Synergies and trade-offs between insect and pathogen resistance in maize leaves and roots

Plant, Cell and Environment

Volumn 34, Issue 7, 2011, Pages 1088-1103

  Erb, Matthias ^a   Balmer, Dirk ^a   De Lange, Elvira S ^a   Von Merey, Georg ^a   Planchamp, Chantal ^a   Robert, Christelle A M ^a   Röder, Gregory ^a   Sobhy, Islam ^a   Zwahlen, Claudia ^a   Mauch Mani, Brigitte ^a   Turlings, Ted C J ^a  

^a UNIVERSITY OF NEUCHÂTEL   (Switzerland)

Author keywords

Herbivore induced plant volatiles; Induced defence; Pathogens; Resistance; Root herbivory; Synergy; Zea mays

Indexed keywords

GREEN FLUORESCENT PROTEIN; VOLATILE ORGANIC COMPOUND;

CORRELATION; DEFENSE BEHAVIOR; DISEASE RESISTANCE; ECOTYPE; FUNCTIONAL MORPHOLOGY; HERBIVORE; INBREEDING; INSECT; INTRASPECIFIC VARIATION; LEAF; MAIZE; MEASUREMENT METHOD; OPTIMIZATION; PATHOGENICITY; PHYSIOLOGICAL RESPONSE; POPULATION STRUCTURE; REPRODUCTIVE BEHAVIOR; ROOT; SYNERGISM; TRADE-OFF;

ANIMAL; ARMYWORM; ARTICLE; ASCOMYCETES; BEETLE; BIOMASS; CHEMISTRY; COLLETOTRICHUM; FEEDING BEHAVIOR; GENETIC LINKAGE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INNATE IMMUNITY; LARVA; MAIZE; MICROBIOLOGY; PARASITOLOGY; PATHOGENICITY; PLANT DISEASE; PLANT LEAF; PLANT ROOT;

ANIMALS; ASCOMYCOTA; BEETLES; BIOMASS; COLLETOTRICHUM; FEEDING BEHAVIOR; GENETIC LINKAGE; GENOTYPE; GREEN FLUORESCENT PROTEINS; IMMUNITY, INNATE; LARVA; PLANT DISEASES; PLANT LEAVES; PLANT ROOTS; SPODOPTERA; VOLATILE ORGANIC COMPOUNDS; ZEA MAYS;

HEXAPODA; ZEA MAYS;

EID: 79958752327     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2011.02307.x     Document Type: Article

References (54)

1. Acquaah G. (2007) Principles of Plant Genetics and Breeding. Blackwell Publishing Ltd, United Kingdom.
2. Ali J.G., Alborn H.T. & Stelinski L.L. (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. Journal of Chemical Ecology 36, 361-368.
3. Ballhorn D.J., Kautz S., Lion U. & Heil M. (2008) Trade-offs between direct and indirect defences of lima bean (Phaseolus lunatus). Journal of Ecology 96, 971-980.
4. Bernasconi M.L., Turlings T.C.J., Ambrosetti L., Bassetti P. & Dorn S. (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomologia Experimentalis et Applicata 87, 133-142.
5. Biere A., Marak H.B. & van Damme J.M.M. (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140, 430-441.
6. Bruce T.J.A. & Pickett J.A. (2007) Plant defence signalling induced by biotic attacks. Current Opinion in Plant Biology 10, 387-392.
7. Carroll M.J., Schmelz E.A., Meagher R.L. & Teal P.E.A. (2006) Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. Journal of Chemical Ecology 32, 1911-1924.
8. De Moraes C.M., Mescher M.C. & Tumlinson J.H. (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577-580.
9. De Vos M., Van Zaanen W., Koornneef A., Korzelius J.P., Dicke M., Van Loon L.C. & Pieterse C.M.J. (2006) Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiology 142, 352-363.
10. Degen T., Dillmann C., Marion-Poll F. & Turlings T.C.J. (2004) High genetic variability of herbivore-induced volatile emission within a broad range of maize inbred lines. Plant Physiology 135, 1928-1938.
11. Dicke M., van Loon J.J.A. & Soler R. (2009) Chemical complexity of volatiles from plants induced by multiple attack. Nature Chemical Biology 5, 317-324.
12. Donald C.M. & Hamblin J. (1976) Biological yield and harvest index of cereals as agronomic and plant breeding criteria. Advances in Agronomy 28, 361-405.
13. Erb M., Flors V., Karlen D., de Lange E., Planchamp C., D'Alessandro M., Turlings T.C.J. & Ton J. (2009a) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. The Plant Journal 59, 292-302.
14. Erb M., Gordon-Weeks R., Camañes G., Turlings T.C.J. & Ton J. (2009b) Belowground ABA boosts aboveground production of DIMBOA and primes induction of chlorogenic acid in maize. Plant Signaling & Behavior 4, 639-642.
15. Felton G.W. & Korth K.L. (2000) Trade-offs between pathogen and herbivore resistance. Current Opinion in Plant Biology 3, 309-314.
16. Fernandez P. & Hilker M. (2007) Host plant location by Chrysomelidae. Basic and Applied Ecology 8, 97-116.
17. Frey M., Chomet P., Glawischnig E., etal. (1997) Analysis of a chemical plant defense mechanism in grasses. Science 277, 696-699.
18. 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.
19. Gazzarrini S. & McCourt P. (2003) Cross-talk in plant hormone signalling: what Arabidopsis mutants are telling us. Annals of Botany 91, 605-612.
20. Halitschke R., Stenberg J.A., Kessler D., Kessler A. & Baldwin I.T. (2008) Shared signals -'alarm calls' from plants increase apparency to herbivores and their enemies in nature. Ecology Letters 11, 24-34.
21. Held M., Gase K. & Baldwin I.T. (2004) Microarrays in ecological research: a case study of a cDNA microarray for plant-herbivore interactions. BMC Ecology 4, 13.
22. Kant M.R., Bleeker P.M., Van Wijk M., Schuurink R.C. & Haring M.A. (2009) Plant volatiles in defence. In Plant Innate Immunity (ed. L.C. Van Loon) pp. 613-666. Advances in Botanical Research, Academic Press, Maryland Heights, USA.
23. Karban R. & Baldwin I.T. (1997) Induced Responses to Herbivory. University of Chicago Press, Chicago, IL, USA.
24. Köllner T.G., Held M., Lenk C., Hiltpold I., Turlings T.C.J., Gershenzon J. & Degenhardt J. (2008) A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties. The Plant Cell 20, 482-494.
25. Koul O. (2008) Phytochemicals and insect control: an antifeedant approach. Critical Reviews in Plant Sciences 27, 1-24.
26. Landolt P.J., Tumlinson J.H. & Alborn D.H. (1999) Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environmental Entomology 28, 973-978.
27. Leimu R. & Koricheva J. (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. The American Naturalist 168, E15-E37.
28. 2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiology 148, 818-828.
29. Maffei M.E., Mithofer A. & Boland W. (2007) Before gene expression: early events in plant-insect interaction. Trends in Plant Science 12, 310-316.
30. McCluskey K. (2003) The fungal genetics stock center: from molds to molecules. Advances in Applied Microbiology 52, 245-262.
31. Mitchell-Olds T., James R.V., Palmer M.J. & Williams P.H. (1995) Genetics of Brassica rapa (syn campestris). Multiple disease resistance to 3 fungal pathogens -Peronospora parasitica, Albugo candida and Leptosphaeria maculans. Heredity 75, 362-369.
32. Neveu N., Grandgirard J., Nenon J.P. & Cortesero A.M. (2002) Systemic release of herbivore-induced plant volatiles by turnips infested by concealed root-feeding larvae Delia radicum L. Journal of Chemical Ecology 28, 1717-1732.
33. Núñez-Farfán J., Fornoni J. & Valverde P.L. (2007) The evolution of resistance and tolerance to herbivores. Annual Review of Ecology Evolution and Systematics 38, 541-566.
34. Rasmann S. & Agrawal A.A. (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Current Opinion in Plant Biology 12, 473-478.
35. Rasmann S. & Turlings T.C.J. (2008) First insights into specificity of belowground tritrophic interactions. Oikos 117, 362-369.
36. Rasmann S., Köllner T.G., Degenhardt J., Hiltpold I., Toepfer S., Kuhlmann U., Gershenzon J. & Turlings T.C.J. (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732-737.
37. Rausher M.D. (1996) Genetic analysis of coevolution between plants and their natural enemies. Trends in Genetics 12, 212-217.
38. Rausher M.D. (2001) Co-evolution and plant resistance to natural enemies. Nature 411, 857-864.
39. Rebourg C., Chastanet M., Gouesnard B., Welcker C., Dubreuil P. & Charcosset A. (2003) Maize introduction into Europe: the history reviewed in the light of molecular data. Theoretical and Applied Genetics 106, 895-903.
40. Rostas M. (2007) The effects of 2, 4-dihydroxy-7-methoxy-1, 4-benzoxazin-3-one on two species of Spodoptera and the growth of Setosphaeria turcica in vitro. Journal of Pest Science 80, 35-41.
41. Rudgers J.A., Strauss S.Y. & Wendel J.E. (2004) Trade-offs among anti-herbivore resistance traits: insights from Gossypieae (malvaceae). American Journal of Botany 91, 871-880.
42. Schmelz E.A., Alborn H.T., Banchio E. & Tumlinson J.H. (2003) Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216, 665-673.
43. Schwachtje J. & Baldwin I.T. (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiology 146, 845-851.
44. Shivaji R., Camas A., Ankala A., Engelberth J., Tumlinson J.H., Williams W.P., Wilkinson J.R. & Luthe D.S. (2010) Plants on constant alert: elevated levels of jasmonic acid and jasmonate-induced transcripts in caterpillar-resistant maize. Journal of Chemical Ecology 36, 179-191.
45. Spoel S.H., Johnson J.S. & Dong X. (2007) Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proceedings of the National Academy of Sciences of the United States of America 104, 18842-18847.
46. Strauss S.Y., Sahli H. & Conner J.K. (2005) Toward a more trait-centered approach to diffuse (co)evolution. New Phytologist 165, 81-89.
47. Sukno S.A., Garcia V.M., Shaw B.D. & Thon M.R. (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Applied and Environmental Microbiology 74, 823-832.
48. Ter Braak C.J.F. & Smilauer P. (2002) CANOCO Reference Manual and CanoDraw for Windows User's Guide: Software for Canonical Community Ordination (Version 4.5). Microcomputer Power, Ithaca, NY, USA.
49. Troyer A.F. (1999) Background of US hybrid corn. Crop Science 39, 601-626.
50. Turlings T.C.J., Davison A.C. & Tamo C. (2004) A six-arm olfactometer permitting simultaneous observation of insect attraction and odour trapping. Physiological Entomology 29, 45-55.
51. Van Oosten V.R., Bodenhausen N., Reymond P., Van Pelt J.A., Van Loon L.C., Dicke M. & Pieterse C.M.J. (2008) Differential effectiveness of microbially induced resistance against herbivorous insects in Arabidopsis. Molecular Plant-Microbe Interactions 21, 919-930.
52. Voelckel C. & Baldwin I.T. (2004) Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. The Plant Journal 38, 650-663.
53. Wang R.L., Stec A., Hey J., Lukens L. & Doebley J. (1999) The limits of selection during maize domestication. Nature 398, 236-239.
54. Wooley S.C., Donaldson J.R., Gusse A.C., Lindroth R.L. & Stevens M.T. (2007) Extrafloral nectaries in aspen (Populus tremuloides): heritable genetic variation and herbivore-induced expression. Annals of Botany 100, 1337-1346.