Indole is an essential herbivore-induced volatile priming signal in maize
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Indole is an essential herbivore-induced volatile priming signal in maize
Matthias Erb 0
Nathalie Veyrat 1
Christelle A.M. Robert 0
Hao Xu 1
Monika Frey 2
Jurriaan Ton 3
Ted C.J. Turlings 1
0 Institute of Plant Sciences, Department of Biology, University of Bern , Altenbergrain 21, 3013 Bern , Switzerland
1 Laboratory for Fundamental and Applied Research in Chemical Ecology, Faculty of Science, University of Neucha?tel , Rue Emile-Argand 11, 2009 Neucha?tel , Switzerland
2 Lehrstuhl fu ?r Genetik, TU Munich , Emil-Ramann-Strabe 8, 85354 Freising , Germany
3 Department of Animal and Plant Sciences, University of Sheffield , Western Bank, S10 2TN
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
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neighbouring plants for incoming attacks.
I defences that can reduce herbivore damage, including blends
n response to herbivore attack, plants activate a wide array of
of volatile organic compounds (VOCs) that can be used as
foraging cues by natural enemies of the herbivores1?4.
Herbivoreinduced plant volatiles (HIPVs) have also been implicated in
plant?plant communication, as they can be perceived by
neighbouring plants5,6, and prime them for an enhanced
response upon subsequent insect attack7. By targeting jasmonic
acid (JA)-inducible genes, HIPVs have been shown to enhance
both direct and indirect defence responses8,9, which can benefit
the receiver by decreasing herbivore damage8,10. However,
the benefit for the emitter plant is not evident in this context,
leading to the notion that plants do not communicate, but
eavesdrop on each other11. As an adaptive explanation for
why plants emit HIPVs, a role of HIPVs as within-plant signal
has been proposed12. Indeed, HIPV-mediated within-plant
communication has been demonstrated in several plant species
including sagebrush, lima beans, poplar and blueberry13?16. In
these cases, HIPVs released from an attacked part of the plant
primed the healthy parts of the same plant to respond more
strongly15,17. Within-plant communication through HIPVs is
especially efficient when the vascular connectivity is limited or
when adjacent leaves are spatially but not anatomically close18. As
discussed by Heil and Ton9, herbivorous insects often move from
one leaf to another, but adjacent leaves are not always directly
connected via the plant?s vascular system. Therefore, volatile
compounds may reach distal parts of the plant faster than
vascular signals.
An important step to understand the mechanistic
underpinnings of airborne and vascular systemic priming is the
elucidation of the actual messengers19. Methylated forms of plant
hormones, including methyl jasmonic acid and methyl salicylic
acid, have been identified as volatile signals in this context20?22.
In Arabidopsis thaliana, however, none of these signals are strictly
required for systemic acquired resistance23 and the existence of
other volatile priming agents has been proposed24. Other
candidate volatiles that may prime systemic tissues are green
leaf volatiles (GLVs) and terpenoids. Exposing lima bean
(Phaseolus lunatus) leaves to volatiles from spider mite-infested
lima bean leaves as well as to the terpenoids b-ocimene,
(3E)-4,8dimethyl-1,3,7-nonatriene (DMNT) or
(3E,7E)-4,8,12-trimethyl1,3,7,11-tridecatetraene (TMTT) resulted in the induction of
defence-related genes25,26. However, in maize, there is no
indication that terpenoids can prime defence responses in the
receiver plants27. Evidence for GLVs as priming signals, on the
other hand, has been found in multiple plant species, including
maize. Exposure to (Z)-3-hexenyl acetate for instance was
sufficient to induce extra floral nectar secretion in lima bean
plants28. Treatment of A. thaliana seedlings with (E)-2-hexenal
induced the transcription of several genes involved in the plant?s
defence response including LOX and PAL29. Furthermore,
exposure to (Z)-3-hexenol led to a higher production of VOCs
in tomato30. The same volatile has (...truncated)