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MBE Advance Access originally published online on April 17, 2007
Molecular Biology and Evolution 2007 24(7):1458-1463; doi:10.1093/molbev/msm073
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Research Articles

Compensatory Change of Interacting Amino Acids in the Coevolution of Transcriptional Coactivator MBF1 and TATA-Box–Binding Protein

Qing-Xin Liu*,1, Naomi Nakashima-Kamimura{dagger},1, Kazuho Ikeo*, Susumu Hirose{dagger} and Takashi Gojobori*

* Center for Information Biology and DNA Data Bank of Japan, National Institute of Genetics, Mishima, Shizuoka, Japan
{dagger} Department of Developmental Genetics, National Institute of Genetics, Mishima, Shizuoka, Japan

E-mail: tgojobor{at}genes.nig.ac.jp.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Supplementary Material
 Acknowledgements
 References
 
To elucidate the transcriptional regulation in eukaryotic genome network, it is important to understand coevolution of transcription factors, transcriptional coactivators, and TATA-box–binding protein (TBP). In this study, coevolution of transcriptional coactivator multiprotein-bridging factor 1 and its interacting target TBP was first evaluated experimentally by examining if compensatory amino acid changes took place at interacting sites of both proteins. The experiments were conducted by identifying interaction sites and comparing the amino acids at these sites among different organisms. Here, we provide evidence for compensatory changes of transcription coactivator and its interacting target, presenting the 1st report that transcription coactivator may have undergone coevolution with TBP.

Key Words: compensatory change • coevolution • transcriptional coactivator • MBF1 • TBP


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Supplementary Material
 Acknowledgements
 References
 
Transcription factors are components of the regulatory network and are involved in multiple interactions with other proteins. Thus, the evolution of transcription factor families takes place within a framework defined by these interactions. Because the conserved domains within transcription factors often contain sites that mediate these interactions, their conservation most likely reflects the conservation of classes of interactions that were established early in evolution and under the limitations of tolerable (i.e., functional) changes. Many transcription factors have been evolutionarily conserved (Ge et al. 2002Go; Stevens et al. 2002Go; Taatjes et al. 2004Go; Bustamante et al. 2005Go); however, the evolutionary mechanism of transcription factors remains unclear. Multiprotein-bridging factor 1 (MBF1) is a transcriptional coactivator that mediates transcriptional activation by bridging a sequence-specific activator and TATA-box–binding protein (TBP) (Li et al. 1994Go; Takemaru et al. 1997Go, 1998Go; Liu et al. 2003Go; Jindra et al. 2004Go). Interaction between MBF1 and TBP is conserved from Archaea to humans (Aravind and Koonin 1999Go; Kabe et al. 1999Go; Millership et al. 2004Go). To understand the evolutionary mechanism of transcription coactivator, we have analyzed the evolution of MBF1 and TBP. Here, we examine whether coevolution can be evaluated by an experimental method in which we first identified interacting amino acids between 2 proteins and then carried out evolutionary analysis.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Supplementary Material
 Acknowledgements
 References
 
Polymerase Chain Reaction Mutagenesis
The tbp (TBP gene–containing mutations) library was made by error-prone polymerase chain reaction (PCR) as described (Lin-Goerke et al. 1997Go). In brief, the yeast TBP (yTBP) gene was amplified by PCR using Taq DNA polymerase in a reaction mixture containing 0.25 mM MnCl2. The PCR products were then purified and inserted into a YCplac22 vector, TRP1-marked plasmid.

Screening for tbp Genes
The Saccharomyces cerevisiae yeast strain used for screening was N107-1 (MATa ade2-1 ura3-1 trp1-1 leu2-3, 112 can1-100 {Delta}tbp::LEU2 [Ycplac33-yTBP]). This strain has chromosomal TBP gene deletion replaced by an URA3-marked plasmid carrying the TBP gene. The tbp library was transformed into N107-1 and spread onto plates with synthetic complete (SC) media but did not contain tryptophan. Strains expressing tbp were grown on 5-fluoroorotic acid (5-FOA) to remove plasmid-carrying TBP and then shifted to submaster plates either containing aminotriazole (AT) or not containing AT. We screened strains that were AT sensitive but showed normal growth.

Glutathione S-transferase Pull-Down Assay
Q68L and Q68I tbp genes were subcloned into 6HisT-pET11d to produce TBP proteins bearing 6 histidine residues in Escherichia coli. His-tagged recombinant proteins were purified using a Ni-column (Novagen, San Diego) and used for assay. The Glutathione S-transferase (GST) pull-down assay was performed using GST–MBF1 as described (Takemaru et al. 1998Go). Bound proteins were detected on western blots using an anti-TBP antibody.

Protein Sequence Analysis
All available sequences were obtained using the Entrez Protein database at National Center for Biotechnology Information (NCBI) (http://www.ncbi.nlm.nih.gov/). Accession numbers and species were compiled in a supplementary table S1 (Supplementary Material online). Protein-coding sequences were aligned using the ClustalX program (Thompson et al. 1997Go). All amino acid positions with gaps were excluded from this analysis. For phylogenetic reconstruction of TBP (Supplementary fig. 1, Supplementary Material online), the Neighbor-Joining method was used (Saitou and Nei 1987Go) with observed differences as implemented Njplot (Perriere and Gouy 1996Go). Bootstrap analysis with 1,000 replicates was used to assess the support for tree nodes (Felsenstein 1985Go). Phylogenetic distribution of interaction amino acids between MBF1 and TBP is based on phylogenetic analysis of full-length TBP sequences and recent studies (Hedges 2002Go).

Compensatory Change Analysis
The S. cerevisiae yeast strain used for compensatory change of interaction amino acid analysis was N111-4A (ade2-1 ura3-1 trp-1 leu2-3, 112 can1-100 {Delta}mbf1::LEU2 {Delta}tbp::LEU2 [yCplac33-TBP]). Ycplac22-TBP and Ycplac22-tbp mutant plasmids were transformed into N111-4A and spread onto plates with SC media but do not contain tryptophan. Strains expressing tbp were grown on 5-FOA to remove plasmid-carrying TBP. Ycplac33-MBF1 or Ycplac33-mbf1 mutant plasmids were then transformed into strains and spread onto plates with SC media but not contain Uracil. These strains were then shifted to submaster plates either containing AT or not containing AT. Point mutations of MBF1 and TBP were introduced by site-directed PCR mutagenesis.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Supplementary Material
 Acknowledgements
 References
 
Q68 of yTBP Is Required for yMBF1 Binding
MBF1 and TBP sequences are evolutionarily conserved from Archaea to humans (supplementary table S1, Supplementary Material online). To obtain evidence for the coevolution of MBF1 and TBP, we identified amino acids involved in the interaction between MBF1 and TBP in the yeast S. cerevisiae. It has been shown that D112 of yMBF1 is necessary for the yTBP binding (Takemaru et al. 1998Go) although the binding site in yTBP is not known. To identify the interaction site in yTBP, we constructed a yTBP mutant library and screened mutants that are defective in the yMBF1 binding. The yMBF1 mediated GCN4-dependent transcriptional activation that is essential for derepression of the amino acid biosynthesis genes (Takemaru et al. 1998Go). The disruptant of yMBF1 was sensitive to AT, an inhibitor of the HIS3 gene product. This sensitivity was also observed in the D112 yMBF1 mutant, indicating that interaction between yMBF1 and yTBP is required for the activation of HIS3 gene transcription. We therefore screened AT-sensitive TBP mutants and obtained 4 candidates, Q68L, Q68I, R79W, and T215S. Because TBP is a general transcription factor, mutations in a site involved in a general function (e.g., DNA binding site) reduce transcription of many genes, including HIS3 and showing AT sensitivity. To eliminate such mutations, we compared strain growth in AT-containing medium (cell requires General control non-depressible 4[GCN4] activity) and galactose-containing medium (cell requires Galactose 4 activity) and found that Q68 was a specific site for the GCN4-dependent transcriptional activation (data not shown). Q68L and Q68I mutants were viable in the absence of AT (fig. 1A) and able to grow on glucose, galactose, sucrose, or inositol-free media (Supplementary fig. 1, Supplementary Material online), indicating that these mutants can achieve most TBP functions and have not destructed the TBP structure. To confirm the interaction via Q68, we performed a GST pull-down assay using a series of bacterially expressed yTBP and GST–yMBF1 fusion proteins. GST pull-down assays with these purified proteins showed that wild-type yTBP and yMBF1 bind directly, but TBP harboring Q68I or Q68L mutation showed a significantly reduced capability of the binding to yMBF1 (fig. 1B). These results demonstrate that the amino acid Q68 is important for the yMBF1 binding. Whereas D112 of yMBF1 is present in the 3rd helix of the C-terminal domain, Q68 of yTBP is on top of the saddle-shaped molecule (fig. 1C).


Figure 1
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  		FIG. 1.— Analysis of yTBP mutants. (A) Q68 mutations show AT sensitivity. The {Delta}tbp strain, containing the wild-type (WT) TBP, Q68L tbp, or Q68I tbp gene, was streaked on plates in the presence or absence of 20 mM AT and incubated for 3 days at 30 °C. (B) Q68 is required for binding with MBF1. Bacterially expressed and purified WT yTBP (lanes 5 and 6), Q68L (lane 7), or Q68I (lane 8) was incubated with either GST (lane 5) or GST–MBF1 (lanes 6–8). The bound yTBP was electrophoresed by Sodium dodecyl sulfate–polyacrylamide gel electrophoresis and detected with an anti-TBP antibody. Lanes 1–4 were 1/10 of the input TBP or its mutants. (C) The structure of Bombyx mori MBF1 (residues 67–146) corresponds to 73–151 of yMBF1 (top) and the structure of yTBP (residues 61–240) and DNA (bottom). D112 of yMBF1 and Q68 of yTBP are indicated by arrows. H indicates the helix motif.

 
Alignment Analysis of MBF1 and TBP
To understand how interacting amino acids evolve, we next analyzed the sequences of MBF1 and TBP of various organisms (figs. 2 and 3). Archaeal MBF1 contains a Zn-ribbon motif that is absent in their eukaryotic counterparts. Eukaryotic MBF1 consists of 2 structural domains; a well-structured C-terminal half that binds to TBP and a flexible N-terminal half that participates in binding to various activators (Ozaki et al. 1999Go). Archaeal MBF1 harbors its own DNA-binding domain (Zn-ribbon motif, fig. 2) and hence serves for a single activator. In contrast, eukaryotic MBF1 does not directly bind to DNA but interacts with various activators. Eukaryotic MBF1 seems to lose a DNA-binding motif to accommodate a variety of activator partners. In Archaea, the amino acid of MBF1 corresponding to yMBF1 D112 is lysine, arginine, serine, or asparagine, but it changes to aspartic acid, glutamine, or glutamic acid in eukaryotes (fig. 2). In Archaea, the amino acid of TBP corresponding to yTBP Q68 is glutamic acid or glutamine, whereas it changes to histidine or glutamine in eukaryotes (fig. 3). Amino acid substitution in MBF1, therefore, appears to accompany the compensatory change in TBP to maintain MBF1–TBP interaction. These results strongly suggest the coevolution of MBF1 with TBP.


Figure 2
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  		FIG. 2.— Sequence alignment of MBF1 proteins. The Zn-ribbon motif is shown by red column. Bar represents a well-structured domain, {alpha}1–{alpha}4 denotes 4 amphipathic helices. The dot indicates the amino acid bound to TBP. The number below the dot shows the amino acid position of yMBF1.

 

Figure 3
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  		FIG. 3.— Sequence alignment of TBP proteins. Only the conserved C-terminal domain is shown. The dot indicates the amino acid bound to MBF1. The number below the dot shows the amino acid position of yTBP.

 
Compensatory Change Analysis In Vivo
To confirm the compensatory change of interacting amino acids, we did an in vivo analysis of interacting amino acids of MBF1 and TBP in the yeast S. cerevisiae. We made mutants of MBF1 and TBP according to the results of the evolutionary analysis (fig. 4; Supplementary fig. 2, Supplementary Material online). The mutants TBP-68Q, MBF1-112K and TBP-68E, MBF1-112D were sensitive to 3AT (fig. 5), indicating that the interactions between MBF1 and TBP were disrupted in these mutants. As expected from the evolutionary analysis (fig. 4), the mutants TBP-68Q, MBF1-112R; TBP-68E, MBF1-112R; TBP-68E, MBF1-112N; TBP-68H, MBF1-112E; and TBP-68E, MBF1-112K were resistant to AT (fig. 5). These results suggest that the compensatory change occurred and was selected from the neutral mutations during the evolution of MBF1 and TBP.


Figure 4
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  		FIG. 4.— Phylogenetic distribution of interacting amino acids of MBF1 and TBP. The cladogram of relationship is based on recent studies (Hedges 2002Go).

 

Figure 5
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  		FIG. 5.— Functional analysis of mutants in yeast. (A) Schematic illustration of mutants using this study, yeast wild type (68Q, 112D) as a control. (B and C) Growth of yeast strains in a synthetic medium without histidine in the presence (B) or in the absence (C) of the inhibitor 20 mM 3AT.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Supplementary Material
 Acknowledgements
 References
 
Coevolution of MBF1 and TBP
Coevolution is a process in which an inheritable change in one entity exerts selective pressure for a change in another entity. The coevolution of proteins has been well studied (Pazos et al. 1997Go; Goh et al. 2000Go; Goh and Cohen 2002Go; Ramani and Marcotte 2003Go). If the conformation of one protein is interrupted by a mutation, a compensatory change may be selected in its interacting partner. When such compensatory changes occur, this provides evidence of coevolution. In this study, we examined coevolution of transcription factor and coactivator for the first time and found that MBF1 coevolves with TBP. For Archaea, MBF1 binds to TBP through lysine, arginine, serine, or asparagine to glutamic acid interaction, or arginine–glutamine interaction. For protists, MBF1 binds to TBP through aspartic acid or glutamic acid to glutamine interaction, or glutamic acid–histidine interaction. For fungi, MBF1 binds to TBP through aspartic acid or glutamine to glutamine interaction. For plants, MBF1 binds to TBP through glutamic acid to glutamine interaction. For animals, MBF1 binds to TBP through glutamic acid or aspartic acid to glutamine interaction. As lysine does not interact with glutamine and aspartic acid does not interact with glutamic acid (fig. 5), our data indicates that an amino acid substitution in one protein results in giving selection pressure for a reciprocal change in the interacting partner. These findings suggest that a compensatory change of interacting amino acids were selected during the coevolution of MBF1 and TBP.

Why Is Interaction between MBF1 and TBP Conserved?
MBF1 is conserved among all organisms in which TBP is used as the general transcription factor. The coactivator is preserved even in a parasitic protozoan Cryptosporidium parvum where many essential genes are lost from its genome and their functions are supplied by the host counterparts (Abrahamsen et al. 2004Go). This study demonstrated the coevolution of MBF1 and the essential protein TBP. All these findings suggest the importance of MBF1. Nevertheless, null mutants of MBF1 are viable in both yeast and Drosophila under laboratory conditions. Does this contradict the neutral theory of evolution (Kimura 1955Go), which predicts the importance of conserved genes? The answer is no. Recently, studies revealed diverse biological function of MBF1. Yeast MBF1 supports the GCN4-dependent activation of the HIS3 gene (Takemaru et al. 1998Go), and Drosophila MBF1 serves as a coactivator of basic leucine Zipper protein Tracheae defective during morphogenesis of the tracheal and nervous systems (Liu et al. 2003Go). Drosophila MBF1 also interacts with AP-1 to preserve redox-dependent AP-1 activity during oxidative stress (Jindra et al. 2004Go). Rat MBF1 has been isolated as a calmodulin-associated peptide 19 (Smith et al. 1998Go), and human MBF1 has been identified as endothelial differentiation–related factor 1 (Mariotti et al. 2000Go). Tomato MBF1 is induced immediately and transiently in ethylene-treated late immature fruit (Zegzouti et al. 1999Go). Potato MBF1 is upregulated during fungal attack, upon wounding, and by treatment with salicylic acid and the ethylene precursor ethephon (Godoy et al. 2001Go). Tobacco MBF1 is induced by the combined effect of drought stress and heat shock (Rizhsky et al. 2002Go). Therefore, the interaction between MBF1 and TBP appears to be essential in the real world where organisms are subject to nutrient starvation and various kinds of stresses, and proper differentiation timing is critical for life.


   Supplementary Material
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Supplementary Material
Acknowledgements
 References
 
Supplementary table S1 and Supplementary figures 1 and 2 are available at Molecular Biology and Evolution online (http://www.mbe.oxfordjournals.org/).


   Acknowledgements
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Supplementary Material
 Acknowledgements
References
 
We thank Dr Naruya Saitou and Dr Yoshiyuki Suzuki for helpful discussions. This work was supported by Grants-in-aid for Scientific Research from the Ministry of Education, Science, Sports, Culture and Technology of Japan.


   Footnotes
 
1 Equal contribution to this work. Back

Yoko Satta, Associate Editor


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Supplementary Material
 Acknowledgements
 References
 

    Abrahamsen MS, Templeton TJ, Enomoto S, et al. Complete genome sequence of the Apicomplexan, Cryptosporidium parvum. Science (2004) 304:441–445. (20 co-authors).[Abstract/Free Full Text]

    Aravind L, Koonin EV. DNA-binding proteins and evolution of transcription regulation in the archaea. Nucleic Acids Res (1999) 27:4658–4670.[Abstract/Free Full Text]

    Bustamante CD, Fledel-Alon A, Williamson S, et al. Natural selection on protein-coding genes in the human genome. Nature (2005) 437:1153–1157. (14 co-authors).[CrossRef][Medline]

    Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution (1985) 39:738–791.

    Ge K, Guermah M, Yuan CX, Ito M, Wallberg AE, Spiegelman BM, Roeder RG. Transcription coactivator TRAP220 is required for PPAR2-stimulated adipogenesis. Nature (2002) 417:563–567.[CrossRef][Medline]

    Godoy AV, Zanetti ME, San SB, Casalongué CA. Identification of a putative Solanum tuberosum transcriptional coactivator up-regulated in potato tubers by Fusarium solani f. sp. eumartii infection and wounding. Physiol Plant (2001) 112:217–222.[CrossRef][Medline]

    Goh CS, Bogan AA, Joachimiak M, Walther D, Cohen FE. Co-evolution of proteins with their interaction partners. J Mol Biol (2000) 299:283–293.[CrossRef][ISI][Medline]

    Goh CS, Cohen FE. Co-evolutionary analysis reveals insights into protein–protein interactions. J Mol Biol (2002) 324:177–192.[CrossRef][ISI][Medline]

    Hedges SB. The origin and evolution of model organisms. Nat Rev Genet (2002) 3:838–849.[CrossRef][ISI][Medline]

    Jindra M, Gaziova I, Uhlirova M, Okabe M, Hiromi Y, Hirose S. Coactivator MBF1 preserves the redox-dependent AP-1 activity during oxidative stress in Drosophila. EMBO J (2004) 23:3538–3547.[CrossRef][ISI][Medline]

    Kabe Y, Goto M, Shima D, Imai T, Wada T, Morohashi K, Shirakawa M, Hirose S, Handa H. The role of human MBF1 as a transcriptional coactivator. J Biol Chem (1999) 274:34196–34202.[Abstract/Free Full Text]

    Kimura M. Solution of a process of random genetic drift with a continuous model. Proc Natl Acad Sci USA (1955) 41:144–150.[Free Full Text]

    Li FQ, Ueda H, Hirose S. Mediators of activation of fushi tarazu gene transcription by BmFTZ-F1. Mol Cell Biol (1994) 14:3013–3021.[Abstract/Free Full Text]

    Lin-Goerke JL, Robbins DJ, Burczak JD. PCR-based random mutagenesis using manganese and reduced dNTP concentration. Biotechniques (1997) 23:409–412.[ISI][Medline]

    Liu QX, Jindra M, Ueda H, Hiromi Y, Hirose S. Drosophila MBF1 is a co-activator for Tracheae Defective and contributes to the formation of tracheal and nervous systems. Development (2003) 130:719–728.[Abstract/Free Full Text]

    Mariotti M, De Benedictis L, Avon E, Maier JAM. Interaction between endothelial differentiation-related factor-1 and calmodulin in vitro and in vivo. J Biol Chem (2000) 275:24047–24051.[Abstract/Free Full Text]

    Millership JJ, Waghela P, Cai X, Cockerham A, Zhu G. Differential expression and interaction of transcription co-activator MBF1 with TATA-binding protein (TBP) in the apicomplexan Cryptosporidium parvum. Microbiology (2004) 150:1207–1213.[Abstract/Free Full Text]

    Ozaki J, Takemaru K, Ikegami T, Mishima M, Ueda H, Hirose S, Kabe Y, Handa H, Shirakawa M. Identification of the core domain and the secondary structure of the transcriptional coactivator MBF1. Genes Cells (1999) 4:415–424.[Abstract]

    Pazos F, Helmer-Citterich M, Ausiello G, Valencia A. Correlated mutations contain information about protein-protein interaction. J Mol Biol (1997) 271:511–523.[CrossRef][ISI][Medline]

    Perriere G, Gouy M. WWW-Query: an on-line retrieval system for biological sequence banks. Biochimie (1996) 78:364–369.[Medline]

    Ramani AK, Marcotte EM. Exploiting the co-evolution of interacting proteins to discover interaction specificity. J Mol Biol (2003) 327:273–284.[CrossRef][ISI][Medline]

    Rizhsky L, Liang H, Mittler R. The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol (2002) 130:1143–1151.[Abstract/Free Full Text]

    Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol (1987) 4:406–425.[Abstract]

    Smith ML, Johanson RA, Roger KE, Coleman PD, Slemmon JR. Identification of a neuronal calmodulin-binding peptide, CAP-19, containing an IQ motif. Brain Res Mol Brain Res (1998) 62:12–24.[Medline]

    Stevens JL, Cantin GT, Wang G, Shevchenko A, Shevchenko A, Berk AJ. Transcription control by E1A and MAP kinase pathway via Sur2 mediator subunit. Science (2002) 296:755–758.[Abstract/Free Full Text]

    Taatjes DJ, Marr MT, Tjian R. Regulatory diversity among metazoan co-activator complexes. Nat Rev Mol Cell Biol (2004) 5:403–410.[CrossRef][ISI][Medline]

    Takemaru K, Harashima S, Ueda H, Hirose S. Yeast coactivator MBF1 mediates GCN4-dependent transcriptional activation. Mol Cell Biol (1998) 18:4971–4976.[Abstract/Free Full Text]

    Takemaru K, Li FQ, Ueda H, Hirose S. Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci USA (1997) 94:7251–7256.[Abstract/Free Full Text]

    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res (1997) 25:4876–4882.[Abstract/Free Full Text]

    Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latch A, Pech JC, Bouzayen M. Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J (1999) 18:589–600.[CrossRef][ISI][Medline]

Accepted for publication March 15, 2007.


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