions encoding other types of proteins, perhaps as a direct result of the movement of PPR genes.
Variation in PPR gene location between two paralogous gene regions on chromosome I of Arabidopsis
Several restorer genes from various plant species have thus far shown homology to a cluster of PPR genes found in the Arabidopsis thaliana genome . This particular set of PPR genes is the largest grouping in the Arabidopsis genome of highly homologous PPR genes. This genome segment is located at about the 23 Mb mark of chromosome 1 and includes loci At1g62260 through At1g63630, encompassing 18 PPR genes and pseudogenes . Rfp, the restorer of fertility for polima CMS of Brassica napus, has been mapped to a genomic region that is syntenic to a portion of the Arabidopsis genome located near the 4.3 Mb coordinate of chromosome 1 .
Conservation of genes within two regions of Arabidopsis chromosome 1.
4.3 Mb region2
23 Mb region3
Number of genes/ORFs
2 (+ 1 transposon)
% conserved genes1 (all, discounting PPRs)
Relatedness of genes of the 4.3 and 23 Mb syntenic regions of Arabidopsis in pairwise comparisons of coding regions at the nucleotide and protein levels.
4.3 Mb region locus
23 Mb region locus
% nucleotide identity1
% amino acid identity/similarity1
DREB subfamily Transcription factor
DREB subfamily Transcription factor
DREB subfamily Transcription factor
DREB subfamily Transcription factor pseudogene
O-acyl transferase protein
O-acyl transferase protein
F-box family protein
F-box family protein
Rhomboid family protein
Rhomboid family protein
Zinc finger protein
Zinc finger protein
The overall degree of similarity between between the restorer genes and the related Arabidopsis P subfamily PPR genes of the 23 and 4.3 Mb regions is 49%I/66%+, a much higher percentage than between restorers and unrelated P and PLS subfamily PPR genes. This evidence taken together indicates that PPR-encoding restorer genes originate from the same subset of P subfamily PPR genes; no PPR-encoding restorer genes have yet been shown to originate from any other subtype of PPR gene.
Annotation and subcellular localization of PPR-encoding proteins from various plants.
Similar to At1g12300
Brassica cosmid P2-9
Similar to At1g12775
Brassica cosmid IJC2
Similar to At1g12775
Radish Rfo region
Arabidopsis chromosome 1, 4.3 Mb region
Arabidopsis chromosome 1, 23 Mb region
As can be seen in Figure 4, the order of genes, and their direction of transcription, is conserved for the non-PPR encoding genes. PPR genes, however, appear to be distributed randomly throughout the two regions. Comparisons of the PPR sequences of the two regions do not reveal a significant correlation of homology between closely linearly aligned PPR genes. For example, At1g12700 shares 50% homology and 65% identity with At1g63070 and At1g63080, with which it is most closely linearly aligned, but this is about the same degree of similarity as is found between it and the other PPR genes in the 23 Mb region.
PPR genes in the radish Rfo region have been subject to diversifying selection
Synonymous and nonsynonymous nucleotide substitution in pairwise comparisons of sequences from radish and Arabidopsis.
Synonymous nucleotide substitutions (Ks)
Nonsynonymous nucleotide substitutions (Ka)
Pentatricopeptide repeats (PPR) are structural motifs encoded by a large number of genes in plants and other organisms, although the PPR gene family is greatly expanded in plants. It was hypothesized that this could be due to novel functions served by PPR proteins in plants that are not required in other organisms, or that PPR proteins replace functions performed by other genes in other organisms . Recent evidence shows that PPR proteins can function in chloroplast RNA editing via post-transcriptional conversion of cytosines to uracil , supporting the first hypothesis.
Restoration of male fertility is a plant-specific function encoded by PPR genes. Several recently identified restorers of male fertility in plants encode PPRs that are related to each other at the amino acid level. Rf1 of petunia , Rf-1 from rice , and Rfo from radish  are restorers of fertility encoding pentatricopeptide repeat proteins that share approximately 50% amino acid similarity to one another. Since the PPR-encoding restorer genes discovered thus far share sequence similarity, and arise in related gene regions (as is the case with Rfo from radish ), it seems reasonable to speculate that these genes have arisen from a small number, perhaps even a single, progenitor PPR gene or genes. It is possible that sequences similar to a restorer gene progenitor are located in the 23 Mb region of chromosome I, and that a progenitor of one these genes may have functioned as a restorer gene at some point in the evolutionary past.
We have found that through comparisons of closely related orthologous sequences as well as comparisons of paralogous regions within the Arabidopsis and Brassica genomes, the locations of genes encoding PPR domain proteins are highly variable relative to the locations of other types of genes. A consideration of the most abundant type of plant disease resistance genes (R genes), NBS-LRR genes, may be useful for understanding the mechanisms underlying PPR gene diversity and evolution. PPR genes and NBS-LRR type R genes share several features in common. Both types of genes encode proteins with a variable number of repetitive motifs, leucine-rich repeats (LRRs) in the case of NBS-LRR type R genes. In both cases, a single dominant gene determines the phenotype, and, in addition, it is the sequence variability within the repeats that lends specificity of action [10, 16, 27, 28]. Finally, the genomic positions of many R genes are not conserved in otherwise syntenic regions of grass genomes , similar to the variability in genomic location of PPR genes shown here.
The evolution and diversity of plant disease resistance genes is a result of tandem and segmental gene duplication, recombination, mutation and natural selection . Two sources of gene duplication include local chromosomal rearrangement and large scale genomic duplications ; this is consistent with the conserved synteny model of gene evolution that states that these two mechanisms are the cause of gene distribution and long-distance (ectopic) duplication of genes . However, most gene duplications are within restricted local chromosomal segments. These local events are the most recent duplications and are most evident when they interrupt the colinearity of gene order in duplicated chromosomal fragments .
A nonconservative mechanism (i.e. a local change of location) would explain the lack of conservation of synteny we observe for PPR genes within closely related genomic segments. Lurin et al.  suggest that one or more bursts reverse transposition and reintegration could account for the wide distribution of PPR genes among chromosomes, as well as the paucity of introns in these genes. Our data suggest that if retrotransposition underlies transience in location observed among PPR genes, such events occur relatively frequently. Moreover, our findings suggest that following such a transposition event, the original gene copy would be quickly be lost, as we find no evidence for such remnants of PPR genes in comparisons in regions where a PPR gene exists in one, but not other related genomic regions. It is possible that the "nomadic" character of PPR genes reflects as yet unrecognised mechanism of gene duplication and transposition, and results in deviations in synteny in orthologous and paralogous comparisons.
Paralogous PPR genes such as those found in the syntenic Arabidopsis 4.3 and 23 Mb regions are likely the result of genomic duplications. Such duplicated regions are thought to diverge because they are physically too distant from one another for to allow for intergenic exchange . Instead, sequence variability and changes in copy number within such regions likely results from interallelic recombination and diversifying selection . Over time, tandem gene duplication can occur as is seen in the radish Rfo region. Interestingly, this tandem duplication is not evident in Arabidopsis PPR gene distribution. PPR genes are for the most part found as singlets with PPR gene subgroup members evenly distributed in the Arabidopsis genome amongst the five chromosomes, whereas R genes are found more often in clusters of related genes . This may be a result of the large diversifying selective pressure exerted on disease resistance loci as plants are continually adapting to new plant pathogens .
Previous studies showed only one defined cluster of PPR genes in Arabidopsis thaliana; it is the cluster related to restorer genes of rice, petunia and radish . It is possible that this clustering indicates diversifying selection acting on PPR genes from that region as a result of plants adapting to newly emerging sterility inducing genes. The diversifying selective pressure exerted on the mini-cluster of PPR genes at the radish Rfo locus is one example of this effect acting on PPR genes and not on other genes of the same region. Again, the PPR genes of the Rfo region are out of synteny with the PPR genes of Arabidopsis, while the non-PPR encoding gene locations are conserved. Diversifying selection may partly explain why non-PPR genes are not apt to fall out of synteny with their paralogous partners. If diversifying selection is not acting on a gene then any changes in the sequence are less likely to lead to changes in gene structure, location or in the amino acid sequence of the encoded protein; synonymous substitution would outweigh nonsynonymous substitution and there would be little selection for sequence location changes [27, 33].
Mitochondrially-encoded CMS genes, as well as associated nuclear restorer genes, arise naturally in plant populations. It has been suggested that the spread of maternally-inherited male sterility in a hermaphroditic plant populations may be advantageous, since female individuals would not need to invest resources into the production of pollen . If the frequency of such a gene were to become sufficiently high, it would create selective pressure for the evolution of a corresponding nuclear restorer gene. This scenario has been termed an "intra-genomic arms race" . It is possible that such selective pressure is responsible for the diversification of at least a portion of the PPR genes in a particular plant genome, such as that in the Rfo region of radish. Moreover, the maintenance of CMS genes within the mitochondrial genome would provide selective pressure for the maintenance of corresponding restorers in the nuclear genome. The eventual loss of the CMS gene from the mitochondria would allow loss of the restorer gene from the nucleus. This scenario provides one mechanism for the "Birth-and-Death" of plant PPR genes.
The presence of so-called false PPR genes  also follows the Birth-and-Death model adopted by Michelmore and Meyers  for R genes, which indicates that following gene duplication due to diversifying selection some members have become redundant; mutations which cause frameshifts or premature stop codons in the coding sequences of these genes have had their function disabled. It has been noted that PPR genes contain, on average, many fewer introns than other Arabidopsis genes, thus increasing the likelihood that mutations will affect coding regions .
We show here that PPR genes, at least those in the P subfamily, possess a novel, "nomadic" character in that their positions are highly variable in otherwise co-linear segments of closely related genomes. This suggests that they may be undergoing a "Birth-and-Death" process that would involve either non-conservative transposition or conservative transposition followed by rapid loss of the non-transposed copy of the gene. They resemble, in several respects, another versatile gene family of plants, disease resistance genes. The common features exhibited by both types of genes are consistent with the view that PPR genes may, like R genes function as proteins with malleable binding capacities that can undergo rapid alterations in response to changing selective pressures. Since it appears that most PPR genes in plants function by binding to one or a small number of specific target organelle transcripts, it is possible that changes in organelle genomes drive PPR gene evolution and thus the evolution of this gene family in plants likely reflects the co-evolution of nuclear and organelle genomes. This work suggests that evolution of PPR genes in plants may involve novel molecular mechanisms and illustrates one additional feature of this interesting and enigmatic gene family.
Brassica rapa cosmid clones
The Rfp gene has been mapped to a region of the Brassica napus genome syntenic with Arabidopsis genome sequence surrounding the 4.3 Mb coordinate on chromosome 1 . Primers for the amplification of gene sequences in this region were designed using the online software Primer3 . These primers were used to amplify the corresponding sequences from Brassica napus cv. Westar total DNA using the polymerase chain reaction (PCR) with annealing temperatures varying depending on the degree of homology between primers and their corresponding Brassica sequence.
The amplified sequences were labelled with digoxygenin according the manufacturer's (Roche Diagnostics, Laval, Quebec) instructions and hybridised to colony lifts of a genomic library derived from a B. rapa Rfp containing doubled haploid individual, as described .
Sequencing and sequence assembly was performed by DNALandmarks (St-Jean-sur-Richelieu)  and Genome Quebec (Montreal) using the Applied Biosystems 3730XL DNA analyzer for capillary sequencing and the Phred/Phrap programs for some of the sequence assembly. Additional sequences obtained via shotgun sequencing were assembled using CodonCode Aligner v.1.3.4 . Sequences were analysed using ORF finder  to detect ORFs, Genscan  to detect promotor regions, introns/exons and polyA signals, and Augustus to detect ORFs, intons and exons . Blast and Blast2Sequences  were used for data mining from nucleotide and protein databases and for aligning pairs of sequences. Tree building was performed with TreeTop  using the Blosum62 matrix and phylip tree building software. Multiple sequence alignments were performed using ClustalW online . Protein comparisons were based on the ClustalW aligments whenever possible. The output was shaded using Boxshade online . Subcellular targeting predictions were made using online programs Mitoprot  and Predotar . The sequences of clones P2, P2-9 and IJC2 have been deposited in GenBank and are listed under accession numbers EF584011, EF584012 and EF584013 respectively.
Criteria for choosing pairs of duplicated genes included online annotation mapping [47, 48] and BLAST sequence alignment of the entire CDS and protein sequences with a cutoff expect value of 1e-20 and bit score of >100.
This work was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada. Hilary Geddy provided assistance with the formatting of the figures.
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