Plant volatiles carry both public
and private messages
“Within-plant signalling by volatiles leads to
induction and priming of an indirect plant
defence in nature”
Martin Heil and Juan Carlos Silva Bueno
2007, PNAS, 104, 5467-5472
Claudia Voelckel
Molecule-encoded messages…
Max-Planck Institute for Chemical Ecology Jena, Germany
„Chemical languages“
C hemische
MPI
„Interacting organisms“
Ö kolog ie
Plants: produce compounds
that attract pollinators, repel
herbivores, attract predators
and inhibit competitors
Herbivores: avoid, detoxify,
excrete, sequester and
modify plant compounds for
their own purposes
Examples from plant and herbivore chemical vocabularies:
 Caterpillars make fatty acid-amino acid conjugates that
alter the plant’s wound response
 Plants make volatile organic compounds (VOC) that
attract herbivore antagonists
Volatile organic compounds (VOCs) – A bit of history
Jonathan Gershenzon, PNAS 104: 5257-5258
Plant volatiles carry both public and private messages
“Plants have never worried about compliance with the Kyoto Protocol. For
millennia, they have released large amounts of gaseous compounds, such as
carbon dioxide, oxygen, water vapor, and ethylene, from their foliage into the
lower atmosphere. Thanks to improvements in headspace sampling techniques
and mass spectrometry in the last 20 years, the list of plant volatiles has greatly
expanded and now includes methanol, acetone, formaldehyde, and other short
chain carbonyl compounds, plus a host of terpenes, phenylpropanoids,
benzenoids, and fatty-acid derivatives.
Are plants just passing gas by emitting compounds that are by-products of
essential processes or do the released substances have any real function in
their lives?”
Public messages:
 Floral scent attracts pollinators
 “Talking trees”
 Botanical cry for help
Public messages 1 - “Botanical cry for help”
T. C. J. Turlings, J. H. Tumlinson, and W. J. Lewis (1990)
Exploitation of Herbivore-Induced Plant Odours by Host-Seeking Parasitic
Wasps Science 250, 1251
 Corn seedlings release volatiles after fed upon by caterpillars but artificially
damaged seedlings don’t
 parasitic wasps learn to associate volatiles with the presence of their prey
A. Kessler and I. T. Baldwin (2001)
Defensive Function of Herbivore-Induced Plant Volatile Emissions in Nature
Science 291, 2141
Mimic of volatile release in wild tobacco:
 Increased egg predation rates by a generalist predator and
 Decreased lepidopteran oviposition rates
 Through VOCs plants control herbivores “top down” and
“bottom up”
Public messages 2 - “Talking trees”
I. T. Baldwin, R. Halitschke, A. Paschold, C. C. v.Dahl, and
C. A. Preston (2006) Volatile Signalling in Plant-Plant
Interactions: ‘‘Talking Trees’’ in the Genomics Era
Science 311, 812
What do plants talk about? The probability of being attacked…
 Exposure to volatiles
from damaged
sagebrush primes the
elicitation of defensive
proteinase inhibitors in
wild tobacco
 Exposed plants
subsequently receive
less damage
New: The private part of volatile signalling…
“Within-plant signalling by volatiles leads to induction and priming of an indirect
plant defence in nature.” M. Heil and J. C. S. Bueno, PNAS, 104, 5467-5472
The model system - Phaseolus lunatus, L. Fabacae (lima bean)
(E)/ (Z)-β-ocimene
linalool
(Z)-jasmone
DMNT
TMTT
methyl-salicylate
(E)-caryophyllene
(Z)-3-hexenyl-acetate
Extrafloral nectaries
(attract ants, wasps and flies)
Volatile organic compounds
(induced by beetles, jasmonic acid)
Slide provided by C. Kost
New: The private part of volatile signalling…
Experiment 1: VOCs induce defences in neighbouring plants in the field
Experiment 2: VOCs as a means of within-plant signalling and priming of
EFN production under natural conditions
Experiment 3: Support for experiment 2 with seedlings transplanted to the
greenhouse
Experiment 1
VOC-exposed parts:
 Higher amounts of EFN
 More ants
 More leaves,
 More growing shoot tips,
 Less herbivory
= part of defensive effect due
to EFN-mediated increase in
ant numbers
Undamaged
emitters
Herbivore-induced
emitters
Are VOCs perceived by the emitter itself?
Experiment 2
Experiment 2 – EFN secretion by VOCs in the field
Artificial damage of leaves 4+5
Af: Emitter shoot
Cf: Emitter shoot + plastic bag
Bf, Df: Receiver shoot
Ef: Untreated control
 Undamaged Af leaves receive
external + internal signals while
undamaged Cf leaves only receive
internal signals
 EFN response in undamaged Cf
much weaker than in undamaged Af,
 Intra-shoot information transfer due to
VOC rather than internal signal
6
7
4
5
2
3
1
Experiment 2 – Priming of EFN secretion
Priming: primed plants respond
stronger once attacked themselves
than non-primed plants
All leaves damaged after day 1
except previously damaged
leaves (4+5 of Af, Cf)
Af: Emitter shoot
Cf: Emitter shoot + plastic bag
Bf, Df: Receiver shoot
Ef: Untreated control
 Significant induction observed in most
leaf groups
6
7
2
5
4
 Presence of VOCs augmented
response (leaves 1-3 of Af, leaves 1-3 and
4-5 of Bf)
3
1
 Strongest effect in leaves exposed to
highest dose of volatiles (4-5 of Bf)
Experiment 3 - Setup
Goal: exclude effects of root signalling, volatiles of other plants, influence of
closed bags on potential internal signals
Artificial damage/
beetle damage
of leaves 4+5
in A, B and C
Ap: Blowing VOCs from
4+5 to leaves 1-3
Bp: Blowing VOCs away
from the plant
Cp: Gasflow unaffected
Dp: Air from uninduced
4+5 redirected to 1-3
Experiment 3 - Results
 No difference in Ap and Cp and in Bp
and Dp in EFN production
 Bp shows that VOCs are more
important than internal signalling for intraplant communication in lima bean
Implications
 Systemic spread of information in plants not just via phloem and xylem
(Ryan and co-workers: wounding triggers an increase in defences in distal leaves,
candidate molecules are phloem-travellers systemin and jasmonic acid)
 Future studies on systemic responses of plants to local damage should control
airflow to disentangle internal and external signals
 Airborne within plant signalling is adaptive: foliage in close proximity often only
has remote vascular links
A VOC Signalling
B Short-range
vascular signalling
C Long-range
vascular signalling
Towards a deeper understanding of plant messages
What’s first? Private or public talk?
 Internal roles of VOCs probably evolved first
 Herbivore enemies, herbivores, neighbouring plants could “eavesdrop”
on VOCs with intraplant messages
How do plants talk?
 Who are the messengers? – green leaf volatiles and terpenes
are good candidates
 VOC synthesis, release, re-uptake, receptor binding, downstream cascades (pathways and their regulators)
 What are the costs and benefits of intra-plant communication?
Manipulate VOC production in the field (mute and deaf plants)!
Questions?