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First published online May 21, 2004; 10.1104/pp.103.037770 Plant Physiology 135:1100-1112 (2004) © 2004 American Society of Plant Biologists Arabidopsis Downy Mildew Resistance Gene RPP27 Encodes a Receptor-Like Protein Similar to CLAVATA2 and Tomato Cf-91Horticulture Research International, Wellesbourne, Warwick CV35 9EF, United Kingdom (M.T., A.C., A.W.-T., E.B.H.); Department of Bioengineering, University of California, Berkeley, California 94720–1762 (D.B., K.S.); and Sainsbury Laboratory, Norwich Research Park, Colney, Norwich NR4 7UH, United Kingdom (J.D.G.J.)
The Arabidopsis Ler-RPP27 gene confers AtSgt1b-independent resistance to downy mildew (Peronospora parasitica) isolate Hiks1. The RPP27 locus was mapped to a four-bacterial artificial chromosome interval on chromosome 1 from genetic analysis of a cross between the enhanced susceptibility mutant Col-edm1 (Col-sgt1) and Landsberg erecta (Ler-0). A Cf-like candidate gene in this interval was PCR amplified from Ler-0 and transformed into mutant Col-rpp7.1 plants. Homozygous transgenic lines conferred resistance to Hiks1 and at least four Ler-0 avirulent/Columbia-0 (Col-0) virulent isolates of downy mildew pathogen. A full-length RPP27 cDNA was isolated, and analysis of the deduced amino acid sequences showed that the gene encodes a receptor-like protein (RLP) with a distinct domain structure, composed of a signal peptide followed by extracellular Leu-rich repeats, a membrane spanning region, and a short cytoplasmic carboxyl domain. RPP27 is the first RLP-encoding gene to be implicated in disease resistance in Arabidopsis, enabling the deployment of Arabidopsis techniques to investigate the mechanisms of RLP function. Homology searches of the Arabidopsis genome, using the RPP27, Cf-9, and Cf-2 protein sequences as a starting point, identify 59 RLPs, including the already known CLAVATA2 and TOO MANY MOUTHS genes. A combination of sequence and phylogenetic analysis of these predicted RLPs reveals conserved structural features of the family.
A wide range of parasites, including viruses, bacteria, fungi, nematodes, and insects, exploit plants as a source of food and shelter. Plants have evolved mechanisms to recognize the potential colonists and defend themselves. The defense is often activated by the direct or indirect interaction of the disease resistance (R) gene in the plant and the avirulence (Avr) gene in the pathogen (Dangl and Jones, 2001  ; Holub, 2001). The absence of either of these genes results in infection by the pathogen.
To date, numerous R genes have been cloned from a wide range of plant species, including Arabidopsis, flax (Linum usitatissimum), tomato (Lycopersicon esculentum), tobacco (Nicotiana tabacum), sugar beet (Beta vulgaris), apple (Malus domestica), rice (Oryza sativa), barley (Hordeum vulgare), and maize (Zea mays). Their structural and functional comparisons have been well documented, revealing several different classes (Hammond-Kosack and Jones, 1997
The second group contains the cytoplasmic Ser/Thr kinase and has been represented by PTO (Martin et al., 1993
The third group of R genes encodes the receptor-like kinases (RLKs). The characteristic features of these proteins are an extracellular LRR domain with a single transmembrane spanning region and a cytoplasmic kinase domain. This group contains the rice Xa21 gene (Song et al., 1995
Receptor-like proteins (RLPs) comprise the fourth group of R genes. These are similar to RLK genes in that they encode extracellular LRRs and a C-terminal membrane anchor but lack the cytoplasmic kinase domain. Members of this group include the tomato Cf-2, Cf-4, Cf-5, and Cf-9 genes conferring resistance to the fungal pathogen Cladosporium fulvum (Jones et al., 1994 To date, all cloned Arabidopsis R genes conferring resistance to the oomycete downy mildew pathogen belong to the NB-LRR class. Here, we describe the molecular cloning of the Arabidopsis RPP27 gene that confers resistance to several isolates of P. parasitica and encodes an RLP. The coding sequence of this gene predicts a protein with topological features similar to Arabidopsis CLAVATA2 (CLV2) and tomato Cf-9.
Identification and Isolation of the RPP27 Gene
RPP27 was previously identified as a gene in the accession Landsberg erecta (Ler-0) that functions independently of AtSGT1b and confers resistance to Peronospora isolate Hiks1. Generation of mapping material and segregation data from the cross between a 35-kb deletion mutant Col-sgt1b and Ler-0 were described previously (Tör et al., 2002
Transgenic Complementation of RPP27 Function
The wild-type Columbia-0 (Col-0) carries the RPP7 gene that recognizes the downy mildew isolate Hiks1 (Holub et al., 1994
Homozygous T3 families were then obtained from these transgenic lines and examined for their capacity to generate H2O2 24 h after inoculation with Hiks1 using 3,3'-diaminobenzidine (DAB). This compound captures H2O2 and forms a reddish brown polymer at sites of peroxidase activity (Thordal-Christensen et al., 1997
We examined the pathogen development and interaction phenotype in detail. Three days after inoculation, normal pathogen development was observed in the cotyledons of control nontransformed seedlings, and host cells appeared to be intact (Fig. 2C). However, less pathogen growth and trailing necrosis was observed in colonized areas of transgenic seedlings (Fig. 2D). Trailing necrosis was more extensive in transgenic seedlings 7 d after inoculation, and occasionally the pathogen produced conidiophores (Fig. 2E).
We extended the analysis to see whether RPP27 confers resistance to any isolate of downy mildew other than Hiks1. Col-0 compatible isolates but Ler-0incompatible isolates, including Aswa1, Edco1, Emco2, Emco5, Emwa2, Goco1, Gowa1, Maks9, Noco2, and Noks1, were used to inoculate homozygous transgenic lines along with controls, including wild-type resistant Ler-0, wild-type susceptible Col-0, and nontransgenic mutant Col-rpp7.1. Asexual sporulation was measured by quantifying sporangiophore production as described previously (Tör et al., 2002
Sequence Analysis of the RPP27 Gene and Transcript The construct MT27 that carries the Ler-0 genomic DNA fragment was sequenced using a primer walking strategy and shown to contain a 6,461-bp insert. This region has been annotated in the EMBL database in the original BAC clone as gene F20D21.29, encoding a protein of 818 amino acids similar to Cf-like genes in tomato. However, this region has been annotated in the Munich Information Center for Protein Sequences (MIPS) database as two genes, At1g54470 encoding an 112-amino acid hypothetical protein and At1g54480 encoding a 550-amino acid protein similar to disease resistance genes. Similarly, The Institute for Genomic Research (TIGR; Rockville) database showed two genes, At1g54470 encoding a 113-amino acid hypothetical protein and an At1g54480 encoding a 551-amino acid protein similar to the LRR protein family. Extensive database searches revealed no expressed sequence tags corresponding to the RPP27 genomic sequence. Since there were no ESTs for RPP27 and the MIPS and TIGR annotations of the region disagreed, we carried out several reverse transcription (RT)-PCR experiments with RNA isolated from Hiks1 infected and noninfected seedlings from Col-0 and Ler-0 to determine the expression level of RPP27. A very low level of expression of RPP27 was observed in tissues of both Col-0 and Ler-0 (data not shown). The 3' RACE from Ler-0 revealed a predicted stop codon, a 3' untranslated region of 102 bp, and a polyadenylation site. The 5' end of the transcript from Ler-0 indicated a single major transcription site 37 bp upstream of the predicted ATG. Based on the cDNA 5' RACE and 3' poly(A) site, the RPP27 transcript is found to be 3,274 bases long. Comparison of the genomic and the cDNA sequences allowed us to define six exons and five introns (Fig. 1D). When the RPP27 genomic sequence in the construct MT27 was compared with the corresponding region of Col-0 on the BAC clone F20D21, we observed 11 sites to be polymorphic. Of these 11 sites, six were single nucleotide polymorphisms and the other five were insertions/deletions (INDELs) (Table II). Six of these polymorphic sites were in the promoter region; three were in introns; one (a large deletion of 68 nucleotides in Col-0) was in the largest exon; and one came just after the 3' untranslated region. The large INDEL caused a frameshift in the largest exon resulting in a premature stop codon. These polymorphisms therefore have a significant effect on the predicted amino acid sequences of RPP27 protein from Col-0 accession and may also have played a role in the misannotation of the region described above.
Predicted RPP27 Protein Structure
The open reading frame of the RPP27 gene encodes a predicted protein of 1,044 amino acids (molecular mass of 116.9 kD) with structural similarity to other RLPs, including Arabidopsis CLV2 (Jeong et al., 1999
Domain C constitutes the majority of the predicted RPP27 protein and consists of 30 imperfect copies of extracellular LRRs with a consensus sequence of LxxLxxLxxLxLxxNxLSGxIPxx. This region has an island of variable and mostly hydrophobic sequences between positions 789F and 855D that matches similar regions in other RLPs; the exact structure of this region cannot be specified using sequence analysis methods. It is possible that this region provides a flexible hinge to the two flanking LRR domains (C1 and C3), allowing them to articulate relative to each other. Despite similarities between RPP27 and the product of Cf genes (particularly Cf-2 and Cf-9), there are two striking differences. First, relative to the tomato Cf proteins and the vast majority of other Arabidopsis RLPs, RPP27 has a highly divergent amino-terminal B domain, with an initial region of approximately 120 amino acids preceding a region of significant homology with Cf-2 and Cf-9.
Second, in contrast to all other plant RLPs identified thus far, which are predicted to have a single transmembrane domain at the C terminus, transmembrane prediction using the TMHMM server identifies two putative transmembrane (TM) domains in RPP27, one at the C terminus and one in the variable N-terminal domain (66G–88I). However, since transmembrane prediction algorithms are known to be misled by hydrophobic stretches (Chen et al., 2002
The consensus RLP fold consists of multiple LRRs, followed by a transmembrane domain and a short cytoplasmic tail. Because LRRs are often found in proteins with non-RLP folds, sequence-based methods of homolog detection can inadvertently include many non-RLPs in database searches. Similarly, transmembrane prediction tools can overpredict TM domains in hydrophobic stretches. To discriminate true RLPs from sequences with different overall folds, we employed a multistep analysis. First, we used RPP27, Cf-2, and Cf-9 as BLAST queries against Arabidopsis. We then scored Arabidopsis proteins with a hidden Markov model (HMM; Krogh et al., 1994 We then constructed a series of multiple sequence alignments for these 59 sequences, as well as for the tomato Cf-2 and Cf-9 proteins. These alignments were examined and the highest quality alignment selected. From this alignment, we constructed two separate alignments, one that was essentially global (removing columns with mostly gaps) and one restricted to theC-terminal conserved domains C3 to F (Fig. 4). Phylogenetic trees were estimated using parsimony, neighbor-joining, and maximum likelihood methods, with bootstrap analysis to identify subtrees with high bootstrap support. Tree topologies were examined and found to be fairly consistent both across methods and across the two alignments; most differences were restricted to the coarse branching order in the trees. A consensus tree topology was inferred using bootstrap analysis and the PHYLIP consense software (Fig. 5).
The Arabidopsis RLP family contains 59 genes, including RPP27, CLV2, TMM, and 56 previously unidentified family members. These are distributed throughout the genome as follows: 17 genes, including CLV2, TMM, and RPP27, on chromosome 1; 12 on chromosome 2; 16 on chromosome 3; 8 on chromosome 4; and 6 on chromosome 5. The distribution is similar to NB-LRR genes, with several complex loci containing 3 or more RLPs and others that are singlets or doublets (Fig. 6). Further details are available at http://phylogenomics.berkeley.edu/PlantResistanceGene/ArabRLPs.html.
The predicted polypeptide encoded by the RPP27 gene has structural features that indicate a receptor-like function. The signal peptide targeting the membrane at the amino terminus, the putative extracytoplasmic protein-protein interaction domain (LRR), the single transmembrane domain, and the short cytoplasmic tail present an overall structure of the large class of RLPs found in many species across the kingdom. To date, only two functional RLPs have been identified in Arabidopsis: CLV2 and TMM. CLV2 (Jeong et al., 1999 ) is involved in meristem and organ development and is required for the accumulation and stability of the receptor kinase CLV1 (Clark et al., 1997). TMM (Nadeau and Sack, 2002) is involved in stomatal and epidermal development. Functional RLPs that are involved in disease resistance have been described in other plant species, including the tomato Cf genes (Hammond-Kosack and Jones, 1997; Joosten and De Wit, 1999) for leaf mold resistance and the Ve genes for Verticullium resistance (Kawchuk et al., 2001). RPP27 provides the first example of an RLP in Arabidopsis that is associated with disease resistance. As discussed below, this discovery is particularly interesting because the pathogen downy mildew is an obligate biotrophic parasite that produces haustorial feeding structures in host cells. We have identified 59 RLPs in Arabidopsis using RPP27, Cf-9, and Cf-2. In a recent study, Shiu and Bleecker (2003) identified a superfamily of putative RLPs from the Arabidopsis genome. Their aim was to identify essentially all Arabidopsis proteins in Col-0 that share any recognizable sequence similarity with the extracellular portion of the RLKs. They used the extracellular domains of 35 representative RLKs to conduct BLAST searches of the Arabidopsis genome, with a cutoff value of 10 e–10. Shiu and Bleecker (2003) selected a final set of 173 proteins for cluster analysis, using the unweighted pair group method with arithmetic mean algorithm based on pairwise BLAST e-values, and produced a hierarchical tree shown in their paper. Examination of these clusters reveals a significant fraction of proteins that do not match the canonical RLP topology (transmembrane region and extracellular LRR). These proteins may well be related in some way to RLPs but are likely to have different functions. By contrast, our approach was deliberately conservative and designed to produce a set of proteins that matched the canonical RLP structure; we excluded any proteins containing structural domains not found in the RLPs and required a single transmembrane domain at the C terminus. Examination of the two sets of proteins shows that all but one of the proteins we identify as RLPs are also found by Shiu and Bleecker (2003). The exception, At1g58190, is clearly a member of the RLP class, which contains 49 LRRs, a transmembrane domain (identified by TMHMM), and a short cytoplasmic tail. Of the 117 proteins included by Shiu and Bleecker (2003) but not by us, all but four contain additional domains not found in RLPs (e.g. GDPD, B-Lectin, etc.) or are missing identifiable transmembrane segments at the C terminus. However, none of these four contain recognizable LRRs and therefore do not match the canonical RLP structure. Phylogenetic tree estimation of these RLPs (along with the tomato Cf genes) place RPP27, CLV2, TMM, Cf-2, and Cf-9 on the same branch of the evolutionary tree, suggesting that proteins involved in both disease resistance and development may have evolved from a common origin (Fig. 5). We expect that RPP27 is not the sole example of disease resistance among these RLPs in Arabidopsis. Putative T-DNA mutants inCol-0 background exist for at least 31 of these RLPs. Challenging these mutants with Col-avirulent isolates of bacterial and filamentous pathogens such as P. syringae and downy mildew, respectively, may yield more information on the involvement of these RLPs in disease resistance. The RPP27 protein has an overall topology consistent with the canonical RLP fold (Fig. 3): an amino-terminal signal peptide (M1-S20), followed by Leu-rich (Q21-S143) and LRR domains (I144-G946), an acidic region (D973-L997), a transmembrane domain (A998-F1020), and a short cytoplasmic tail (D1021-P1044). Analysis of the family of Arabidopsis RLPs reveals a conserved region of approximately 150 amino acids immediately preceding the transmembrane domain (Fig. 4). The number of LRR motifs is extremely variable across Arabidopsis RLPs; some members of the family have as few as four apparent repeats, while others have as many as 49 repeats. The LRR motif itself varies in form across family members and at positions; some are extremely hard to detect using sequence-based methods. A hypervariable region of approximately 50 to 75 amino acids is found nested between detectable LRR motifs in many RLPs; the precise role played by this region is not known. In RPP27, this hypervariable region is found between residues 789 and 855.
The majority of the RPP27 protein comprises extracellular LRR. However, there is no signal transduction domain, suggesting that additional proteins are required to facilitate the transmission of an Avr-induced conformational change from the extracytoplasmic to cytoplasmic domain and subsequently to activate the defense response. A possible function for the RPP27 protein can be proposed based on the hypothesized model of the CLV family in Arabidopsis. According to this model, the RLP encoded by CLV2 (Jeong et al., 1999
Similar modes of action for some of the R genes are also proposed. The rice gene Xa21 encodes an RLK and confers resistance to the bacterial pathogen X. oryzae pv oryzae (Song et al., 1995
To date, information on the RLP-mediated defense responses have come mainly from the studies with the Cf genes. Early Cf-mediated responses, including the production of active oxygen species (Piedras et al., 1998
Inoculation of RPP27 transgenic Col-rpp7.1 plants with different Ler-0 incompatible isolates of downy mildew showed that RPP27 confers full resistance to four isolates and partial resistance to Emco5 (Table I). Results with the isolate Noco2 are intriguing because this isolate was used to clone RPP5 from Ler-0, and there was no indication from genetic analysis for an additional R-gene specificity on chromosome 1 (Parker et al., 1997
In a plant-pathogen interaction, the products of R genes recognize the effector molecules of the pathogen either directly (Bryan et al., 2000
Downy mildew genes that elicit a defense response in Arabidopsis have been described as Arabidopsis thaliana-recognized (ATR) avirulence determinants, including the genetic identification of ATR loci that match six known RPP genes (Gunn et al., 2002
Plant Lines
Arabidopsis Col-0 and Ler-0 were used in this study. The mutants Col-sgt1b and Col-rpp7.1 were described elsewhere (Tör et al., 2002
All isolates of downy mildew (Peronospora parasitica) were maintained on Wassilewskija-eds1 (Parker et al., 1996
Seedlings of infected and noninoculated controls were stained with DAB to detect H2O2 as described previously (Thordal-Christensen et al., 1997
The linkage of RPP27 locus to the molecular marker g4026 on chromosome 1 was described previously (Tör et al., 2002
The construct MT27 was electroporated into Escherichia coli strain DH10B, and positive clones were identified by PCR and sequencing. The construct was then introduced into Agrobacterium tumefaciens strain GV3101 by electroporation, and the Col-rpp7.1 plants were transformed by the floral dip method (Clough and Bent, 1998
Total RNA was isolated from infected and noninfected cotyledons and flowers using the RNeasy plant mini kit (Qiagen USA, Valencia, CA) according to the manufacturer's instructions. RT-PCR was performed as described (Tör et al., 2002 For all sequencing, both DNA strands were sequenced using BigDye termination kit (Applied Biosystems, Foster City, CA) and separated on ABI 377 sequencer. Cloned products were sequenced using the universal M13 primers.
Arabidopsis databases TIGR (http://www.tigr.org/) and MIPS (http://mips.gsf.de/) were used for the initial annotation of the RPP27 region. Bioinformatics software used to refine predictions of DNA and amino acid sequences included NIX and PIX (http://hgmp.mrc.ac.uk/). Structure prediction of RPP27 was achieved using several Web servers, including Phylofacts (https://phylogenomics.berkeley.edu/phylofacts/), InterPro (http://www.ebi.ac.uk/), SMART (http://smart.embl-heidelberg.de/), and PFAM (http://pfam.wustl.edu/). Signal peptide and transmembrane domain prediction used the SignalP (http://www.cbs.dtu.dk/services/SignalP-2.0/) and TMHMM (http://www.cbs.dtu.dk/services/TMHMM/) Web servers. The RLP family HMM was created and scored with custom software; other HMMs constructed for these analyses used the Sequence Alignment and Modeling software from University of California Santa Cruz (http://www.cse.ucsc.edu/research/compbio/sam.html). Multiple sequence alignments were constructed using the MAFFT software (Katoh et al., 2002 The accession number of the BAC F20D21 is AC005287. The accession numbers for the RPP27 genomic and the cDNA sequences are AJ585978 and AJ585979, respectively. The accession numbers for CLV2, TMM, Cf-9, and Cf-2 are NP_17617, Q9SSD1, CAA05274, and T10504, respectively. Sequence data from this article have been deposited with the EMBL/GenBank data libraries under accession numbers AC005287, AJ585978, AJ585979, NP_17617, Q9SSD1, CAA05274, and T10504.
We thank Prof. Richard Napier for critically reading the manuscript and for helpful discussion. We also thank Rachel Edwards and Zübeyir Devran for technical assistance in sequencing and DNA isolation, and Margaret Jones and Mike Smith for photographic assistance. Received December 15, 2003; returned for revision February 6, 2004; accepted February 11, 2004.
1 This work was supported by the Biotechnology and Biological Science Research Council (grants to M.T., A.W.-T., A.C., and E.B.H.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.103.037770. * Corresponding author; e-mail mahmut.tor{at}hri.ac.uk; fax 44–1789–470552.
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