A maize (E)-beta-caryophyllene synthase implicated in indirect defense responses against herbivores is not expressed in most American maize varieties.
The sesquiterpene (E)-beta-caryophyllene is emitted by maize (Zea mays) leaves in response to attack by lepidopteran larvae like Spodoptera littoralis and released from roots after damage by larvae of the coleopteran Diabrotica virgifera virgifera. We identified a maize terpene synthase, Terpene Synthase 23 (TPS23), that produces (E)-beta-caryophyllene from farnesyl diphosphate. The expression of TPS23 is controlled at the transcript level and induced independently by D. v. virgifera damage in roots and S. littoralis damage in leaves. We demonstrate that (E)-beta-caryophyllene can attract natural enemies of both herbivores: entomopathogenic nematodes below ground and parasitic wasps, after an initial learning experience, above ground. The biochemical properties of TPS23 are similar to those of (E)-beta-caryophyllene synthases from dicotyledons but are the result of repeated evolution. The sequence of TPS23 is maintained by positive selection in maize and its closest wild relatives, teosinte (Zea sp) species. The gene encoding TPS23 is active in teosinte species and European maize lines, but decreased transcription in most North American lines resulted in the loss of (E)-beta-caryophyllene production. We argue that the (E)-beta-caryophyllene defense signal was lost during breeding of the North American lines and that its restoration might help to increase the resistance of these lines against agronomically important pests.
Köllner
Tobias G
TG
Max Planck Institute for Chemical Ecology, D-07745 Jena, Germany.
Held
Matthias
M
Lenk
Claudia
C
Hiltpold
Ivan
I
Turlings
Ted C J
TC
Gershenzon
Jonathan
J
Degenhardt
Jörg
J
D019883:Alkyl and Aryl Transferases / Q000235:genetics / Q000378:metabolism*; D000595:Amino Acid Sequence; D000818:Animals; D002849:Chromatography, Gas; D015971:Gene Expression Regulation, Enzymologic; D018506:Gene Expression Regulation, Plant; D006863:Hydrogen-Ion Concentration; D007113:Immunity, Innate / Q000235:genetics; D007814:Larva / Q000254:growth & development; D007915:Lepidoptera / Q000254:growth & development; D008969:Molecular Sequence Data; D015394:Molecular Structure; D010935:Plant Diseases / Q000235:genetics / Q000469:parasitology; D018515:Plant Leaves / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism* / Q000502:physiology; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000469:parasitology; D000081223:Polycyclic Sesquiterpenes; D011106:Polyisoprenyl Phosphates / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D012717:Sesquiterpenes / Q000378:metabolism; D003313:Zea mays / Q000235:genetics / Q000378:metabolism* / Q000469:parasitology
D010940:Plant Proteins; D000081223:Polycyclic Sesquiterpenes; D011106:Polyisoprenyl Phosphates; D012717:Sesquiterpenes; C004808:farnesyl pyrophosphate; C024714:caryophyllene; D019883:Alkyl and Aryl Transferases; C108877:terpene synthase