Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana

Abstract. A family of 40 terpenoid synthase genes (AtTPS) was discovered by genome sequence analysis in Arabidopsis thaliana. This is the largest and most diverse group of TPS genes currently known for any species. AtTPS genes cluster into five phylogenetic subfamilies of the plant TPS superfamily. Surprisingly, thirty AtTPS closely resemble, in all aspects of gene architecture, sequence relatedness and phylogenetic placement, the genes for plant monoterpene synthases, sesquiterpene synthases or diterpene synthases of secondary metabolism. Rapid evolution of these AtTPS resulted from repeated gene duplication and sequence divergence with minor changes in gene architecture. In contrast, only two AtTPS genes have known functions in basic (primary) metabolism, namely gibberellin biosynthesis. This striking difference in rates of gene diversification in primary and secondary metabolism is relevant for an understanding of the evolution of terpenoid natural product diversity. Eight AtTPS genes are interrupted and are likely to be inactive pseudogenes. The localization of AtTPS genes on all five chromosomes reflects the dynamics of the Arabidopsis genome; however, several AtTPS genes are clustered and organized in tandem repeats. Furthermore, some AtTPS genes are localized with prenyltransferase genes (AtGGPPS, geranylgeranyl diphosphate synthase) in contiguous genomic clusters encoding consecutive steps in terpenoid biosynthesis. The clustered organization may have implications for TPS gene evolution and the evolution of pathway segments for the synthesis of terpenoid natural products. Phylogenetic analyses highlight events in the divergence of the TPS paralogs and suggest orthologous genes and a model for the evolution of the TPS gene family.

[1]  J. Rowe.  Natural Products of Woody Plants , 1989, Springer Series in Wood Science.

[2]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[3]  Francisco A. Tomás-Barberán,et al.  Ecological chemistry and biochemistry of plant terpenoids , 1992 .

[4]  M. Kanehisa,et al.  A knowledge base for predicting protein localization sites in eukaryotic cells , 1992, Genomics.

[5]  P. Facchini,et al.  Gene family for an elicitor-induced sesquiterpene cyclase in tobacco. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[6]  B. M. Lawrence.  Essential oils as sources of natural aroma chemicals , 1992 .

[7]  J. Knudsen,et al.  Floral scents-a checklist of volatile compounds isolated by head-space techniques , 1993 .

[8]  C. Mau,et al.  Cloning of casbene synthase cDNA: evidence for conserved structural features among terpenoid cyclases in plants. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[9]  36 Secondary Metabolism in Arabidopsis , 1994 .

[10]  J. Sacchettini,et al.  Crystal structure of recombinant farnesyl diphosphate synthase at 2.6-A resolution. , 1994, Biochemistry.

[11]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[12]  S. Somerville,et al.  Secondary Metabolism in Arabidopsis , 1994 .

[13]  T. Sun,et al.  The Arabidopsis GA1 locus encodes the cyclase ent-kaurene synthetase A of gibberellin biosynthesis. , 1994, The Plant cell.

[14]  J. Chappell,et al.  Cloning and Bacterial Expression of a Sesquiterpene Cyclase from Hyoscyamus muticus and Its Molecular Comparison to Related Terpene Cyclases (*) , 1995, The Journal of Biological Chemistry.

[15]  G. J. Graham,et al.  Tandem genes and clustered genes. , 1995, Journal of theoretical biology.

[16]  R. Croteau,et al.  cDNA cloning, characterization, and functional expression of 4S-(-)-limonene synthase from Perilla frutescens. , 1996, Archives of biochemistry and biophysics.

[17]  Peter G. Korning,et al.  Splice Site Prediction in Arabidopsis Thaliana Pre-mRNA by Combining Local and Global Sequence Information , 1996 .

[18]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[19]  E. Pichersky,et al.  Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. , 1996, The Plant cell.

[20]  Jonathan D. G. Jones,et al.  Novel Disease Resistance Specificities Result from Sequence Exchange between Tandemly Repeated Genes at the Cf-4/9 Locus of Tomato , 1997, Cell.

[21]  S. Brunak,et al.  SHORT COMMUNICATION Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites , 1997 .

[22]  S. Aubourg,et al.  Structure, organization and putative function of the genes identified within a 23.9-kb fragment from Arabidopsis thaliana chromosome IV. , 1997, Gene.

[23]  J. Bohlmann,et al.  Monoterpene Synthases from Grand Fir (Abies grandis) , 1997, The Journal of Biological Chemistry.

[24]  D. Cane,et al.  Crystal structure of pentalenene synthase: mechanistic insights on terpenoid cyclization reactions in biology. , 1997, Science.

[25]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[26]  J. Bohlmann,et al.  Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Yamaguchi,et al.  The GA2 locus of Arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. , 1998, Plant physiology.

[28]  R. Croteau,et al.  Truncation of limonene synthase preprotein provides a fully active 'pseudomature' form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair. , 1998, Biochemistry.

[29]  P. Bork,et al.  Measuring genome evolution. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. Pichersky,et al.  Structure and evolution of linalool synthase. , 1998, Molecular biology and evolution.

[31]  W. Eisenreich,et al.  The deoxyxylulose phosphate pathway of terpenoid biosynthesis in plants and microorganisms. , 1998, Chemistry & biology.

[32]  R. Croteau,et al.  Monoterpene Synthases from Common Sage (Salvia officinalis)* , 1998, The Journal of Biological Chemistry.

[33]  D. Christianson,et al.  Managing and manipulating carbocations in biology: terpenoid cyclase structure and mechanism. , 1998, Current opinion in structural biology.

[34]  J. Bohlmann,et al.  Plant terpenoid synthases: molecular biology and phylogenetic analysis. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  H. Robertson.  Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. , 1998, Genome research.

[36]  Joseph Chappell,et al.  Structural Basis for Cyclic Terpene Biosynthesis by Tobacco 5‐epi‐Aristolochene Synthase , 1998 .

[37]  M. Borodovsky,et al.  GeneMark.hmm: new solutions for gene finding. , 1998, Nucleic acids research.

[38]  J. Tumlinson,et al.  Plant volatiles as a defense against insect herbivores , 1999, Plant physiology.

[39]  R. Croteau,et al.  Geranyl diphosphate synthase: cloning, expression, and characterization of this prenyltransferase as a heterodimer. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Ramana V. Davuluri,et al.  Evaluation of gene prediction software using a genomic data set: application to <$O_SSF>Arabidopsis thaliana<$C_SSF>sequences , 1999, Bioinform..

[41]  D. Eisenberg,et al.  Detecting protein function and protein-protein interactions from genome sequences. , 1999, Science.

[42]  D. Cane.  2.06 – Sesquiterpene Biosynthesis: Cyclization Mechanisms , 1999 .

[43]  Hartmut K. Lichtenthaler,et al.  THE 1-DEOXY-D-XYLULOSE-5-PHOSPHATE PATHWAY OF ISOPRENOID BIOSYNTHESIS IN PLANTS. , 1999, Annual review of plant physiology and plant molecular biology.

[44]  T. Koyama,et al.  2.04 – Isopentenyl DiphosphateIsomerase and Prenyltransferases , 1999 .

[45]  R. Hammerschmidt.  PHYTOALEXINS: What Have We Learned After 60 Years? , 1999, Annual review of phytopathology.

[46]  J. Bohlmann,et al.  cDNA cloning, characterization, and functional expression of four new monoterpene synthase members of the Tpsd gene family from grand fir (Abies grandis). , 1999, Archives of biochemistry and biophysics.

[47]  J. Gershenzon,et al.  Limonene synthase, the enzyme responsible for monoterpene biosynthesis in peppermint, is localized to leucoplasts of oil gland secretory cells , 1999, Plant physiology.

[48]  P. Rouzé,et al.  Genome annotation: which tools do we have for it? , 1999, Current opinion in plant biology.

[49]  J. Chappell,et al.  Isoprenoid biosynthesis in plants: carbon partitioning within the cytoplasmic pathway. , 1999, Critical reviews in biochemistry and molecular biology.

[50]  David E. Cane,et al.  Isoprenoids including carotenoids and steroids , 1999 .

[51]  K. Wang,et al.  Chain-length determination mechanism of isoprenyl diphosphate synthases and implications for molecular evolution. , 1999, Trends in biochemical sciences.

[52]  M. Rohmer.  The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. , 1999, Natural product reports.

[53]  Thomas Schiex,et al.  EUGÈNE: An Eukaryotic Gene Finder That Combines Several Sources of Evidence , 2000, JOBIM.

[54]  R. Croteau,et al.  Cyclization Enzymes in the Biosynthesis of Monoterpenes, Sesquiterpenes, and Diterpenes , 2000 .

[55]  T. Saito,et al.  Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. , 2000, Plant physiology.

[56]  E. Pichersky,et al.  Biochemical and molecular genetic aspects of floral scents. , 2000, Plant physiology.

[57]  R. Backhaus,et al.  Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. , 2000, The Plant journal : for cell and molecular biology.

[58]  J. Gershenzon,et al.  Terpenoid secondary metabolism in Arabidopsis thaliana: cDNA cloning, characterization, and functional expression of a myrcene/(E)-beta-ocimene synthase. , 2000, Archives of biochemistry and biophysics.

[59]  J. Gershenzon,et al.  Biochemical, molecular genetic and evolutionary aspects of defense-related terpenoid metabolism in conifers , 2000 .

[60]  Junji Takabayashi,et al.  Herbivory-induced volatiles elicit defence genes in lima bean leaves , 2000, Nature.

[61]  M. H. Beale,et al.  Comprehensive Natural Products Chemistry , 2000 .

[62]  D. Cane,et al.  Crystal Structure Determination of Aristolochene Synthase from the Blue Cheese Mold, Penicillium roqueforti * , 2000, The Journal of Biological Chemistry.

[63]  Z. Zheng,et al.  A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wild-type and mutant alleles. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[64]  B. Miller,et al.  First isolation of an isoprene synthase gene from poplar and successful expression of the gene in Escherichia coli , 2001, Planta.

[65]  R. Peters,et al.  Bifunctional abietadiene synthase: free diffusive transfer of the (+)-copalyl diphosphate intermediate between two distinct active sites. , 2001, Journal of the American Chemical Society.

[66]  R. Croteau,et al.  Genomic organization of plant terpene synthases and molecular evolutionary implications. , 2001, Genetics.

[67]  Comprehensive Natural Products Chemistry, Volume 2: Isoprenoids Including Carotenoids and Steroids , 2002 .

[68]  P. Ronald,et al.  The evolution of disease resistance genes , 2004, Plant Molecular Biology.

[69]  M. Dicke,et al.  Herbivore-Induced Volatile Production by Arabidopsis thaliana Leads to Attraction of the Parasitoid Cotesia rubecula: Chemical, Behavioral, and Gene-Expression Analysis , 2001, Journal of Chemical Ecology.