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Plant Physiology 138:611-623 (2005) © 2005 American Society of Plant Biologists Phylogenomic Analysis of the Receptor-Like Proteins of Rice and Arabidopsis1,[w]Department of Molecular and Cell Biology (L.K.F.-L.) and Department of Bioengineering (N.K., K.V.S.), University of California, Berkeley, California 94720; Warwick HRI, University of Warwick, Wellesbourne, Warwick CV35 9EF, United Kingdom (M.T.); and Sainsbury Laboratory, Norwich NR4 7UH, United Kingdom (J.D.G.J.)
The tomato (Lycopersicon esculentum) Cf-9 resistance gene encodes the first characterized member of the plant receptor-like protein (RLP) family. Other RLPs such as CLAVATA2 and TOO MANY MOUTHS are known to regulate development. The domain structure of RLPs consists of extracellular leucine-rich repeats, a transmembrane helix, and a short cytoplasmic region. Here, we identify 90 RLPs in rice (Oryza sativa) and compare them with functionally characterized RLPs from different plant species and with 56 Arabidopsis (Arabidopsis thaliana) RLPs, including the downy mildew resistance protein RPP27. Many RLPs cluster into four distinct superclades, three of which include RLPs known to be involved in plant defense. Sequence comparisons reveal diagnostic amino acid residues that may specify different molecular functions in different RLP subtypes. This analysis of rice RLPs thus identified at least 73 candidate resistance genes and four genes potentially involved in development. Due to the synteny between rice and other Gramineae, this analysis should provide valuable tools for experimental studies in rice and other cereals.
Diverse pathogens cause plant disease, and plants have evolved a variety of defense mechanisms. Many plant resistance genes (R-genes) have been cloned and characterized (Dangl and Jones, 2001  ). A common structural unit in many R proteins is the Leu-rich repeat (LRR). LRRs are found throughout the tree of life and are thought to mediate protein-protein interactions (Kobe and Kajava, 2001). LRR-containing plant proteins have diverse overall structures and functions, including disease resistance (Jones and Jones, 1997). A 23- to 25-amino acid plant-specific extracellular LRR motif contains a conserved consensus sequence, LxxLxxLxLxxNxLt/sgxIpxxLG (Jones and Jones, 1997).
Several classes of plant proteins involved in defense signaling contain extracellular LRR-containing receptor-like proteins (RLPs), receptor-like kinases (RLKs), and polygalacturonase inhibiting proteins (PGIPs; Fig. 1). The first RLP identified was Cf-9 (Jones et al., 1994
RLPs are known to be involved both in defense and development. Characterized RLP genes involved in resistance include the Cf genes from tomato (Lycopersicon esculentum) that confer resistance against the fungal pathogen Cladosporium fulvum (Jones et al., 1994 ; Dixon et al., 1996, 1998; Thomas et al., 1997), tomato Ve genes (Kawchuk et al., 2001), apple (Malus domestica) HcrVf2 (Vinatzer et al., 2001), Arabidopsis (Arabidopsis thaliana) RPP27 (Tör et al., 2004), and tomato LeEIX1 and LeEIX2 (Ron and Avni, 2004). Developmental RLPs in Arabidopsis include TMM (Yang and Sack, 1995; Nadeau and Sack, 2002), which is involved in stomatal patterning, and CLAVATA2 (CLV2; Jeong et al., 1999) and its maize (Zea mays) ortholog FASCIATED EAR2 (FEA2; Taguchi-Shiobara et al., 2001), which are involved in meristem development.
The RLKs are a large gene family in plants involved in signaling (Shiu et al., 2004
PGIPs are another group of plant proteins related to RLPs and RLKs. PGIPs are cell wall proteins that bind and inhibit polygalacturonases, cell wall-degrading enzymes thought to aid fungal penetration into host tissues (Albersheim and Anderson, 1971
Genes involved in development tend to have certain characteristics differentiating them from R-genes. R-genes are often found in multiple copies at genomic loci and are under strong diversifying selection, producing highly divergent sequences and structural variants with distinct recognition capacities (Bai et al., 2002
In earlier work, we described 58 RLPs in Arabidopsis (Tör et al., 2004
Identification and Genomic Organization of Rice RLPs
Since LRRs are often found in proteins with non-Cf-RLP folds, sequence-based methods of homolog detection can inadvertently include many non-Cf-RLPs in database searches. To discriminate canonical Cf-RLPs (referred to here as RLPs for simplicity) from proteins with different overall folds, we employed an intentionally stringent approach designed to include only those proteins sharing the canonical Cf-9-like RLP structure (described in "Materials and Methods"). This produced a set of 90 sequences in rice. For comparison, Cf-RLPs from other organisms as well as characterized RLK and PGIP sequences were identified using literature search and included in these analyses. A complete list of all Arabidopsis and rice RLP sequences, along with Cf-RLPs from other organisms and RLK and PGIP sequences, is available (Supplemental Table I). The rice sequences mapped to large clusters of genes on chromosomes 1, 2, 11, and 12, with smaller clusters and singletons scattered throughout the genome (Fig. 2). The rice genome has 38 loci containing RLPs, while Arabidopsis has 33 such loci. Thus, rice and Arabidopsis contain a similar number of RLP loci, yet rice has almost twice the number of genes predicted to encode RLPs. Furthermore, rice has an average of six RLPs at each locus containing more than one RLP, compared to 2.6 in Arabidopsis. This supports a hypothesis of recent tandem duplication contributing to the enlargement of the RLP family in rice. A similar conclusion was reached following analysis of the nucleotide-binding-LRR class of R-genes in rice (Bai et al., 2002
Classification into Global Homology Groups
The Cf-RLPs of rice and Arabidopsis exhibit great variation in sequence and in the number of LRRs, making identification of the Cf-9-like domains difficult. To compensate for this, we clustered the full-length sequences into globally alignable subgroups (global homology groups, or GHGs), requiring all sequences in a GHG to have a length difference of no more than 15% and to share
Cf-RLPs of Rice and Arabidopsis Fall into Four Major Distinct Superclades Although Cf-RLPs have low overall sequence similarity, domains C3 through F (the TM helix) are well conserved; we chose this region (C3-F) as the basis for phylogenetic tree construction (Fig. 4A). Phylogenetic analysis using several methods supports a set of 16 conserved clades (Fig. 4B; Table I). We defined clades as subtrees containing at least two sequences, greater than 60% bootstrap support, and no less than 50% average sequence identity. Of the 182 sequences in the tree, 123 are found in the 16 clades; we termed the remaining 59 phylogenetic singletons. Most clades segregate rice and Arabidopsis sequences, except for clades 12, 13, 14, and 15, which contain proteins from both species. Interestingly, among all the LRR-RLKs included in this analysis, only the carrot (Daucus carota) phytosulfokine receptor kinase (PSKR) groups with rice and Arabidopsis RLPs in clade 13. This is the only functionally characterized RLK that clusters with RLPs in our analyses.
A coarser cut of the C3-F-region-based phylogenetic tree produced a higher-order classification, identifying four distinct superclades of RLPs with an average identity of at least 48% within the C3-F region (Fig. 4B; Table II). Eighty-three of the 90 rice RLPs and 47 of 56 Arabidopsis RLPs belong to a superclade. Each of these superclades contains at least one functionally characterized member, allowing us to infer possible functions for the proteins in each superclade. Although the phylogenetic tree is based on the C3-F region alone, the superclades defined by this tree correlate very well with phylogenetic distribution and genomic clusters and with domain architecture defined by the GHGs.
The Cf-9 superclade contains proteins from clades one through eight, including 24 rice and 35 Arabidopsis sequences and tomato Ve1 and homologs. While most superclades correspond to a single GHG, this superclade spans several GHGs due to variable numbers of LRRs in the C1 region. This is consistent with the observed variability of Cf-9 and Cf-2 homologs in the number of LRRs (Thomas et al., 1997 ; Dixon et al., 1998). The rice sequences in the Cf-9 superclade map to large genomic clusters on rice chromosomes 1 and 12. The RPP27 superclade consists of sequences from clade 12 along with seven phylogenetic singletons from Arabidopsis and nine from rice. All sequences from the GHG H and the genomic cluster on rice chromosome 4 are represented in this class. The LeEIX superclade contains HcrVf proteins and also includes clades 9 and 16, as well as six phylogenetic singletons from rice and no Arabidopsis sequences. This superclade includes sequences from the GHG D and the rice genomic cluster on chromosome 11. The PSKR superclade consists of clade 13, including the carrot RLK PSKR and two phylogenetic singletons from Arabidopsis and 16 from rice. This superclade corresponds to GHG B, as well as the rice genomic cluster on chromosome 2.
As discussed earlier, developmental genes are less likely to be duplicated than R-genes, and are also more structurally and functionally conserved between distant species. Using these guidelines, we identified putative developmental orthologs (PDOs) between rice (OsPDO) and Arabidopsis (AtPDO). Candidate ortholog pairs were required to meet the following criteria: (1) global alignability (found in the same GHG), (2) support from bidirectional BLAST (i.e. each is the other's top-scoring hit in BLAST search of its genome), (3) placement in the same phylogenetic clade, (4) singleton at a genomic locus, and (5) significant sequence identity (at least two SDs above the mean pairwise identity between rice and Arabidopsis Cf-RLPs). The first three criteria serve to ensure the two sequences are orthologous; the last two support a putative role in development. Only four rice RLPs (OsPDO1–OsPDO4) satisfied these stringent criteria. OsPDO1 has approximately 60% sequence identity with its Arabidopsis ortholog AtPDO1 (At4g18760.1). OsPDO2 has approximately 45% sequence identity with AtPDO2 (At1g28340.1). Putative orthologs in other plant species are identifiable for both OsPDO1 and OsPDO2 in expressed sequence tag (EST) databases (Fig. 5) with an average of 70% and 55% identity with their top-scoring matches, respectively. In addition to the significant sequence conservation supporting a role in development for these proteins, EST data for PDO2 in other species reveal a consistent pattern of expression in seed-developing organs.
OsPDO3 and OsPDO4 are rice orthologs of CLV2 and TMM, respectively, with 45% and 48% identity. OsPDO3 also has 83% identity with the maize protein FEA2, which has a similar mutant phenotype to CLV2 (Taguchi-Shiobara et al., 2001 ). Finally, two Arabidopsis genes, At5g65830 and At3g49750, are closely related to each other and to three rice genes, and might represent an additional class involved in development. Interestingly, both of these Arabidopsis genes show increased expression in embryonic tissues, according to GENEVESTIGATOR, a Web-based interface used to mine publicly available Arabidopsis Affymetrix GeneChip data (Zimmermann et al., 2004). Since rice and Arabidopsis diverged about 150 million years ago (Chaw et al., 2004), it is conceivable that some of the genomic singleton RLPs that are not members of the superclades, such as At2g42800 or rice 1950.m00149, may be involved in a developmental function that is only maintained in the dicot or monocot clade.
The clustering of sequences into global homology groups facilitated the identification of Cf-9-like domains and conserved motifs. Here, we describe conserved motifs in the Cf-RLPs that appear potentially important for maintaining the structure and/or function of these proteins.
The LRRs of Cf-9 are flanked by domains B and D, both of which contain conserved Cys. We found two structural variants in domain B of the Cf-RLPs. The first group has a single pair of conserved Cys and includes the RLPs known to be involved in development. The second group includes RLPs characterized in defense pathways (except Cf-2) and contains two pairs of conserved Cys. Sequence analysis suggests a homology between members of this second group and the amino-terminal 44 amino acids of PGIP (Protein Data Bank ID 1OGQA; average pairwise identity is 40% with very few gaps; Fig. 6A). The N terminus of the PGIP structure contains two pairs of conserved Cys, which form disulfide bridges capping its solenoid structure (Di Matteo et al., 2003
The variable C2 region connects the C1 LRRs with the more conserved C3 LRRs. Various models have been proposed for the structural role of the C2 domain. The first hypothesis is that C2 is a flexible hinge-like region, which enables the two surrounding LRR regions to articulate relative to each other (Jones and Jones, 1997 ). Alternately, the C2 region could form a loop between the two LRR domains, minimally affecting the structure of the LRR scaffold. A third possibility is that this region folds into the regular LRR structure, forming an unbroken solenoid shape, much like the structure of PGIP. In total, 73 rice RLPs were identified that contain a C2 region varying nonintegrally in length from 30 to 80 amino acids. The variability in the C2 region belies its potential functional role. For example, mutation of conserved Gly in the C2 region of the Arabidopsis RLK BRI1 results in loss of brassinosteroid perception (Dievart and Clark, 2003), and this region has recently been proven to bind brassinolide (Kinoshita et al., 2005). Recent work has investigated conserved Cys and Trp in Cf-9 domain B, and putative glycosylation sites throughout the protein, as well as providing a model for domains B-D of Cf-9 (Van der Hoorn et al., 2005). We also noted a novel conserved Yx(6-8)KG motif in the C2 region of 33 rice and 37 Arabidopsis RLPs (Fig. 6B); the function of this motif is unknown.
The GXXXG motif found in some TM regions has been shown to be involved in protein-protein interactions via intermolecular hydrogen bonds (Curran and Engelman, 2003
The cytoplasmic tails of Cf-RLPs vary in length from one to 215 amino acids. A small fraction (nine of the 56 Arabidopsis Cf-RLPs and 20 of the 90 rice sequences) contained the YXXØ motif (where Ø represents any bulky, hydrophobic amino acid), shown to be required for rapid movement of TM proteins to lysosomes and lysosome-related organelles (Bonifacino and Traub, 2003
RLPs have been found in diverse plant species and are known to be involved in both defense and developmental pathways. R-gene families often expand by gene duplication and are under diversifying selection (Leister, 2004 ). Cf-RLPs in rice have been grouped by genomic locus, phylogenetic analysis, and global domain structure to form 16 clades and four superclades. The 16 clades contain more than 80% of the rice and Arabidopsis Cf-RLP sequences, of which 12 contain members from only one organism. This is in agreement with the findings of Shiu et al. (2004) showing 2-fold greater expansion of R-gene copies in rice. Superclade analysis shows three of the four include RLPs known to be involved in disease resistance. Most of the rice sequences in these superclades are clustered at genomic loci, indicating evolution by tandem gene duplication. We conclude therefore that the majority of Cf-RLPs are involved in resistance rather than development.
The PSKR superclade is the only one that includes an RLK. PSKR is a receptor for the plant peptide hormone phytosulfokine (Matsubayashi et al., 2002 Our analysis identifies four putative developmental genes in rice, OsPDOs 1 to 4. Attempts to determine a specific functional role and/or tissue-specific expression pattern based on comparisons with ESTs have not been fruitful for OsPDO1. However, EST data for close homologs for OsPDO2 allow us to infer that OsPDO2 may be expressed during seed production. Of the nine Arabidopsis RLPs that are not part of a superclade, six have been discussed here: the AtPDOs and At5g65830 and At3g49750. It is possible that the remaining three (At4g04220, At5g45720, and At2g42800) are involved in Arabidopsis-specific developmental processes. Recent experimental investigation in functional characterization of Arabidopsis RLPs provides additional support for a developmental role for OsPDO1. To date, 20 homozygous T-DNA insertion lines have been obtained and challenged with a small range of microorganisms, including bacterial, oomycete, and fungal plant pathogens. Thus far, we have identified three RLPs involved in the defense response and one that has shown a developmental phenotype with slow growth, few leaf numbers, and late flowering (M. Tör, unpublished data). Interestingly, the gene for this mutant corresponds to AtPDO1 (At4g18760), supporting our inference that its rice ortholog, OsPDO1, may also play a role in development. Further characterization of this mutant is in progress.
Structural analyses of LRR proteins reveal a shared solenoid scaffold, with a
Our analyses of Cf-RLPs identified several motifs that may facilitate intramolecular and intermolecular interactions. In LRR proteins, the hydrophobic amino acids of the LRR are protected from solvent exposure by their flanking regions (Kobe and Kajava, 2001
The N-terminal LRRs (domain C1) of many RLPs and RLKs are separated from the membrane-proximal four LRRs (domain C3) by an "island" or "loop-out" region of 30 to 80 amino acid sequences, referred to as the C2 domain. This domain in BRI1 has now been shown to be involved in direct binding to brassinolide (Kinoshita et al., 2005
Another conserved motif likely to be involved in protein-protein interactions is found in the TM region. The TM GXXXG motif is known to aid dimerization and activation of ErbB2, a mammalian receptor kinase (Bennasroune et al., 2004
R-genes are known to be under diversifying selection to adapt to different pathogen challenges. Several gene families involved in defense response in plants, such as the nucleotide-binding-LRR proteins (Meyers et al., 2003 ), have been found in large genomic clusters, supporting a hypothesis of rapid evolution by tandem duplication and gene shuffling events. Our phylogenetic analysis identified four superclades of Cf-RLPs containing a majority of the rice and Arabidopsis Cf-RLPs (120 of the 146). All superclades contain sequences at multicopy tandem repeat-encoding loci, and three of the four also contain at least one functionally characterized R-gene. We hypothesize that the genes in these superclades are likely to function in disease resistance.
This analysis has identified 73 candidate R-genes in rice and at least four probable developmental genes for further experimental validation. Due to the close synteny between Gramineae (Paterson et al., 2003
Multiple Sequence Alignment
We used two methods for multiple sequence alignment. MUSCLE (Edgar, 2004
Hidden Markov models (HMMs) from the PFAM suite (http://pfam.wustl.edu) were used to identify the presence of LRRs and other structural domains. The TM prediction server TMHMM (version 2.0; Krogh et al., 2001
To identify rice (Oryza sativa) proteins sharing the canonical Cf-RLP structure, we required sequences from release 2 of the TIGR Pseudomolecules (Yuan et al., 2003
Unlike Arabidopsis, the genomic loci of rice proteins are not immediately available. To identify genomic locations of the rice RLPs, we used each sequence as a query in translated BLAST (Altschul et al., 1997
We clustered rice and Arabidopsis RLPs, RLKs, and PGIPs into globally alignable sequence clusters, which we call GHGs, using a combination of BLAST, HMM, and heuristic methods. To enable us to assume the same overall architecture for all members of a GHG, we required all sequences in a GHG to have a minimum of 30% pairwise identity and a bidirectional alignment coverage (i.e. the percentage of a sequence's amino acids that are aligned to the other sequences in the cluster) of at least 85%.
Phylogenetic trees were estimated using the conserved C3-F region as input. We used several programs in these analyses, including Neighbor-Joining and Parsimony from the PHYLIP software suite (http://evolution.genetics.washington.edu/phylip.html), Mr Bayes (Ronquist and Huelsenbeck, 2003
J.D.G.J. thanks Joe Ecker at the Salk Institute for kindly hosting a sabbatical visit, during which this project was initiated. Received October 5, 2004; returned for revision February 4, 2005; accepted March 23, 2005.
1 This work was supported in part by the National Science Foundation (PECASE Award DBI–0238311 to K.V.S.) and in part by the Gatsby Charitable Foundation (to J.D.G.J.). 
2 These authors contributed equally to the paper.
[w] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.104.054452. * Corresponding author; e-mail kimmen{at}berkeley.edu; fax 510–642–9932.
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TOP
ABSTRACT
RESULTS
30% sequence identity. Roughly 40% of Cf-RLPs from rice and Arabidopsis fell into nine GHGs containing three to 16 sequences (
-sheet forming the concave side and stacked helices forming the convex side (Kobe and Kajava, 2001
-helical region that caps the LRRs. A motif similar to the N terminus of PGIP was seen in several Cf-RLPs, including RLPs known to be involved in defense (the developmental RLPs and the RLKs contain only one pair of Cys). Mutation of one of the N-terminal Cys in the RLK BRI1 leads to a weak brassinosteroid response phenotype (Dievart and Clark, 2003
