Novel acidic sesquiterpenoids constitute a dominant class of pathogen-induced phytoalexins in maize

Plant Physiology

Volumn 156, Issue 4, 2011, Pages 2082-2097

  Huffaker, Alisa ^a   Kaplan, Fatma ^a   Vaughan, Martha M ^a   Dafoe, Nicole J ^a   Ni, Xinzhi ^b   Rocca, James R ^c   Alborn, Hans T ^a   Teal, Peter E A ^a   Schmelz, Eric A ^a  

^a CENTER FOR MEDICAL   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGI; GIBBERELLA ZEAE; OSTRINIA NUBILALIS; ZEA MAYS;

EID: 79961205348     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.111.179457     Document Type: Article

References (63)

1. Basse CW (2005) Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiol 138: 1774-1784
2. Bhatnagar D, Yu J, Ehrlich KC (2002) Toxins of filamentous fungi. Chem Immunol 81: 167-206
3. Bily AC, Reid LM, Taylor JH, Johnston D, Malouin C, Burt AJ, Bakan B, Regnault-Roger C, Pauls KP, Arnason JT, et al (2003) Dehydrodimers of ferulic acid in maize grain pericarp and aleurone: resistance factors to Fusarium graminearum. Phytopathology 93: 712-719
4. Bohlmann J, Crock J, Jetter R, Croteau R (1998) Terpenoid-based defenses in conifers: cDNA cloning, characterization, and functional expression of wound-inducible (E)-alpha-bisabolene synthase from grand fir (Abies grandis). Proc Natl Acad Sci USA 95: 6756-6761
5. Boué SM, Carter CH, Ehrlich KC, Cleveland TE (2000) Induction of the soybean phytoalexins coumestrol and glyceollin by Aspergillus. J Agric Food Chem 48: 2167-2172
6. Bowers WS, Fales HM, Thompson MJ, Uebel EC (1966) Juvenile hormone: identification of an active compound from balsam fir. Science 154: 1020-1021
7. Brooks CJW, Watson DG (1991) Terpenoid phytoalexins. Nat Prod Rep 8: 367-389
8. Capehart T, Allen E (2011) Feed outlook. United States Department of Agriculture Economic Research Service Report: Report Number ERS-FDS-11d. http://usda.mannlib.cornell.edu/usda/current/FDS/FDS-04-12-2011.pdf
9. Chappell J, Nable R (1987) Induction of sesquiterpenoid biosynthesis in tobacco cell suspension cultures by fungal elicitor. Plant Physiol 85: 469-473
10. Chassy BM (2010) Food safety risks and consumer health. New Biotechnol 27: 534-544
11. Chen ZY, Brown RL, Damann KE, Cleveland TE (2010) PR10 expression in maize and its effect on host resistance against Aspergillus flavus infection and aflatoxin production. Mol Plant Pathol 11: 69-81
12. Cool LG (2005) Sesquiterpenes from Cupressus macrocarpa foliage. Phytochemistry 66: 249-260
13. Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TC (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci USA 106: 13213-13218
14. Delannoy E, Lyon BR, Marmey P, Jalloul A, Daniel JF, Montillet JL, Essenberg M, Nicole M (2005) Resistance of cotton towards Xanthomonas campestris pv. malvacearum. Annu Rev Phytopathol 43: 63-82
15. Desjardins AE, Gardner HW, Weltring KM (1992) Detoxification of sesquiterpene phytoalexins by Gibberella pulicaris (Fusarium sambucinum) and its importance for virulence on potato tubers. J Ind Microbiol Biotechnol 9: 201-221
16. Dohlemann G, Wahl R, Horst RJ, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, et al (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56: 181-195
17. Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D'Alessandro M, Turlings TC, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59: 292-302
18. Frey M, Chomet P, Glawischnig E, Stettner C, Grün S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, et al (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277: 696-699
19. Frey M, Schullehner K, Dick R, Fiesselmann A, Gierl A (2009) Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry 70: 1645-1651
20. 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
21. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414
22. Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR chemical shifts of common laboratory solvents as trace impurities. J Org Chem 62: 7512-7515
23. Hamilton RH (1964) A corn mutant deficient in 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one with an altered tolerance of atrazine. Weeds 12: 27-30
24. Harris LJ, Saparno A, Johnston A, Prisic S, Xu M, Allard S, Kathiresan A, Ouellet T, Peters RJ (2005) The maize AN2 gene is induced by Fusarium attack and encodes an ent-copalyl diphosphate synthase. Plant Mol Biol 59: 881-894
25. Heath RR, Dueben BD (1998) Analytical and preparative gas chromatography. In JG Millar, KF Haynes, eds, Methods in Chemical Ecology: Chemical Methods, Vol 1. Kluwer, New York, pp 85-126
26. Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis Elicitor Peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol 155: 1325-1338
27. Kiesselbach TA (1999) The Structure and Reproduction of Corn. 50th Anniversary Edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
28. Kim JH, Yu J, Mahoney N, Chan KL, Molyneux RJ, Varga J, Bhatnagar D, Cleveland TE, Nierman WC, Campbell BC (2008) Elucidation of the functional genomics of antioxidant-based inhibition of aflatoxin biosynthesis. Int J Food Microbiol 122: 49-60
29. Kirchberger S, Leroch M, Huynen MA, Wahl M, Neuhaus HE, Tjaden J (2007) Molecular and biochemical analysis of the plastidic adp-glucose transporter (zmbt1) from Zea mays. J Biol Chem 282: 22481-22491
30. Kodama O, Suzuki T, Miyakawa J, Akatsuka T (1988) Ultraviolet-induced accumulation of phytoalexins in rice leaves. Agric Biol Chem 52: 2469-2473
31. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TC, Gershenzon J, Degenhardt J (2008a) A maize (E)-b-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed inmost American maize varieties. Plant Cell 20: 482-494
32. Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J (2008b) Protonation of a neutral (S)-b-bisabolene intermediate is involved in (S)-b-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283: 20779-20788
33. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDC T method. Methods 254: 402-408
34. McCluskey K, Wiest A, Plamann M (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35: 119-126
35. Melanson D, Chilton MD, Masters-Moore D, Chilton WS (1997) A deletion in an indole synthase gene is responsible for the DIMBOAdeficient phenotype of bxbx maize. Proc Natl Acad Sci USA 94: 13345-13350
36. Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, Bak S (2008) b-Glucosidases as detonators of plant chemical defense. Phytochemistry 69: 1795-1813
37. Niemeyer HM (2009) Hydroxamic acids derived from 2-hydroxy-2H-1,4-benzoxazin-3(4H)-one: key defense chemicals of cereals. J Agric Food Chem 57: 1677-1696
38. Oikawa A, Ishihara A, Hasegawa M, Kodama O, Iwamura H (2001) Induced accumulation of 2-hydroxy-4,7-dimethoxy-1,4-benzoxazin-3-one glucoside (HDMBOA-Glc) in maize leaves. Phytochemistry 56: 669-675
39. Oikawa A, Ishihara A, Tanaka C, Mori N, Tsuda M, Iwamura H (2004) Accumulation of HDMBOA-Glc is induced by biotic stresses prior to the release of MBOA in maize leaves. Phytochemistry 65: 2995-3001
40. Peters RJ (2006) Uncovering the complex metabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants. Phytochemistry 67: 2307-2317
41. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TC (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434: 732-737
42. Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003a) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133: 295-306
43. Schmelz EA, Alborn HT, Tumlinson JH (2003b) Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect-induced volatile emission in Zea mays. Physiol Plant 117: 403-412
44. Schmelz EA, Engelberth J, Alborn HT, O'Donnell P, Sammons M, Toshima H, Tumlinson JH III (2003c) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci USA 100: 10552-10557
45. Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci USA 106: 653-657
46. Schmelz EA, Engelberth J, Tumlinson JH, Block A, Alborn HT (2004) The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J 39: 790-808
47. Schmelz EA, Kaplan F, Huffaker A, Dafoe NJ, Vaughan MM, Ni X, Rocca JR, Alborn HT, Teal PE (2011) Identity, regulation, and activity of inducible diterpenoid phytoalexins in maize. Proc Natl Acad Sci USA 108: 5455-5460
48. Schnee C, Kö llner TG, Held M, Turlings TC, 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
49. Selitrennikoff CP (2001) Antifungal proteins. Appl Environ Microbiol 67: 2883-2894
50. Smissman EE, LaPidus JB, Beck SD (1957) Corn plant resistance factor. J Org Chem 22: 220
51. Smith CJ (1996) Accumulation of phytoalexins: defence mechanism and stimulus response system. New Phytol 132: 1-45
52. Stoessla A, Stothersb JB, Ward EWB (1976) Sesquiterpenoid stress compounds of the solanaceae. Phytochemistry 15: 855-872
53. Suzuki R, Iijima M, Okada Y, Okuyama T (2007) Chemical constituents of the style of Zea mays L. with glycation inhibitory activity. Chem Pharm Bull (Tokyo) 55: 153-155
54. Tomasi N, Monte R, Rizzardo C, Venuti S, Zamboni A, Cesco S, Pinton R, Varanini Z (2009) Effects of water-extractable humic substances on molecular physiology of nitrate uptake in two maize inbread lines with different nitrogen use efficiency. The Proceedings of the International Plant Nutrition Colloquium XVI. Department of Plant Sciences, University of California, Davis, CA
55. Toyomasu T (2008) Recent advances regarding diterpene cyclase genes in higher plants and fungi. Biosci Biotechnol Biochem 72: 1168-1175
56. Turlings TC, Loughrin JH, McCall PJ, Röse US, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92: 4169-4174
57. Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivoreinduced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253
58. van der Linde K, Kastner C, Kumlehn J, Kahmann R, Dohlemann G (2011) Systemic virus-induced gene silencing allows functional characterization of maize genes during biotrophic interaction with Ustilago maydis. New Phytol 189: 471-483
59. Venard C, Vaillancourt L (2007) Colonization of fiber cells by Colletotrichum graminicola in wounded maize stalks. Phytopathology 97: 438-447
60. Virtanen AI, Hiet-aletal/et-ala PK (1955) 2(3)-Benzoxazolinone, an anti-Fusarium factor in rye seedlings. Acta Chem Scand 9: 1543-1544
61. Wagacha JM, Muthomi JW (2008) Mycotoxin problem in Africa: current status, implications to food safety and health and possible management strategies. Int J Food Microbiol 124: 1-12
62. Yu J, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178: 539-551
63. Zhang J, Boone L, Kocz R, Zhang C, Binns AN, Lynn DG (2000) At the maize/Agrobacterium interface: natural factors limiting host transformation. Chem Biol 7: 611-621