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Plant Physiology 139:1107-1124 (2005) © 2005 American Society of Plant Biologists Evolutionary Expansion, Gene Structure, and Expression of the Rice Wall-Associated Kinase Gene Family1,[w]Department of Plant and Microbial Biology, University of California, Berkeley, California 94720 (S.Z., C.C., L.M., J.S., P.G.L.); Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut 06520–8104 (L.L., X.-W.D.); Department of Horticulture, Michigan State University, East Lansing, Michigan 48824 (N.J.); and Department of Biology, San Francisco State University, San Francisco, California 94132 (Z.-H.H.)
The wall-associated kinase (WAK) gene family, one of the receptor-like kinase (RLK) gene families in plants, plays important roles in cell expansion, pathogen resistance, and heavy-metal stress tolerance in Arabidopsis (Arabidopsis thaliana). Through a reiterative database search and manual reannotation, we identified 125 OsWAK gene family members from rice (Oryza sativa) japonica cv Nipponbare; 37 (approximately 30%) OsWAKs were corrected/reannotated from earlier automated annotations. Of the 125 OsWAKs, 67 are receptor-like kinases, 28 receptor-like cytoplasmic kinases, 13 receptor-like proteins, 12 short genes, and five pseudogenes. The two-intron gene structure of the Arabidopsis WAK/WAK-Likes is generally conserved in OsWAKs; however, extra/missed introns were observed in some OsWAKs either in extracellular regions or in protein kinase domains. In addition to the 38 OsWAKs with full-length cDNA sequences and the 11 with rice expressed sequence tag sequences, gene expression analyses, using tiling-microarray analysis of the 20 OsWAKs on chromosome 10 and reverse transcription-PCR analysis for five OsWAKs, indicate that the majority of identified OsWAKs are likely expressed in rice. Phylogenetic analyses of OsWAKs, Arabidopsis WAK/WAK-Likes, and barley (Hordeum vulgare) HvWAKs show that the OsWAK gene family expanded in the rice genome due to lineage-specific expansion of the family in monocots. Localized gene duplications appear to be the primary genetic event in OsWAK gene family expansion and the 125 OsWAKs, present on all 12 chromosomes, are mostly clustered.
Efficient communication between the plant cell wall and the cytoplasm is important in plant development and in responding to biotic and abiotic stresses (Kohorn, 2000  ; Brownlee, 2002; Somerville et al., 2004). The wall-associated kinase (WAK) gene family, which belongs to the receptor-like kinase (RLK) superfamily in plants (Shiu and Bleecker, 2001, 2003), plays a critical role in this communication (He et al., 1996; Kohorn, 2001). WAK1, the first member of the WAK gene family identified in Arabidopsis (Arabidopsis thaliana), encodes a protein containing an intracellular Ser-Thr kinase domain and extracellular domains with similarities to vertebrate epidermal growth factor (EGF)-like domains (He et al., 1996). From the Arabidopsis genome (Arabidopsis Genome Initiative, 2000), 26 WAK and WAK-Like (WAKL) genes were identified and most of the 26 members are expressed in Arabidopsis (Verica and He, 2002; Verica et al., 2003).
Functional studies of the different WAK members in Arabidopsis demonstrated that they are involved in various functions in plants, including pathogen resistance (He et al., 1998
To further understand the functions and evolution of the WAK gene family in plants, we analyzed the WAK gene family in rice (Oryza sativa). Rice is one of the most important cereals and also considered a model for other cereal species, including maize (Zea mays), wheat (Triticum aestivum), barley (Hordeum vulgare), and sorghum (Sorghum bicolor). Rice genomic sequences are now available from both subspecies indica (Yu et al., 2002 Here we present a detailed analysis of the rice WAK/WAKL (OsWAK) gene family from japonica. First, through public database searches, we retrieved all genes annotated as putative OsWAKs, followed by reiterative database searches from which we obtained additional putative OsWAK gene family members. Manual reannotation was performed to correct or reannotate the misannotated putative OsWAK genes, such as split genes, fused genes, short genes, and pseudogenes. We determined expression characteristics for certain OsWAK members and, based on domain composition, we classified OsWAKs into five groups and performed comparative phylogenetic analyses of WAKs in Arabidopsis, rice, and barley to understand the possible mechanisms of gene family expansion.
Identification and Classification of OsWAKs from Genome Sequences of Rice Subsp. japonica cv Nipponbare
Four analytical steps were used to identify and classify OsWAKs from japonica subsp. cv Nipponbare. First, all genes annotated as putative OsWAKs were retrieved from three public databases: (1) The Institute for Genomic Research (TIGR) Rice Genome Annotation Database (Osa1, release 1 and 2; Yuan et al., 2005 In the third step, each putative OsWAK sequence was manually assessed for the EGF-like domains, kinase domain, or its sequence similarity to other putative OsWAKs. In our analyses, in order for a gene to be defined as a putative OsWAK, the gene had to fit into one of the five OsWAK types (see Table I). Based on these five criteria, a total of 129 putative OsWAKs were initially identified from japonica cv Nipponbare.
As the last step, manual reannotation was performed to correct or reannotate the misannotated putative OsWAKs, as described below. This analysis included 10 putative split OsWAKs merged into five OsWAK-RLKs, four fused putative OsWAKs split into five different OsWAKs, and six non-OsWAKs, leaving a final total of 125 OsWAKs; the numbers of each type of OsWAK are shown in Table I. For the 125 OsWAKs, the detailed annotations (Supplemental Tables I and II), genomic and predicted coding/full-length (FL)-cDNA sequences (Supplemental Data 1), and predicted protein sequences (Supplemental Data 2) are presented.
Automated annotations of rice genome sequences of japonica cv Nipponbare in TIGR and GenBank are useful as initial resources for gene annotation, but individual genes and gene families are generally not verified and corrected. Several types of annotation errors were found in the automated annotation of the Arabidopsis genome, including intron numbers/positions, merged/split genes, and missed short genes; approximately 35% of the initially annotated genes from Arabidopsis were corrected from FL-cDNA sequences (Haas et al., 2003
Split/Fused OsWAK Genes
Fourteen other putative, split OsWAKs (seven putative OsWAK-RLPs and seven putative OsWAK-RLCKs) also matched complementally to various OsWAK-RLKs (data not shown). However, for each of these pairs, one to eight different genes interrupt the sequence (Fig. 2). These split OsWAKs appear to have already become independent genes; for example, the pair, OsWAK84 and OsWAK85, has two different FL-cDNA sequences. Therefore, these 14 putative, split OsWAKs remain annotated as independent OsWAKs.
Three putative OsWAKs (OsWAK5/2768.t00008, OsWAK73/9636.t03851, OsWAK89/9637.t03234) from Osa1 in TIGR were found to be three fused genes. Putative OsWAK5 and OsWAK73 are fused with non-OsWAKs, and the third has two fused OsWAKs (Fig. 3). Therefore, the three fused genes were split, obtaining four OsWAKs (OsWAK5, OsWAK73, OsWAK89a, OsWAK89b). OsWAK89a and OsWAK89b have 57% identity in overall protein sequence and >93% identity in their kinase domains; both contain EGF-like domains in their extracellular regions, suggesting they are independent OsWAK-RLKs that likely derived from tandem duplication. Interestingly, putative OsWAK69 is fused to a Pack-Mu-like element (MULE; Jiang et al., 2004 ) on its 5' side, and an approximately 2-kb space is found between the Pack-MULE and the kinase domain. The sequence of a FL-cDNA (AK064911) matched only to the Pack-MULE, not to the kinase domain (Fig. 4). Accordingly, the fusion is believed to be an annotation artifact and the kinase domain of the original OsWAK69 was split out as an OsWAK-RLCK.
OsWAK Short Genes Five putative OsWAKs (OsWAK17, OsWAK19, OsWAK54, OsWAK62, OsWAK67) were initially identified as OsWAK short genes. This was due to the fact that their predicted protein sequences were <300 amino acids and did not encode an EGF-like or kinase domain, but they had >40% amino acid identity to the longer OsWAKs. From the FL-cDNA sequence analyses described above, seven more putative OsWAKs (OsWAK18, OsWAK23, OsWAK35, OsWAK37, OsWAK52, OsWAK101, OsWAK127) were reannotated as OsWAK short genes. This was also due to the fact that the deduced protein sequences from their longest open reading frames (ORFs) are <300 amino acids and do not encode an EGF-like or kinase domain. Of the seven OsWAK short genes, four (OsWAK18, OsWAK52, OsWAK101, OsWAK127) had antisense transcripts and the other three (OsWAK23, OsWAK35, OsWAK37) had sense transcripts. In order to further understand how the OsWAK short genes might have arisen in the rice genome, genomic sequences adjacent to the seven OsWAK short genes were analyzed. These analyses found various transposable elements (TEs) were inserted at either the 5' or 3' ends of the FL-cDNAs of five of the OsWAK short genes (Table II).
Further analyses indicated that the inserted TEs likely did not interrupt the OsWAKs; however, they either provided novel splicing sites or initialized antisense transcriptions, which resulted in short ORFs for the OsWAKs. For example, the 3' end of the OsWAK23 FL-cDNA is located inside a long interspersed nuclear element (LINE) that appears to provide a novel splicing acceptor site. As a result, both the EGF-like and kinase domains were spliced out and thus do not present in the FL-cDNA sequence of OsWAK23 (Fig. 4). OsWAK35 has one sense and three antisense transcripts, and one of the antisense transcripts (AK100568) appears to be initialized from a solo long-terminal repeat (LTR; Fig. 4).
OsWAK Pseudogenes
Intron Number and Position of OsWAKs
Arabidopsis RLK-type WAK/WAKLs have a two-intron/three-exon gene structure pattern within their coding regions (Verica and He, 2002
Excluding the five OsWAK pseudogenes and the 38 OsWAKs with FL-cDNAs (Fig. 5), domain composition and organization were analyzed for the other 82 OsWAKs, using their predicted protein sequences to search the Simple Modular Architecture Research Tool (SMART) database (http://smart.embl-heidelberg.de) for EGF-like domains, the kinase domain, and the transmembrane domain. Of the 82 OsWAKs, 53 OsWAK-RLKs contain both extracellular EGF-like domains (EGF-2 and/or EGF-Ca2+) and a cytoplasmic protein kinase domain; 15 OsWAK-RLCKs contain only one to two kinase domains; nine OsWAK-RLPs contain only the extracellular EGF-like domains; and five OsWAK short genes contain no domain (Fig. 6).
Expression Analysis of OsWAKs Thirty-eight OsWAKs have corresponding FL-cDNA sequences (Fig. 5), indicating that they are expressed in rice. Rice EST database searches in Sputnik (http://mips.gsf.de/proj/sputnik/oryza) were also performed for each of the 125 OsWAKs. Eleven OsWAKs that previously had no FL-cDNA matched to one to five different EST sequences (details in Supplemental Table III), indicating they are also expressed. The matched EST sequences were derived from various rice tissues and also from libraries made from plants following biotic and abiotic stress treatments. Of the 38 OsWAKs with FL-cDNAs, four (OsWAK18, OsWAK52, OsWAK101, OsWAK127) appear to be expressed as antisense genes because of the antisense orientation of their FL-cDNA sequences (Fig. 5D). Six OsWAKs (OsWAK10, OsWAK53, OsWAK112, OsWAK118, OsWAK18, OsWAK127) appear to be alternatively spliced, since they have more than one FL-cDNA sequence; and two (OsWAK35, OsWAK129) are transcribed in both directions (Fig. 5E). In addition, five different OsWAKs were chosen for expression analysis using reverse transcription (RT)-PCR, OsWAK7, OsWAK50, OsWAK125, plus two short genes, OsWAK17 (48% amino acid identity to the C terminus of OsWAK53) and OsWAK62 (92% amino acid identity to the extracellular region of OsWAK63). DNA samples from leaf tissues were used in PCR analyses; three RNA samples from the root tip, root base, and shoot tissues were used in RT-PCR analyses. OsWAK50, which has a FL-cDNA sequence available, had RT-PCR products of an expected size (1,084 bp) from all three tissues; because two introns were present, its PCR product was larger (1,308 bp). This result confirmed OsWAK50 is an expressed gene and showed there was no DNA contamination in RNA samples used for RT-PCR reactions. The same DNA and RNA samples were used for the other four OsWAKs. OsWAK7 and OsWAK125 that are without FL-cDNA sequences also had RT-PCR products from one or more rice tissues; because they had no intron, their RT-PCR products (OsWAK7, 758 bp; OsWAK125, 800 bp) were the same sizes as their PCR products (Fig. 7). The short gene, OsWAK17, which had an RT-PCR product from the root base and shoot, indicating the short gene, resembling the C-terminal region of an RLK, is also expressed. Because of the presence of two introns, the PCR product of OsWAK17 was much larger (2,178 bp) than its RT-PCR product (731 bp). Only a PCR product (207 bp) was obtained from OsWAK62, indicating it may not be expressed or may be expressed in other tissues.
For functional studies of all OsWAKs, further experimental confirmation of gene expression patterns is needed. To perform this type of analysis, rice microarrays containing all 125 OsWAKs would be ideal; however, this type of custom microarray is not yet available. We therefore took advantage of available rice tiling-path microarrays representing the entire rice chromosome 10 that have been successfully used to detect gene transcription activity (Li et al., 2005 ). Two independent sets of 36-mer probes, with 10-nucleotide intervals, tiled throughout chromosome 10 of japonica and indica, were designed for the microarrays; rice subsp. japonica cv Nipponbare and rice subsp. indica cv 93-11, respectively, were used for the experiments. The mRNA samples used for the microarray hybridization were from four normally growing tissues: 7-d-old seedling shoot and root, panicle (heading and filling stages), and suspension culture cells. Determination of the signal-to-noise ratio and expression level of a given gene model was previously described (Li et al., 2005). Based on the results of that analysis, we examined transcription activity for the 20 OsWAKs on chromosome 10. Fifteen out of the 20 OsWAKs were shown to be expressed in japonica tissues, and 10 in both japonica and indica (Table III). Surprisingly, of the three OsWAKs (OsWAK98, OsWAK101, OsWAK112) already having FL-cDNA sequences available, only OsWAK101 was expressed based on the microarray experiment, suggesting the other two might be expressed under specific stress or developmental conditions.
Phylogenetic Analyses of Rice OsWAKs, Arabidopsis WAK/WAKLs, and Barley HvWAKs
Intracellular protein kinase domains are typically the conserved regions of RLKs and are used in phylogenetic analyses (Shiu and Bleecker, 2001
This analysis revealed that most OsWAKs and Arabidopsis WAK/WAKLs cluster in species-specific distinct clades, except for four OsWAKs (OsWAK1, OsWAK2, OsWAK10, OsWAK25) and four WAKL-IV members (WAK14, WAK15, WAK20, WAK21) that cluster in the same clade. This result indicates that most OsWAKs and Arabidopsis WAK/WAKLs expanded in a species-specific manner; only a few members likely originated from the common ancestral genes that existed before divergence of monocots and dicots. To further investigate whether expansion of OsWAKs is rice specific or due to lineage-specific expansion of this family in monocots, we identified 10 barley WAKs (HvWAKs) from the barley EST database (HarvEST; http://harvest.ucr.edu). Because only partial predicted protein sequences (of either extracellular regions or kinase domains) of HvWAKs were obtained (Supplemental Data 3), we used predicted, FL protein sequences of 43 OsWAK-RLKs containing both extracellular regions and kinase domains in the phylogenetic analyses. Ten HvWAKs cluster with individual OsWAKs, rather than diverging in a group unique to barley (Fig. 9), suggesting that OsWAK expansion in rice likely resulted from lineage-specific expansion of the family in monocots.
Localized Duplications Resulted in Expansion of OsWAKs Examination of individual OsWAKs in different subclades of the rice-specific clades (Fig. 8) revealed that many small OsWAK groups (two to seven genes) located close together on the same chromosomes are clustered in the same subclades, i.e., OsWAKs 14 to 16 from chromosome 2; OsWAKs 42 to 47 and 49 from chromosome 4; OsWAKs 70 to 72 from chromosome 7; OsWAKs 79 to 82, 85, and 89 to 92 from chromosome 9; OsWAKs 116 to 119 and 121 to 123 from chromosome 11; and OsWAKs 126, 128, and 129 from chromosome 12. The high sequence similarity of these physically, closely located OsWAKs indicates that likely they arose from localized gene duplications. For example, based on sequence similarity and physical location, the four OsWAKs (OsWAK5, OsWAK6, OsWAK8, OsWAK9) on chromosome 1 likely derived from duplication of a gene pair and, after duplication, 11 genes inserted between OsWAK5 and OsWAK6 (Fig. 10A). The five OsWAKs (OsWAK89a, OsWAK89b, OsWAK90, OsWAK91, OsWAK92) on chromosome 9 likely derived from four gene duplications and, after the duplication, 10 genes inserted between OsWAK91 and OsWAK92 (Fig. 10B). The 20 OsWAKs on chromosome 10 are physically located as two clusters within 16 cM at the end of the short arm. Twelve likely derived from several localized gene duplications; six were duplicated to or from the OsWAKs on chromosome 11, and two were duplicated to or from the OsWAKs on chromosome 4 (Fig. 10C).
Ratios of Nonsynonymous versus Synonymous Substitution Rates between OsWAK EGF-Ca2+ Domain Regions
The EGF-Ca2+ domains, the typical extracellular domains in Arabidopsis WAK/WAKLs (Verica and He, 2002
Since all rice clones used for genomic sequencing in the International Rice Genome Sequencing Project can be physically anchored on the 12 rice chromosomes, as are the pseudomolecules assembled in TIGR (http://www.tigr.org/tdb/e2k1/osa1/pseudomolecules/info.shtml), the 125 OsWAKs encoded on individual clones can be correspondingly mapped on japonica chromosomes (Fig. 11). This analysis showed that OsWAKs are clustered on chromosomes in most cases; however, in a few cases only a single OsWAK is present at a given chromosomal location, e.g., OsWAK10 on chromosome 1. The majority of OsWAKs (56.8%; 71 of 125) are located on chromosomes 2, 4, 9, and 10.
Identification of OsWAK Gene Family Members Through a reiterative database search and manual reannotation, we identified 125 OsWAK gene family members from rice japonica cv Nipponbare. Thirty-seven (approximately 30%) of the identified OsWAKs were corrected/reannotated from their earlier automated annotations, such as five merged genes from 10 split genes, five split genes from four fused genes, seven corrected as short genes, and six reannotated from putative pseudogenes. A few of the reannotations were based on sequence similarities to the other OsWAK family members; a few other reannotations/corrections were found by sequence extension of the previously annotated genes to recover the missing exons from the 5' or 3' ends.
Most reannotations, however, were based on the corresponding FL-cDNA sequences available in rice (Kikuchi et al., 2003
Of the 125 OsWAK gene family members, 67 are OsWAK-RLKs containing both extracellular EGF-like domains and an intracellular kinase domain; 28 are OsWAK-RLCKs containing only the kinase domain; 13 are OsWAK-RLPs with only the extracellular EGF-like domains; 12 are OsWAK short genes; and five are pseudogenes. Functions of these various OsWAKs are yet to be determined.
The unique character of OsWAK-RLPs and OsWAK-RLKs is the EGF-like domain at the N-terminal extracellular region. The function of EGF-like domains in OsWAKs and Arabidopsis WAK/WAKLs is yet to be determined. Analysis of other EGF-containing proteins from plants and animals suggests several possible roles for the EGF-like domains in the OsWAK-RLKs and OsWAK-RLPs. In the plant vacuolar sorting protein, BP-80, EGF domains were shown to alter the structural conformation of the ligand-binding domains, thereby increasing their affinity for ligand binding (Cao et al., 2000
In plants, several different RLK members were characterized and found to function in a diverse array of signaling processes, including phytohormone responses (Chang et al., 1993
Several RLP members in plants were also shown to have important functions. For example, CLV2 functions in shoot meristem development in Arabidopsis (Kayes and Clark, 1998
Especially interesting are recent studies showing that plant RLK, RLP, and RLCK members could function together in the same signaling pathways. For example, in the self-incompatibility signaling pathway in Brassica, the S-receptor kinase (an RLK member), the S-locus glycoprotein (an RLP member resembling the extracellular part of the S-receptor kinase), and the M-locus protein kinase (an RLCK member) function as a single complex in signaling (Cui et al., 2000
Twelve OsWAK family members are short genes with less than 300 amino acids and no known domain. This type of short gene was also identified in the Arabidopsis FL-cDNA sequence analyses (Haas et al., 2003
The two-intron gene structure pattern of Arabidopsis WAK/WAKLs (Verica and He, 2002
Antisense expression, bidirectional transcription, and alternative splicing were observed in a few of the 38 OsWAKs with FL-cDNA sequences. This type of antisense and bidirectional transcription was also observed from FL-cDNA sequence analysis of many other rice genes (Osato et al., 2003
Compared to the 26 Arabidopsis WAKs/WAKLs (Verica and He, 2002
Phylogenetic analyses of OsWAKs and Arabidopsis WAK/WAKLs show that most OsWAKs and Arabidopsis WAK/WAKLs are clustered in distinct species-specific clades, suggesting species-specific expansion in both plants. Further phylogenetic analyses, comparing OsWAKs with barley HvWAKs, indicate that OsWAK expansion was mainly due to its lineage-specific expansion in monocot species. This type of divergence between monocot (rice) and dicot (Arabidopsis) species was also observed for a large gene family involved in pathogen resistance, the nucleotide-binding site (NBS)-LRR gene family (Bai et al., 2002
It has been suggested that the expansion of Arabidopsis WAK/WAKLs is due to both local tandem duplications and large-scale genomic duplications (Verica and He, 2002
Sequence Retrieval and Analysis
The DNA and predicted protein sequences, annotated as putative OsWAKs from the genome sequence of rice (Oryza sativa) japonica cv Nipponbare, were retrieved from three public databases: (1) TIGR Rice Genome Annotation Database (Osa1; http://www.tigr.org/tdb/e2k1/osa1; Yuan et al., 2005
The SMART database (http://smart.embl-heidelberg.de) was used to search for EGF-like domains, protein kinase domains, and transmembrane domains. BioEdit software (http://www.mbio.ncsu.edu/BioEdit/bioedit.html) was utilized as a tool for diagramming domain positions for OsWAKs.
Total DNA and RNA, used in PCR and RT-PCR respectively, were isolated from 2-week-old seedlings of rice japonica cv Nipponbare. DNA extraction was performed on young leaf tissues (Cone, 1989
Predicted protein sequences of OsWAKs were retrieved from public databases as described in "Results." Arabidopsis (Arabidopsis thaliana) WAK/WAKL protein sequences were obtained from GenBank as described in Verica and He (2002)
All sequenced contigs from japonica cv Nipponbare were physically constructed as pseudomolecules (release 2) in TIGR (http://www.tigr.org/tdb/e2k1/osa1/pseudomolecules/info.shtml), representing the 12 rice chromosomes. OsWAKs were then mapped on individual chromosomes, based on corresponding contigs on rice chromosomes.
The authors are grateful to Barbara Alonso for providing expert assistance with the figures, and to the anonymous reviewers for their helpful comments. Received July 28, 2005; returned for revision August 22, 2005; accepted August 24, 2005.
1 This work was supported by the National Science Foundation (NSF) Plant Genome Research Program (grant no. 0110512) and NSF Research Experience for Undergraduate (REU; to P.G.L.), and by the National Institutes of Health (NIH grant no. S06 GM52588 to Z.-H.H.).  The authors 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) are: Peggy G. Lemaux (lemauxpg{at}nature.berkeley.edu) and Shibo Zhang (shibo{at}nature.berkeley.edu).
[w] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.105.069005. * Corresponding author; e-mail shibo{at}nature.berkeley.edu; fax 510–642–7356.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402 Anderson CM, Wagner TA, Perret M, He ZH, He D, Kohorn BD (2001) WAKs: cell wall-associated kinases linking the cytoplasm to the extracellular matrix. Plant Mol Biol 47: 197–206[CrossRef][ISI][Medline]
Appella E, Robinson EA, Ullrich SJ, Stoppelli MP, Corti A, Cassani G, Blasi F (1987) The receptor-binding sequence of urokinase: a biological function for the growth-factor module of proteases. J Biol Chem 262: 4437–4440 Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408: 796–815[CrossRef][Medline]
Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, et al (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12: 1871–1884
Baumberger N, Doesseger B, Guyot R, Diet A, Parsons RL, Clark MA, Simmons MP, Bedinger P, Goff SA, Ringli C, et al (2003) Whole-genome comparison of leucine-rich repeat extensins in Arabidopsis and rice. A conserved family of cell wall proteins form a vegetative and a reproductive clade. Plant Physiol 131: 1313–1326 Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273: 1406–1409[Abstract] Brownlee C (2002) Role of the extracellular matrix in cell-cell signalling: paracrine paradigms. Curr Opin Plant Biol 5: 396–401[CrossRef][ISI][Medline]
Cao X, Rogers SW, Butler J, Beevers L, Rogers JC (2000) Structural requirements for ligand binding by a probable plant vacuolar sorting receptor. Plant Cell 12: 493–506
Castelli V, Aury JM, Jaillon O, Wincker P, Clepet C, Menard M, Cruaud C, Quetier F, Scarpelli C, Schachter V, et al (2004) Whole genome sequence comparisons and "full-length" cDNA sequences: a combined approach to evaluate and improve Arabidopsis genome annotation. Genome Res 14: 406–413
Chang C, Kwok SF, Bleecker AB, Meyerowitz EM (1993) Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262: 539–544
Clark KL, Larsen PB, Wang X, Chang C (1998) Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci USA 95: 5401–5406 Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89: 575–585[CrossRef][ISI][Medline] Cone K (1989) Yet another rapid plant DNA prep. Maize Genet Coop Newsl 63: 68
Cui Y, Bi YM, Brugiere N, Arnoldo M, Rothstein SJ (2000) The S locus glycoprotein and the S receptor kinase are sufficient for self-pollen rejection in Brassica. Proc Natl Acad Sci USA 97: 3713–3717 Feng Q, Zhang Y, Hao P, Wang S, Fu G, Huang Y, Li Y, Zhu J, Liu Y, Hu X, et al (2002) Sequence and analysis of rice chromosome 4. Nature 420: 316–320[CrossRef][Medline]
Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98: 373–378
Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92–100
Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131: 1855–1867 Haas BJ, Volfovsky N, Town CD, Troukhan M, Alexandrov N, Feldmann KA, Flavell RB, White O, Salzberg SL (2003) Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol 3: RESEARCH0029
He ZH, Fujiki M, Kohorn BD (1996) A cell wall-associated, receptor-like protein kinase. J Biol Chem 271: 19789–19793 He ZH, He D, Kohorn BD (1998) Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J 14: 55–63[CrossRef][ISI][Medline] Heldin CH (1995) Dimerization of cell surface receptors in signal transduction. Cell 80: 213–223[CrossRef][ISI][Medline] Hobe M, Muller R, Grunewald M, Brand U, Simon R (2003) Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol 213: 371–381[CrossRef][ISI][Medline] International Rice Genome Sequence Project (2005) The map-based sequence of the rice genome. Nature 436: 793–800[CrossRef][Medline]
Jeong S, Trotochaud AE, Clark SE (1999) The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 11: 1925–1934 Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR (2004) Pack-MULE transposable elements mediate gene evolution in plants. Nature 431: 569–573[CrossRef][Medline]
Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14: 108–117
Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JDG (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266: 789–793 Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125: 3843–3851[Abstract] Kikuchi S, Satoh K, Nagata T, Kawagashira N, Doi K, Kishimoto N, Yazaki J, Ishikawa M, Yamada H, Ooka H, et al (2003) Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301: 376–379 |
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ABSTRACT
RESULTS
99.5%). For the other 19, the FL-cDNA sequences were either shorter (seven) or longer (12) than the predicted coding sequences. All of the FL-cDNA sequences, except one, have both 5' untranslated region (UTR) and 3' UTR, indicating they are most likely intact cDNA sequences. Therefore, these 19 putative OsWAKs were corrected using their corresponding FL-cDNA sequences, although it is possible that some or all of the shorter FL-cDNAs could derive from truncated sequences. Reannotation of 14 out of the 19, along with 13 additional putative OsWAKs, is described below. 
