A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes

Planta. 2015 Jun;241(6):1351-61. doi: 10.1007/s00425-015-2254-z. Epub 2015 Feb 14.

Abstract

Of the three functional FPPS identified in maize, fpps3 is induced by herbivory to produce FDP important for the formation of the volatile sesquiterpenes of plant defense. Sesquiterpenes are not only crucial for the growth and development of a plant but also for its interaction with the environment. The biosynthesis of sesquiterpenes proceeds over farnesyl diphosphate (FDP), which is either used as a substrate for protein prenylation, converted to squalene, or to volatile sesquiterpenes. To elucidate the regulation of sesquiterpene biosynthesis in maize, we identified and characterized the farnesyl diphosphate synthase (FPPS) gene family which consists of three genes. Synteny analysis indicates that fpps2 and fpps3 originate from a genome duplication in an ancient tetraploid ancestor. The three FPPSs encode active enzymes that produce predominantly FDP from the isopentenyl diphosphate and dimethylallyl diphosphate substrates. Only fpps1 and fpps3 are induced by elicitor treatment, but induced fpps1 levels are much lower and only increased to the amounts of fpps3 levels in intact leaves. Elicitor-induced fpps3 levels in leaves increase to more than 15-fold of background levels. In undamaged roots, transcript levels of fpps1 are higher than those of fpps3, but only fpps3 transcripts are induced in response to herbivory by Diabrotica virgifera virgifera. A kinetic of transcript abundance in response to herbivory in leaves provided further evidence that the regulation of fpps3 corresponds to that of tps23, a terpene synthase, that converts FDP to the volatile (E)-ß-caryophyllene. Our study indicates that the differential expression of fpps1 and fpps3 provides maize with FDP for both primary metabolism and terpene-based defenses. The expression of fpps3 seems to coincide with the herbivore-induced emission of volatile sesquiterpenes that were demonstrated to be important defense signals.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkyl and Aryl Transferases / genetics
  • Alkyl and Aryl Transferases / metabolism
  • Amino Acid Sequence
  • Biosynthetic Pathways* / genetics
  • Gene Expression Regulation, Enzymologic
  • Gene Expression Regulation, Plant
  • Geranyltranstransferase / genetics
  • Geranyltranstransferase / metabolism*
  • Herbivory / physiology*
  • Kinetics
  • Molecular Sequence Data
  • Multigene Family*
  • Phylogeny
  • Plant Leaves / enzymology
  • Plant Proteins / chemistry
  • Plant Proteins / metabolism
  • Plant Roots / enzymology
  • Polyisoprenyl Phosphates / metabolism*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Sequence Alignment
  • Sesquiterpenes / metabolism*
  • Zea mays / enzymology*
  • Zea mays / genetics

Substances

  • Plant Proteins
  • Polyisoprenyl Phosphates
  • RNA, Messenger
  • Sesquiterpenes
  • farnesyl pyrophosphate
  • Alkyl and Aryl Transferases
  • terpene synthase
  • Geranyltranstransferase