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First published online May 1, 2003; 10.1104/pp.102.013722 Plant Physiology 132:907-925 (2003) © 2003 American Society of Plant Biologists Comparative Analysis of SET Domain Proteins in Maize and Arabidopsis Reveals Multiple Duplications Preceding the Divergence of Monocots and Dicots1,[w]Department of Agronomy, University of Wisconsin, 1575 Linden Drive, Madison, Wisconsin 53706 (N.M.S., H.F.K., S.M.K.); Department of Plant Sciences, University of Arizona, Tucson, Arizona 85721 (C.A.N., V.L.C.); and Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211 (K.C.C.); Pioneer Hi-Bred International, Inc., Johnston, Iowa 50131 (D.A.S.); and Arizona Cancer Center, University of Arizona, Tucson, Arizona 85724 (R.P.)
Histone proteins play a central role in chromatin packaging, and modification of histones is associated with chromatin accessibility. SET domain [Su(var)3-9, Enhancer-of-zeste, Trithorax] proteins are one class of proteins that have been implicated in regulating gene expression through histone methylation. The relationships of 22 SET domain proteins from maize (Zea mays) and 32 SET domain proteins from Arabidopsis were evaluated by phylogenetic analysis and domain organization. Our analysis reveals five classes of SET domain proteins in plants that can be further divided into 19 orthology groups. In some cases, such as the Enhancer of zeste-like and trithorax-like proteins, plants and animals contain homologous proteins with a similar organization of domains outside of the SET domain. However, a majority of plant SET domain proteins do not have an animal homolog with similar domain organization, suggesting that plants have unique mechanisms to establish and maintain chromatin states. Although the domains present in plant and animal SET domain proteins often differ, the domains found in the plant proteins have been generally implicated in protein-protein interactions, indicating that most SET domain proteins operate in complexes. Combined analysis of the maize and Arabidopsis SET domain proteins reveals that duplication of SET domain proteins in plants is extensive and has occurred via multiple mechanisms that preceded the divergence of monocots and dicots.
Transcriptional regulation in eukaryotes is orchestrated by a combination of trans-acting factors that recognize cis-DNA elements acting in concert with temporal and spatial variation in the chromatin environment of a gene. Factors determining the expression potential of the chromatin environment include DNA modifications, histone modifications, and the composition of associated proteins (Pirrotta, 1998  ; Cheung et al., 2000; Strahl and Allis, 2000; Jenuwein and Allis, 2001). Chromatin states are important for determining gene expression potential in developmental regulation and for epigenetic silencing. For example, mutants in several plant chromatin proteins have been identified on the basis of their effect on plant development (Goodrich et al., 1997; Grossniklaus et al., 1998; Luo et al., 1999; Ohad et al., 1999; Gendall et al., 2001; Kaya et al., 2001; Yoshida et al., 2001; Wagner and Meyerowitz, 2002). Mutations in chromatin proteins have also been shown to affect epigenetic silencing in plants (Finnegan et al., 1996; Ronemus et al., 1996; Jeddeloh et al., 1998; Lindroth et al., 2001). Although numerous examples exist of chromatin level control of gene expression in plants, the specific details of molecular mechanisms controlling plant chromatin states remain poorly understood. Histone modification is emerging as a central theme in the control of chromatin states across organisms.
The observation that a complex system of histone modifications is important in controlling chromatin state has led to the histone code hypothesis (Strahl and Allis, 2000
SET domain proteins have been found in chromatin-associated complexes that play a role in either promoting or inhibiting gene expression (Francis and Kingston, 2001
Biochemical evidence from a number of studies indicates that the SET domain proteins can methylate histones. Homologs of the SU(VAR)3-9 SET domain protein in mammals and Schizosaccharomyces pombe methylate the Lys-9 residue of histone H3 (Rea et al., 2000
Genetic studies have provided evidence that SET domain proteins are important for developmental and epigenetic regulation of gene expression. The PcG and trxG proteins act to stabilize transcriptional states during development. Mutations in SET domain proteins produce both PcG [E(z), Jones and Gelbart, 1990
In plants, two proteins containing an SET domain, CLF (CURLY LEAF) and MEA (MEDEA), were identified by the developmental phenotype associated with loss-of-function mutations (Goodrich et al., 1997 The objective of this study was to analyze SET domain-containing proteins from maize and Arabidopsis using phylogenetic analysis and interpretations based on protein organization. In our analysis, we included sequences representing all orthology groups of D. melanogaster, mouse (Mus musculus), and yeast SET domain proteins and 22 SET domain proteins from maize. The addition of another plant species and additional proteins from non-plant species, together with a thorough analysis of all domains in these proteins, revealed additional classes of SET domains in plants.
BLASTP and TBLASTN searches identified 32 proteins containing an SET domain and five proteins containing an interrupted S-ET domain in the Arabidopsis genome (Table I). The Arabidopsis SET domain proteins that we identified were the same as those reported by Baumbusch et al. (2001 ). We have determined an alternative annotation relative to the predicted annotation available at the GenBank accession for 14 of the Arabidopsis proteins based on cDNA sequences or alignments to other SET domain proteins (Table I), which was confirmed using RT-PCR, EST, or ortholog alignments. Twenty-five maize SET domain genes were identified through searches of EST databases. The sequences of 21 of these genes have been extended or completed by further sequencing of EST clones or through RACE analysis. Each of the proteins was assigned a name, SDGX, with X being a number assigned based on the order each gene was discovered. The existing synonyms are listed in Tables I and II. The Arabidopsis SET-domain containing proteins are labeled SDG followed by a number less than 100, and the maize SET proteins are labeled SDG followed by a number greater than 100. Sequence, expression, and map information for the maize and Arabidopsis SET domain genes are located at the ChromDB Web site (www.chromdb.org) and are updated regularly.
In addition to documenting a large family of plant proteins containing an intact SET domain, our analysis also revealed the presence of plant proteins containing a disrupted SET domain in which the N-terminal one-third of the SET domain is separated from the C-terminal two-thirds of the domain by 50 to 120 amino acids. Jenuwein and Allis (2001
We sought to classify the SET domain proteins of maize and Arabidopsis on the basis of phylogenetic analyses and domain organization. Thirty-one Arabidopsis, 19 maize, eight D. melanogaster, 12 mouse, and four yeast proteins were included in our phylogenetic analysis (SDG11 from Arabidopsis was not included because we could not align the full SDG domain; SDG108, SDG128 and SDG129 from maize were not included because we do not have sequence for the entire SET domain; none of the S-ET sequences were included from any species; in the first alignment, we used an additional six D. melanogaster and five mice genes that did not cluster with any of the plant groups within the analysis, and these sequences were removed for the final analysis). The SET domain of each protein, bounded by GWG on the N terminus and TYDY on the C terminus, was aligned using ClustalW (see Supplementary Fig. 1 at http://www.plantphysiol.org). The structure of four different SET domain proteins has been determined (Min et al., 2002
We divided the SET domain proteins of plants into five classes on the basis of this phylogenetic analysis and the domain organization of plant proteins within a clade (indicated in Fig. 2). Some classes, such as class I, contain plant and animal proteins that are conserved across all domains of the protein (data not shown). Other classes, such as class II, are conserved only in the SET domain, whereas the organization of domains outside of the SET domain in the plant proteins and the overall length of the protein are quite different from the most closely related animal proteins (Fig. 3). We have defined the presence of 19 putative orthology groups of SET domain genes in plants. The term orthology group will be used to refer to a group of proteins that are likely to have evolved from a single progenitor present in the last common ancestor of maize and Arabidopsis. These groups were inferred based upon the phylogenetic analysis in this study and relationships with sequences from other plant species. This more detailed level of evolutionary interpretation was possible relative to previous studies (Baumbusch et al., 2001
The class I SET domain proteins, which include the D. melanogaster PcG protein E(Z) and the Arabidopsis CLF (SDG1) and MEA (SDG5) proteins, have been well characterized in plants and animals. A limited expansion of class I proteins has occurred in plants, with two orthology groups of class I proteins present in both maize and Arabidopsis. A third type of class I SET domain protein, represented by MEDEA in Arabidopsis, has only been found in dicots to date (Springer et al., 2002
The sequence characteristics of the plant class I SET domain proteins have been previously described (Goodrich et al., 1997
On the basis of domain organization outside the SET domain, the proteins included in class II are a structurally diverse group, both between plant orthology groups and between plants and animals (Fig. 3). The animal proteins in class II include the D. melanogaster ASH1 (Tripoulas et al., 1994 Although the support for the clustering of all class II sequences was much lower than the support for other classes, there are several common features of the plant and animal class II SET domain proteins that make it logical to consider all of these sequences as a single class. All class II SET domain proteins (except SDG4) contain an AWS domain located just N terminal of the SET domain. The AWS domain is a subdomain of the PreSET domain that contains several highly conserved Cys residues. Another common feature of the plant and animal class II proteins is the location of the SET domain. In all other classes, the SET domain is found very near the C terminus of the protein, whereas the SET domain of class II proteins is more centrally located. The relationship of the SET domain location and common presence of AWS domains in plant and animal class II SET domain proteins suggests that they are likely to be related based on origin and function. The plant class II proteins were characterized based on overall structure and phylogenetic relationships generated from the SET domain (Fig. 3). Based on this analysis, there are four orthology groups of plant class II proteins. Orthology group II-1 proteins are relatively short (approximately 350 amino acids) and contain an SET domain along with AWS and PostSET domains (Fig. 3). The SDG7 and SDG24 genes are located in collinear duplicated regions of the Arabidopsis genome on chromosomes 2 and 3. The maize gene, Sdg110, is most closely related to SDG7 and SDG24 and contains a similar organization of domains (Fig. 3).
A single Arabidopsis sequence, SDG4, represents the second orthology group (II-2) of class II SET domain proteins. The SET domain of SDG4 is similar to the SET domains of orthology group II-1 proteins, but the N-terminal and C-terminal regions of the proteins are different. The N-terminal extension contains a PHD zinc finger domain. PHD domains are found in a number of chromatin-associated proteins and are thought to be involved in protein-protein interactions important in the assembly of multiprotein complexes (Aasland et al., 1995 Orthology group II-3 of the plant class II SET domain proteins includes SDG26 from Arabidopsis and SDG102 from maize. The SET and PostSET domains of orthology group II-3 proteins are located near the N terminus or in the middle of the protein (Fig. 3). The alignment of SDG8 and SDG102 shows significant conservation in an approximately 80-amino acid Cys-rich region located on the N-terminal side of the SET domain. The final orthology group of class II proteins is represented by SDG8, which is a long protein (1,767 amino acids) with both C- and N-terminal extensions relative to SDG26 and SDG102 (the C-terminal extension has been supported by EST data, whereas the N-terminal extension is based upon a predicted annotation). We were able to find a rice genomic sequence, AP004876, which is more closely related to SDG8 than it is to SDG102 or SDG26. It is likely that there is a maize gene belonging to orthology group II-4 that has not yet been detected by EST sequencing projects.
The class III SET domain proteins include the D. melanogaster TRX (TRITHORAX) and TRR (TRITHORAX-RELATED) proteins, the mouse HRX and MLL3-like proteins, and the yeast SET1 protein. Two Arabidopsis homologs of Trx were previously identified and named ATX1 (SDG27) and ATX2 (SDG30; Alvarez-Venegas and Avramova, 2001
Analysis of the plant class III SET domain proteins supports the existence of four orthology groups (Fig. 4). Orthology group III-1 includes SDG27 and SDG30, which both contain a similar arrangement of domains including a PWWP domain, an FYR domain (named DAST by Alvarez-Venegas and Avramova, 2001
We have documented the presence of a maize gene, Sdg128, which encodes a class III orthology group III-1 protein. Although the sequence is not currently complete, it does provide evidence for a maize member of group III-1. A second orthology group (III-2) of the class III plant SET domain proteins includes SDG14, SDG16, SDG29, and SDG115. The domain organization of these proteins is similar; they all contain a PWWP domain, two PHD domains, and a PostSET domain in addition to the SET domain (Fig. 4). SDG16 and SDG29 are located in collinear duplicated regions of Arabidopsis chromosomes 4 and 5. The maize gene Sdg106 is currently represented by a partial sequence. This sequence is closely related to both groups III-1 and III-2, and it is not currently possible to assign this gene to one orthology group.
The final two orthology groups (III-3 and III-4) of class III SET domain proteins found in plants are represented by SDG2 and SDG25 from Arabidopsis and SDG108 and SDG127 from maize. The yeast ScSET1 catalyzes histone H3 Lys-4 methylation (Briggs et al., 2001
Our phylogenetic analysis supports the existence of a class of SET domain proteins only present in yeast and plants. The class IV SET domain proteins include two proteins from Arabidopsis and two proteins from yeast (Fig. 2). These four SET domain proteins all contain an SET domain and a PHD domain (Fig. 5) but lack a PreSET or PostSET domain. A maize gene, Sdg129, which is related to the Arabidopsis SDG15 and SDG34 has been identified. The partial sequence obtained for SDG129 does not include the SET domain; therefore, this protein is not included in the phylogenetic analysis.
Null mutants for either ScSET3 or ScSET4 and the double mutant are viable (Pijnappel et al., 2001
The class V proteins are the largest group of SET domain proteins in plants. The D. melanogaster, mouse, and human genomes each contain two or three class V SET domain proteins compared with 15 in the Arabidopsis genome (Fig. 6). This is the only class of SET domain proteins that contains both PreSET and PostSET domains.
The PreSET domain is a Cys-rich putative Zn+-binding domain that is only found associated with SET domains. A partial PreSET domain (the AWS domain) is found in class II SET domain proteins, including ASH1 and NSD1. The PostSET domain is a small Cys-rich region often found at the C terminus of SET domains. To date, at least one member of each class of animal proteins containing both PreSET and- PostSET domains has been shown to be functional histone methyltransferase enzymes (Rea et al., 2000
The animal class V SET domain proteins can be divided into two groups based on domain structure. The SU(VAR)3-9 protein and mammalian homologs all contain a chromodomain near the N terminus. The G9a protein and a related D. melanogaster sequence (AAF45487) both contain ankyrin repeats. The domain organization of the plant class V SET domains is distinct from that of the animal proteins. None of the plant class V SET domain proteins contain a chromodomain or ankyrin repeats.
The orthology groups V-1, V-2, V-3, and V-5 are all YDG/PreSET/SET/PostSET domain proteins, whereas the orthology groups V-4, V-6, and V-7 all lack the YDG domain. The YDG domain is also referred to as a SET and RING-finger associated domain (SRA) (Baumbusch et al., 2001
Comparison of the maize and Arabidopsis class V SET domain proteins suggests that the amplification of class V proteins in plants occurred through duplication events both before and after the divergence of monocots and dicots (Fig. 6). The parsimonious analysis of class V SET domain proteins shown in Figure 6 supports the presence of at least seven class V orthology groups. In our analysis, we have chosen the minimum number of orthology groups, and it is likely that some of the groups we have designated as a single group may actually represent multiple orthology groups. The orthology groups V-1, V-2, V-3, and V-5 are all YDG/PreSET/SET/PostSET domain proteins, whereas the orthology groups V-4, V-6, and V-7 all lack the YDG domain.
Baumbusch et al. (2001
The majority of the maize SDG genes are constitutively expressed (Fig. 8). We tested the expression of 18 SDG genes by PCR of cDNA from eight different tissue sources. In all cases, one of the primers used was located in the 3'-untranslated region, which is expected to be more divergent than coding sequences and should allow for specific amplification of the target gene. Genomic controls were performed for all primers pairs and in every case except Sdg101, Sdg104, Sdg105, Sdg106, and Sdg113, the product amplified from genomic DNA was larger than that amplified from cDNA, indicating that the primers used flanked introns (data not shown). We did not detect any amplification products when two primer pairs specific for genomic DNA (one primer located within an intron) were used to test for genomic contamination of our cDNA (data not shown). Sdg101, Sdg102, Sdg105, Sdg106, Sdg107, Sdg108, Sdg110, Sdg113, Sdg116, Sdg117, Sdg118, Sdg119, Sdg124, Sdg125, and Sdg126 transcripts were detected in all tissues tested. Sdg103 transcripts were only detected in 3-DAP whole-kernel and 11-DAP whole-kernel tissues. The absence of products in 11-DAP endosperm tissue suggests that Sdg103 might be expressed specifically in embryo tissue. Sdg104 and Sdg115 transcripts were not detected in endosperm tissue.
We have characterized 25 expressed SET domain genes from maize and compared these sequences with the 32 SET domain proteins present in the Arabidopsis genome, 30 of which are expressed. Our phylogenetic analysis suggests that the plant SET domain proteins form five classes, and further domain analysis suggests these can be subdivided into 19 orthology groups. The presence of a larger number of SET domain proteins in plants relative to non-plant species results from SET domain protein duplication that occurred via multiple mechanisms. Importantly, the domains outside of the SET domain are often quite different from those found in animal SET domain proteins. The domains present in many of the plant SET domain proteins are predicted to play roles in mediating protein-protein interactions, indicating that the plant putative histone methyltransferases may act in complexes quite distinct from those found in animals and yeast. The significant difference between plant and animal SET proteins indicates that detailed biochemical characterization of plant chromatin remodeling complexes will be necessary to fully understand their unique function.
Plant SET domain genes show an increased degree of duplication relative to other organisms. For example, Arabidopsis contains 32 SET domain proteins, whereas D. melanogaster contains 14, mouse contains 17, and yeast contains four. The plant proteins have been divided into three class I orthology groups, four class II orthology groups, four class III orthology groups, one class IV orthology group, and seven class V orthology groups. The 19 orthology groups of SET domain proteins identified in plants are much larger than the nine orthology groups present in between D. melanogaster and mouse. This indicates that there was significant duplication and divergence of SET domain proteins in the plant lineage before the divergence of monocots and dicots. We identified at least one maize gene in 15 of the 19 orthology groups and detected a monocot homologs for two of the four other orthology groups. The barley (Hordeum vulgare) EST BG345006 belongs to orthology group II-2, and the barley ESTs AV915295 and AV920392 represent orthology group V-3. The presence of ESTs from monocot species for these orthology groups indicates that it is likely that an as yet uncharacterized maize representative for these orthology groups exists. We did not detect any ESTs from other plant species or any genomic sequences from rice representing the other two orthology groups, I-1 (represented by SDG5/MEA in Arabidopsis) and V-5 (represented by SDG9 in Arabidopsis). This could reflect the fact that these genes are expressed at very low levels or in specific tissues, or it could indicate that these are genes specific to Arabidopsis and close relatives.
Phylogenetic analyses of SET domain genes indicate that there have been numerous gene duplication events in plants. One type of duplication event that has occurred in both maize and Arabidopsis is the result of polyploidization or chromosome addition. In Arabidopsis, duplications consistent with ancient polyploid or chromosome duplication events include the SDG7/24, SDG27/30, and SDG16/29 pairs of genes found in collinear duplicated genomic regions (Baumbusch et al., 2001 A second type of duplication event is represented by related genes found in non-collinear regions, such as SDG15/34, SDG3/22, SDG17/21, SDG19/32, and SDG13/18 from Arabidopsis. These gene pairs are found in regions of the Arabidopsis genome not classified as collinear regions (http://mips.gsf.de/proj/thal/db/gv/rv/rv_frame.html). These duplications may have arisen from the same mechanisms that gave rise to the duplications found in the collinear region, followed by successive reorganizations. Alternatively, these duplications may have occurred via small-scale transposition or illegitimate recombination events.
The third type of duplication event of the plant SDG genes has occurred via a putative retrotransposition-like event (Baumbusch et al., 2001
The large number of conserved SET domain proteins in plants suggests that many of the products of gene duplication events have adopted distinct functions. When a gene duplication event occurs, both products must adopt at least partially nonoverlapping function or one will tend to be lost by mutation (Lynch and Conery, 2000
Several studies have documented that the SET domain is a histone methyltransferase motif in yeast and animals and that different SET domain proteins often display substrate preferences for specific Lys residues within histones H3 and H4 (Rea et al., 2000
Several of the animal class I proteins (Enhancer of zeste and homologs) have been shown to methylate predominately Lys-27 of histone H3 with a lower affinity for Lys-9 of histone H3 (Cao et al., 2002
Animal class II proteins that have been shown to encode functional histone methyltransferase enzymes include ScSET2 and ASH1 (Beisel et al., 2002
Several class III proteins, including ScSET1 and HRX, have been shown to encode functional histone methyltransferases (Briggs et al., 2001
The animal class V SET domain proteins, including SU(VAR)3-9 (Rea et al., 2000 The significant conservation within the SET domain suggests that many of the plant SET domain proteins will encode functional histone methyltransferase enzymes and that like the animal proteins, they may display substrate specificity for the modification of specific Lys residues present in histone tails. Further studies on the function of the SET domain and associated regions will provide a more detailed model for the exact biochemical modifications catalyzed by the plant SET proteins.
The majority of SET domain proteins characterized in animals are present in large protein complexes. The domains present in many of the plant SET domain proteins, such as the PHD, PWWP, and YDG domains, suggest that they are likely to be present in protein complexes also. The PHD domain is a putative zinc finger that is involved in mediating protein-protein interactions (Aasland et al., 1995 Many of the SET domain proteins in animals are present in large protein complexes. Although it is expected that some of these complexes will be conserved in plants, it is likely that many of the plant SET domain proteins will exist in complexes that are specific to plants. The class I and several class III plant proteins contain a domain structure very similar to related animal proteins, and these are predicted to exist in similar complexes as in animals. Other plant SET domain proteins do not contain any similarity to animal proteins outside of the SET domain; these will probably exist in complexes that are plant specific.
The duplication of SET domain proteins in plants may have required duplications of other interacting proteins, or it could be that the SET domain protein determines the specificity of a complex and a single complex can interact with multiple SET domain proteins. In some cases, there is evidence that the associated proteins have not undergone duplication. All three of the class I SET domain proteins from Arabidopsis, CLF, MEA, and EZA1, physically interact with the same protein, FIE (Luo et al., 2000
Although many of the basic mechanisms of chromatin-based regulation are conserved in plants and animals, the flexibility of these systems and the ability of these systems to respond to developmental and environmental cues is likely to be quite different in plants and animals. In animals, developmental decisions regarding gene expression and differentiation are complete at an early stage of development. Plants often switch developmental fates throughout their life cycle, especially to respond to environmental stimuli such as light, temperature, and water availability. The presence of a much larger family of SET domain proteins may allow plants more specific control of developmental decisions. The Su(z)12 homologs of Arabidopsis provide an example of amplification of a chromatin protein that has adopted specific functions in regulation of development. Arabidopsis encodes three Su(z)12 homologs, Fis2 (Fertilization independent seed 2), Emf2 (Embryonic flower 2), and Vrn2 (Vernalization 2; Luo et al., 1999 This study has further characterized the SET domain proteins of plants. Our analysis has suggested functional relationships between plant SET domain proteins that will be important for the interpretation of data from a model system, such as Arabidopsis, to other economically important crops, such as maize. The analysis presented in this paper will serve as a framework for ongoing functional analysis of this diverse group of proteins.
SET Domain Gene Discovery and Annotation in Arabidopsis
The Arabidopsis SET domain group (SDG) protein sequences used in this study were identified by nucleic acid and protein BLAST analysis using E(Z) (AAC46462), ASH1 (AAF49140), TRX (AAF55041), TRR (AAF45684), G9a like (AAF45487), and SU(VAR3-9) (CAB93768) as queries. The resulting Arabidopsis SDG domain proteins were then used to query the Arabidopsis genome to find other Arabidopsis proteins. These proteins are the same proteins identified by Baumbusch et al. (2001
The SET domain protein sequences from Arabidopsis were used to search all maize ESTs present in GenBank (last searched August 5, 2002). Putative SET domain proteins, identified by automated searching, were arbitrarily named SDG101 to SDG130. In some cases, further sequencing revealed that two ESTs actually corresponded to the same gene, and one name was dropped. We obtained full-length cDNA sequence for Sdg102 (BE345442) and Sdg105 (AW216196) by sequencing EST clones. Full-length sequence for Sdg104, Sdg110, Sdg113, and Sdg118 was obtained by RACE. RACE reactions were performed using the Marathon cDNA kit (CLONTECH, Palo Alto, CA) on cDNA produced from 10-day-old B73 seedlings. Advantage2 polymerase (CLONTECH) was used in the RACE reactions. The primers used in the RACE reactions were Set104R1 (5'-CCT CTG ATT GAC TGC AAC AGC CAC C-3') and Set104R2 (5'-GTG CGC ATG ACA CGA TAC TAA CAG CC-3') for Sdg104, Set110R1 (5'-CCA CAA TGA CAA ACC TGA GCT GCT CC-3') and Set110R2 (5'-TCC AAC CCT GGT CTC TCC ATC AAC AG-3') for Sdg110, Set113R1 (5'-GCT TTG CTC CCC TAT CAA TTC AGG TCC-3') and Set113R2 (5'-ATG AAC CAG CCC GTA TAG CGT CCC-3') for Sdg113, and Set118R1 (5'-CTG CCC AAG CGA TAA CCG TAG CC-3') and Set118R2 (5'-GGA GCT CAT GAC GCA CTG GAC G-3') for Sdg118. RACE products were gel purified and cloned into pCR-BluntII (Invitrogen, Carlsbad, CA). For Sdg101, Sdg103, Sdg106, Sdg107, Sdg108, Sdg114, Sdg115, Sdg116, and Sdg117 we have extended the EST sequence either by sequencing of EST clones or through RACE analysis. Because these sequences are not full length, they have not yet been submitted to GenBank but are publicly available at http://www.chromdb.org.
Many of the Arabidopsis class V SET domain genes are intron-less as first described by Baumbusch et al. (2001
The protein sequences of all SET domain proteins were analyzed for additional recognizable domains using NCBI-CD searches (http://ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi). The low-complexity filter was turned off, and the expect value was set at 1 to detect short domains or regions of less conservation in this analysis. Domains were not considered significant unless the alignment included more than 70% of the domain. All domains were referred to using the names present in the SMART domain database (Schultz et al., 2000
The complete group of nonredundant yeast (Saccharomyces cerevisiae), mouse (Mus musculus), and Drosophila melanogaster SET domain proteins were obtained using the SMART database (Schultz et al., 2000
Genomic DNA was purified from young leaves of the inbred lines B73 and Mo17 by CsCl centrifugation as described previously (Cone et al., 1986
RT-PCR was used to assess expression patterns because of the relatively low expression of the maize PcG homologs and because most of the genes were duplicated. Total RNA was extracted with Trizol (Invitrogen) from 10 tissues from the inbred B73 (endosperm [11 DAP], whole kernel [3 DAP], whole kernel [11 DAP], 10-d-old seedling [whole plant included], root tips, immature leaf [leaves three–five], mature leaf [fully expanded leaf 10], and meiotic tassel). One microgram of total RNA was used to make cDNA with the SMART cDNA synthesis kit according to the manufacturer's instructions (CLONTECH). PCR reactions were performed in a 25-µL total volume containing approximately 0.5 ng of cDNA, 5 pmol of each primer, 1 unit of Taq polymerase (Promega, Madison, WI), 2.5 µL of 10x reaction buffer, 2 µL of 25 mM MgCl2, and 0.3 µL of 25 mM dNTPs. Primers used for the RT-PCR reactions were Set101F1 (5'-CGC GGA CGA CCT AGG AAA ATT GAT ACC-3') and Set101R1 (5'-CAG CAA TTC CGG TGC ATA GTT CCA TC-3') for Sdg101, FLSet102F1 (5'-GTT CAG TCT TCA GAG CTG GGT TCG G-3') and Set102R2 (5'-GCT CTC CGT TTG GCT TCC TTC C-3') for Sdg102, Set103F2 (5'-GGA GCA GCG TTC ATT GAA GAT GAG-3') and FLSet103R1 (5'-CAG CAG CAT CTC GTG TCA TCA TCT AGG-3') for Sdg103, Set104F1 (5'-TGG GAC CAA CGT TTT CCG AGA CG-3') and Set104R1 (5'-CCT CTG ATT GAC TGC AAC AGC CAC C-3') for Sdg104, Set105F2 (5'-GCG GCT TCA AGG ATC CAT TTT GC-3') and Set105R2 (5'-GCA AGC AAA CGC TCT GGC ATC C-3') for Sdg105, Set106F1 (5'-CTT TTA TGG GCG ATG CGT GTC TC-3') and Set106R1 (5'-GCA GGG CTT TGA ACC ATT TAT GCG-3') for Sdg106, Set107F1 (5'-CTC TTA GAT GCT GGT TGG GGT CCT G-3') and Set107R2 (5'-GGA CCC CAA CCA GCA TCT AAG AGC AC-3') for Sdg107, Set108F1 (5'-GCA TGG AAA AAC AGG CAC AGA GAC C-3') and FLSet108R1 (5'-CTC CGC AAG GTA TGT AGG GAC TGG-3') for Sdg108, FLSet110F2 (5'-CGT CAC CCT TCG CCT AAA TCA CC-3') and Set110R1 (5'-CCA CAA TGA CAA ACC TGA GCT GCT CC-3') for Sdg110, Set113F3 (5'-GAT GGG GTT GCA ATC TGG AAG ATG-3') and Set113R2 (5'-ATG AAC CAG CCC GTA TAG CGT CCC-3') for Sdg113, Set115F1 (5'-GAG TAT CGC GGT GAG CTG GTC AG-3') and FLSet115R1 (5'-ACT GGC CGT AGT GAA TAC AAC TGT GG-3') for Sdg115, Set116F1 (5'-GAA GCG CGG AGA CGA CAC AAG G-3') and FLSet116R1 (5'-CTG TAA GCA GGA AAC ACA TGT CCA GC-3') for Sdg116, Set117F1 (5'-CAT GTA TTT GTG ACT CGT CCT GCC AG-3') and FLSet117R1 (5'-CTC GCC TAC GAA CAG AGC AGC C-3') for Sdg117, Set118F3 (5'-TGA GGA GGA CTG AAG ATC TGG ATG G-3') and FLSet118R1 (5'-ATC AAA ATG GAA ACA CAC TGC AGG TC-3') for Sdg118, Set119F1 (5'-GAA GTG TTG GAA TGT TGG CAA GAA GG-3') and Set119R1 (5'-GTC CGA GCA GCC GTT TGT ACA GTT G-3') for Sdg119, Mez1F1 (5'-GGG TGT GGT GAT GGT ACA TTG G-3') and Mez1R1 (5'-CGG GAC CTA ACT CTA CGG ATG G-3') for Sdg124, Mez2F8 (5'-CCC CTG TTT TGC AGC CAG TCG TGA-3') and Mez2R8 (5'-GGT GAG AGA AGG ATG CCT CGT CC-3') for Sdg125, Mez3F3 (5'-AGT ATG TGT TGG ATG CTT ATC GCA AGG-3') and Mez3R2 (5'-GGT TGT CAG TTT GTC ACC TTC CGA CC-3') for Sdg126, and Ubi1F1 (5'-TAA GCT GCC GAT GTG CCT GCG TCG-3') and Ubi1R1 (5'-CTG AAA GAC AGC ACA TAA TGA GCA CAG GC-3') for Ubiquitin. Conditions of the PCR were as follows: 94°C for 2 min, 35 cycles of 94°C for 30 s, 63°C for 30 s, 72°C for 2 min, followed by 72°C for 7 min. Amplified products were separated in a 1% (w/v) agarose Tris-borate/EDTA buffer gel and visualized by ethidium bromide staining.
We would like to thank Dean Bergstrom, Erin Guthrie, Sarah Kerns, Laura Schmitt, and Lyudmila Sidorenko for help with cloning and sequencing; Dean Bergstrom and Miriam Hankins for generating DNA gel-blot data; and Lewis Lukens for helpful discussions about phylogenetic analysis. Received October 30, 2002; returned for revision October 30, 2002; accepted February 11, 2003.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.102.013722.
1 This work was supported by the National Science Foundation (grant no. 9975930).
[w] The online version of this article contains Web-only data. The supplemental material is available at http://www.plantphysiol.org. * Corresponding author; e-mail smkaeppl{at}facstaff.wisc.edu; fax 608–262–5217.
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) and SET (*) domains are indicated above the alignment. Schematic diagrams of these proteins are shown below the alignment.
