Restoring (E)-β-Caryophyllene Production in a Non-producing Maize Line Compromises its Resistance against the Fungus Colletotrichum graminicola

Journal of Chemical Ecology

Volumn 41, Issue 3, 2015, Pages 213-223

  Fantaye, Chalie Assefa ^a   Köpke, Diana ^a   Gershenzon, Jonathan ^a   Degenhardt, Jörg ^b  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

(E) caryophyllene; Colletotrichum graminicola; Plant defense; Volatile sesquiterpenes; Zea mays

Indexed keywords

ANTIFUNGAL AGENT; BENZOXAZINE DERIVATIVE; CARYOPHYLLENE; GLUCOSIDE; SESQUITERPENE;

CHEMISTRY; COLLETOTRICHUM; DRUG EFFECTS; FUSARIUM; GROWTH, DEVELOPMENT AND AGING; INBREEDING; MAIZE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE;

ANTIFUNGAL AGENTS; BENZOXAZINES; COLLETOTRICHUM; FUSARIUM; GLUCOSIDES; INBREEDING; PLANT DISEASES; SESQUITERPENES; ZEA MAYS;

EID: 84937765357     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-015-0556-z     Document Type: Article

References (57)

1. Aharoni A, Jongsma MA, Bouwmeester HJ (2005) Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci 10:594–602
2. Ahmad S, Veyrat N, Gordon-Weeks R, Zhang Y, Martin J, Smart L, Glauser G, Erb M, Flors V, Frey M, Ton J (2011) Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. J Plant Physiol 157:317–327
3. Armstrong CL, Green CE, Phillips RL (1991) Development and availability of germplasm with high Type II culture formation response. Maize Genet Newsletter. www.agron.missouri.edu/mnl/65/146armstrong.html. Accessed 30 May 2012
4. Asran MR, Buchenauer H (2003) Pathogenecity of Fussarium graminearum isolates on maize (Zea mays L.) cultivars and relation with deoxynivalenol and ergosterol contents. J Plant Dis Prot 110:209–219
5. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA (2006) Volatile signaling in plant-plant interactions: “talking trees” in the genomics era. Science 311:812–815
6. Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488
7. Bergstrom GC, Nicholson RL (1999) The biology of corn anthracnose - knowledge to exploit for improved management. Plant Dis 83:596–608
8. Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol Exp Appl 87:133–142
9. Birch ANE, Geoghegan IE, Griffiths DW, McNicol JW (2002) The effect of genetic transformations for pest resistance on foliar solanidine-based glycoalkaloids of potato (Solanum tuberosum). Ann Appl Biol 140:143–149
10. Cambier V, Hance T, de Hoffmann E (2000) Variation of DIMBOA and related compounds content in relation to the age and plant organ in maize. Phytochemistry 53:223–229
11. Cavanagh HMA (2007) Antifungal activity of the volatile phase of essential oils: a brief review. Nat Prod Commun 2:1297–1302
12. Cellini F, Chesson A, Colquhoun I, Constable A, Davies HV, Engel KH, Gatehouse AMR, Karenlampi S, Kok EJ, Leguay JJ, Lehesranta S, Noteborn HPJM, Pedersen J, Smith M (2004) Unintended effects and their detection in genetically modified crops. Food Chem Toxicol 42:1089–1125
13. Dafoe NJ, Huffaker A, Vaughan MM, Duehl AJ, Teal PE, Schmelz EA (2011) Rapidly induced chemical defenses in maize stems and their effects on short-term growth of Ostrinia nubilalis. J Chem Ecol 37:984–991
14. De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580
15. 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. J Plant Physiol 135:1928–1938
16. Degenhardt J, Hiltpold I, Koellner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TCJ (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci U S A 106:13213–13218
17. Dicke M (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomol Exp Appl 91:131–142
18. Droby S, Eick A, Macarisin D, Cohen L, Rafael G, Stange R, McColum G, Dudai N, Nasser A, Wisniewski M, Shapira R (2008) Role of citrus volatiles in host recognition, germination and growth of Penicillium digitatum and Penicillium italicum. Postharvest Biol Technol 49:386–396
19. Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D’Alessandro M, Turlings TCJ, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302
20. Erb M, Balmer D, De Lange ES, Von Merey G, Planchamp C, Robert CAM, Roeder G, Sobhy I, Zwahlen C, Mauch-Mani B, Turlings TCJ (2011) Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots. Plant Cell Environ 34:1088–1103
21. Fontana A, Held M, Fantaye CA, Turlings TC, Degenhardt J, Gershenzon J (2011) Attractiveness of constitutive and herbivore-induced sesquiterpene blends of maize to the parasitic wasp Cotesia marginiventris (Cresson). J Chem Ecol 37:582–591
22. Frandsen RJN, Nielsen NJ, Maolanon N, Sorensen JC, Olsson S, Nielsen J, Giese H (2006) The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol Microbiol 61:1069–1080
23. Grant M, Lamb C (2006) Systemic immunity. Curr Opin Plant Biol 9:414–420
24. Grover RK, Moore JD (1962) Toximetric studies of fungicides against the brown root organisms, Sclerotinia fructicola and S. laxa. J Phytopathol 52:876–880
25. Hammerschmidt R, Nicholson RL (1977) Resistance of maize to anthracnose-changes in host phenols and pigments. J Phytopathol 67:251–258
26. Hipskind J, Wood K, Nicholson RL (1996) Localized stimulation of anthocyanin accumulation and delineation of pathogen ingress in maize genetically resistant to Bipolaris maydis race O. Physiol Mol Plant Pathol 49:247–256
27. Huang M, Sanchez-Moreiras AM, Abel C, Sohrabi R, Lee S, Gershenzon J, Tholl D (2012) The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-beta-caryophyllene, is a defense against a bacterial pathogen. New Phytol 193:997–1008
28. Huffaker A, Dafoe NJ, Schmelz EA (2011) ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. J Plant Physiol 155:1325–1338
29. Jin SM, Xu RL, Wei YD, Goodwin PH (1999) Increased expression of a plant actin gene during a biotrophic interaction between round-leaved mallow, Malva pusilla, and Colletotrichum gloeosporioides f. sp malvae. Planta 209:487–494
30. Junker RR, Gershenzon J, Unsicker SB (2011) Floral odor bouquet loses its ant repellent properties after inhibition of terpene biosynthesis. J Chem Ecol 37:1323–1331
31. Knudsen JT, Eriksson R, Gershenzon J, Stahl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
32. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004a) 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
33. Köllner TG, Schnee C, Gershenzon J, Degenhardt J (2004b) The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distribution. Phytochemistry 65:1895–1902
34. Köllner TG, Held M, Lenk C, Hiltpold I, Turlings TCJ, Gershenzon J, Degenhardt J (2008a) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. Plant Cell 20:482–494
35. 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 maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem 283:20779–20788
36. Köllner TG, Lenk C, Schnee C, Köpke S, Lindemann P, Gershenzon J, Degenhardt J (2013) Localization of sesquiterpene formation and emission in maize leaves after herbivore damage. BMC Plant Biol 13:15
37. Lyons PC, Nicholson RL (1989) Evidence that cyclic hydroxamate concentrations are not related to resistance of corn leaves to anthracnose. Can J Plant Pathol 11:215–220
38. Mendgen K, Wirsel SGR, Jux A, HoVmann J, Boland W (2006) Volatiles modulate the development of plant pathogenic rust fungi. Planta 224:1353–1361
39. 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
40. Presello DA, Iglesias J, Botta G, Reid LM, Lori GA, Eyherabide GH (2006) Stability of maize resistance to the ear rots caused by Fusarium graminearum and F. verticillioides in Argentinian and Canadian environments. Euphytica 147:403–407
41. Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614
42. 2. J Plant Physiol 115:137–149
43. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737
44. Robert C, Erb M, Hiltpold I, Hibbard B, Gaillard M, Bilat J, Degenhardt J, Cambet-Petit-Jean X, Turlings T, Zwahlen C (2013) Genetically engineered maize plants reveal distinct costs and benefits of constitutive volatile emissions in the field. Plant Biotechnol J 11:628–639
45. Rodov V, Benyehoshua S, Fang DQ, Kim JJ, Ashkenazi R (1995) Preformed antifungal compounds of lemon fruit-citral and its relation to disease resistance. J Agric Food Chem 43:1057–1061
46. Rodriguez A, San Andres V, Cervera M, Redondo A, Alquezar B, Shimada T, Gadea J, Jesus Rodrigo M, Zacarias L, Palou L, Lopez MM, Castanera P, Pena L (2011) Terpene down-regulation in orange reveals the role of fruit aromas in mediating interactions with insect herbivores and pathogens. J Plant Physiol 156:793–802
47. Schmelzer E (2002) Cell polarization, a crucial process in fungal defense. Trends Plant Sci 7:411–415
48. 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 U S A 103:1129–1134
49. Shivaji R, Camas A, Ankala A, Engelberth J, Tumlinson JH, Williams WP, Wilkinson JR, Luthe DS (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. J Chem Ecol 36:179–191
50. Smith WEC, Shivaji R, Williams WP, Luthe DS, Sandoya GV, Smith CL, Sparks DL, Brown AE (2012) A Maize line resistant to herbivory constitutively releases (E)-beta-caryophyllene. J Econ Entomol 105:120–128
51. Sukno SA, Garcia VM, Shaw BD, Thon MR (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Appl Environ Microbiol 74:823–832
52. Tholl D, Chen F, Gershenzon J, Pichersky F (2004) Arabidopsis thaliana, a model system for investigating volatile terpene biosynthesis, regulation, and function. In: JT Romeo (ed) Secondary metabolism in model systems, vol 38, pp 1–18
53. Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757–771
54. Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithoefer A (2012) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. J Plant Physiol 159:1159–1175
55. Vargas WA, Sanz Martin JM, Rech GE, Rivera LP, Benito EP, Diaz-Minguez JM, Thon MR, Sukno SA (2012) Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. J Plant Physiol 158:1342–1358
56. Vigier B, Reid LM, Dwyer LM, Stewart DW, Sinha RC, Arnason JT, Butler G (2001) Maize resistance to gibberella ear rot: symptoms, deoxynivalenol, and yield. Can J Plant Pathol 23:99–105
57. Weibull J, Niemeyer HM (1995) Changes in dihydroxymethoxybenzoxazione glycoside content in wheat plants infected by 3 plant-pathogenic fungi. Physiol Mol Plant Pathol 47:201–212