Extensive Functional Diversification of the Populus Glutathione S-Transferase Supergene Family[C][W]

Identifying how genes and their functions evolve after duplication is central to understanding gene family radiation. In this study, we systematically examined the functional diversification of the glutathione S-transferase (GST) gene family in Populus trichocarpa by integrating phylogeny, expression, substrate specificity, and enzyme kinetic data. GSTs are ubiquitous proteins in plants that play important roles in stress tolerance and detoxification metabolism. Genome annotation identified 81 GST genes in Populus that were divided into eight classes with distinct divergence in their evolutionary rate, gene structure, expression responses to abiotic stressors, and enzymatic properties of encoded proteins. In addition, when all the functional parameters were examined, clear divergence was observed within tandem clusters and between paralogous gene pairs, suggesting that subfunctionalization has taken place among duplicate genes. The two domains of GST proteins appear to have evolved under differential selective pressures. The C-terminal domain seems to have been subject to more relaxed functional constraints or divergent directional selection, which may have allowed rapid changes in substrate specificity, affinity, and activity, while maintaining the primary function of the enzyme. Our findings shed light on mechanisms that facilitate the retention of duplicate genes, which can result in a large gene family with a broad substrate spectrum and a wide range of reactivity toward different substrates.

[1]  T. Mantle,et al.  Glutathione S-transferases. , 1990, Biochemical Society transactions.

[2]  Blake C. Meyers,et al.  Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009308. , 2003, The Plant Cell Online.

[3]  Xavier Deupi,et al.  Conformational complexity of G-protein-coupled receptors. , 2007, Trends in pharmacological sciences.

[4]  W B Jakoby,et al.  Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. , 1974, The Journal of biological chemistry.

[5]  A. Oakley Glutathione transferases: new functions. , 2005, Current opinion in structural biology.

[6]  Ziheng Yang PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[7]  Josep M. Comeron,et al.  K-Estimator: calculation of the number of nucleotide substitutions per site and the confidence intervals , 1999, Bioinform..

[8]  M. G. Jeppesen,et al.  The Crystal Structure of the Glutathione S-Transferase-like Domain of Elongation Factor 1Bγ from Saccharomyces cerevisiae* , 2003, Journal of Biological Chemistry.

[9]  V. Walbot,et al.  AN9, a petunia glutathione S-transferase required for anthocyanin sequestration, is a flavonoid-binding protein. , 2000, Plant physiology.

[10]  J. W. Thornton,et al.  Evolution of a New Function by Degenerative Mutation in Cephalochordate Steroid Receptors , 2008, PLoS genetics.

[11]  Dmitri A. Petrov,et al.  Pervasive and Persistent Redundancy among Duplicated Genes in Yeast , 2008, PLoS genetics.

[12]  S. Chin,et al.  Human and mouse oligonucleotide-based array CGH , 2005, Nucleic acids research.

[13]  Wen-Hsiung Li,et al.  Patterns of expansion and expression divergence in the plant polygalacturonase gene family , 2006, Genome Biology.

[14]  C. Jang,et al.  Expression diversity and evolutionary dynamics of rice duplicate genes , 2009, Molecular Genetics and Genomics.

[15]  K. Uchida,et al.  Glutathione and a UV Light–Induced Glutathione S-Transferase Are Involved in Signaling to Chalcone Synthase in Cell Cultures , 2000, Plant Cell.

[16]  Richard C. Moore,et al.  The evolutionary dynamics of plant duplicate genes. , 2005, Current opinion in plant biology.

[17]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[18]  Kousuke Hanada,et al.  Large-Scale, Lineage-Specific Expansion of a Bric-a-Brac/Tramtrack/Broad Complex Ubiquitin-Ligase Gene Family in Rice[W] , 2007, The Plant Cell Online.

[19]  Y. Machida,et al.  Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members , 2009, The Plant journal : for cell and molecular biology.

[20]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[21]  T. Vision,et al.  Divergence in expression between duplicated genes in Arabidopsis. , 2007, Molecular biology and evolution.

[22]  Blake C Meyers,et al.  Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. , 2002, Genome research.

[23]  Guillaume Blanc,et al.  Functional Divergence of Duplicated Genes Formed by Polyploidy during Arabidopsis Evolution , 2004, The Plant Cell Online.

[24]  B. Walsh Population-Genetic Models of the Fates of Duplicate Genes , 2003, Genetica.

[25]  M. Basantani,et al.  Plant glutathione transferases — a decade falls short , 2007 .

[26]  A. Hughes The evolution of functionally novel proteins after gene duplication , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[28]  J. Hayes,et al.  Glutathione S‐transferases , 2002 .

[29]  A. Force,et al.  Preservation of duplicate genes by complementary, degenerative mutations. , 1999, Genetics.

[30]  Ralf Morgenstern,et al.  Structural basis for detoxification and oxidative stress protection in membranes. , 2006, Journal of molecular biology.

[31]  J. Byrnes,et al.  Role of positive selection in the retention of duplicate genes in mammalian genomes , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Lapthorn,et al.  Plant glutathione transferases , 2002, Genome Biology.

[33]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[34]  R. Edwards,et al.  Dimerisation of maize glutathione transferases in recombinant bacteria , 1999, Plant Molecular Biology.

[35]  W. Atkins,et al.  Functional Promiscuity Correlates with Conformational Heterogeneity in A-class Glutathione S-Transferases* , 2007, Journal of Biological Chemistry.

[36]  G. Agrawal,et al.  A pathogen-induced novel rice (Oryza sativa L.) gene encodes a putative protein homologous to type II glutathione S-transferases , 2002 .

[37]  E. Koonin,et al.  The role of lineage-specific gene family expansion in the evolution of eukaryotes. , 2002, Genome research.

[38]  R Edwards,et al.  Plant glutathione S-transferases: enzymes with multiple functions in sickness and in health. , 2000, Trends in plant science.

[39]  Dr. Susumu Ohno Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[40]  R. Michelmore,et al.  Genome-Wide Analysis of NBS-LRR–Encoding Genes in Arabidopsis Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009308. , 2003, The Plant Cell Online.

[41]  Eric J. Deeds,et al.  Protein structure and evolutionary history determine sequence space topology. , 2004, Genome research.

[42]  Jeffery P. Demuth,et al.  The life and death of gene families , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[43]  F. Regnier,et al.  Proteomic Analysis of Arabidopsis Glutathione S-transferases from Benoxacor- and Copper-treated Seedlings* , 2004, Journal of Biological Chemistry.

[44]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[45]  T. Takano-Shimizu,et al.  Enhanced fixation and preservation of a newly arisen duplicate gene by masking deleterious loss-of-function mutations. , 2009, Genetics research.

[46]  J. Roth,et al.  Ohno's dilemma: Evolution of new genes under continuous selection , 2007, Proceedings of the National Academy of Sciences.

[47]  John M. Hancock,et al.  Gene factories, microfunctionalization and the evolution of gene families. , 2005, Trends in genetics : TIG.

[48]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[49]  A. Sali,et al.  Modeller: generation and refinement of homology-based protein structure models. , 2003, Methods in enzymology.

[50]  N. Goldman,et al.  Codon-substitution models for heterogeneous selection pressure at amino acid sites. , 2000, Genetics.

[51]  Ilia J Leitch,et al.  The dynamic ups and downs of genome size evolution in Brassicaceae. , 2008, Molecular biology and evolution.

[52]  M. Atallah,et al.  A Novel Plant Glutathione S-Transferase/Peroxidase Suppresses Bax Lethality in Yeast* , 2000, The Journal of Biological Chemistry.

[53]  J. M. González,et al.  A fluorimetric method for the estimation of G+C mol% content in microorganisms by thermal denaturation temperature. , 2002, Environmental microbiology.

[54]  John B. Anderson,et al.  CDD: a Conserved Domain Database for protein classification , 2004, Nucleic Acids Res..

[55]  W. Wong,et al.  Bayes empirical bayes inference of amino acid sites under positive selection. , 2005, Molecular biology and evolution.

[56]  N. Soranzo,et al.  Organisation and structural evolution of the rice glutathione S-transferase gene family , 2004, Molecular Genetics and Genomics.

[57]  B. Turner,et al.  Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase , 1998, The EMBO journal.

[58]  Klaus F. X. Mayer,et al.  Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice , 2004, The Plant Cell Online.

[59]  A. Caccuri,et al.  Colorimetric and fluorometric assays of glutathione transferase based on 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole. , 1994, Analytical biochemistry.

[60]  Jeroen Raes,et al.  Nonrandom divergence of gene expression following gene and genome duplications in the flowering plant Arabidopsis thaliana , 2006, Genome Biology.

[61]  Abdelali Barakat,et al.  The cinnamyl alcohol dehydrogenase gene family in Populus: phylogeny, organization, and expression , 2009, BMC Plant Biology.

[62]  C. Frova The plant glutathione transferase gene family: genomic structure, functions, expression and evolution , 2003 .