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Evolutionary History of the GH3 Family of Acyl Adenylases in Rosids

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Evolutionary History of the GH3 Family of Acyl Adenylases in Rosids Plant Mol Biol DOI 10.1007/s11103-011-9776-y Evolutionary history of the GH3 family of acyl adenylases in rosids Rachel A. Okrent • Mary C. Wildermuth Received: 8 October 2010 / Accepted: 10 April 2011 Ó Springer Science+Business Media B.V. 2011 Abstract GH3 amino acid conjugases have been identi- identified in poplar, grape, columbine, maize and rice fied in many plant and bacterial species. The evolution of suggesting descent from a common ancestral chromosome GH3 genes in plant species is explored using the sequenced dating to before the eudicot/monocot split. In addition, the rosids Arabidopsis, papaya, poplar, and grape. Analysis of clade containing PBS3 has undergone a unique expansion the sequenced non-rosid eudicots monkey flower and col- in Arabidopsis, with expression patterns for these genes umbine, the monocots maize and rice, as well as spikemoss consistent with specialized and evolving stress-responsive and moss is included to provide further insight into the functions. origin of GH3 clades. Comparison of co-linear genes in regions surrounding GH3 genes between species helps Keywords GH3 Á Rosids Á Phylogeny Á Synteny Á Acyl reconstruct the evolutionary history of the family. Com- adenylase Á Salicylic acid Á Phytohormone bining analysis of synteny with phylogenetics, gene expression and functional data redefines the Group III GH3 Abbreviations genes, of which AtGH3.12/PBS3, a regulator of stress- Compounds induced salicylic acid metabolism and plant defense, is a BTH 1,2,3-benzothiodiazole-7-carbothioic acid S-methyl member. Contrary to previous reports that restrict PBS3 to ester Arabidopsis and its close relatives, PBS3 syntelogs are IAA Indole-3-acetic acid JA Jasmonic acid Accession numbers: AtGH3.1, At2g14960; AtGH3.2, At4g37390; SA Salicylic acid AtGH3.3, At2g23170; AtGH3.4, At1g59500; AtGH3.5, At4g27260; AtGH3.6, At5g54510; AtGH3.7, At1g23160; AtGH3.8, At5g51470; Genes AtGH3.9, At2g47750; AtGH3.10, At4g03400; AtGH3.11, bZIP Basic-domain leucine-zipper At2g46370; AtGH3.12, At5g13320; AtGH3.13, At5g13350; AtGH3.14, At5g13360; AtGH3.15, At5g13370; AtGH3.16, ERF Ethylene response factor At5g13380; AtGH3.17, At1g28130; AtGH3.18, At1g48670; GDG1 GH3-like defense gene 1 AtGH3.19, At1g48660. GH3 Gretchen Hagen 3 ICS1 Isochorismate synthase 1 Electronic supplementary material The online version of this article (doi:10.1007/s11103-011-9776-y) contains supplementary JAR1 Jasmonic acid resistant 1 material, which is available to authorized users. PBS3 avrPphB susceptible 3 WIN3 HopW1-1-interacting 3 R. A. Okrent Á M. C. Wildermuth (&) Department of Plant and Microbial Biology, University Organisms of California, 221 Koshland Hall, Berkeley 94720, USA Ac Aquilegia coerulea (columbine) e-mail: [email protected] At Arabidopsis thaliana Present Address: Cp Carica papaya (papaya) R. A. Okrent Mg Mimulus guttatus (monkey flower) Department of Botany and Plant Pathology, Oregon State Os Oryza sativa (rice) University, Corvallis, OR 97331, USA 123 Plant Mol Biol Pp Physcomitrella patens (moss) Gossypium hirsutum (cotton), all in the Eurosids II subc- Pt Populus trichocarpa (poplar) lade of the rosids superfamily of eudicotyledonous plants Sm Selaginella moellendorffii (spikemoss) (Terol et al. 2006). Substrate specificity of assayed proteins Vv Vitis vinifera (grape) tended to correspond to these phylogenetic relationships Zm Zea mays (maize) (Staswick et al. 2002, 2005). The JAR1 enzyme active on JA was placed in GH3 Group I (comprised of 2 GH3 genes Terms in A. thaliana), with GH3 enzymes active on IAA in Group ML Maximum likelihood II (8 AtGH3 genes), and enzymes including PBS3 active on MP Maximum parsimony neither of these compounds in Group III (9 AtGH3 genes). NJ Neighbor joining We are interested in the evolutionary history of the GH3 PID Percent identity family as a means of gaining insight into the evolved WGD Whole genome duplication functions of these enzymes in plants. As mentioned above, this family of enzymes catalyzes the amino acid conjuga- tion of small molecules, including the hormones IAA and Introduction JA. In doing so, these GH3 proteins alter the activity of the hormone and its extensive impact on plant metabolism and GH3 (Gretchen Hagen 3) genes were originally identified physiology. For example, JAR1 catalyzes the conjugation in Glycine max (soybean) as responsive to the phytohor- of Ile to JA forming JA-Ile, the active form of the hormone, mone auxin (Hagen et al. 1984) and have since been resulting in the degradation of a JA repressor protein and identified in many plant species (Terol et al. 2006). Several the subsequent activation of downstream transcriptional Arabidopsis thaliana genes were identified in genetic responses (Chini et al. 2007). The function of the Group III screens for altered phytohormone-mediated responses to enzymes has remained more elusive, as a substrate for only auxin [e.g., DFL1 (Nakazawa et al. 2001)], or jasmonic one enzyme, PBS3, has been identified (Okrent et al. acid [e.g., JAR1 (Staswick et al. 1992)]. However, the 2009). Though PBS3 does not act directly on the phyto- molecular function of these genes remained unknown until hormone SA, its function is required for full activation of Staswick et al. identified structural similarity between the SA-dependent defense responses (Nobuta et al. 2007; A. thaliana GH3 and the firefly luciferase-like superfamily Jagadeeswaran et al. 2007; Lee et al. 2007). If the Group III of proteins (Staswick et al. 2002). The firefly luciferase- GH3 genes were only present in a small group of related like superfamily, also called the adenylate-forming super- species, it would suggest the encoded enzymes evolved a family, is a diverse group of enzymes that catalyzes the new function. Possibly, this function, e.g., acting on a addition of AMP to carboxyl groups on a wide variety of unique substrate, would be specifically required by these substrates. This family includes nonribosomal peptide species or confer a growth or reproductive benefit. synthetases, 4-coumarate-CoA ligases, acyl-CoA ligases, Herein, we explore the evolutionary history of the GH3 and oxidoreductases (Conti et al. 1996). These enzymes family, focusing particularly on Group III. The recent typically contain three conserved motifs that form a bind- sequencing of multiple plant genomes coupled with new ing pocket for AMP and the substrate (Chang et al. 1997). computational tools such as the CoGe suite of comparative Staswick et al. identified the three conserved motifs in the genomics programs (Lyons and Freeling 2008; Lyons et al. A. thaliana GH3 proteins. Furthermore, in vitro activity 2008) allows us to leverage information from whole gen- assays revealed that one, JAR1 (GH3.11), catalyzes the omes to infer descent from a common ancestral gene by addition of amino acids to the plant hormone jasmonic acid analyzing co-linearity of neighboring genes. We performed (Staswick et al. 2002) and that several others catalyze the our analysis focusing primarily on genome sequence data addition of amino acids to auxin (Staswick et al. 2005). from the rosids Arabidopsis thaliana and Arabidopsis PBS3 (GH3.12), among others, was not active on any of lyrata, order Brassicales; Carica papaya (papaya), order the phytohormone substrates tested (Staswick et al. 2002). Brassicales; Populus trichocarpa (poplar), order Mal- Our subsequent work determined that 4-substituted ben- pighiales; and Vitis vinifera (grape), order Vitales. For zoates serve as substrates of PBS3 (Okrent et al. 2009). comparison, we also used genome data from the asterid Previously published phylogenetic trees constructed Mimulus guttatus (monkey flower); order Lamilaes; the using distance methods divided plant GH3 proteins into basal eudicot Aquilegia coerulea (columbine), order Ran- three major clades, identified as Groups I, II, and III (Felten unculales; the monocot grasses Oryza sativa (rice) and Zea et al. 2009; Staswick et al. 2002; Terol et al. 2006). Groups mays (maize); the lycophyte Selaginella moellendorffii I and II contained genes from many more species than did (spikemoss); and the moss Physcomitrella patens (Fig. 1). Group III, which contained genes from only three species, This syntenic analysis is coupled with investigation of Arabidopsis thaliana, Brassica napus (rapeseed), and expression patterns of the GH3 genes and available 123 Plant Mol Biol Populus trichocarpa 13 (Rensing et al. 2008)], Populus trichocarpa [JGI, v2 rosids (Tuskan et al. 2006)], Selaginella moellendorffii (JGI v1), Arabidopsis thaliana 19 Vitis vinifera [v1, French-Italian Public Consortium for 9 eudicots Carica papaya 6 Grapevine Genome Characterization (Jaillon et al. 2007)], 3 and Zea mays cultivar B73 [Maize sequence.org v2 (Sch- Vitis vinifera 8 nable et al. 2009)]. The regions of potential synteny com- piled in (Lyons et al. 2008) were used as a starting point, Mimulus guttatus 10 modified with new genome sequence data, evaluated for Aquilegia coerulea 6 accuracy, and expanded with additional analyses. The monocots V. vinifera genome, less subject to rearrangements, dupli- Zea mays 13 cations and gene loss than other genomes (Jaillon et al. 2007; Semon and Wolfe 2007), was used as a bridge Oryza sativa 13 between A. thaliana and the other genomes to identify Selaginella moellendorffii 20 regions of co-linearity and possible synteny. It should be noted that genes from some of the sequenced plants have Physcomitrella patens 2 not yet been assigned to chromosomes (Phytozome 6.0). Paleohexaploidy Four Arabidopsis GH3 genes were used as
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