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GENOME ANALYSIS

Divergence of the Dof Gene Families in Poplar, Arabidopsis, and Rice Suggests Multiple Modes of Gene Evolution after Duplication^1,[W]

Department of Plant Sciences, University of Tennessee, Knoxville, Tennessee 37996 (X.Y., G.A.T., Z.-M.C.); and Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831 (X.Y., G.A.T.)

	ABSTRACT

TOP ABSTRACT RESULTS AND DISCUSSION CONCLUSION MATERIALS AND METHODS LITERATURE CITED

 
It is widely accepted that gene duplication is a primary source of genetic novelty. However, the evolutionary fate of duplicated genes remains largely unresolved. The classical Ohno's Duplication-Retention-Non/Neofunctionalization theory, and the recently proposed alternatives such as subfunctionalization or duplication-degeneration-complementation, and subneofunctionalization, each can explain one or more aspects of gene fate after duplication. Duplicated genes are also affected by epigenetic changes. We constructed a phylogenetic tree using Dof (DNA binding with one finger) protein sequences from poplar (Populus trichocarpa) Torr. & Gray ex Brayshaw, Arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). From the phylogenetic tree, we identified 27 pairs of paralogous Dof genes in the terminal nodes. Analysis of protein motif structure of the Dof paralogs and their ancestors revealed six different gene fates after gene duplication. Differential protein methylation was revealed between a pair of duplicated poplar Dof genes, which have identical motif structure and similar expression pattern, indicating that epigenetics is involved in evolution. Analysis of reverse transcription-PCR, massively parallel signature sequencing, and microarray data revealed that the paralogs differ in expression pattern. Furthermore, analysis of nonsynonymous and synonymous substitution rates indicated that divergence of the duplicated genes was driven by positive selection. About one-half of the motifs in Dof proteins were shared by non-Dof proteins in the three plants species, indicating that motif co-option may be one of the forces driving gene diversification. We provided evidence that the Ohno's Duplication-Retention-Non/Neofunctionalization, subfunctionalization/duplication-degeneration-complementation, and subneofunctionalization hypotheses are complementary with, not alternative to, each other.

Based on the above information, we hypothesized that both genetic and epigenetic changes are involved in the evolution of duplicated genes (Fig. 1 ). Genetic changes in proteins include retention (R), indicating that a copy retains the original motif organization and function; degeneration (D), indicating that a copy degenerates or loses one or more motifs and functions; and neofunctionalization (N), indicating that a copy acquires one or more motifs and functions. There are six possible combinations of these three types of genetic changes in coding regions for duplicated genes: RR, RD, RN, DD, NN, and ND. Epigenetic changes in proteins (i.e. protein methylation) or in promoter regions (i.e. DNA methylation) can cause functional diversification in duplicated genes that share the same motif structure and change them from RR into RD or DD type. RD and RN correspond to Ohno's hypothesis (Ohno, 1970), DD corresponds to the SF or DDC model (Hughes, 1994; Force et al., 1999), and NN corresponds to the SNF model (He and Zhang, 2005b). We consider that gene function consists of both protein function conferred by the coding region, as suggested by Hughes (1994), and the pattern of gene expression mostly controlled by regulatory elements, as suggested by Force et al. (1999).

View larger version (15K): [in this window] [in a new window]   Figure 1. Possible evolutionary modes of paralogs in the protein coding region after gene duplication.

	RESULTS AND DISCUSSION

TOP ABSTRACT RESULTS AND DISCUSSION CONCLUSION MATERIALS AND METHODS LITERATURE CITED

 

The Dof Gene Family and Conservative Motifs in the Dof Proteins

Using the 66 Dof protein sequences from Arabidopsis and rice to query the recently sequenced poplar genome, we identified 41 poplar Dof genes (Supplemental Table S1) and manually verified their uniqueness. These genes were analyzed along with the 36 and 30 Dof genes from Arabidopsis and rice, respectively (Supplemental Table S1).

A total of 41 conserved motifs were identified in all 107 Dof protein sequences (Table I ). The motif 1 was identified to be the Dof domain using the Conserved Domain Search Service (Marchler-Bauer and Bryant, 2004). Although many motifs are shared by poplar, Arabidopsis, and rice, species-specific motifs were also found (motifs 18, 20, 25, 33, and 37 in poplar and 36 in Arabidopsis; Supplemental Table S2). We also found two motifs (17 and 29) shared by rice and poplar only, one (34) shared by rice and Arabidopsis only, and three (12, 23, and 28) shared by Arabidopsis and poplar only (eudicot specific; Supplemental Table S2). In addition, several motifs were commonly linked (e.g. 8, 2, and 3). These results suggest that motif acquisition/divergence had continued to occur in poplar, Arabidopsis, and rice after the monocot/eudicot split and the eurosids I/eurosids II split.

We constructed a maximum-likelihood phylogenetic tree using full-length protein sequences of the Dof genes (Fig. 2 ). From the phylogenetic tree, we identified 27 pairs of paralogous genes in the terminal nodes, which were well supported by bootstrap analysis. We predicted the immediate ancestral protein sequences of the 27 pairs of paralogs and identified protein motif structure of the duplicated genes and their ancestors (Fig. 3 ).

View larger version (14K): [in this window] [in a new window]   Figure 2. Phylogenetic analysis of full-length protein sequences of 107 Dof genes in poplar, Arabidopsis, and rice. Two maize Dof proteins, Dof1 (GenBank accession no. CAA46875) and Dof2 (CAA56287), were also included to validate the tree topology. Maximum-likelihood tree was built using 100 bootstrap replicates.

View larger version (46K): [in this window] [in a new window]   Figure 3. Motif structure of gene duplicates located in the terminals of the phylogenetic tree in Figure 2 and their ancestors. Boxes labeled with numbers are protein motifs.

All of the six evolutionary outcomes resulted from genetic changes (Fig. 1) that existed in the 27 Dof paralogs (Table II ), and there were 10 RR, six RN, two RD, three NN, three DN, and three DD evolutionary outcomes. According to Ohno's hypothesis (Ohno, 1970), there are two potential fates of duplicated genes equivalent to RD and RN. However, these types of gene fates (two RD + six RN) account for only 30% of the 27 pairs of Dof paralogs. According to the DDC model (Force et al., 1999), there are three potential fates equivalent to DD, RD, and DN, respectively. However, these types of gene fates (three DD + two RD + three DN) account for only 30% of the 27 pairs of paralogs. According to the SNF model (He and Zhang, 2005b), there are three potential fates of duplicate gene pairs equivalent to NN, DD, and RN, respectively. However, these types of gene fates (three NN + three DD + six RN) account for only 44% of the 27 pairs of paralogs. These results indicate that none of the three existing hypotheses (Ohno, DDC, and SNF) could explain the majority (50%) of the genetic changes in the coding region of the Dof paralogs. Although some proteins evolved following the DDC model, such as hemoglobin (Hughes, 2005) and the tRNA endonucleases in the hyperthermophilic, sulfate-reducing Archaeoglobus fulgidus and the thermophilic, methane-producing Methanococcus jannaschii (Tocchini-Valentini et al., 2005), we found only three typical DDC cases (DD type) in the coding regions of the Dof paralogs (Table II). Recently, He and Zhang (2005a) reported that duplicate genes in yeast generally have longer protein sequences and more functional domains than singleton genes. Therefore, we suggest that DDC is not a major route for protein sequence evolution after gene duplication.

View larger version (10K): [in this window] [in a new window]   Figure 4. The synonymous substitution rate (ks) of different gene fate categories. Values shown represent the average ± 95% confidence interval.

View larger version (50K): [in this window] [in a new window]   Figure 5. Expression of Dof duplicates in poplar revealed by RT-PCR analysis. 18S rRNA was used as an internal standard.

View larger version (64K): [in this window] [in a new window]   Figure 6. Expression of Dof duplicates in Arabidopsis revealed by analysis of microarray data using GENEVESTIGATOR (Zimmermann et al., 2004). All gene-level profiles were normalized for coloring such that for each gene the highest signal intensity obtains value 100% (dark) and absence of signal obtains value 0% (white).

View larger version (96K): [in this window] [in a new window]   Figure 7. Comparative analysis of the 1,000-bp region upstream of the translation start codon (ATG) of the RR paralogs. Solid dark lines connect similar regions and gray broken lines connect matched regions in reversed orientation.

To explore whether Darwinian positive selection was involved in driving gene divergence after duplication, we calculated the nonsynonymous/synonymous substitution ratio (k_a/k_s) for the coding region of some recently duplicated paralogs using a sliding window of 20 amino acids. Generally, a k_a:k_s ratio > 1 indicates positive selection, a ratio < 1 indicates negative or purifying selection, and a ratio = 1 indicates neutral evolution (Wang et al., 2005). For the Dof paralogs, k_a:k_s ratios were always near zero for motif 1, the conserved Dof domain, suggesting strong purifying selection on this motif. In contrast, much higher k_a:k_s ratios were generally found in the regions outside the motif 1, especially in the intermotif regions (Fig. 8 ). Such positive selections have also been observed in the RLK/Pelle gene family in Arabidopsis and rice (Shiu et al., 2004). A higher proportion of new exons had k_a:k_s ratios > 1 and a higher frequency of insertions/deletions (indels) than did the old exons, implying that positive selection played an important role in the evolution of new domains (Wang et al., 2005). Therefore, positive selection is one of the major driving forces for the emergence of new motifs/functions in protein after gene duplication.

View larger version (37K): [in this window] [in a new window]   Figure 8. The nonsynonymous to synonymous substitution ratio (ka:ks) for the coding region of several recently duplicated paralogs with a sliding window of 20 amino acids and a step size of 10 amino acids. Boxes labeled with numbers are protein motifs.

View larger version (15K): [in this window] [in a new window]   Figure 9. Methylation sites (indicated by arrows) predicted in RR paralogs suggest epigenetic divergence. Boxes labeled with numbers are protein motifs. The ruler indicates the size of the proteins in amino acids.

To investigate possible involvement of epigenetic changes, we performed computer prediction of potential methylation sites in protein sequences of duplicated poplar genes (RR) that share the same motif structure. Our analysis revealed two Arg methylation sites within the motif regions in Ptr_DOF14, whereas another copy of the duplicate, Ptr_DOF04, does not have the methylation sites (Fig. 9). It is interesting that the expression pattern of Ptr_DOF04 is very similar to that of Ptr_DOF14 (Fig. 5). Because Ptr_DOF04 and Ptr_DOF14 are similar in terms of expression and protein motif structure, we suggest that the diversification of these two genes resulted from epigenetic changes such as Arg methylation. It has been reported that Arg methylation plays important roles in RNA processing, transcriptional regulation, and signal transduction (Bedford and Richard, 2005; Boisvert et al., 2005; Chen et al., 2006). Arg methylation has been observed on a variety of proteins associated with gene regulation, including DNA-binding transcriptional activators, transcriptional coactivators, and many RNA-binding proteins involved in RNA processing, transport, and stability (Lee et al., 2005). Experiments need to be done to confirm the predicted methylation and to investigate its effect on protein function.

In spite of the aforementioned possibility that sequence difference in the promoter regions accounts for the expression difference between duplicated genes (Table III; Figs. 5 and 6), it is still possible that epigenetics plays a role in expression diversification of these genes.

	CONCLUSION

TOP ABSTRACT RESULTS AND DISCUSSION CONCLUSION MATERIALS AND METHODS LITERATURE CITED

 
Our results show that the duplication and subsequent divergence of the Dof gene family in three plant species do not fit Onho's classical DRNNF model, or the more recently proposed alternatives SF/DDC or SNF alone, in terms of gene functions conferred by the coding regions. We conclude that the existing models are complementary with, not alternative to, one another. We anticipate that the six gene fates (RR, RD, RN, DD, NN, and ND) may also fit other gene families at variable ratios among them. We also suggest that epigenetics may play an important role in gene diversification after duplication. Based on our analysis of the Dof gene families in poplar, Arabidopsis, and rice, we also conclude that after a gene duplication event, the evolution of the duplicated genes is driven by purifying selection, Darwinian positive selection, local duplication and translocations, and domain co-option. The divergent expression may also be affected by epigenetic regulations.

	MATERIALS AND METHODS

TOP ABSTRACT RESULTS AND DISCUSSION CONCLUSION MATERIALS AND METHODS LITERATURE CITED

 

Sequences

The Arabidopsis (Arabidopsis thaliana) Dof gene name list was obtained from two Arabidopsis transcription factor databases (http://Arabidopsis.med.ohio-state.edu/AtTFDB/ and http://datf.cbi.pku.edu.cn). The corresponding coding and protein sequences were downloaded from http://www.arabidopsis.org/ (The Institute for Genomic Research [TIGR] annotation release 5). The 5' end of AT5G62430 was found truncated and it was corrected according to http://datf.cbi.pku.edu.cn. The rice (Oryza sativa) Dof gene name list was obtained from http://ricetfdb.bio.uni-potsdam.de/ and the corresponding coding and protein sequences were downloaded from http://www.tigr.org/ (TIGR rice pseudomolecules release 3). Os03g42200 was manually corrected. The 5' end of Os07g48570 was found truncated after searching the expressed sequence tag database and was corrected according to http://ricetfdb.bio.uni-potsdam.de/. 9640.m03713 in TIGR rice pseudomolecules release 2 was assigned as Os12g38200 in TIGR rice pseudomolecules release 3. The sequence of Os12g38200 was found to be incorrect and was replaced by the sequence of 9640.m03713, which was confirmed by examining the pseudomolecules of the rice genome (Build 4.0) released recently by The International Rice Genome Sequencing Project (International Rice Genome Sequencing Project, 2005). To obtain populus Dof gene sequences, Arabidopsis and rice Dof protein sequences were used to search the populus genome annotation (http://genome.jgi-psf.org/Poptr1/Poptr1.home.html) using tBLASTn (Altschul et al., 1990). Pt_DOF15, Pt_DOF27, and Pt_DOF29 were found to be 3' truncated and were manually corrected.

k_s and k_a Calculations

Pairwise alignments of the paralogous nucleotide sequences were made using ClustalW (Thompson et al., 1994), with the corresponding protein sequences as the alignment guides. Gaps in the alignments were removed. k_s (synonymous substitution rate) and k_a (nonsynonymous substitution rate) analysis was carried out using the K-Estimator program (Comeron, 1999).

Tree Construction

A multiple alignment analysis was performed with M-Coffee (Wallace et al., 2006). Phylogeny was created by maximum-likelihood analysis using PHYML (Guindon and Gascuel, 2003) with protein model JTT+I+G, which was selected by modelGenerator (Keane et al., 2006). Bootstrap analysis of 100 replicates was then performed, and the consensus tree was then displayed with bootstrap values.

Prediction of Ancestral Protein Sequences

Gapped Ancestral Sequence Prediction (Edwards and Shields, 2004) was used to predict ancestral sequences from phylogenetic trees and the corresponding multiple sequence alignments. The input tree was unrooted and it was rooted automatically by midpoint rooting in Gapped Ancestral Sequence Prediction analysis.

Motif Identification

Protein motifs of the Dof genes were identified statistically using MEME (Bailey and Elkan, 1994) with motif length set as 6 to 200, motif sites 2 to 107, and e value < 1 x 10^–10. The MAST program (Bailey and Gribskov, 1998) was used to search protein motifs of the extant Dof proteins in non-Dof genes as well as the ancestral Dof protein sequences. The motifs were further characterized using the Conserved Domain Search Service (Marchler-Bauer and Bryant, 2004).

Gene Expression

The tissue-specific expression analysis of Arabidopsis genes was performed using Meta-Analyzer in GENEVESTIGATOR (Zimmermann et al., 2004) with ATH1-22k array. The tissue-specific expression data of rice genes were obtained from the MPSS database (20-bp signatures; http://mpss.udel.edu/rice/?).

For multiple-tissue RT-PCR analysis of gene expression in poplar (Populus trichocarpa) "Nisqually-1," stem and leaf tissues were taken from plants grown in vitro on media containing Murashige and Skoog salts (Murashige and Skoog, 1962), 3% Suc, and 0.25% Gelrite (PhytoTechnology Laboratories) at 23°C ± 1°C under cool-white fluorescent light (approximately 125 µmol m^–2 s^–1, 16-h photoperiod). Root, shoot tip, petiole, and bark tissues were taken from plants grown in a greenhouse in Knoxville, TN, under natural lighting and temperatures ranging from 25°C to 35°C. Total RNA was extracted from root, stem, shoot tip, petiole, leaf, and bark using the Spectrum Plant Total RNA kit (Sigma-Aldrich) and then treated with AMPD1 DNase I (Sigma-Aldrich) to eliminate DNA, according to the manufacturer's instructions. RNA purity was determined spectrophotometrically, and quality was determined by examining rRNA bands on agarose gels. cDNA was synthesized from 2 µg of RNA using the PowerScript PrePrimed Single Shots with random hexamers as primer (CLONTECH Laboratories) in a 20-µL reaction. For PCR reactions using gene-specific primers (Supplemental Table S3), the cDNA was diluted 50-fold, and 2.0 µL was used for a 20-µL PCR reaction. For PCR reactions using 18S rRNA-specific primers (QuantumRNA Universal 18S Internal Standard; Ambion), the cDNA was diluted 20,000 times, and 2.0 µL was used for a 20-µL PCR reaction containing 0.5 units TaKaRa Taq HS (Takara Mirus Bio), 1x PCR buffer, 200 µM of each dNTP, and 0.5 µM of each gene-specific primer (or 0.25 µM of 18S rRNA-specific primers). PCR was performed as follows: one round at 94°C for 2 min; 35 cycles: 94°C for 30 s, 60°C for 30 s, 72°C for 1 min; and a final step at 72°C for 7 min. The amplified products (18 µL each) were separated on a 1% agarose gel, stained with ethidium bromide, and documented with Gel Doc 2000 (Bio-Rad).

Comparative Analysis of Promoter Sequences

Comparative analysis of the 1,000-bp region upstream of the translation start codon (ATG) was performed using the GATA program (Nix and Eisen, 2005), with window size of 7 and lower cutoff score of 12 bit.

Protein Methylation Prediction

Protein sequence alignment was performed with M-Coffee (Wallace et al., 2006). Protein methylation prediction was performed with the MeMo Web server (Chen et al., 2006).

Sequence data from this article can be found in the GenBank/EMBL data libraries under accession numbers CAA46875 (Dof1) and CAA56287 (Dof2).

Supplemental Data

The following materials are available in the online version of this article.

Supplemental Table S1. Dof gene list in Arabidopsis, rice, and poplar.

Supplemental Table S2. Summary of motif distributions.

Supplemental Table S3. Primers for RT-PCR.

	ACKNOWLEDGMENTS

 
We thank F. Chen and R.C. Moore for reviewing the manuscript and valuable comments. We also thank the anonymous reviewers for the inspiring comments on the manuscript.

Received May 15, 2006; accepted August 26, 2006; published September 15, 2006.

	FOOTNOTES

 
¹ This work was supported by the National Science Foundation (grant no. 0421743 to G.A.T. and Z.-M.C.), by the U.S. Department of Energy/Oak Ridge National Laboratory (subcontract to Z.-M.C.), and by the Tennessee Agricultural Experiment Station.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: (Max) Zong-Ming Cheng (zcheng{at}utk.edu).

^[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.106.083642

^* Corresponding author; e-mail zcheng{at}utk.edu; fax 865–974–5365.

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