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Plant Physiology 145:593-600 (2007) © 2007 American Society of Plant Biologists Genome-Wide Annotation of Remorins, a Plant-Specific Protein Family: Evolutionary and Functional Perspectives1,[W]Laboratoire de Biogenèse Membranaire, Centre National de la Recherche Scientifique/Université Victor Segalen Bordeaux 2, 33076 Bordeaux cedex, France (S.R., S.M.); and Laboratoire des Interactions Plantes Micro-organismes, Institut National de la Recherche Agronomique-Centre National de la Recherche Scientifique, 31326 Castanet Tolosan cedex, France (P.G., A.N., T.O.)
Remorins were discovered in a screen for plasma membrane (PM) proteins differentially phosphorylated in the presence of oligogalacturonides (Farmer et al., 1989
Several proteomic approaches on PM preparations from tobacco (Nicotiana tabacum) leaves and Arabidopsis (Arabidopsis thaliana) seedlings now suggest localization of remorins in association with PMs (Watson et al., 2003
Some remorins share physical properties with viral movement proteins due to their hydrophobic N-terminal region. The C-terminal domain is generally predicted to consist of coiled-coil domains, a feature that appears to be common to all remorin proteins. This region was found to be responsible for the ability of remorins to form oligomeric filamentous structures in vitro, suggesting that these proteins might be structural components of plant cytoskeletons and/or the membrane skeletons (Bariola et al., 2004 Searches in databases of fully sequenced plant species revealed the existence of eight, 16, and 19 remorin genes in Populus trichocarpa, Arabidopsis, and rice (Oryza sativa), respectively (Supplemental Table S1). Patterns of differentially regulated remorin genes and proteins have been reported in an increasing number of transcriptomic and proteomic studies. Since many of these are annotated as "unknown function," they need to be properly classified and given suitable nomenclature. Here, we report on a genome-wide survey of the remorin family throughout fully sequenced plant genomes. We combined a phylogenetic approach with various in silico sequence-scanning tools (alignments, and motif and domain predictions) and analysis of available genetic and genomic data to identify a specific remorin signature and to define several groups within the remorin family. We used this classification to propose a general nomenclature for remorins that should help to differentiate between the different members in future studies.
Keyword and BLAST searches among available data allowed us to retrieve approximately 1,000 remorin sequences corresponding to more than 130 remorin proteins from 55 different plant species (Supplemental Table S1). Importantly, no significant hits were identified among sequence data from other kingdoms (fungi, animals, archaeabacteria, and eubacteria). Unexpectedly, no remorin genes were found in algae (neither by BLAST against publicly available data nor in the Ectocarpus siliculosus full-genome sequence; M. Cock, personal communication), while remorins were identified in mosses and ferns.
Canonical remorins, such as StREM (Reymond et al., 1996 A striking property of the Remorin_C domain is the high content of charged residues (e.g. 45% for StREM1.3), illustrated by well-conserved charged regions as shown in Figure 1 . The presence of remarkably hydrophilic domains with GRAVY (grand average of hydropathy) indices between –1.4 and –0.5 (Supplemental Table S1) results in a high hydrophilicity, posing the question how these proteins are tightly associated with membranes. Neither transmembrane domains nor membrane anchor signatures were found in any of the studied sequences (Supplemental Table S2).
Some particularly conserved residues can be outlined: position 11 of Remorin_C is occupied by an aromatic residue (mainly Trp); positions 18, 22, and 25 by positively charged residues; and position 30 by an aliphatic residue for all but one sequence (Fig. 1). Position 33 harbors a Trp in all sequences, except in Physcomitrella patens and Ceratopteris richardii, and positions 75 and 80 are Alas in most of the proteins. Because of their very high conservation, these amino acids can be considered as identifying features of the Remorin_C domain. In addition, a 23-amino-acid-long coiled-coil structure between Remorin_C residues 40 to 63 is predicted with a very high probability (Marcoils probability >90%). Prediction of the different positions in heptad repeats (Fig. 1, top diagram) reveals aliphatic residues for sites a and d that form the core of the coiled-coil region. In comparison with coiled-coil domains from other proteins, in remorins these motifs consist of a higher number of charged residues (56% for StREM1.3) in positions b, c, d, and e. This characteristic could be responsible for the high stability of protein interactions mediated by this domain (Burkhard et al., 2001  ).
With the aim of considering only full-length proteins and to avoid a bias of the study toward only highly expressed family members, we focused mainly on genes/proteins from plants with annotated genomes. As recent proteomic studies report the identification of remorins in legumes (Watson et al., 2003 ; Wienkoop and Saalbach, 2003; Valot et al., 2006; Lefebvre et al., 2007), all 10 remorin sequences of the partially sequenced model legume M. truncatula have been included in the analysis as representative remorins for the Fabaceae family. Considering that plant species that diverged early in evolution are likely to contain ancestral remorin sequences, all available remorins from ferns, mosses, and gymnosperms were also incorporated. This led to a list of 85 remorins (Supplemental Table S1) on which phylogenetic analysis was performed, as described in detail in Supplemental Materials and Methods S1. Two distinct phylogenetic trees were built, one using the full-length amino acid sequences (Fig. 2 ) and the other using only Remorin_C domain sequences (data not shown). Both trees were very similar, with the main exception that using full-length sequences allows clustering of remorins that lack an N-terminal domain in a single group. Considering that N-terminal regions may confer functional specificity to the proteins, we favored the use of full-length sequences in the following analyses.
For the final grouping leading to the proposed nomenclature, results from the phylogenetic analysis were combined with domain features and similarities between different remorin proteins. Due to significant differences, mainly in the N-terminal regions, the remorin family was subdivided into six separate groups. Such subdivision based on domain features enabled us to discriminate between groups 1, 2, and 3 on those parts of the tree where phylogenetic separation was less clear (Fig. 2; Table I ).
Group 1 (Subgroups 1a and 1b): Canonical Remorins with a Pro-Rich N-Terminal Region This group gathers all remorins that possess both Remorin_N and Remorin_C domains identified by InterProScan. Genomic data support coherence of this group as most genes consist of five exons, except for AtREM1.3 and OsREM1.2, in which the last two exons were fused by deletion of an intron. Generally, group 1 remorins are characterized by a high Pro content in the N-terminal region (only group 4 members have similar numbers of Pros in this region). Group 1 remorins were subdivided into group 1a (8.9% Pros) and group 1b (14.4% Pros) based on their N-terminal amino acid composition (Table I; Supplemental Fig. S2).
Group 1a remorins are about 200 amino acids long with a very homologous N-terminal region (about 82 amino acids). Four well-conserved motifs were identified by MEME/MAST (Multiple Em for Motif Elicitation/Motif Alignment and Search Tool; Bailey and Elkan, 1994 One of them, AtREM1.1, shows increased expression in senescing leaves, roots, and xylem, and after salt and osmotic stress and abscisic acid (ABA) treatment (Supplemental Table S3). The set of Arabidopsis genes showing the best expression correlation to AtREM1.1 expression is markedly enriched in genes associated with cell wall biology and extracellular functions (Fig. 3 ). Several of the well-correlated genes encode proteins with structural, signaling, or kinase activity. These data point to a possible link of group 1 remorins with cell wall biology and/or assembly.
Group 1b is the second group of proteins comprising both Remorin_N and Remorin_C domains, but their N-terminal regions contain twice the number of Pro residues compared to group 1a remorins. Only dicotyledonous plant species fall into this subgroup, suggesting that the Pro enrichment of the Remorin_N domain occurred after divergence of dicots. Group 1b contains the first discovered remorins, StREM1.3 (Reymond et al., 1996 ) and LeREM1 (Bariola et al., 2004; now named SlREM1.2), to which most of the current literature refers. The described Arabidopsis remorin AtDBP (AtREM1.3) and most remorins currently identified in proteomic screens of membrane preparations also cluster in this group (Watson et al., 2003; Marmagne et al., 2004; Mongrand et al., 2004; Sazuka et al., 2004; Nelson et al., 2006; Valot et al., 2006). Association with membranes thus seems to be a common feature of group 1b remorins. MEME motifs found in the N-terminal part of group 1b remorins are close to those found for group 1a (Supplemental Table S2). In addition to the Eukaryotic Linear Motif identified in group 1a, group 1b well-conserved motifs also notably bear an endoplasmic reticulum retention and retrieving signal. Abundance of group 1b remorins in proteomic studies may be explained by the high expression level of the corresponding genes. Indeed, AtREM1.2 and AtREM1.3 are among the 10% most highly and ubiquitously expressed genes in Arabidopsis (Supplemental Table S3). AtREM1.2 and AtREM1.4 are likely to represent genes derived from a recent duplication event (Supplemental Fig. S1), and their function may therefore be redundant.
Expression of group 1b genes in Arabidopsis is markedly increased in mature and/or senescing tissues (mature leaves, roots, mature pollen, flowers) and in vascular tissue (Bariola et al., 2004
Group 2 remorins contain the canonical Remorin_C domain (Fig. 1), while their N-terminal domain shows no significant protein homology to the Remorin_N domain of group 1 remorins and contains fewer Pro residues. Moreover, the MEME motifs found in their N-terminal regions differ from those of group 1. So far, group 2 contains only proteins from legumes (exemplified by sequences from M. truncatula) and P. trichocarpa (no group 2 remorins being found in Arabidopsis or rice).
Interestingly, a group 2 remorin was found during transcriptome and proteome approaches to be induced during symbiotic interactions between legumes and rhizobial bacteria (Fedorova et al., 2002
In addition, a gene encoding a group 2 remorin was found to be strongly induced during the symbiotic interaction between the model legume L. japonicus and the mycorrhizal fungus Glomus intraradices (Kistner et al., 2005
Remorins from group 3 only consist of a Remorin_C domain that is more divergent with some conserved, positively charged residues being replaced by aliphatic amino acids. Nevertheless, it includes the essential residues of the remorin signature. The absence of an N-terminal domain suggests that group 3 may serve basic functions. AtREM3.1 and AtREM3.2 show high sequence similarities with the C-terminal regions of AtREM6.6 (group 6) and AtREM1.2 (group 1), respectively. These genes are believed to result from ancient gene duplications (Supplemental Fig. S1). Differential expression of AtREM3.2 has been found under abiotic stress conditions, while for AtREM3.1 no expression data have been deposited in the AtGenExpress database.
The Remorin_C domain of group 4 remorins is very similar to that of canonical remorins, and this group also contains genes comprising only two exons. Group 4 remorins are characterized by a long Pro- and Ser-rich N-terminal region (about 160 amino acids), that does not show any significant homology to the group 1 Remorin_N domain. Conserved motifs found in group 4 N-terminal regions (Supplemental Table S2) indicate that most of these remorins possess (1) two positions resembling phosphopeptide-binding sites from proteins associated with cell-cycle checkpoint and DNA repair functions, and (2) a site predicted to mediate protein-protein interaction through binding of short Pro-rich regions within proteins. Sequence similarities suggest that AtREM4.1 and AtREM4.2 were derived from each other by a recent duplication event within the Arabidopsis genome (Supplemental Fig. S1). These two genes are predominantly expressed in green, aerial plant organs, namely, cauline and senescing leaves, as well as stems. They are strongly stress responsive, showing a marked increase after osmotic, salt, and drought stresses, and treatment of plants with phytohormones such as ABA and brassinosteroids. Furthermore, these genes are transcriptionally induced upon pathogen infections (Supplemental Table S3). Such links are supported by the expression of group 4 remorins being correlated with those of genes associated with chloroplasts and plastids, energy pathways, as well as abiotic or biotic stimuli (Fig. 3).
Group 5 remorins show a more divergent Remorin_C domain, as indicated by lower score values given by protein motif-scanning programs (Table I). This group consists of a highly variable N-terminal region, although all members contain two conserved MEME motifs that bear putative phosphorylation sites (Supplemental Table S2). Due to the absence of the group 5 remorin (AtREM5.1) from the ATH1 GeneChip and the lack of any significant sequence similarity of their N-terminal regions, it remains difficult to predict the functionality of remorins from this group. However, MtREM5.1 of M. truncatula, the putative ortholog of AtREM5.1, is one of the major remorins expressed in seeds (V. Benedito and M. Udvardi, personal communication).
The last group contains remorins ranging from 240 to 522 amino acids in length. The size of their N-terminal regions is variable and may reflect the existence of several subgroups, which are difficult to define based on currently available data. Interestingly, sequence similarities in the N-terminal regions of some members of group 6 were found with a xylulokinase homolog from Strongylocentrotus purpuratus (involved in pentose and glucuronate interconversion; GI:72085098) and MurB reductase from P. patens (involved in amino-sugar conversion; GI:76880168). In addition, four conserved MEME motifs can be detected in their N-terminal regions, indicating that many remorins of this group contain (1) conserved putative phosphorylation sites, (2) a predicted protein-protein interaction motif, and, for a subgroup of them, (3) a predicted Tyr-based sorting signal responsible for the interaction with an adaptor protein complex.
Transcript levels of Arabidopsis remorins AtREM6.5 and AtREM6.1 are highest in meristematic tissues. A remarkable consistency in repression of these genes after pathogen infection, cold and osmotic stress, as well as induction after salt stress was also noted (see Supplemental Table S3). Interestingly, another study predicted a putative recognition site for the bacterial effector protein AvrRpt2, encoding a Cys protease, within a group 6 remorin (AtREM6.1; Chisholm et al., 2005
Remorin proteins appear to be specific to the plant kingdom. The absence of remorins in algae, but their presence in mosses, ferns, and higher plants, suggests that the emergence of remorins coincided with the colonization of land. It is very likely that this colonization required chemical adaptation of cell walls to cope with particularly rigorous selection pressure. Evolution in cell wall composition is probably related to the emergence of an upright position and the acquisition of vascular tissue. Major differences in primary cell wall components were found by comparing taxa from charophytes (the closest extant algal ancestor of land plants), bryophytes, and pteridophytes to vascular plants. For example, major components of cell walls, such as xyloglucan (the main hemicellulose) and Hyp-rich glycoproteins (major components of cell walls), are present in bryophytes, pteridophytes, and vascular plants, but are not detectable in charophytes. Similarly, acid hydrolysis of cell wall-rich material revealed that uronic acids were more abundant in ancestral plants than in more recent vascular ones, and that GalUA is more abundant in bryophytes and charophytes than in vascular plants. Finally, mixed-linkage glucan was absent from all algae and bryophytes tested (for review, see Popper and Fry, 2003 ).
Interestingly, the canonical potato StREM1.3 was found to be able to bind both simple and complex galacturonides, and interaction with polyanionic cell or cell wall components can be hypothesized (Reymond et al., 1996 Precise biological roles of different remorins from the various groups remain to be investigated, but gene expression data suggest that some of these proteins might have key functions during responses to biotic and abiotic stimuli and might possibly be involved in hormone-mediated responses and signal transduction. Transient and rapid induction of gene expression (e.g. AtREM1.2, AtREM1.4, and AtREM6.1) upon biotic stimuli, such as powdery mildew infection, suggests possible roles in early stages of plant-microbe interactions. Whether such roles can be directly linked to cell wall- and/or PM-associated functions remains to be elucidated. With respect to the variability of the N-terminal parts among the different groups and the hypothesis that this region confers functional specificity of the protein, different functions might be expected. Interestingly, no homozygous insertion mutants are available for any remorin gene in Arabidopsis, possibly indicating lethal phenotypes when remorin gene expression is completely abolished. Other model systems, such as symbiotic root nodulation, as described above, may therefore be helpful to elucidate the biological functions of certain remorins. The nomenclature suggested here should simplify analysis and classification of detected remorin transcripts and proteins during future experiments and lead to a more comprehensive view of this novel protein family.
The following materials are available in the online version of this article.
We thank Steven Ball for fruitful discussion and Mark Cock for the BLAST analysis on E. siliculosus sequences. Furthermore, we would like to thank Julie Cullimore and Clare Gough for critical reading of the manuscript. Received September 5, 2007; accepted September 13, 2007; published November 7, 2007.
1 This work was supported by the French Agence Nationale de la Recherche (contract ANR–JC05–45555 "Plant rafts"; S.R. and S.M.) and the European Union (Marie Curie Intra-European Fellowship grant no. MEIF–CT–2005–024587; T.O.).  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: Thomas Ott (thomas.ott{at}toulouse.inra.fr).
[W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.107.108639 * Corresponding author; e-mail thomas.ott{at}toulouse.inra.fr.
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IDENTIFICATION OF A GENERIC...
THE REMORIN FAMILY CONSISTS...
, aromatic residues; +, positively charged residues; 
, aliphatic residues; % refers to the number of sequences showing the indicated residue at the indicated position, among the list of 85 remorins given in Supplemental Table S1.
