Herbivore-induced SABATH methyltransferases of maize that methylate anthranilic acid using S-adenosyl-L-methionine

Plant Physiology

Volumn 153, Issue 4, 2010, Pages 1795-1807

  Köllner, Tobias G ^a,b   Lenk, Claudia ^a   Zhao, Nan ^c   Seidl Adams, Irmgard ^d   Gershenzon, Jonathan ^b   Chen, Feng ^c   Degenhardt, Jörg ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c UNIVERSITY OF TENNESSEE   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRANILIC ACID; ANTHRANILIC ACID DERIVATIVE; COMPLEMENTARY DNA; METHYLTRANSFERASE; S ADENOSYLMETHIONINE; VEGETABLE PROTEIN;

ANIMAL; CHEMICAL STRUCTURE; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; MAIZE; METABOLISM; MOLECULAR GENETICS; MULTIGENE FAMILY; SEQUENCE HOMOLOGY; SITE DIRECTED MUTAGENESIS; SPODOPTERA;

ANIMALS; DNA, COMPLEMENTARY; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTAGENESIS, SITE-DIRECTED; ORTHO-AMINOBENZOATES; PLANT PROTEINS; S-ADENOSYLMETHIONINE; SEQUENCE HOMOLOGY, AMINO ACID; SPODOPTERA; SUBSTRATE SPECIFICITY; ZEA MAYS;

EID: 77955701990     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.158360     Document Type: Article

References (63)

1. Barkman TJ, Martins TR, Sutton E, Stout JT (2007) Positive selection for single amino acid change promotes substrate discrimination of a plant volatile-producing enzyme. Mol Biol Evol 24: 1320-1329.
2. Cardoza YJ, Tumlinson JH (2006) Compatible and incompatible Xanthomonas infections differentially affect herbivore-induced volatile emission by pepper plants. J Chem Ecol 32: 1755-1768.
3. Chen F, D'Auria JC, Tholl D, Ross JR, Gershenzon J, Noel JP, Pichersky E (2003) An Arabidopsis thaliana gene for methylsalicylate biosynthesis, identified by a biochemical genomics approach, has a role in defense. Plant J 36: 577-588.
4. D'Alessandro M, Held M, Triponez Y, Turlings TCJ (2006) The role of indole and other shikimic acid derived maize volatiles in the attraction of two parasitic wasps. J Chem Ecol 32: 2733-2748.
5. D'Auria JC, Chen F, Pichersky E (2003) The SABATH family of MTS in Arabidopsis thaliana and other plant species. In JT Romeo, ed, Integrative Phytochemistry: From Ethnobotany to Molecular Ecology. Recent Advances in Phytochemistry, Vol 37. Elsevier, Oxford, pp 253-283.
6. Degen T, Dillmann C, Marion-Poll F, Turlings TCJ (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiol 135: 1928-1938.
7. Degenhardt J, Gershenzon J (2000) Demonstration and characterization of (E)-nerolidol synthase from maize: a herbivore-inducible terpene synthase participating in (3E)-4,8-dimethyl-1,3,7-nonatriene biosynthesis. Planta 210: 815-822.
8. Degenhardt J, Gershenzon J, Baldwin IT, Kessler A (2003) Attracting friends to feast on foes: engineering terpene emission to make crop plants more attractive to herbivore enemies. Curr Opin Biotechnol 14: 169-176.
9. Degenhardt J, Kollner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70: 1621-1637.
10. de Kraker JW, Luck K, Textor S, Tokuhisa JG, Gershenzon J (2007) Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine. Plant Physiol 143: 970-986.
11. Dicke M (1994) Local and systemic production of volatile herbivoreinduced terpenoids: their role in plant-carnivore mutualism. J Plant Physiol 143: 465-472.
12. Dobson HEM, Bergstrom G (2000) The ecology and evolution of pollen odors. Plant Syst Evol 222: 63-87.
13. Effmert U, Saschenbrecker S, Ross J, Negre F, Fraser CM, Noel JP, Dudareva N, Piechulla B (2005) Floral benzenoid carboxyl methyltransferases: from in vitro to in planta function. Phytochemistry 66: 1211-1230.
14. Frey M, Spiteller D, Boland W, Gierl A (2004) Transcriptional activation of Igl, the gene for indole formation in Zea mays: a structure-activity study with elicitor-active N-acyl glutamines from insects. Phytochemistry 65: 1047-1055.
15. Frey M, Stettner C, Pare PW, Schmelz EA, Tumlinson JH, Gierl A (2000) An herbivore elicitor activates the gene for indole emission in maize. Proc Natl Acad Sci USA 97: 14801-14806.
16. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180: 722-733.
17. Fukami H, Asakura T, Hirano H, Abe K, Shimomura K, Yamakawa T (2002) Salicylic acid carboxyl methyltransferase induced in hairy root cultures of Atropa belladonna after treatment with exogeneously added salicylic acid. Plant Cell Physiol 43: 1054-1058.
18. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9: 813-817.
19. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104: 5467-5472.
20. Hoballah ME, Kollner TG, Degenhardt J, Turlings TCJ (2004) Costs of induced volatile production in maize. Oikos 105: 168-180.
21. Hoballah MEF, Tamo C, Turlings TCJ (2002) Differential attractiveness of induced odors emitted by eight maize varieties for the parasitoid Cotesia marginiventris: is quality or quantity important? J Chem Ecol 28: 951-968.
22. Hopke J, Donath J, Blechert S, Boland W (1994) Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a b-glucosidase and jasmonic acid. FEBS Lett 352: 146-150.
23. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59: 41-66.
24. Huang J, Cardoza YJ, Schmelz EA, Raina R, Engelberth J, Tumlinson JH (2003) Differential volatile emissions and salicylic acid levels from tobacco plants in response to different strains of Pseudomonas syringae. Planta 217: 767-775.
25. James DG (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. J Chem Ecol 31: 481-495.
26. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72: 1-120.
27. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008a) A maize (E)-b-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20: 482-494.
28. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004a) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65: 1895-1902.
29. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004b) The variability of sesquiterpenes emitted from two Zea mays cultivars is controlled by allelic variation of two terpene synthase genes encoding stereoselective multiple product enzymes. Plant Cell 16: 1115-1131.
30. Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J (2008b) Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)-beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283: 20779-20788
31. Koo YJ, Kim MA, Kim EH, Song JT, Jung C, Moon JK, Kim JH, Seo HS, Song SI, Kim JK, et al (2007) Overexpression of salicylic acid carboxyl methyltransferase reduces salicylic acid-mediated pathogen resistance in Arabidopsis thaliana. Plant Mol Biol 64: 1-15.
32. Kwon S, Hamada K, Matsuyama A, Yasuda M, Nakashita H, Yamakawa T (2009) Biotic and abiotic stresses induce AbSAMT1, encoding S-adenosyl-L-methionine: salicylic acid carboxyl methyltransferase, in Atropa belladonna. Plant Biotechnol 26: 207-215.
33. Landolt PJ, Wixson T, Remke LJ, Lewis RR, Zack RS (2000) Methyl anthranilate attracts males of Thaumatomyia glabra (Meigen) (Diptera: Chloropidae). J Kans Entomol Soc 73: 189-194.
34. Leitner M, Boland W, Mithofer A (2005) Direct and indirect defences induced by piercing-sucking and chewing herbivores in Medicago truncatula. New Phytol 167: 597-606.
35. Murai T, Imai T, Maekawa M (2000) Methyl anthranilate as an attractant for two thrips species and the thrips parasitoid Ceranisus menes. J Chem Ecol 26: 2557-2565.
36. Negre F, Kolosova N, Knoll J, Kish CM, Dudareva N (2002) Novel S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, an enzyme responsible for biosynthesis of methyl salicylate and methyl benzoate, is not involved in floral scent production in snapdragon flowers. Arch Biochem Biophys 406: 261-270.
37. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF-Chimera: a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
38. Pott MB, Hippauf F, Saschenbrecker S, Chen F, Ross J, Kiefer I, Slusarenko A, Noel JP, Pichersky E, Effmert U, et al (2004) Biochemical and structural characterization of benzenoid carboxyl methyltransferases involved in floral scent production in Stephanotis floribunda and Nicotiana suaveolens. Plant Physiol 135: 1946-1955.
39. Qin GJ, Gu HY, Zhao YD, Ma ZQ, Shi GL, Yang Y, Pichersky E, Chen HD, Liu MH, Chen ZL, et al (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17: 2693-2704.
40. Ralph S, Oddy C, Cooper D, Yueh H, Jancsik S, Kolosova N, Philippe RN, Aeschliman D, White R, Huber D, et al (2006) Genomics of hybrid poplar (Populus trichocarpa 3 deltoides) interacting with forest tent caterpillars (Malacosoma disstria): normalized and full-length cDNA libraries, expressed sequence tags, and a cDNA microarray for the study of insect-induced defences in poplar. Mol Ecol 15: 1275-1297.
41. Ross JR, Nam KH, D'Auria JC, Pichersky E (1999) S-Adenosyl-Lmethionine:salicylic acid carboxyl methyltransferase, an enzyme involved in floral scent production and plant defense, represents a new class of plant methyltransferases. Arch Biochem Biophys 367: 9-16.
42. Ruther J, Furstenau B (2005) Emission of herbivore-induced volatiles in absence of a herbivore-response of Zea mays to green leaf volatiles and terpenoids. Z Naturforsch C 60: 743-756.
43. Sarwar G, Botting HG (1993) Evaluation of liquid chromatographic analysis of nutritionally important amino acids in food and physiological samples. J Chromatogr 615: 1-22.
44. Schnee C, Kollner TG, Gershenzon J, Degenhardt J (2002) The maize gene terpene synthase 1 encodes a sesquiterpene synthase catalyzing the formation of (E)-beta-farnesene, (E)-nerolidol, and (E,E)-farnesol after herbivore damage. Plant Physiol 130: 2049-2060.
45. Schnee C, Kollner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103: 1129-1134.
46. Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31: 3381-3385.
47. Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98: 4788-4793.
48. Shen BZ, Zheng ZW, Dooner HK (2000) A maize sesquiterpene cyclase gene induced by insect herbivory and volicitin: characterization of wildtype and mutant alleles. Proc Natl Acad Sci USA 97: 14807-14812.
49. Song MS, Kim DG, Lee SH (2005) Isolation and characterization of a jasmonic acid carboxyl methyltransferase gene from hot pepper (Capsicum annuum L.). J Plant Biol 48: 292-297.
50. Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49: 16-26.
51. Turlings TCJ, Benrey B (1998a) Effects of plant metabolites on the behavior and development of parasitic wasps. Ecoscience 5: 321-333.
52. Turlings TCJ, Jeanbourquin PM, Held M, Degen T (2005) Evaluating the induced-odour emission of a Bt maize and its attractiveness to parasitic wasps. Transgenic Res 14: 807-816.
53. Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998b) Timing of induced volatile emissions in maize seedlings. Planta 207: 146-152.
54. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivoreinduced plant odors by host-seeking parasitic wasps. Science 30: 1251-1253.
55. van den Boom CEM, Van Beek TA, Posthumus MA, De Groot A, Dicke M (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J Chem Ecol 30: 69-89.
56. Wang J, De Luca V (2005) The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including 'foxy' methylanthranilate. Plant J 44: 606-619.
57. Xu RR, Song FM, Zheng Z (2006) OsBISAMT1, a gene encoding S-adenosyl-L-methionine:salicylic acid carboxyl methyltransferase, is differentially expressed in rice defense responses. Mol Biol Rep 33: 223-231.
58. Yuan JS, Kollner TG, Wiggins G, Grant J, Degenhardt J, Chen F (2008) Molecular and genomic basis of volatile-mediated indirect defense against insects in rice. Plant J 55: 491-503.
59. Zhang Z, Kishino H (2004) Genomic background predicts the fate of duplicated genes: evidence from the yeast genome. Genetics 166: 1995-1999.
60. Zhao N, Ferrer JL, Ross J, Guan J, Yang Y, Pichersky E, Noel JP, Chen F (2008) Structural, biochemical, and phylogenetic analyses suggest that indole-3-acetic acid methyltransferase is an evolutionarily ancient member of the SABATH family. Plant Physiol 146: 455-467.
61. Zhao N, Guan J, Ferrer J-L, Engle N, Chern M, Ronald P, Tschaplinski TJ, Chen F (2010) Emission, biosynthesis and regulation of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol Biochem 48: 279-287.
62. Zhao N, Guan J, Lin H, Chen F (2007) Molecular cloning and biochemical characterization of indole-3-acetic acid methyltransferase from poplar. Phytochemistry 68: 1537-1544.
63. Zubieta C, Ross JR, Koscheski P, Yang Y, Pichersky E, Noel JP (2003) Structural basis for substrate recognition in the salicylic acid carboxyl methyltransferase family. Plant Cell 15: 1704-1716.