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Cited by 467Insect-Plant Interactions and ControlPlant-Microbe Interactions and ImmunityPlant biochemistry and biosynthesis

Indole is an essential herbivore-induced volatile priming signal in maize

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Erb, Matthias, Veyrat, Nathalie, Robert, Christelle A. M., Xu, Hao, Frey, Monika, Ton, Jurriaan, Turlings, Ted C. J.·2015·Nature Communications
DOI 10.1038/ncomms7273PMC PMC4339915
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Abstract

Herbivore-induced volatile organic compounds prime non-attacked plant tissues to respond more strongly to subsequent attacks. However, the key volatiles that trigger this primed state remain largely unidentified. In maize, the release of the aromatic compound indole is herbivore-specific and occurs earlier than other induced responses. We therefore hypothesized that indole may be involved in airborne priming. Using indole-deficient mutants and synthetic indole dispensers, we show that herbivore-induced indole enhances the induction of defensive volatiles in neighbouring maize plants in a species-specific manner. Furthermore, the release of indole is essential for priming of mono- and homoterpenes in systemic leaves of attacked plants. Indole exposure markedly increases the herbivore-induced production of the stress hormones jasmonate-isoleucine conjugate and abscisic acid, which represents a likely mechanism for indole-dependent priming. These results demonstrate that indole functions as a rapid and potent aerial priming agent that prepares systemic tissues and neighbouring plants for incoming attacks.

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  • In maize, mutants defective in volatile indole production are unable to prime systemic tissues to rapidly release terpenes upon herbivore attack; adding indole restores priming.

    “In maize, for instance, mutants that are defective in their capacity to produce volatile indole are unable to prime their systemic tissues to rapidly release terpenes upon herbivore attack (Erb et al., 2015).Adding indole to the headspace of maize plants restores this priming phenotype (Erb et al., 2015).”

    From Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy (2020) · cites this paper as Erb et al., 2015

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Research works printed but not linked: 46

  1. Turlings T. C. J., Tumlinson J. H. & Lewis W. J. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250, 1251– 1253 (1990). 17829213
  2. Dicke M., Sabelis M. W., Takabayashi J., Bruin J. & Posthumus M. A. Plant strategies of manipulating predator prey interactions through allelochemicals: Prospects for application in pest control. J. Chem. Ecol. 16, 3091– 3118 (1990). 24263298
  3. Chen M. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15, 101– 114 (2008). 28035791
  4. Baldwin I. T., Halitschke R., Paschold A., von Dahl C. C. & Preston C. A. Volatile signaling in plant-plant interactions: "talking trees" in the genomics era. Science 311, 812– 815 (2006). 16469918
  5. Engelberth J., Alborn H. T., Schmelz E. A. & Tumlinson J. H. Airborne signals prime plants against insect herbivore attack. Proc. Natl Acad. Sci. USA 101, 1781– 1785 (2004). 14749516 PMC341853
  6. Ton J.. Priming by airborne signals boosts direct and indirect resistance in maize. Plant J. 49, 16– 26 (2007). 17144894
  7. Heil M. & Ton J. Long-distance signalling in plant defence. Trends Plant Sci. 13, 264– 272 (2008). 18487073
  8. Heil M. & Karban R. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25, 137– 144 (2010). 19837476
  9. Farmer E. E. Surface-to-air signals. Nature 411, 854– 856 (2001). 11459069
  10. Karban R., Shiojiri K., Huntzinger M. & McCall A. C. Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87, 922– 930 (2006). 16676536
  11. Frost C. J.. Within‐plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 10, 490– 498 (2007). 17498148
  12. Heil M. & Bueno J. C. S. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl Acad. Sci. USA 104, 5467– 5472 (2007). 17360371 PMC1838500
  13. Rodriguez-Saona C. R., Rodriguez-Saona L. E. & Frost C. J. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J. Chem. Ecol. 35, 163– 175 (2009). 19159981
  14. Frost C. J., Mescher M. C., Carlson J. E. & De Moraes C. M. Why do distance limitations exist on plant–plant signaling via airborne volatiles. Plant Signal. Behav 3, 466– 468 (2008). 19704487 PMC2634431
  15. Heil M. & Bueno J. C. S. Herbivore-induced volatiles as rapid signals in systemic plant responses: how to quickly move the information? Plant Signal. Behav 2, 191– 193 (2007). 19704694 PMC2634055
  16. Jung H. W., Tschaplinski T. J., Wang L., Glazebrook J. & Greenberg J. T. Priming in systemic plant immunity. Science 324, 89– 91 (2009). 19342588
  17. Attaran E., Zeier T. E., Griebel T. & Zeier J. Methyl salicylate production and jasmonate signaling are not essential for systemic acquired resistance in Arabidopsis. Plant Cell 21, 954– 971 (2009). 19329558 PMC2671706
  18. Yao Y.. UV-C-irradiated Arabidopsis and tobacco emit volatiles that trigger genomic instability in neighboring plants. Plant Cell 23, 3842– 3852 (2011). 22028460 PMC3229153
  19. Arimura G.. Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406, 512– 515 (2000). 10952311
  20. Ruther J. & Furstenau B. Emission of herbivore-induced volatiles in absence of a herbivore--response of Zea mays to green leaf volatiles and terpenoids. Z. Naturforsch. C 60, 743– 756 (2005). 16320618
  21. Bate N. J. & Rothstein S. J. C6-volatiles derived from the lipoxygenase pathway induce a subset of defense-related genes. Plant J. 16, 561– 569 (1998). 10036774
  22. Farag M. A. & Paré P. W. C6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61, 545– 554 (2002). 12409021
  23. Sugimoto K.. Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. Proc. Natl Acad. Sci. USA 111, 7144– 7149 (2014). 24778218 PMC4024874
  24. Ruther J. & Kleier S. Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J. Chem. Ecol. 31, 2217– 2222 (2005). 16132223
  25. Farag M. A.. Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220, 900– 909 (2005). 15599762
  26. De Boer J. G., Posthumus M. A. & Dicke M. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J. Chem. Ecol. 30, 2215– 2230 (2004). 15672666
  27. Zhuang X.. Biosynthesis and emission of insect herbivory-induced volatile indole in rice. Phytochemistry 73, 15– 22 (2012). 22000657
  28. Frey M., Spiteller D., Boland W. & Gierl A. Transcriptional activation of Igl, the gene for indole formation in Zea mays: a structure-activity study with elicitor-active N-acyl glutamines from insects. Phytochemistry 65, 1047– 1055 (2004). 15110684
  29. Frey M.. Analysis of a chemical plant defense mechanism in grasses. Science 277, 696– 699 (1997). 9235894
  30. Frey M., Schullehner K., Dick R., Fiesselmann A. & Gierl A. Benzoxazinoid biosynthesis, a model for evolution of secondary metabolic pathways in plants. Phytochemistry 70, 1645– 1651 (2009). 19577780
  31. Frey M.. An herbivore elicitor activates the gene for indole emission in maize. Proc. Natl Acad. Sci. USA 97, 14801– 14806 (2000). 11106389 PMC18999
  32. Ahmad S., Gordon-Weeks R., Pickett J. & Ton J. Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol. Plant Pathol. 11, 817– 827 (2010). 21029325 PMC6640509
  33. Ahmad S.. Benzoxazinoid metabolites regulate innate immunity against aphids and fungi in maize. Plant Physiol. 157, 317– 327 (2011). 21730199 PMC3165881
  34. Butrón A., Chen Y. C., Rottinghaus G. E. & McMullen M. D. Genetic variation at bx1 controls DIMBOA content in maize. Theor. Appl. Genet. 120, 721– 734 (2010). 19911162
  35. Turlings T. C. J. & Tumlinson J. H. Systemic release of chemical signals by herbivore-injured corn. Proc. Natl Acad. Sci. USA 89, 8399– 8402 (1992). 11607325 PMC49926
  36. Schmelz E. A., Alborn H. T., Banchio E. & Tumlinson J. H. Quantitative relationships between induced jasmonic acid levels and volatile emission in Zea mays during Spodoptera exigua herbivory. Planta 216, 665– 673 (2003). 12569409
  37. Kessler A., Halitschke R., Diezel C. & Baldwin I. T. Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148, 280– 292 (2006). 16463175
  38. Frost C. J.. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis‐3‐hexenyl acetate. New Phytol. 180, 722– 734 (2008). 18721163
  39. Ozawa R.. Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. J. Chem. Ecol. 30, 1797– 1808 (2004). 15586675
  40. Schmelz E. A., Alborn H. T. & Tumlinson J. H. Synergistic interactions between volicitin, jasmonic acid and ethylene mediate insect‐induced volatile emission in Zea mays. Physiol. Plant. 117, 403– 412 (2003). 12654041
  41. Stamm I., Lottspeich F. & Plaga W. The pyruvate kinase of Stigmatella aurantiaca is an indole binding protein and essential for development. Mol. Microbiol. 56, 1486– 1395 (2005). 15882428
  42. Koehler A.. Within-plant distribution of 1,4-benzoxazin-3-ones contributes to herbivore niche differentiation in maize. Plant Cell Environ doi: 10.1111/pce.12464 (2014). 25293400 · DOI
  43. Meihls L. N.. Natural variation in maize aphid resistance is associated with 2,4-dihydroxy-7-methoxy-1,4-benzoxazin-3-one glucoside methyltransferase activity. Plant Cell 25, 2341– 2355 (2013). 23898034 PMC3723630
  44. Karban R.. Kin recognition affects plant communication and defence. Proc. R. Soc. B 280, 20123062 (2013). PMC3574382 23407838
  45. Degen T., Bakalovic N., Bergvinson D. & Turlings T. C. J. Differential performance and parasitism of caterpillars on maize inbred lines with distinctly different herbivore-induced volatile emissions. PLoS ONE 7, e47589 (2012). 23112820 PMC3480431
  46. Trautenhan R.. XCMS Online: A web-based platform to process untargeted metabolomic data. Anal. Chem. 84, 5035– 5039 (2012). 22533540 PMC3703953

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Authors
Erb, M., Veyrat, N., Robert, C. A. M., Xu, H., Frey, M., Ton, J., & Turlings, T. C. J.
Affiliations
  • University of Bern (CH)
  • University of Neuchâtel (CH)
  • Technical University of Munich (DE)
  • University of Sheffield (GB)
Corresponding author
  • Erb, Matthias
  • Turlings, Ted C. J.
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2015-02-16
Volume
6
Issue
1
Pages
6273-6273
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/ncomms7273
PMC
PMC4339915
OpenAlex
W2009204329
Cited by
467
References
1
Citations by year
2026: 38 · 2025: 39 · 2024: 42 · 2023: 47 · 2022: 59 · 2021: 46 · 2020: 43 · 2019: 41 · 2018: 34 · 2017: 25 · 2016: 38 · 2015: 14
FWCI
39.40
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • Bern Open Repository and Information System (University of Bern) (submittedVersion, cc-by)
  • Open Access CRIS of the University of Bern
Topics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant biochemistry and biosynthesis
Keywords
indole, herbivore-induced plant volatiles, maize, plant defense, systemic defense, terpenes, abscisic acid, plant-plant communication
MeSH terms
Abscisic Acid, Animals, Zea mays, Cyclopentanes, Indoles, Mutation, Plant Growth Regulators, Terpenes, Oxylipins, Volatile Organic Compounds, Herbivory

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