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First published online February 3, 2006; 10.1104/pp.105.073080 Plant Physiology 140:998-1008 (2006) © 2006 American Society of Plant Biologists Point Mutations with Positive Selection Were a Major Force during the Evolution of a Receptor-Kinase Resistance Gene Family of Rice1,[W]National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan 430070, China
The rice (Oryza sativa) Xa26 gene, which confers resistance to bacterial blight disease and encodes a leucine-rich repeat (LRR) receptor kinase, resides at a locus clustered with tandem homologous genes. To investigate the evolution of this family, four haplotypes from the two subspecies of rice, indica and japonica, were analyzed. Comparative sequence analysis of 34 genes of 10 types of paralogs of the family revealed haplotype polymorphisms and pronounced paralog diversity. The orthologs in different haplotypes were more similar than the paralogs in the same haplotype. At least five types of paralogs were formed before the separation of indica and japonica subspecies. Only 7% of amino acid sites were detected to be under positive selection, which occurred in the extracytoplasmic domain. Approximately 74% of the positively selected sites were solvent-exposed amino acid residues of the LRR domain that have been proposed to be involved in pathogen recognition, and 73% of the hypervariable sites detected in the LRR domain were subject to positive selection. The family is formed by tandem duplication followed by diversification through recombination, deletion, and point mutation. Most variation among genes in the family is caused by point mutations and positive selection.
Plants are constantly being subjected to pathogen attack and depend on the presence of specific genetic systems against the rapid evolution of pathogens. More than 40 resistance (R) genes against various plant diseases caused by bacteria, fungi, viruses, and nematodes have been characterized, providing insight into their function and evolution (Martin et al., 2003  ). The most prevalent domain encoded by functionally defined R genes is the Leu-rich repeat (LRR), which is considered to contribute to specificity in pathogen recognition (Dangl and Jones, 2001). Three classes of R genes encode proteins with an LRR domain (Hammond-Kosack and Parker, 2003). The largest class encodes intracellular nucleotide-binding site (NBS)-LRR proteins. The next largest class of LRR-containing R genes encodes extracellular LRR (eLRR)-transmembrane (TM) proteins. The third class encodes eLRR-TM-kinase or LRR receptor-kinase proteins. Only three genes—two, Xa21 and Xa26, from rice (Oryza sativa) and one, FLS2, from Arabidopsis (Arabidopsis thaliana)—have been identified as belonging to the third class (Song et al., 1995; Gomez-Gomez and Boller, 2000; Sun et al., 2004).
Increasing evidence indicates that R genes tend to be clustered in the genome (for review, see Michelmore and Meyers, 1998
R-gene polymorphism is a significant source of resistance-specificity diversity. The tandem repeated homologous members (or paralogs) of a haplotype and their alleles (or orthologs) in different haplotypes provide a structural reservoir for evolutionary forces to generate rapid variation in resistance specificity in a plant species (Michelmore and Meyers, 1998
The Xa26 gene, which confers resistance to Xanthomonas oryzae pv oryzae, the cause of bacterial blight disease, belongs to a multigene family that is clustered in the long arm of rice chromosome 11 (Yang et al., 2003 In this study, we analyzed the Xa26 family in four rice haplotypes from three indica varieties—Minghui 63, which carries the Xa26 gene; Teqing, which carries another bacterial blight R gene, Xa4; and 93-11, which carries at least one uncharacterized bacterial blight R gene—and one japonica variety, Nipponbare. Comparative sequence analysis of this genomic region from the four varieties revealed that haplotype polymorphism occurs in numbers, order of arrangement, and the level of diversity among the paralogs. The orthologs are more similar than the paralogs, which indicates a birth-and-death model of evolution. Positive selection on point mutation for diversification is also observed in limited amino acid sites located on the extracellular domain of the encoding products of the Xa26 family.
Organization of the Xa26 Gene Family in Four Rice Varieties
A bacterial artificial chromosome (BAC) clone, 3H8, from indica rice variety Minghui 63, carries the Xa26 gene (Sun et al., 2004
A BAC clone 26N11 from another indica variety Teqing carrying the Xa4 gene, which confers resistance to bacterial blight disease, was identified using the sequence of the Xa26 family of Minghui 63 as a probe. Sequence analysis of approximately 120 kb of 26N11 identified 10 genes in one family that showed sequence homology with the Xa26 family members and were distributed in tandem in a more than 90-kb region. Four members were alleles of MRKa, Xa26, MRKc, and MRKd in Minghui 63, respectively, according to their sequence similarity and corresponding locations in the family, and thus were named TRKa, TRKb, TRKc, and TRKd. The other six members were designated as TRKe, TRKf, TRKg, TRKh, TRKi, and TRKj (Fig. 1). Four of these, TRKa, TRKb, TRKc, and TRKe, were intact genes and had structures similar to those of MRKa, Xa26, and MRKc (Supplemental Fig. 1). The other six were either truncated or pseudogenes. TRKf, TRKh, TRKi, and TRKj were truncated in the kinase domain, LRR domain, or the region between the LRR and kinase domains (using the paralogs TRKa, TRKb, TRKc, and TRKe as the reference; Supplemental Fig. 1). TRKd, TRKf, TRKg, TRKh, and TRKi each carried one or two in-frame stop codons, and TRKi also contained one frame-shift site. In addition, the predicted coding regions of TRKd, TRKf, and TRKh each were interrupted by an insert of 3,954, 580, and 167 bp, respectively. The predicted coding regions of TRKa, TRKb, TRKc, TRKd, TRKe, TRKf, and TRKg shared 63% to 80% nucleotide sequence identity. The coding regions of the three heavily truncated paralogs, TRKh, TRKi, and TRKj, also showed sequence similarity with other paralogs of this family in their corresponding regions. A BLAST search of the genomic sequences of indica variety 93-11 (http://www.genomics.org.cn), using the sequences of the Xa26 family from Teqing, identified five long homologous sequences: AAAA02033155, AAAA02033250, AAAA02033253, AAAA02032784, and AAAA02033267. Analysis of the homologous sequences of the Xa26 family from 93-11 identified eight putative genes in one family. These eight genes in 93-11 showed high degree of sequence similarity respective to TRKa, TRKb, TRKc, TRKd, TRKe, TRKf, TRKg, and TRKh; they were designated 9RKa, 9RKb, 9RKc, 9RKd, 9RKe, 9RKf, 9RKg, and 9RKh. The eight paralogs of 93-11 were arranged in the same way as their orthologs in Teqing in terms of their linear order of distribution in the family and the transcription orientations, and they covered a region of more than 83 kb (Fig. 1). In addition, most of the intergenic regions of the Xa26 family also shared 99% to 100% sequence identity between 93-11 and Teqing (Fig. 1). The sequences of all the members in 93-11, except 9RKc and 9RKg, were identical to that of their orthologs in Teqing. 9RKg shared 99.7% sequence identity with TRKg. The intactness of 9RKc could not be determined because of the unfinished sequencing of the 93-11 genome in this region; however, 9RKc showed 100% sequence identity to the corresponding region of TRKc in Teqing. 9RKa, 9RKb, and 9RKe were predicted to be intact genes (Supplemental Fig. 1). The other four members, 9RKd, 9RKf, 9RKg, and 9RKh, were pseudogenes, each with an in-frame stop codon, a frame-shift site, and/or an insert or truncation (Supplemental Fig. 1). The predicted coding regions of the untruncated paralogs in 93-11 shared 63% to 80% nucleotide sequence identity among themselves. Two overlapping sequences, AC146937 and AC116367 harboring the Xa26 family, were identified from the finishing genomic sequences of the japonica variety Nipponbare by BLAST analysis, using the Xa26 family sequences from the other three varieties described above as queries. The Xa26 family in Nipponbare covered a region of approximately 230 kb and consisted of 12 paralogs that were named NRKa1, NRKa2, NRKb1, NRKb2, NRKc1, NRKc2, NRKd1, NRKd2, NRKe, NRKf1, NRKf2, and NRKf3 on the basis of sequence similarity to their orthologs, a, b, c, d, e, and f of the other three varieties (Fig. 1). NRKa2, NRKe, NRKf1, and NRKf3 were predicted to be intact genes, whereas the other eight members—NRKa1, NRKb1, NRKb2, NRKc1, NRKc2, NRKd1, NRKd2, and NRKf2—were pseudogenes with an in-frame stop codon, a frame-shift site, and/or an insert or truncation (Supplemental Fig. 1). The predicted coding regions of the 12 paralogs shared 61% to 98% sequence identity with each other. Compared with the organization of the Xa26 family in the other three varieties, it was easy to recognize that the 12 paralogs of Nipponbare could be divided into two clusters according to their physical location. NRKa1, NRKb1, NRKd1, NRKe, and NRKf1 were in cluster 1, and NRKa2, NRKb2, NRKc1, NRKc2, NRKd2, NRKf2, and NRKf3 were in cluster 2. Although most of the intergenic regions of the Xa26 family shared very high degree of sequence identity between Teqing and 93-11, the corresponding intergenic regions between Minghui 63 and Nipponbare, as well as between Minghui 63 or Nipponbare and Teqing or 93-11, generally had very low sequence similarity. However, some intergenic regions with more than 95% sequence identity were identified among the Xa26 family of Teqing or 93-11 and cluster 1 of Nipponbare (Fig. 1), which indicates that cluster 1 could be generated by a tandem duplication through an unequal crossover between indica and japonica subspecies in recent cross-breeding.
Analysis of the sequences showed that all the members of the Xa26 family in the four rice varieties were composed of two exons and one short intron located in the kinase domain (Supplemental Fig. 1). Comparative sequence analyses of the predicted coding regions and deduced proteins of the paralogs in each variety revealed pronounced divergence in rice lines 93-11, Teqing, and Minghui 63 (Fig. 2 ). Most of the paralogous comparisons in Nipponbare also showed pronounced divergence, but a few showed limited sequence variance. Comparison of the nucleotide-site difference and amino acid-site difference among orthologs showed that the average divergences within each ortholog comparison of a, b, c, and d were much lower than that within each paralog comparison (Fig. 2). In addition, the orthologs within the b and d groups had lower rates of sequence divergence than orthologs within the a and c groups.
Phylogenetic analysis classified the Xa26 family members into two groups by either the coding regions or introns (Fig. 3 ). Group I consisted of the members of a, b, d, and e, whereas group II was composed of the members of c, f, g, h, and j. TRKi in variety Teqing was excluded from the analysis because none of its domains was intact (Supplemental Fig. 1). It is worth noting that all the members in the same phylogenetic group had adjacent locations and the same transcription orientation in three indica varieties and cluster 1 of the japonica variety Nipponbare (Fig. 1). However, the family members of the same phylogenetic group in cluster 2 of Nipponbare had different transcription orientations and locations. The difference between cluster 2 of Nipponbare and the indica varieties was caused by two changes: (1) the relative positions of NRKb2 and NRKf2, and (2) the transcription orientation of NRKb2, NRKf2, and NRKf3 (Fig. 1). Two 465-bp regions located near NRKb2 of Nipponbare and TRKb of Teqing shared 94% sequence identity with each other, which suggests that an inversion event of a fragment carrying NRKb2 and NRKf2 might have occurred in Nipponbare during its evolution (Fig. 1). There was a 12% nucleotide difference between NRKc1 and NRKc2 and an 18% difference between NRKf2 and NRKf3, which demonstrated low sequence divergences among the pairwise-paralog comparisons of the Xa26 family members in Nipponbare (Fig. 2). Thus, NRKf3 and NRKc2 could be generated through tandem duplication of the fragment carrying NRKf2, NRKb2, and NRKc1, followed by a deletion of NRKb2 in the duplicated fragment and subsequent modifications of the original and duplicated members during the course of evolution (Fig. 1).
The phylogenetic analysis also showed that the orthologs of the Xa26 family frequently formed a monophyletic cluster with high bootstrap values in the phylogenetic trees (Fig. 3). In general, the orthologs of the family were more similar to each other than to the paralogs, not only among the three indica varieties but also between indica and japonica varieties.
Comparative sequence analysis of the family members in the four rice varieties showed that some family members were generated by intralocus (between orthologs) or interlocus (between paralogs) genetic exchange. Unequal crossovers resulted in duplication or deletion of some members in different rice varieties. The members of the Xa26 family in Nipponbare were divided into two clusters. Only cluster 1 shows high degree of sequence similarity in the intergenic regions flanking the a, b, d, and e orthologs with that in Teqing and 93-11 (Fig. 1), suggesting that the cluster 1 may have been generated by unequal crossover between the progenitors of Teqing or 93-11 and Nipponbare. Cluster 2 of Nipponbare may represent the original japonica Xa26 family because the divergence time between indica and japonica rice should be reflected by these differences between the intergenic regions of the Xa26 family members. Both TRKf and 9RKf had a truncated 3' exon, which could have resulted from an unequal crossover before the divergence of the two rice varieties. This unequal recombination most likely occurred through an intralocus exchange, given that orthologs of the Xa26 family were more similar to each other than to the paralogs. The large truncation of TRKh, TRKi, and 9RKh may also have been the result of unequal crossovers (Fig. 1; Supplemental Fig. 1). A 3.6-kb region including part of TRKg and its 3' flanking region showed 99% sequence identity to TRKj and its 3' flanking region, which indicates that an interlocus unequal crossover generated TRKj (Fig. 1). Among the orthologs of the Xa26 family in the four rice varieties, the members of the a group showed the greatest sequence divergence (Fig. 2). NRKa2 of Nipponbare had an approximately 14% nucleotide difference from NRKa1, MRKa, TRKa, or 9RKa, whereas nucleotide differences among NRKa1, MRKa, TRKa, and 9RKa were less than 1.6%. The pronounced difference between NRKa2 and the other four a members occurred mainly in the LRR region (Fig. 3). The nucleotide differences in the kinase domain among the five a members were less than 2.3%, but the differences in the LRR domain between NRKa2 and the other four a members—NRKa1, MRKa, TRKa, and 9RKa—ranged from 19.7% to 19.9%. These results imply that the LRR region of NRKa2 might have been formed by a crossover with a paralog or another gene that does not belong to the Xa26 family. The Geneconv program was used to determine gene conversion tracts among the coding sequences of all genes in the Xa26 gene family. A total of 70 significant gene-conversion events were detected (Supplemental Fig. 2). The gene-conversion fragments ranged from 25 to 1,999 bp, and about one-third of the fragments were less than 100 bp. Most of the gene conversions were found in the kinase domain, and only 12 were detected in the LRR domain, which included three gene-conversion events spanning the LRR domain and the region between the LRR and kinase domains. This result implies that gene conversion may not be the major evolutionary force for the diversification of the LRR domain of the Xa26 family.
The LRR domain of R proteins of plants is suggested to interact directly or indirectly with pathogen elicitors to determine race specificity. All the members of the Xa26 family in the four rice varieties, except those with a truncation in the LRR region, were predicted to encode 26 LRR repeats. The LRR consensus sequence consisted of 24 amino acids with a characteristic structure of LxxLxxLxxLxLxxNxLxGxIPxx (or xxLxLxxNxLxGxIPxxLxxLxxL). The xxLxLxx motifs in the LRRs are predicted to form a solvent-exposed parallel
The number of alternate amino acid residues at a given site was further examined by alignment of deduced amino acid sequences of the Xa26 family members in the four rice varieties using the ClustalX program. The alignment results showed that all the regions of these LRR receptor-kinase proteins of the family contained variable amino acid sites (Supplemental Table I). However, the xx(L)x(L)xx motif was more variable than other regions. All of the 45 hypervariable sites (Parniske et al., 1997
Identification of Amino Acid Sites under Positive Selection
The whole coding regions of the Xa26 family members, except those encoding the signal peptide (corresponding to the amino acid residues from N terminal to the Ala at position 33 of XA26) and the COOH end (corresponding to the amino acid residues from Ile at position 1,086 to C terminal of XA26), were tested for positive selection at individual amino acid sites. Two likelihood ratio (LR) tests were applied. The first LR test compared M3, the free-ratio model that assumes independent
The second LR test, a more specific test that examined variation in For comparison, the positive-selection sites of other R-gene families, the rice Xa21 family and the tomato Cf-4/9 family, which all encode extracytoplasmic LRR domains, were also analyzed using the same two LR tests (Supplemental Table II). Eight sites were potentially under positive selection in the LRR domain of the Xa21 family, and six of these eight were solvent-exposed amino acid sites (Supplemental Fig. 3). Fifty-two of 68 sites that were potentially under positive selection were located in the LRR domain of the Cf-4/9 family (Supplemental Fig. 3). Approximately 62% (32) of sites under positive selection in the LRR domain were solvent-exposed amino acid residues. Approximately 24% (16) of the positive-selection sites were discovered outside the LRR region in the Cf-4/9 family. Among the 24% sites, one was in the signal peptide; 10, most of which had posterior probability >0.95, were clustered in the region between the signal peptide and the LRR domain; and five were in the C-terminal region of the proteins (Supplemental Table II).
The Xa26 Family Has Extensive Paralog Diversity
Several R-gene families encoding the extracytoplasmic LRR domain show a high degree paralog similarity (Parniske et al., 1997 This study identified a high degree of nucleotide sequence divergence between paralogs in all four rice haplotypes (Fig. 2). Like the Xa21 family, the paralogs of the Xa26 family in each rice variety were also classified into two groups. However, the sequences of paralogs were highly divergent, even in the same group. The average nucleotide sequence identities of paralogs were 77.9%, 80.3%, 79.0%, and 79.6% for phylogenetic group I in Minghui 63, Nipponbare, Teqing, and 93-11, and 73.3%, 67.2%, and 67.8% for phylogenetic group II in Nipponbare, Teqing, and 93-11 (the heavily truncated members TRKh, TRKi, TRKj, and 9RKh were excluded), respectively. The average nucleotide sequence identities between the two phylogenetic groups were even lower—64.5%, 63.2%, 64.0%, and 64.2% in Minghui 63, Nipponbare, Teqing, and 93-11, respectively. Duplication and the subsequent divergence of a progenitor have been suggested to be a way to form a multigene family with clustered homologous members. Thus, the degree of intraspecific sequence variation of a gene family should represent the relative age, the mutation rate, or the level of unequal recombination (or gene conversion) of a family. Since the LRR domain was highly variable compared with the kinase domain and most of the gene-conversion events detected were in the kinase domain of the Xa26 family, the extensive paralog diversity of the family may suggest that it is an evolutionary old family and/or it has been subject to a higher rate of mutation and a lower level of unequal recombination or gene conversion in the LRR domain.
Evidence for positive evolution has been identified in the xx(L)x(L)xx motif of the LRR domain in some R-gene families by use of the average
Analysis of the rice Xa21 family and tomato Cf-4/9 family also revealed that only a small number of amino acid sites, most of which were solvent-exposed amino acid residues, were under positive selection (Supplemental Table II). However, positively selected sites were also observed in the region between the signal peptide and the LRR domain in both the Xa26 family and the Cf-4/9 family. Domain-swap or recombination studies revealed that pathogen resistance specificity was affected by the Toll/interleukin-1 receptor homology region in flax (Linum usitatissimum) L6 protein and by the determinants residing in the region between the signal peptide and the LRR domain in the tomato Cf-4 protein (Ellis et al., 1999
It has been suggested that a multigene family would be subject to evolution by a birth-and-death mechanism in which the genes in a family are formed first by duplication, followed by diversification, deletion, or dysfunction of the original genes (Nei et al., 1997
The specificity of R genes may be generated by several mechanisms, such as unequal crossover, gene conversion, intergenic recombination, and gene mutations, but there is still controversy about the major mechanism. Michelmore and Meyers (1998) The solvent-exposed residues of the LRR domain are hypervariable in the Xa26 family. Such changes are more likely to have arisen from point mutations than from sequence exchanges. The cultivated rice is a self-pollination plant, and most of the genes in its genome are homozygous. Thus, there are a few chances to alter the gene composition through gene recombination. An inbreeding mating system will tend to favor the accumulation of structural variants and point mutations because they would rapidly become homozygous. This mechanism with positive selection would result in the accumulation of point mutations and the different physical organization of the gene family among rice varieties, as shown in the Xa26 gene family. The fact that most of the hypervariable sites in the LRR region of the Xa26 gene family are overlapping with the positively selected sites also supports this inference.
An inbreeding plant would tend to promote genetic instability in crosses with near relatives but repress recombination in more distant crosses. Outbreeding species, such as maize (Zea mays), may be more unstable as duplications would tend to be hemizygous, therefore promoting a variety of pairing possibilities (Michelmore and Meyers, 1998 Although recombination easily causes the loss of resistance, this mechanism could be used to generate novel R genes. The clustered R-gene family members provide a continually horizontal sequence reservoir for generating novel recognition specificity. Crossing with different rice varieties and providing more chances for intergenic recombination could promote the generation of new R genes for different pathogens. In addition, because the cultivated rice infrequently cross-pollinates and wild rice (Zizania palustris) occurs more frequently than cultivar, the cross-breeding strategy between cultivated rice and wild rice for rice improvement has been used widely during recent years.
The sequences from four haplotypes provide clear evidence to propose a model for the evolution of the Xa26 family. Duplication of a progenitor gene through an event, which perhaps involves aberrant behavior of the DNA replication fork, as proposed by Noël et al. (1999)
Compared with the Xa21 and Cf4/9 gene families, the Xa26 family exhibits much higher divergence among paralogs and different physical structure among haplotypes. Phylogenetic analysis indicates that the Xa26 gene family clearly experienced evolution by a birth-and-death process. Most positively selected sites locate on the solvent-exposed residues in the LRR region and are overlapping with the hypervariable sites. These results suggest that the majority of changes in the diversity of Xa26 family members were caused by accumulation of mutations with positive selection. Recombination between orthologs or paralogs and unequal crossover were observed, but these contribute less to the generation of novel variation in the Xa26 gene family. The Xa26 family would tend to promote instability in crosses with near relatives, which could be used to generate the novel resistance specificity in this complex R locus.
Materials
A BAC clone, 3H8, from rice variety Minghui 63 (Oryza sativa subsp. indica) carrying the Xa26 gene (Sun et al., 2004
The nucleotide sequences of rice BAC clones were determined using a shotgun approach. A partial digestion of the BAC clones with the restriction enzyme Sau3AI was also used to construct bigger fragment subclones of the BAC clones. The M13 universal forward and reverse primers were used for sequencing. The sequences were assembled using the computer program Sequencher 4.1.2 (Gene Codes).
The similarity analyses of DNA and protein sequences were performed using BLAST programs, including BLASTN, BLASTX, and BLASTP (Altschul et al., 1997
The deduced amino acid sequences of the Xa26 family members were first aligned using the ClustalX program. The amino acid alignment was then used to guide the alignment of nucleotide sequences of the family using the protal2dna program (http://bioweb.pasteur.fr/seqanal/interfaces/protal2dna.html). The codon-based models implemented in the maximum-likelihood method were applied to infer amino acid sites under positive selection by estimating the ratio Sequence data from this article can be found in the EMBL/GenBank data libraries under accession numbers DQ355952 to DQ355956. Received October 18, 2005; returned for revision January 10, 2006; accepted January 23, 2006.
1 This work was supported by grants from the National Program on the development of Basic Research in China and the National Natural Science Foundation of China.  The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Shiping Wang (swang{at}mail.hzau.edu.cn).
[W] The online version of this article contains Web-only data. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.073080. * Corresponding author; e-mail swang{at}mail.hzau.edu.cn; fax 86–27–87287092.
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TOP
ABSTRACT
RESULTS
-sheet. The conserved Leu (L) project into the hydrophobic core, whereas the five interstitial residues (x) form a solvent-exposed surface that is involved in ligand binding (Kobe and Deisenhofer, 1995
(the ratio of nonsynonymous nucleotide substitution [dN] to synonymous nucleotide substitution [dS], dN:dS) values for every branch of the phylogeny, versus M0, the null one-ratio model that constrains 
sawyer/geneconv
0.05. 
