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      A maize landrace that emits defense volatiles in response to herbivore eggs possesses a strongly inducible terpene synthase gene

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          Abstract

          Maize ( Zea mays) emits volatile terpenes in response to insect feeding and egg deposition to defend itself against harmful pests. However, maize cultivars differ strongly in their ability to produce the defense signal. To further understand the agroecological role and underlying genetic mechanisms for variation in terpene emission among maize cultivars, we studied the production of an important signaling component ( E)‐caryophyllene in a South American maize landrace Braz1006 possessing stemborer Chilo partellus egg inducible defense trait, in comparison with the European maize line Delprim and North American inbred line B73. The ( E) caryophyllene production level and transcript abundance of TPS23, terpene synthase responsible for ( E) caryophyllene formation, were compared between Braz1006, Delprim, and B73 after mimicked herbivory. Braz1006– TPS23 was heterologously expressed in E. coli, and amino acid sequences were determined. Furthermore, electrophysiological and behavioral responses of a key parasitic wasp Cotesia sesamiae to Cpartellus egg‐induced Braz1006 volatiles were determined using coupled gas chromatography electroantennography and olfactometer bioassay studies. After elicitor treatment, Braz1006 released eightfold higher ( E)‐caryophyllene than Delprim, whereas no ( E)‐caryophyllene was detected in B73. The superior (E)‐caryophyllene production by Braz1006 was positively correlated with high transcript levels of TPS23 in the landrace compared to Delprim. TPS23 alleles from Braz1006 showed dissimilarities at different sequence positions with Delprim and B73 and encodes an active enzyme. Cotesia sesamiae was attracted to egg‐induced volatiles from Braz1006 and synthetic (E)‐caryophyllene. The variation in ( E)‐caryophyllene emission between Braz1006 and Delprim is positively correlated with induced levels of TPS23 transcripts. The enhanced TPS23 activity and corresponding ( E)‐caryophyllene production by the maize landrace could be attributed to the differences in amino acid sequence with the other maize lines. This study suggested that the same analogous genes could have contrasting expression patterns in different maize genetic backgrounds. The current findings provide valuable insight not only into genetic mechanisms underlying variation in defense signal production but also the prospect of introgressing the novel defense traits into elite maize varieties for effective and ecologically sound protection of crops against damaging insect pests.

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          Defensive function of herbivore-induced plant volatile emissions in nature.

          Herbivore attack is known to increase the emission of volatiles, which attract predators to herbivore-damaged plants in the laboratory and agricultural systems. We quantified volatile emissions from Nicotiana attenuata plants growing in natural populations during attack by three species of leaf-feeding herbivores and mimicked the release of five commonly emitted volatiles individually. Three compounds (cis-3-hexen-1-ol, linalool, and cis-alpha-bergamotene) increased egg predation rates by a generalist predator; linalool and the complete blend decreased lepidopteran oviposition rates. As a consequence, a plant could reduce the number of herbivores by more than 90% by releasing volatiles. These results confirm that indirect defenses can operate in nature.
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            Biosynthesis, function and metabolic engineering of plant volatile organic compounds.

            Plants synthesize an amazing diversity of volatile organic compounds (VOCs) that facilitate interactions with their environment, from attracting pollinators and seed dispersers to protecting themselves from pathogens, parasites and herbivores. Recent progress in -omics technologies resulted in the isolation of genes encoding enzymes responsible for the biosynthesis of many volatiles and contributed to our understanding of regulatory mechanisms involved in VOC formation. In this review, we largely focus on the biosynthesis and regulation of plant volatiles, the involvement of floral volatiles in plant reproduction as well as their contribution to plant biodiversity and applications in agriculture via crop-pollinator interactions. In addition, metabolic engineering approaches for both the improvement of plant defense and pollinator attraction are discussed in light of methodological constraints and ecological complications that limit the transition of crops with modified volatile profiles from research laboratories to real-world implementation. © 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.
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              Recruitment of entomopathogenic nematodes by insect-damaged maize roots.

              Plants under attack by arthropod herbivores often emit volatile compounds from their leaves that attract natural enemies of the herbivores. Here we report the first identification of an insect-induced belowground plant signal, (E)-beta-caryophyllene, which strongly attracts an entomopathogenic nematode. Maize roots release this sesquiterpene in response to feeding by larvae of the beetle Diabrotica virgifera virgifera, a maize pest that is currently invading Europe. Most North American maize lines do not release (E)-beta-caryophyllene, whereas European lines and the wild maize ancestor, teosinte, readily do so in response to D. v. virgifera attack. This difference was consistent with striking differences in the attractiveness of representative lines in the laboratory. Field experiments showed a fivefold higher nematode infection rate of D. v. virgifera larvae on a maize variety that produces the signal than on a variety that does not, whereas spiking the soil near the latter variety with authentic (E)-beta-caryophyllene decreased the emergence of adult D. v. virgifera to less than half. North American maize lines must have lost the signal during the breeding process. Development of new varieties that release the attractant in adequate amounts should help enhance the efficacy of nematodes as biological control agents against root pests like D. v. virgifera.
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                Author and article information

                Contributors
                atamiru@icipe.org
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                21 March 2017
                April 2017
                : 7
                : 8 ( doiID: 10.1002/ece3.2017.7.issue-8 )
                : 2835-2845
                Affiliations
                [ 1 ]International Centre of Insect Physiology and Ecology (ICIPE) NairobiKenya
                [ 2 ] Department of Biological Chemistry and Crop ProtectionRothamsted Research HarpendenUK
                [ 3 ] Institute of PharmacyMartin Luther University Halle Halle (Saale)Germany
                [ 4 ]Boyce Thompson Institute Ithaca NYUSA
                Author notes
                [*] [* ] Correspondence

                Amanuel Tamiru, International Centre of Insect Physiology and Ecology (ICIPE), Nairobi, Kenya.

                Email: atamiru@ 123456icipe.org

                Author information
                http://orcid.org/0000-0003-2735-0855
                Article
                ECE32893
                10.1002/ece3.2893
                5395458
                28428873
                2cfcb440-522c-442a-bf65-796437d94472
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 08 November 2016
                : 21 January 2017
                : 28 January 2017
                Page count
                Figures: 6, Tables: 0, Pages: 11, Words: 7718
                Funding
                Funded by: BBSRC–SCPRID project
                Award ID: BB/J011371/1
                Funded by: International Foundation for Science (IFS)
                Funded by: EU funded Integrated Biological Control Applied Research Program (IBCARP)
                Award ID: DCI‐FOOD/2014/346‐739
                Funded by: UK’s Department for International Development (DFID)
                Funded by: Rothamsted International
                Funded by: German Academic Exchange Service (DAAD)
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32893
                April 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.0.9 mode:remove_FC converted:18.04.2017

                Evolutionary Biology
                (e)‐caryophyllene synthase,induced defense,maize landraces,natural enemy,plant–insect interactions,terpene biosynthesis

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