Elsevier

Phytochemistry

Volume 65, Issue 13, July 2004, Pages 1895-1902
Phytochemistry

The sesquiterpene hydrocarbons of maize (Zea mays) form five groups with distinct developmental and organ-specific distributions

https://doi.org/10.1016/j.phytochem.2004.05.021Get rights and content

Abstract

The sesquiterpene hydrocarbon chemistry of maize (Zea mays) inbred line B73 was analyzed by both direct solvent extraction and headspace sampling. In seedlings, 15 olefinic compounds were identified, and 21 olefins were detected in mature plants after anthesis. Both solvent extracts and collections of headspace terpenes were found to contain the same compounds in the same relative proportions suggesting that there is no selective barrier to release from plants. Approximately 25% of the stored pool was found to be released from young seedlings per hour. The individual sesquiterpenes varied extensively in their abundance among different organs and developmental stages. Compounds could be divided into five different groups such that the members of each group always occur together in the same constant ratios to one another. Each group has a distinct distribution pattern. Group A includes the two dominant compounds, (E)-β-farnesene and α-bergamotene, and appears only after herbivore damage in seedlings, but is constitutively present in the leaves and husks after anthesis. The major compounds of group B, including α-copaene, germacrene D and δ-cadinene, were present throughout the seedling but found only in husks of mature plants. The group C compounds, β-bisabolene and an unknown sesquiterpene olefin, are restricted to the roots. The presence of group D and E compounds was confined to the leaves and husk of mature plants. The complex sesquiterpene mixture of group D is identical to the products formed by the previously identified terpene synthase TPS4, suggesting that each of the four other sesquiterpene hydrocarbon mixtures may also represent the products of a single terpene synthase.

Analysis of the sesquiterpene content of young and mature maize plants revealed five groups of hydrocarbons, each with a different spatial and temporal distribution in the plant. Within each group, compounds co-occurred in the same constant ratio to one another, indicative of possible biosynthetic relationships.

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Introduction

Plants form large numbers of structurally diverse terpene natural products (Connolly and Hill, 1991). Although terpenes play many important roles in primary metabolism, most are secondary products that occur in complex mixtures and exhibit enormous variation among and within species (Harborne and Turner, 1984). The toxicity of many terpenes to herbivorous insects and microbes implicates them in the direct defense of plants (Gershenzon and Croteau, 1991). However, terpenes are also involved in another plant defense strategy termed `indirect defense', in which volatile terpenes released from herbivore-damaged plants attract enemies of the attacking herbivore (Dicke, 1999). As yet, little is known about the relative importance of terpenes as direct versus indirect defenses in different plant parts. A genetically-tractable model species in which terpene content could be readily modified would represent an ideal experimental system for such studies.

We have begun to investigate the formation and function of terpene natural products in Zea mays L. (Degenhardt and Gershenzon, 2000; Köllner et al., 2004; Schnee et al., 2002). In this species, indirect defense against herbivores has been studied in detail at the seedling stage where attack by lepidopteran larvae, such as Spodoptera littoralis, leads to the emission of terpene volatiles (Turlings et al., 1990, Turlings et al., 1991; Turlings and Tumlinson, 1992). These volatiles attract parasitic wasps that use the larvae as hosts, thus reducing damage to the plant (Hoballah and Turlings, 2001). The volatile emission rate after herbivore attack is highest in two week-old seedlings (Turlings et al., 1991) and varies among cultivars and species of the genus Zea (Gouinguene et al., 2001). The role of terpenes in direct defense against maize herbivores has also been studied (Binder and Robbins, 1997; Lee et al., 1999). However, the operation of these two defense strategies in different organs and at different growth stages, especially in mature plants, is unknown. Moreover, there is little information about the terpene composition of mature maize except for single analyses of leaves, husk and kernel oil in commercial hybrid cultivars that were not precisely defined (Buttery et al., 1978; Buttery and Ling, 1984). Analyses of silk tissue from several maize cultivars did not detect terpenes (Flath et al., 1978; Zeringue, 2000).

A prerequisite for investigating the ecological role of terpenes in maize is a thorough examination of terpene composition in a genetically well-defined maize cultivar. We chose the inbred line B73 as the subject for this study since it does not exhibit allelic polymorphisms and has been established as the model variety for molecular and genetic studies of maize (Gai et al., 2000). A terpene analysis of B73 will also provide a valuable tool for study of the biochemistry and molecular biology of terpene biosynthesis in this species. Here, we report on the spatial and temporal variation of sesquiterpene hydrocarbon formation in maize line B73. The 21 identified compounds form five distinct groups in which substances co-occur in a constant ratio to one another. Each group has a distinct pattern of occurrence in different organs and developmental stages.

Section snippets

Comparison of sesquiterpene content as measured by solvent extraction and headspace collection

The isolation of sesquiterpenes from maize has previously been carried out by dynamic headspace collection (Buttery and Ling, 1984; Turlings et al., 1991) and steam distillation (Thompson et al., 1974; Flath et al., 1978; Buttery et al., 1978). However, headspace collection does not sample compounds stored in plant tissue, and steam distillation is likely to produce artifacts as a result of degradation and rearrangements (Chaintreau, 2001). To overcome these limitations, we employed a simple

Plant and insect material

Seeds of the maize (Zea mays L.) inbred line B73 were provided by KWS seeds (Einbeck, Germany) and were grown in commercially available potting soil in a climate-controlled chamber with a 16 h photoperiod, 1 mmol (m2)−1 s−1 of photosynthetically-active radiation, a temperature cycle of 22/18 °C (day/night) and 65% relative humidity. Twelve to fifteen day old-plants (15–25 cm high, 4–5 expanded leaves) were used in all experiments. Eggs of Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae)

Acknowledgements

We are grateful to KWS seeds (Einbeck, Germany) for maize B73 seeds, Aventis (Frankfurt, Germany) for Spodoptera littoralis and Wilfried A. König for the donation of sesquiterpene standards. This work was supported by the German National Science Foundation (grant DE-837/2-1) and the Max Planck Society. J.D. was supported by a fellowship of the Claussen–Simon foundation.

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