Analyses of the oligopeptide transporter gene family in poplar and grape
© Cao et al; licensee BioMed Central Ltd. 2011
Received: 10 April 2011
Accepted: 26 September 2011
Published: 26 September 2011
Oligopeptide transporters (OPTs) are a group of membrane-localized proteins that have a broad range of substrate transport capabilities and that are thought to contribute to many biological processes. The OPT proteins belong to a small gene family in plants, which includes about 25 members in Arabidopsis and rice. However, no comprehensive study incorporating phylogeny, chromosomal location, gene structure, expression profiling, functional divergence and selective pressure analysis has been reported thus far for Populus and Vitis.
In the present study, a comprehensive analysis of the OPT gene family in Populus (P. trichocarpa) and Vitis (V. vinifera) was performed. A total of 20 and 18 full-length OPT genes have been identified in Populus and Vitis, respectively. Phylogenetic analyses indicate that these OPT genes consist of two classes that can be further subdivided into 11 groups. Gene structures are considerably conserved among the groups. The distribution of OPT genes was found to be non-random across chromosomes. A high proportion of the genes are preferentially clustered, indicating that tandem duplications may have contributed significantly to the expansion of the OPT gene family. Expression patterns based on our analyses of microarray data suggest that many OPT genes may be important in stress response and functional development of plants. Further analyses of functional divergence and adaptive evolution show that, while purifying selection may have been the main force driving the evolution of the OPTs, some of critical sites responsible for the functional divergence may have been under positive selection.
Overall, the data obtained from our investigation contribute to a better understanding of the complexity of the Populus and Vitis OPT gene family and of the function and evolution of the OPT gene family in higher plants.
Substrate transport is vital for all living organisms, and many transporters play important roles in this process. More than 600 transporter families are currently documented in the Transporter Classification Database (TCDB) [1, 2]. These protein families are further classed into seven subclasses (channels/pores, electrochemical potential-driver transporters, primary active transporters, group translocators, transport electron carriers, accessory factors involved in transport, and incompletely characterized transport systems). In general, they have specific localizations within the cell and are specialized to carry different compounds, including nitrate, phosphate, sucrose, amino acids, peptides, hormones or metals.
The peptide transporter family consists of electrochemical potential-driven transporters that catalyze uptake of their solutes by a cation-solute symport mechanism . In plants, peptide transporters can be classified into three distinct groups based on sequence similarity and mechanism of action, namely the ATP-binding cassette family, the peptide transporter family and the oligopeptide transporter (OPT) family. The plant ATP-binding cassette proteins use the energy generated by ATP hydrolysis to drive the transport of substrates such as peptides, metal chelates or glutathione conjugates . The peptide transporters have been shown to transport nitrate, and di- and tripeptides [5, 6]. Members of the OPT family were first characterized in yeast [7, 8], and since then they have also been found in archaea, bacteria and plants. Phylogenetic analyses of plant OPT members have revealed two distant clades: the yellow stripe-like (YSL) proteins and the OPTs. The YSL transporters are involved in metal homeostasis through the translocation of metal-chelates [9–16]. The OPT proteins likely do not have a common biological function and may be involved in four different processes: long-distance metal distribution , nitrogen mobilization [18–21], heavy metal sequestration [19, 21–23], and glutathione transport [19, 21, 22, 24]. These processes may play a role in plant growth and development [see  for review].
Structurally, OPT proteins are predicted to have about 16 transmembrane strands (TMS). Through detailed bioinformatic analyses of these transporters, Gomolplitinant and Saier  suggested that the 16-TMS proteins might have arisen from a 2-TMS precursor-encoding genetic element that was subject to three sequential duplication events. Since the transporters are predicted to function in peptide uptake, the expansion or fusion of the TMS might make excellent physiological sense in evolution.
The structural features or expression profiles of some OPT homologs have been partially described in Arabidopsis  and rice . Hoverer, there is much less information about this family in woody plant species such as Populus trichocarpa (poplar) and Vitis vinifera (grape). In the present study, we performed a genome-wide identification of OPT family genes in Populus and Vitis. Detailed analyses including sequence phylogeny, gene organization, conserved motifs, expression profiling, functional divergence and adaptive evolution were performed. Our results should provide a framework for further functional investigations on these genes.
Results and Discussion
Identification of the OPT gene family in Populus and Vitis
Oligopeptide transporter genes identified in Populus
No. of TMHs**
P: 11, N: 1, C: 1
P: 8, V: 3, E.R.: 2
P: 9, E.R.: 3, Ch: 2
P: 12, V: 1
P: 9, V: 3, E.R.: 2
P: 10, E.R.: 4
P: 9, V: 2, E.R.: 2
P: 8, G: 3, E.R.: 2
P: 9, C: 3, M: 1
P: 8, G: 3, V: 2
P: 10, E.R.: 2, V: 1
P: 6, Ch: 4, E.R.: 3
V: 8, P: 3, G: 2
P: 10, G: 2, V: 1
P: 8, V: 4, G: 2
P: 7, V: 4, G: 3
G:5, P:4.5, G:4.5, Ch:2, N:1, V:1
P: 8, V: 3, G: 2
Oligopeptide transporter genes identified in Vitis
No. of TMHs*
P: 12, C: 1
P: 12, V: 1.
P: 10, C: 2, V: 1
P: 10, E.R.: 3
P: 8, C: 3, E.R.: 2
P: 12, E.R.: 1
P: 7, V: 4, E.R.: 2
P: 7, C: 4, E.R.: 2
P: 8, E.R.: 4, V: 2
P: 9, V: 2, G: 2
P: 10, V: 2, E.R.: 2
P: 10, G: 2, V: 1
P: 9, V: 2, G: 2
V: 9, P: 4
P: 8, E.R.: 4, V: 2
P: 10, V: 2, E.R.: 2
Phylogenetic analyses, classification and functional relatedness of the OPT genes in Arabidopsis, rice, Populus and Vitis
Genes with same functions often are closely related and this has been confirmed in previous reports [18, 23, 31, 32]. Such a trend is also found in the OPT genes. For instances, Group 4 includes the AtYSL1 and AtYSL3 proteins, both of which are involved in metal ion homeostasis and the loading of metal ions in seeds [33, 34]. AtYSL1 and AtYSL3 proteins also have dual roles in reproduction: their activity in leaves is required for normal fertility and normal seed development, while their activity in inflorescences is required for proper loading of metals into seeds . Another member in this group, OsYSL2, has metal-nicotianamine transport activities in heterologous expression systems . AtOPT6, a member of Group 9, is able to transport glutathione derivatives and metal complexes under sulfur-deprived conditions and may be involved in stress resistance, whereas AtOPT7 of Group 8 is not involved in stress resistance [19, 21]. The high AtOPT6 expression reported in the vasculature of roots, stems and leaves also suggests that this protein is involved in long-distance peptide transport or distribution throughout the plant [19, 20].
Phylogenetic analyses can allow us to identify evolutionarily conservative and divergent OPT genes. Remarkably, Groups 1 and 2 do not include any Arabidopsis, Vitis or Populus OPT proteins but contain only proteins from rice. Likewise, Group 9 does not include any rice OPT proteins but contains only proteins from Populus, Vitis and Arabidopsis. It is possible that these groups have evolved after monocot-dicot divergence and that they have specialized roles in monocots or dicots. Our phylogenetic analyses also show that Groups 4 and 5 contain sequences from rice, Vitis and Populus but not from Arabidopsis, indicating that they were either acquired in rice, Vitis and Populus or lost in Arabidopsis. Although enormous evidences indicates that all these OPT genes encode membrane proteins that translocate their substrates from either the extracellular environment or an organelle into the cytosol, their exact functional roles are different [9–17, 19, 20]. The phylogenetic analyses conducted in our study may also provide potential support for their functional differentiation. Additional evidence supporting this notion comes from the tissue-specific expression profiling available on GENEVESTIGATOR  and the extremely different expression pattern of OPTs in rice (see additional file 1: Microarray based expression profiles of rice OPT genes across a variety of tissue or organs). For example, OsYSL15 is specifically highly expressed in rhizomes, suggesting a specific role in root development. While OsYSL1, OsYSL3, OsYSL4, OsYSL7, OsYSL8 and OsYSL11 show higher expression levels in pollen, indicating a key role in pollen development or reproduction.
Inference of duplication time in paralogous pairs
Data (million years ago)
Exon-intron evolution of the OPT family genes in Arabidopsis, rice, Populus and Vitis
To investigate the mechanisms of the structural evolution of OPT paralogs, we compared the exon-intron structure of individual OPT genes in Arabidopsis, rice, Populus and Vitis. Figure 1 provides a detailed illustration of the distribution and position of introns within each of the OPT paralogs. In general, the positions of some spliceosomal introns are conserved in orthologous genes from the four lineages. In many cases, not only is the intron position shared, but the intron phase is shared as well. Moreover, the conservation of the exon-intron organization or gene structure in paralogous genes is usually strong and sufficient to reveal evolutionary relationships of introns . It is clear that duplication plays an important role in the organization of genes and that intron losses have occurred frequently after segmental duplication . Our study of AtOPT6/AtOPT9 and OsOPT1/OsOPT8 duplication also suggests that this mechanism underlies the evolution of these paralogs and intron losses are associated with duplications (Figure 1). The phenomenon of intron loss following gene duplication also occurred in the evolution of many other genes including the aromatic amino acid hydroxylase (AAAH) family . In general, the structural diversity of gene family members provides a mechanism for the evolution of multiple gene families, while intron loss or gain can be an important step in generating structural diversity and complexity [45, 46]. In this study, we analyzed the structural diversity of OPT genes and found that intron loss/gain events occurred during the expansion and structural evolution of OPT paralogs. We found that most OPT genes in the same subgroups/clades have similar coding sequences and a very similar exon-intron structure, strongly supporting their close evolutionary relationship. The divergent gene structures in the different phylogenetic subgroups may represent gene family expansion from ancient paralogs or multiple origins of gene ancestry.
Chromosomal location of the OPT genes and duplication events in the genome
Gene duplication events are thought to have frequently occurred in organismal evolution [47, 48]. To investigate the relationship between the OPT genes and potential gene duplications within the genome, we also compared the locations of OPT genes in duplicated chromosomal blocks that were previously identified in Populus, Vitis, Arabidopsis and rice [41, 49–52]. The distribution of the OPT genes relative to the corresponding duplicated chromosomal blocks is illustrated in Populus (Figure 2), Vitis (Figure 3), Arabidopsis (see additional file 3: Chromosomal locations of the Arabidopsis OPT genes) and rice (see additional file 4: Chromosomal locations of the rice OPT genes). This result suggests that segmental duplication and transposition events are not the major factors that led to the expansion of the OPT gene family in the four higher plants. It may be that dynamic changes occurred following segmental duplication, leading to loss of many of the genes. Interestingly, we found that some OPT genes are located in tandem clusters on the chromosomes; examples are PtYSL1-PtYSL2, PtOPT8-PtOPT5, AtOPT9-AtOPT8, OsYSL7-OSYSL8, OsYSL2-OsYSL15, OsYSL9-OsYSL16, OsYSL3-OsYSL4, OsOPT2-OsOPT3 and VvOPT1-VvOPT2-VvOPT8 (Figure 2 and 3; see also additional file 3: Chromosomal locations of the Arabidopsis OPT genes and additional file 4: Chromosomal locations of the rice OPT genes). Further analyses indicate that most of the tandemly clustered OPT pairs share relatively high similarities (mostly above 70%). Thus, we propose that tandem duplications might have been an important factor governing the expansion of the OPT gene family in these species.
Conserved domains and motifs in OPT proteins
The major domains of the OPT proteins in Populus, Vitis, Arabidopsis and rice were identified using CDD, Pfam and SMART [27, 28]. Our results show that all OPT proteins in the four species possess only one characteristic and structurally conserved OPT domain essential for their transporter activity. While these tools are suitable for defining the presence or absence of recognizable domains, they are unable to recognize smaller individual motifs and more divergent patterns. Thus, we further used the program MEME  to study the diversification of OPT genes in Populus, Vitis, Arabidopsis and rice. Twenty distinct motifs were identified in these genes (Figure 1). Details of the 20 motifs are presented in additional file 5: Sequence logo and regular expression of the different motifs identified in the OPT gene family. As mentioned above, phylogenetic analyses broadly divided the OPT genes from the four higher plants into two major classes, the OPT class and the YSL class. Noticeably, most of the closely related members in each of these two main classes have common motif compositions, suggesting functional similarities among the OPT proteins within the same class (Figure 1). Most members of OPT class possess 14 motifs, while most members of YSL class have 9 motifs. Three of the motifs (motif 1, motif 2 and motif 7) are shared by all OPT proteins. Whether the motifs that are specific to the OPT class (motif 3, 4, 5, 9, 10, 12, 15, 16, 17, 18 and 19) or to the YSL class (motif 6, 8, 11, 13, 14 and 20) confer unique functional roles to the OPTs remains to be further investigated. In any case, the conserved motifs in the OPT proteins from the same class may provide additional support to results of the phylogenetic analyses. On the other hand, the divergence in motif composition among different classes may indicate that they are functionally diversified.
Differential expression profiles of the Populus and Vitis OPT genes
Duplicated genes may have different evolutionary fates , which can be indicated by divergence in their expression patterns. Because tandem duplications may have governed the expansion of the OPT gene family, we also investigated the expression profiles of the duplicated OPT gene pairs identified above in Populus and Vitis. Our results show that none of the gene pairs share similar expression patterns (Figure 4 and 5), indicating that substantial neofunctionalization may have occurred during the subsequent evolution of the duplicated genes. It seems that the expression patterns of the paralogs have diverged during long-term evolution, suggesting functional diversification of the duplicated genes [55–58]. Such a process may increase the adaptability of duplicated genes to environmental changes, thus conferring a possible evolutionary advantage.
Analysis of functional divergence
Functional divergence estimated in OPT paralogs
Class YSL/Class OPT
Group 2/Group 5
Group 2/Group 6
Group 2/Group 7
Group 2/Group 8
Group 2/Group 9
Group 2/Group 10
Group 2/Group 11
Group 4/Group 5
Group 4/Group 6
Group 4/Group 7
Group 4/Group 8
Group 4/Group 9
Group 4/Group 10
Group 4/Group 11
Group 5/Group 6
Group 5/Group 7
Group 5/Group 8
Group 5/Group 9
Group 5/Group 10
Group 5/Group 11
Group 6/Group 7
Group 6/Group 8
Group 6/Group 9
Group 6/Group 10
Group 6/Group 11
Group 7/Group 8
Group 7/Group 9
Group 7/Group 10
Group 7/Group 11
Group 8/Group 9
Group 8/Group 10
Group 8/Group 11
Group 9/Group 10
Group 9/Group 11
Group 10/Group 11
Variable selective pressures among amino acid sites
This study provides a comparative genome analysis addressing phylogeny, chromosomal location, gene structure, expression profiling, functional divergence and selective pressures of the OPT gene family in Populus and Vitis. Phylogenetic analyses revealed two well-supported classes in the OPT family, each of which can be further classified into 5 to 6 distinct groups. The exon/intron structure and motif compositions of the OPT genes and proteins are highly conserved in each class and in each of the groups, indicative of their functional conservation. The OPTs genes are non-randomly distributed across the Populus and Vitis chromosomes, and a high proportion of the OPT genes may be derived from tandem duplications. An additional comprehensive analysis of the expression profiles has provided insights into the possible functional divergence among members of the OPT gene family. Furthermore, functional divergence analyses suggest that significant site-specific selective constraints may have acted on most OPT paralogs after gene duplication, leading to subgroup-specific functional evolution. These data may provide valuable information for future functional investigations of this gene family.
Sequence retrieval and identification
To identify potential members of the OPT gene family in Populus and Vitis, we performed multiple database searches. Published Arabidopsis and rice OPT gene sequences [18, 23] were retrieved and used as queries in BLAST searches against the Poplar Genome database http://genome.jgj-psf.org and the Genoscope Grape Genome database http://www.cns.fr. BLAST searches were also performed against the Poplar and Grape genomes at National Center for Biotechnology Information (NCBI, http://www.ncbi.nlm.nih.gov) and Phytozome http://www.phytozome.net.
WoLF PSORT http://wolfpsort.org was used to predict protein subcellular localization. The TMHMM server http://www.cbs.dtu.dk/services/TMHMM/ was used to estimate the number of transmembrane helical domains. The isoelectric point (pI), molecular weight and grand average hydropathy (GRAVY) values were estimated using the ProtParam tool from ExPASy http://us.expasy.org/tools/protparam.html.
Phylogenetic analyses of the OPT gene family
Multiple sequence alignments of the full-length protein sequences were performed using MUSCLE 3.52 , followed by manual comparisons and refinement. Gaps and ambiguously aligned regions were removed before phylogenetic analyses. ModelGenerator  was used to determine the substitution model and rate heterogeneity that best fit the OPT protein data. Phylogenetic analyses were performed with a maximum likelihood method using PhyML 3.0  and a Bayesian inference method using PhyloBayes 3 . The LG model of protein sequence substitution  and four gamma rate categories, as determined by ModelGenerator, were used for both maximum likelihood and Bayesian analyses. Bootstrap analyses for maximum likelihood analyses were performed using 100 pseudoreplicates. For Bayesian analyses, two independent runs were carried out with default settings until a maxdiff value = 0.27 was achieved to ensure chain equilibration (4,300 generations). The first 100 points were discarded as burn-in, and the posterior consensus was computed on the remaining trees. The topology depicted in Figure 1 was generated using PhyML.
Inference of duplication time
Pairwise alignment of nucleotide sequences of the OPT paralogs was performed using MEGA 5 . Alignments were performed using ClustalW (codons). The K a and K s values of the paralogous genes were estimated by the program K-Estimator 6.0 . To better explain the patterns of macroevolution, estimates of the evolutionary rates were considered extremely useful. Assuming a molecular clock, the synonymous substitution rates (K s ) of the paralogous genes would be expected to be similar over time. Thus, K s could be used as the proxy for time to estimate the dates of the segmental duplication events. The K s value was calculated for each of the gene pairs and then used to calculate the approximate date of the duplication event (T = K s /2λ), assuming clock-like rates (λ) of synonymous substitution of 1.5 × 10-8 substitutions/synonymous site/year for Arabidopsis , 6.5 × 10-9 for rice , 9.1 × 10-9 for Populus , and 6.5 × 10-9 for Vitis .
Chromosomal location and gene structure of the OPT genes
The chromosomal locations of the OPT genes were determined using the Populus genome browser http://www.phytozome.net/poplar and Vitis genome browser http://www.genoscope.cns.fr/spip/Vitis-vinifera-e.html. Gene intron/extron structure information was collected from the genome annotations of Populus and Vitis from NCBI and Phytozome http://www.phytozome.net databases.
Conserved motifs analyses
The program MEME http://meme.sdsc.edu  was used to identify motifs in the candidate Populus and Vitis OPT protein sequences. MEME was run locally with the following parameters: number of repetitions = any, maximum number of motifs = 30, and with optimum motif widths constrained to between 6 and 200 residues.
The genome-wide microarray data of Populus published by Dharmawardhana and coworkers  were obtained from the NCBI Gene Expression Omnibus (GEO) with Accession Numbers GSE13043 and GSE21481. Probe sets corresponding to the putative Populus OPTs were identified on website http://genome.jgi-psf.org/. The microarray data for Vitis reported by Lund and coworkers  and Fennell  were obtained from GEO with Accession Numbers GSE11406 and GSE17502, respectively. The Plant Expression Database (PLEXdb, http://www.plexdb.org/index.php)  was also used for expression analyses. For genes with more than one set of probes, the median of expression values were used. Finally, the expression data were gene-wise normalized and hierarchically clustered based on Pearson coefficients with average linkage in the Genesis (version 1.7.6) program .
Functional divergence analyses
To estimate the level of functional divergence and to predict amino acid residues responsible for functional differences in the OPT subfamilies, the coefficients of type-I functional divergence were calculated using the method suggested by Gu et al. [59, 60]. The analyses were carried out with DINERGE (version 2.0). The method is based on maximum likelihood procedures to estimate significant changes in the site-specific shift of evolutionary rate or site-specific shift of amino acid properties after the emergence of two paralogous sequences. The advantage of this method is that it uses amino acid sequences and, therefore, is not sensitive to saturation of synonymous sites. Type-I functional divergence designates amino acid configurations that are highly conserved in gene 1 but highly variable in gene 2, or vice versa, implying that these residues have experienced altered functional constraints . Coefficients of functional divergence that are significantly greater than 0 indicate site-specific altered selective constraints or radical shifts of amino acid physiochemical properties after gene duplication. Site-specific posterior analysis was used to predict amino acid residues that were crucial for functional divergence .
Positive selection assessment
Identification of site-specific positive and purifying selection was calculated with the Selecton server http://selecton.tau.ac.il/, which uses a Bayesian inference approach for the evolutionary models [61, 76]. K a /K s values are used to estimate the two types of substitutions events by calculating the synonymous rate (K s ) and the non-synonymous rate (K a ), at each codon site. The server implements several evolutionary models that describe in probabilistic terms how characters evolve. In this study, two of the evolutionary models (M8 and M7) were used. Each of the models uses different biological assumptions so that different hypotheses can be tested and the model that best fits the data can be selected. Briefly, M8 allows for positive selection operating on the protein. A proportion p0 of the sites are drawn from a beta distribution (defined in the interval 0 ), and a proportion p1(= 1-p0) of the sites are drawn from an additional category ωs (defined to be ≥ 1). Thus, sites drawn from the beta distribution are sites experiencing purifying selection, whereas sites drawn from the ωs category are sites experiencing either neutral or positive selection. The M7 model is similar to M8, except that it assumes only a beta distribution with no additional category. Thus, it allows mainly for purifying selection in the protein. These models all assume a statistical distribution to account for heterogeneous K a /K s values among sites. The distributions are approximated using eight discrete categories and the K a /K s values are computed by calculating the expectation of the posterior distribution .
This project is partly supported by grants from the National Science Foundation of China (No. 30871704, and No.30971452) and the "100 Talents" Program of the Chinese Academy of Sciences to XH and from the National Science Foundation of China (No. 31100923) and Jiangsu University Senior Personnel Research Grants (10JDG027) to JC.
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