Evolutionary history of the GH3 family of acyl adenylases in rosids

Plant Molecular Biology

Volumn 76, Issue 6, 2011, Pages 489-505

  Okrent, Rachel A ^a,b   Wildermuth, Mary C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Acyl adenylase; GH3; Phylogeny; Phytohormone; Rosids; Salicylic acid; Synteny

Indexed keywords

ARABIDOPSIS PROTEIN; NUCLEOTIDYLTRANSFERASE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; ASPEN; BINDING SITE; CLASSIFICATION; GENETICS; GRAPE; METABOLISM; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PAPAYA; PHYLOGENY; SEQUENCE ALIGNMENT; STATISTICAL MODEL; SYNTENY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BINDING SITES; CARICA; EVOLUTION, MOLECULAR; LIKELIHOOD FUNCTIONS; MULTIGENE FAMILY; NUCLEOTIDYLTRANSFERASES; PHYLOGENY; PLANT PROTEINS; POPULUS; SEQUENCE ALIGNMENT; SYNTENY; VITIS;

AQUILEGIA; ARABIDOPSIS; BACTERIA (MICROORGANISMS); BRYOPHYTA; CARICA PAPAYA; HAPLORHINI; LILIOPSIDA; MIMULUS (ANGIOSPERM); ROSIDAE; ROSIDS; SELAGINELLA; SELAGINELLACEAE; VITACEAE; ZEA MAYS;

EID: 79960590736     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-011-9776-y     Document Type: Article

References (80)

1. Albertazzi G, Milc J, Caffagni A, Francia E, Roncaglia E et al (2009) Gene expression in grapevine cultivars in response to Bois noir phytoplasma infection. Plant Sci 176: 792-804.
2. Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sata S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39: 170-181.
3. Bierfreund NM, Tintelnot S, Reski R, Decker EL (2004) Loss of GH3 function does not affect phytochrome-mediated development in a moss, Physcomitrella patens. J Plant Physiol 161: 823-835.
4. Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13: 137-144.
5. Bourne DJ, Barrow KD, Milborrow BV (1991) Salicyloylaspartate as an endogenous component of the leaves of Phaseolus vulgaris. Phytochemistry 30: 4041-4044.
6. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
7. Chang K-H, Xiang H, Dunaway-Mariano D (1997) Acyl-adenylate motif of the acyl-adenylate/thioester-forming enzyme superfamily: a site directed mutagenesis study with the Pseudomonas sp. Strain CBS3 4-chlorobenzoate: Coenzyme A ligase. Biochemistry 36: 15650-15659.
8. Chini A, Fonseca S, Fernandez G, Adie B, Chico JM et al (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666.
9. Conti E, Franks NP, Brick P (1996) Crystal structure of firefly luciferase throws light on a superfamily of adenylate-forming enzymes. Structure 4: 287-298.
10. Craigon DJ, James N, Okyere J, Higgins J, Jotham J et al (2004) Nascarrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res 32: D575-D577.
11. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S et al (2008) Phylogeny. Fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36: W465-W469.
12. Ding X, Cao Y, Huang L, Zhao J, Xu C et al (2008) Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell 20: 228-240.
13. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19: 2225-2245.
14. Domingo C, Andres F, Tharreau D, Iglesias DJ, Talon M (2009) Constitutive expression of OsGH3. 1 reduces auxin content and enhances defense response and resistance to a fungal pathogen in rice. Mol Plant-Micro Interact 22: 201-210.
15. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122: 627-634.
16. Edgar RC (2004) Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
17. Felten J, Kohler A, Morin E, Bhalerao RP, Palme K et al (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151: 1991-2005.
18. Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5, or PAD4. Plant J 35: 193-205.
19. Freeling M (2009) Bias in plant gene content following different sorts of duplication: Tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60: 433-453.
20. Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K et al (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55: 526-542.
21. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
22. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7: 465-471.
23. Haberer G, Hindemitt T, Meyers BC, Mayer KFX (2004) Transcriptional similarities, dissimilarities, and conservation of cis-elements in duplicated genes of Arabidopsis. Plant Physiol 136: 3009-3022.
24. Hagen G, Kleinschmidt A, Guilfoyle T (1984) Auxin-regulated gene expression in intact soybean Glycine max cultivar Wayne hypocotyl and excised hypocotyl sections. Planta 162: 147-153.
25. Hall BG (2005) Comparison of the accuracies of several phylogenetic methods using protein and DNA sequences. Mol Biol Evol 22: 792-802.
26. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu SH (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148: 993-1003.
27. Hsieh H-L, Okamoto H, Wang M, Ang L-H, Matsui M et al (2000) FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. Genes Dev 14: 1958-1970.
28. Huelsenbeck JP, Hillis DM (1993) Success of phylogenetic methods in the four-taxon case. Syst Biol 42: 247-264.
29. Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL et al (2007) Arabidopsis GH3-like Defense Gene 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to Pseudomonas syringae. Plant J 51: 234-246.
30. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463-467.
31. Jain M, Kaur N, Tyagi AK, Khurana JP (2006) The auxin-responsive GH3 gene family in rice (oryza sativa). Funct Integr Genomics 6: 36-46.
32. Jansen R, Kaittanis C, Saski C, Lee S-B, Tomkins J et al (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6: 32.
33. Jun J, Mandoiu I, Nelson C (2009) Identification of mammalian orthologs using local synteny. BMC Genomics 10: 630.
34. Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a means of escaping herbivores. Curr Biol 20: 237-242.
35. Khan S, Stone JM (2007) Arabidopsis thaliana GH3. 9 influences primary root growth. Planta 226: 21-34.
36. Krishnaswamy S, Verma S, Rahman MH, Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP2. 6, RAP2. 6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75: 107-127.
37. Lee MW, Lu H, Jung HW, Greenberg JT (2007) A key role for the Arabidopsis WIN3 protein in disease resistance triggered by Pseudomonas syringae that secrete AvrRpt2. MPMI 20: 1192-1200.
38. Lee MW, Jelenska J, Greenberg JT (2008) Arabidopsis proteins important for modulating defense responses to Pseudomonas syringae that secrete HopW1-1. Plant J 54: 452-465.
39. Liu Kl, Kang B-C, Jiang H, Moore SL, Li H et al (2005) A GH3-like gene, CcGH3, isolated from Capsicum chinense l. Fruit is regulated by auxin and ethylene. Plant Mol Biol 58: 447-464.
40. Ludwig-Muller J, Julke S, Bierfreund NM, Decker EL, Reski R (2009) Moss (Physcomitrella patens) GH3 proteins act in auxin homeostasis. New Phytol 181: 323-338.
41. Lyons E, Freeling M (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 53: 661-673.
42. Lyons E, Pedersen B, Kane J, Alam M, Ming R et al (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148: 1772-1781.
43. Martinez C, Pons E, Prats G, Leon J (2004) Salicylic acid regulates flowering time and links defence responses and reproductive development. Plant J 37: 209-217.
44. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A et al (2008) The draft genome of the transgenic tropical fruit tree papaya (Carica papaya linnaeus). Nature 452: 991-996.
45. Molina C, Grotewold E (2005) Genome wide analysis of Arabidopsis core promoters. BMC Genomics 6: 25.
46. Mount DW (2004) Bioinformatics: sequence and genome analysis. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
47. Nakazawa M, Yabe N, Ichikawa T, Yamamoto YY, Yoshizumi T et al (2001) DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. Plant J 25: 213-221.
48. Nobuta K, Okrent RA, Stoutemyer M, Rodibaugh N, Kempema L et al (2007) The GH3 acyl adenylase family member PBS3 regulates salicylic acid-dependent defense responses in Arabidopsis. Plant Physiol 144: 1144-1156.
49. Okrent RA, Brooks MD, Wildermuth MC (2009) Arabidopsis GH3. 12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate. J Biol Chem 284: 9742-9754.
50. Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M et al (2006) The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res 35: D883-D887.
51. Park J-E, Seo PJ, Lee A-K, Jung J-H, Kim Y-S et al (2007a) An Arabidopsis GH3 gene, encoding an auxin-conjugating enzyme, mediates phytochrome B-regulated light signals in hypocotyl growth. Plant Cell Physiol 48: 1236-1241.
52. Park J-E, Park J-Y, Kim Y-S, Staswick PE, Jeon J, Yun J, Kim S-Y, Kim J, Lee Y-H, Park C-M (2007b) GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J Biol Chem 282: 10036-10046.
53. Rensing SA, Lang D, Zimmer AD, Terry A, Salamov A et al (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319: 64-69.
54. Rizzon C, Ponger L, Gaut BS (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2: e115.
55. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112-1115.
56. Semon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17: 505-512.
57. Singh KB, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5: 430-436.
58. Staswick PE, Tiryaki I (2004) The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16: 2117-2127.
59. Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89: 6837-6840.
60. Staswick PE, Tiryaki I, Rowe ML (2002) Jasmonate response locus JAR1 and several related Arabidopsis genes encode enzymes of the firefly luciferase superfamily that show activity on jasmonic, salicylic, and indole-3-acetic acids in an assay for adenylation. Plant Cell 14: 1405-1415.
61. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT et al (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17: 616-627.
62. Steel M (2005) Should phylogenetic models be trying to "Fit an elephant"? Trends Genet 21: 307-309.
63. Sun F, Liu P, Xu J, Dong H (2010) Mutation in RAP2. 6L, a transactivator of the ERF transcription factor family enhances resistance to Pseudomonas syringae. Physiol Mol Plant Pathol 74: 295-301.
64. Suzuki Y, Yanaguchi I, Murofushi N, Takahasi N (1988) Biological conversion of benzoic acid in Lemna paucicostata 151 and its relation to flower induction. Plant Cell Physiol 29: 439-444.
65. Takase T, Nakazawa M, Ishikawa A, Manabe K, Matsui M (2003) DFL2, a new member of the Arabidopsis GH3 family is involved in red light-specific hypocotyl elongation. Plant Cell Physiol 44: 1071-1080.
66. Takase T, Nakazawa M, Ishikawa A, Kawashima M, Ichikawa T, Takahashi N, Shimada H, Manabe K, Matsui M (2004) ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. Plant J 37: 471-483.
67. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4. 0. Mol Biol Evol 24: 1596-1599.
68. Terol J, Domingo C, Talon M (2006) The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. Gene 371: 279-290.
69. Thornton JW, Kolaczkowski B (2005) No magic pill for phylogenetic error. Trends Genet 21: 310-311.
70. Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The botany array resource: E-northerns, expression angling, and promoter analyses. Plant J 43: 153-163.
71. Trennheuser F, Burkhard G, Becker H (1994) Anthocerodiazonin, an alkaloid from Antheroceros agretis. Phytochemistry 37: 899-903.
72. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, populus trichocarpa (torr. & gray). Science 313: 1596-1604.
73. Warren RF, Merritt PM, Holub E, Innes RW (1999) Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis. Genetics 152: 401-412.
74. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV et al (2007) An "electronic fluorescent pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS One 2: e718.
75. Wise RP, Caldo RA, Hong L, Shen L, Cannon E et al (2007) Barleybase/plexdb: a unified expression profiling database for plants and plant pathogens. In: Edwards D (ed) Plant bioinformatics-methods and protocols. Humana Press, Totowa, pp 347-363.
76. Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95: 707-735.
77. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW et al (2007) Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.
78. Zhang Z, Li Q, Li Z, Staswick PE, Wang M et al (2007) Dual regulation role of GH3. 5 in salicylic acid and auxin signaling during Arabidopsis-Pseudomonas syringae interaction. Plant Physiol 145: 450-464.
79. Zhang S-W, Li C-H, Cao J, Zhang Y-C, Zhang S-Q et al (2009) Altered architecture and enhanced drought tolerance in rice via the down-regulation of indole-3-acetic acid by tld1/osgh3. 13 activation. Plant Physiol 151: 1889-1901.
80. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136: 2621-2632.