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Localization of Sesquiterpene Formation and Emission in Maize

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Localization of Sesquiterpene Formation and Emission in Maize Köllner et al. BMC Plant Biology 2013, 13:15 http://www.biomedcentral.com/1471-2229/13/15 RESEARCH ARTICLE Open Access Localization of sesquiterpene formation and emission in maize leaves after herbivore damage Tobias G Köllner1*, Claudia Lenk2, Christiane Schnee1,3, Sabrina Köpke1, Peter Lindemann2, Jonathan Gershenzon1 and Jörg Degenhardt2 Abstract Background: Maize (Zea mays L.) leaves damaged by lepidopteran herbivores emit a complex volatile blend that can attract natural enemies of the herbivores and may also have roles in direct defense and inter- or intra-plant signaling. The volatile blend is dominated by sesquiterpenes of which the majority is produced by two herbivore-induced terpene synthases, TPS10 and TPS23. However, little is known about the pattern of volatile emission within maize leaves. Results: In this study, we restricted herbivore feeding to small sections of the maize leaf with the aim of determining the patterns of volatile sesquiterpene emission throughout the damaged leaf and in neighboring leaves. Sesquiterpene volatiles were released at high rates from damaged leaves, but at much lower rates from neighboring leaves. Release was restricted to the site of damage or to leaf sections located apical to the damage, but was not seen in sections basal to the damage or on the other side of the midrib. The emission pattern correlated well with the transcript pattern of the respective sesquiterpene synthase genes, tps10 and tps23, implying that biosynthesis likely occurs at the site of emission. The concentrations of jasmonic acid and its leucine derivative were also elevated in terpene-emitting tissues suggesting a role for jasmonates in propagating the damage signal. Conclusions: In contrast to other defense reactions which often occur systemically throughout the whole plant, herbivore-induced sesquiterpene production in maize is restricted to the wounding site and distal leaf parts. Since the signal mediating this reaction is directed to the leaf tip and cannot propagate parallel to the leaf axis, it is likely connected to the xylem. The increasing gradient of volatiles from the tip of the leaf towards the damage site might aid herbivore enemies in host or prey finding. Keywords: Zea mays L., Poaceae, Maize, Sesquiterpenes, Volatiles, Terpene biosynthesis, Terpene synthase, Herbivore-induced terpene formation, Jasmonic acid, Solid-phase microextraction (SPME) Background intra- and inter-plant communication [4]. However, The emission of volatiles by plants allows them to inter- some of these roles are only poorly studied. More know- act with other organisms at a distance. For example, ledge about precisely where volatiles are emitted within many plant species emit floral volatiles which have di- a leaf might reveal more about their roles. verse functions in pollinator attraction and repulsion [1]. During the last two decades maize (Zea mays L.) Volatiles are also released from vegetative plant organs, has been established as a model system for studying especially after herbivore damage. Vegetative volatiles herbivore-induced vegetative volatiles. Maize leaves da- can function as attractants for enemies of herbivores [2] maged by lepidopteran larvae emit a complex blend of and have been suggested to serve as direct defenses volatiles that can be utilized by parasitoids of the herbi- against herbivores [2], as defenses against pathogens [3], vore to locate their potential hosts on the infested plant as protectants against abiotic stress, and as signals in [5]. The parasitoids oviposit on or into the host which continues to feed, but often at reduced levels, and even- * Correspondence: [email protected] tually dies without reaching the adult stage [6,7]. Re- 1Max Planck Institute for Chemical Ecology, Hans-Knöll-Strasse 8, D-07745 Jena, Germany cruitment of herbivore enemies can thus be beneficial Full list of author information is available at the end of the article for the plant and has been termed “indirect plant © 2013 Köllner et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Köllner et al. BMC Plant Biology 2013, 13:15 Page 2 of 10 http://www.biomedcentral.com/1471-2229/13/15 defense”. The volatile blend of herbivore-damaged maize nearly all plant organs and seems to be involved in leaves consists of three classes of compounds: 1) mono-, pathogen defense (Fontana A, Köllner TG, Schnee S, sesqui- and homoterpenes produced by the isoprenoid Reichelt M, Rosenberger D, Luck K, Gershenzon J, pathways, 2) green-leaf odors such as saturated and un- Degenhardt J: A complex blend of volatile sesquiter- saturated six-carbon alcohols and esters derived from penes produced by maize terpene synthase 8 (TPS8) the lipoxygenase pathway and 3) aromatic compounds is active against a necrotrophic fungus in planta. like indole, methyl anthranilate and methyl salicylate submitted). generated by the shikimate/tryptophan pathway [5,8]. Despite all of the available information about the The quantitative and qualitative composition of this chemical and molecular bases of terpene emission in blend varies between maize cultivars but is usually domi- maize, we know little about its location within individual nated by sesquiterpenes [8-11]. While the majority of leaves. More knowledge of where volatiles are made and the sesquiterpene volatiles is released from the emitted in maize leaves would not only shed more light herbivore-damaged leaf itself, low levels of volatile emis- on their function, but also increase our understanding of sion have also been observed from adjacent leaves [12]. what controls synthesis and emission. In this study we The composition of the blend from adjacent leaves is have investigated the pattern of sesquiterpene emission different from damaged leaves in that it lacks most ses- and biosynthetic gene expression in herbivore-damaged quiterpenes but still contains the monoterpene linalool vs. control leaves and at the site of herbivory vs. sections and the homoterpenes (3E)-4,8-dimethyl-1,3,7-nona- of the rest of the leaf. To detect the small amounts of triene (DMNT) and (3E,7E)-4,8,12-trimethyl-1,3,7,11-tri- sesquiterpenes emitted by individual leaf parts, we ana- decatetraene (TMTT) [12]. lyzed the volatiles released from macerated tissues and Previous studies with maize have shown a strong cor- used them as an estimate for natural sesquiterpene emis- relation between monoterpene and sesquiterpene emis- sion. Both gene expression and emission data indicate a sion and biosynthesis [10], suggesting that compounds directed movement of a damage-induced signal toward are released soon after synthesis without any long-term the apex of the leaf and not across the midrib. Analysis storage. But the relationship between emission and bio- of defense hormone levels within the leaf suggests the synthesis has never been studied within individual leaves. involvement of jasmonates in the signaling process. The majority of herbivore-induced sesquiterpenes of maize is produced by two terpene synthases (TPS) which Results both convert the farnesyl diphosphate (FPP) substrate Sesquiterpene production is induced in herbivore- into multiple, structurally diverse products. The terpene damaged leaves, but only at low levels in neighboring synthase TPS10 forms (E)-α-bergamotene and (E)-β-far- control leaves nesene along with thirteen minor sesquiterpenes in The response of the leaves of maize cultivar B73 to herbivore-damaged leaves [13]. The efficacy of TPS10 herbivore attack was investigated by measurement of sesquiterpenes for indirect defense against lepidopteran both sesquiterpene release and the transcript level of larvae has been tested with Arabidopsis plants overex- TPS10, the most important enzyme in volatile sesquiter- pressing TPS10. After an initial learning experience, the pene biosynthesis in herbivore-damaged leaves. Since TPS10 volatiles were utilized by the parasitic wasp Cote- there is no standard method sensitive enough to meas- sia marginiventris to find their lepidopteran host [13]. ure head-space volatiles from small areas of plant tissue, The herbivore-induced sesquiterpene synthase TPS23 we macerated leaf samples in liquid nitrogen and ana- forms mostly (E)-β-caryophyllene which can also attract lyzed the release of terpenes from the resulting powder parasitic wasps to leaf-feeding herbivores [14]. In using solid-phase microextraction (SPME). A prelimin- addition, TPS23 is induced in roots after damage by the ary experiment carried out on entire plants comparing western corn rootworm (Diabrotica virgifera virgifera) the maceration method with conventional head-space where the (E)-β-caryophyllene product attracts entomo- volatile collection revealed that the amount of sesquiter- pathogenic nematodes to the attacking herbivore [14,15]. penes released from total leaf powder and collected While nearly all maize cultivars produce the TPS10 pro- using a SPME fiber was directly correlated with the ducts (E)-α-bergamotene and (E)-β-farnesene, the TPS23 amount of head-space sesquiterpenes emitted from in- product (E)-β-caryophyllene is only formed in European tact plants (Additional file 1: Figure S1) demonstrating maize lines [8,14]. Apparently, many maize lines derived the value of the maceration method as a good proxy for from North American breeding
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