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

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Abstract

Main conclusion

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.

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Abbreviations

DMADP:

Dimethylallyl diphosphate

FARM:

First aspartate-rich motif

FDP:

Farnesyl diphosphate

FPPS:

Farnesyl diphosphate synthase

GDP:

Geranyl diphosphate

GGDP:

Geranylgeranyl diphosphate

GGPPS:

Geranylgeranyl diphosphate synthase

IDP:

Isopentenyl diphoshphate

LG:

Linolenoyl-l-glutamine

SARM:

Second aspartate-rich motif

TPS:

Terpene synthase

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Acknowledgments

The authors would like to thank Matthias Erb for D. virgifera-treated root material. We are indebted to Raimund Nagel and Michael Reichelt for help with LC-MS analysis. A. Richter and J. Degenhardt were supported by project B7 of the Collaborative Research Center 648 of the German Research Foundation (DFG). I. Seidl-Adams was supported by two travel Grants of the Collaborative Research Center 648 of the German Research Foundation (DFG).

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Authors and Affiliations

  1. Institute of Pharmacy, Martin Luther University Halle, Hoher Weg 8, 06120, Halle, Germany

    Annett Richter, Claudia Schaff & Jörg Degenhardt

  2. Chemical Ecology, The Pennsylvania State University, University Park, State College, PA, 16802, USA

    Irmgard Seidl-Adams & James H. Tumlinson

  3. Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, 07745, Jena, Germany

    Tobias G. Köllner

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  1. Annett Richter
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  2. Irmgard Seidl-Adams
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  3. Tobias G. Köllner
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Richter, A., Seidl-Adams, I., Köllner, T.G. et al. A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes. Planta 241, 1351–1361 (2015). https://doi.org/10.1007/s00425-015-2254-z

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