Herbivore-induced indirect plant defences of Lima bean (Phaseolus lunatus, Fabaceae) [Elektronische Ressource] / von Christian Kost
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Herbivore-induced indirect plant defences of Lima bean (Phaseolus lunatus, Fabaceae) [Elektronische Ressource] / von Christian Kost

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Herbivore-induced indirect plant defences of Lima bean (Phaseolus lunatus, Fabaceae) Dissertation zur Erlangung des akademischen Grades doctor rerum naturalium (Dr. rer. nat.) vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät der Friedrich-Schiller-Universität Jena von Diplom-Biologe Christian Kost geboren am 9. September 1975 in Bad Sobernheim Gutachter 1. Prof. Dr. Martin Heil (Universität Duisburg-Essen, Deutschland) 2. Prof. Dr. Wolfgang W. Weisser (Friedrich-Schiller-Universität Jena, Deutschland) 3. Prof. Dr. Paulo S. M. C. de Oliveira (Universidade Estadual de Campinas, Brasilien) Tag der Doktorprüfung: 30.01.2006 Tag der öffentlichen Verteidigung: 21.04.2006 Preface I 1 Preface This thesis is the end of a journey that lasted almost three years and that took me along the way twice to Mexico. When I look back and say that I learned a lot dur-ing this time, I mean not only scientific skills and knowledge that I acquired in the course of this interesting, inter-disciplinary project, but I also appreciate invaluable Just as much I owe thanks to Prof. experiences that I gained during my stays Wilhelm Boland (MPI for Chemical Ecol-abroad and my work in Jena. ogy) for teaching organic chemistry to an An enterprise like this Ph.D.

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Herbivore-induced indirect plant defences of Lima bean
(Phaseolus lunatus, Fabaceae)



Dissertation
zur Erlangung des akademischen Grades
doctor rerum naturalium (Dr. rer. nat.)


vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät
der Friedrich-Schiller-Universität Jena







von Diplom-Biologe
Christian Kost


geboren am 9. September 1975 in Bad Sobernheim
























Gutachter

1. Prof. Dr. Martin Heil (Universität Duisburg-Essen, Deutschland)

2. Prof. Dr. Wolfgang W. Weisser (Friedrich-Schiller-Universität Jena, Deutschland)

3. Prof. Dr. Paulo S. M. C. de Oliveira (Universidade Estadual de Campinas, Brasilien)


Tag der Doktorprüfung: 30.01.2006


Tag der öffentlichen Verteidigung: 21.04.2006
Preface I



1



Preface
This thesis is the end of a journey that
lasted almost three years and that took me
along the way twice to Mexico. When I
look back and say that I learned a lot dur-
ing this time, I mean not only scientific
skills and knowledge that I acquired in the
course of this interesting, inter-disciplinary
project, but I also appreciate invaluable
Just as much I owe thanks to Prof.
experiences that I gained during my stays
Wilhelm Boland (MPI for Chemical Ecol-
abroad and my work in Jena.
ogy) for teaching organic chemistry to an
An enterprise like this Ph.D. project
ecologist, for always having an open door,
can certainly not be accomplished without
his contagious enthusiasm, stimulating
the help of numerous people that contrib-
discussions and his unrestricted support.
uted in numerous ways either directly or
Beyond I am indebted to Prof. Wolf-
indirectly to its success. To these people,
gang W. Weisser (FSU Jena) for kindly
that crossed my path during the past three
accepting the official supervision as a rep-
years and made this time unforgettable, I
resentative of the FSU Jena and giving me
would like to express my warm gratitude.
the opportunity to present and discuss my
First of all, I wish to thank my doctoral
results in his group’s seminar.
advisor Prof. Martin Heil (University Du-
To Silvia Schmidt I am endlessly
isburg-Essen) for the opportunity to work
grateful for her love, company during all
on this exciting project in Jena and Mex-
the years, lots of encouraging words when
ico, his invaluable support, and stimulating
things were tough and giving me the feel-
discussions throughout all stages of this
ing of not being alone.
thesis. His advice and encouragement
I owe substantial debt to Sven
were an added spur to my ambition.
Adolph and Mesmin Mekem Sonwa who
patiently taught me organic synthesis and

always kept an eye on me. Also Stefan
Photograph: Cerotoma ruficornis OLIVIER on
Bartram, Christoph Beckmann, An-a leaf of Phaseolus lunatus. Source:
CHRISTIAN KOST.
II Preface


dreas Habel, Georg Pohnert, Doreen (University of Duisburg-Essen), Paulo S.
Schachtschabel and Dieter Spiteller Oliveira (Universidade Estadual de
always stood by me with moral and practi- Campinas, Brazil), Victor Rico-Gray
cal support. (Instituto de Ecología, Veracruz, Mexico),
I am especially grateful to Anja Bie- Flavio Roces (University of Würzburg),
dermann for introducing me into various Georg Pohnert (Ecole polytechnique
methodological techniques and assisting fédérale de Lausanne, Switzerland), Wolf-
me with laboratory work. Furthermore, I gang W. Weisser (Friedrich-Schiller-
am thankful to Angelika Berg for taking University Jena), Ian T. Baldwin, Wilhelm
considerable care for the Mexican bean Boland, Jesse Colangelo-Lillis, Rüdiger
beetles. A great deal of credit goes to Udo Dietrich, Maritta Kuhnert, Heiko Mai-
Kornmesser, Andreas Weber, Tamara schak, Axel Mithöfer, Birgit Schulze,
Krügel, and the rest of the greenhouse Silvia Schmidt, Thomas Wichard (all
team for raising countless plants. Max Planck Institute of Chemical Ecology,
For there company, help and a great Jena) as well as a number of anonymous
time in Mexico I thank Kerstin Ploss, referees.
Martin Heil and Ralf Krüger. I am espe- I especially enjoyed lively scientific
cially grateful to Perla Monica Martinez and non-scientific discussions as well as
Cruz (Universidad del Mar, Puerto Escon- tantalising games evenings with my cof-
dido, Mexico) for a warm welcome in Mex- fee-round Lars Clement and Heiko Mai-
ico as well as logistic support in the field. schak as well as with my group-spanning
Janine Rattke (Elsie Widdowson Labora- interest and discussion group Markus
tory, Cambridge) is thanked for helping Benderoth, Caroline C. von Dahl, Mar-
with the GC-MS analysis of nectar sam- kus Hartl, Anja Paschold and Silvia
ples and Manfred Verhaagh (Staatliches Schmidt.
Museum für Naturkunde, Karlsruhe) for Finally I would like to thank my family
the identification of collected ants. Further, for their love, support, encouragement and
I want to express my thanks to Birgit the privilege to realize my dream of be-
Schulze for introducing me into the se- coming a natural scientist.
crets of JA-extraction and lots of inspiring Financial support by the German
discussions. Research Foundation (DFG Grant He
Several people benefited this thesis 3169/2-1, 2, 3, 4) and the Max Planck
by discussions or reading drafts of manu- Society is gratefully acknowledged.
scripts and commenting on them. Their This work would not have been possi-
advice was time-consuming to them but ble without your help!
immensely valuable to me: Martin Heil
Contents III


Contents

Preface………………………………………………………………………………………………....I
Abbreviations, acronyms and symbols……………………………………………………………IV

1. General introduction……………………………………………………………………………….1
2. Thesis outline – List of manuscripts and author’s contribution………………………………13
3. Manuscript I
Herbivore-induced, indirect plant defences………………………………………….…18

4. Manuscript II
Protection of Lima beans by extrafloral nectar…………………………………..........47

5. Manuscript III
Airborne volatiles induce indirect plant defence……………………………………….65

6. Manuscript IV
Two indirect defences benefit Lima bean in nature……………………………………84

7. Manuscript V
Artefact formation during headspace sampling………………………………………102

8. General discussion ……………………………………………………………………………..111
9. Synthesis…………………………………………………………………………………………121
10. Summary
10.1. Summary…………………………………………………………………………….….123
10.2 Zusammenfassung…………..………………………………………………………....126
11. References………………………………………………………………………………..……129
12. Selbständigkeitserklärung……………………………………………………………….……157
13. Curriculum vitae…………...… ……………...……………………………………………..…158






IV Abbreviations, acronyms and symbols


Abbreviations, acronyms and symbols

ACC 1-aminocyclopropane-1-carboxylic acid
A peak area of the internal standard (1-bromodecane) IS
AFLP amplified fragment length polymorphism
AOC allene oxide cyclase
AOS
ALA alamethicin
A peak area of a volatile organic compound VOC
CAM calmodulin
CDPK calcium-dependent protein kinase
CLSM closed-loop-stripping method
DDQ 4,5-Dichloro-3,6-dioxo-1,4-cyclohexadiene-1,2-dicarbonitrile
DMNT (3E)-4,8-dimethylnona-1,3,7-triene (C -homoterpene) 11
DW dry weight
EAG electroantennogram
EF extrafloral
EFN nectar
EI-MS electron impact mass spectrometer
EI-MS act high resolution mass spectrometer
ERF ethylene-responsive transcription factor
ET ethylene
eq equivalent
FAC fatty acid–amino acid conjugate
FAD ω-3 fatty acid desaturase
Fig. figure
FPP farnesyl diphosphate
GC gas chromatography
GC-MS graph coupled to a mass spectrometer
GPP geranyl diphosphate
HI herbivore-induced
HI-VOCs Herbivore-induced volatile organic compounds
HIPV herbivore-induced plant volatile
13-HPOT 13(S)-hydroperoxy-9(Z),11(E),15(Z)-octa-decanoid acid
HPL 13(S)-hydroperoxy-hydroperoxid lyase
HRMS high resolution mass spectrometer
Abbreviations, acronyms and symbols V


IGP indole-3-glycerol phosphate
Ind individual
JA jasmonic acid
JAs jasmonates
JMT jasmonic acid carboxyl methyltransferase
LOX 13-lipoxygenase
+ •M molecular ion
MAP mitogen activated protein
MAPK mitogen-activated protein kinase
1-MCP 1-methylcyclopropene
MeJA methyl jasmonate
MeSA methyl salicylate
MKP mitogen-activated protein kinase phosphatase
MS mass spectrometer
MSTFA N-methyl-N-trimethylsilyl-trifluoroacetamide
NMR nuclear magnetic resonance
OPC 8:0 3-oxo-2-(2'(Z)-pentenyl)-cyclo pentane-1-octanoic acid
OPDA 12,13(S)-epoxy-octadecatrienoic acid
OPR 12-oxo-phytodieonic acid reductase
ORCA octadecanoid-derivative responsive Catharanthus AP2-domain
P450 P450 monooxygenase
PI proteinase inhibitor
PLA phospholipase A
PLD phospholipase D
r.t. room temperature
SA salicylic acid
SAM S-adenosylmethionine
SAR systemic acquired resistance
SIPK salicylic acid-induced protein kinase
SMT salicylic acid carboxyl methyltransferase
Tab table
TMTT (3E,7E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (C -homoterpene) 16
t retention time ret
TPS terpene synthase
VOC volatile organic compound
WIPK wounding-induced protein kinase
VI Abbreviations, acronyms and symbols


Symbols and letters used in statistics
GLM general linear model
LSD Fisher’s protected least significant differences test (i.e. post-hoc test)
n sample size
probability P
r Pearson product moment correlation (i.e. measure of correlation; varies from -1 to 0)
SEM standard error of the mean
SD standard deviation
indicates a significant result (P < 0.05) * significant result (P < 0.01) **
indicates a significant result (P < 0.001) ***


Abbreviations used for NMR assignment
d dublett
q quartett
δ chemical resonance shift
s singulett
t triplett












General introduction 1


led to coadaptation in which the evolving 1. General introduction
parties continually responded and counter-Ever since the greening of a strip of equa-
responded to the selection pressures im-torial coastline that fringed tropical oceans
posed by each other. Such positive feed-approximately 425 million years ago, both
back loops caused rapid evolutionary plants and animals have expanded their
changes in the interacting partners and ecological reach on land. Today their
thus enhanced speciation (LUNAU, 2004). terrestrial representatives constitute the
Besides relationships which are mutually overwhelming bulk of macroscopic diver-
beneficial, such as between plants and sity on the planet which consists of more
their insect pollinators, the most common than 30 million species with many of them
interaction involves insects preying on being as yet unstudied and unnamed. Two
plants, and plant defences against her-groups, namely flowering plants (Angio-
bivorous insects. This predator-host rela-sperms) and insects (Insecta), contribute
tionship is so common that virtually every preponderance to the terrestrial macro-
plant species is preyed on by at least one scopic diversity we can observe to date.
insect species, and, according to the co-If the earliest forms of land plants and
evolutionary theory of EHRLICH and RA-insects are included, plants and insects
VEN (1964), insect feeding on plants has have coexisted for as long as 350 million
been a determining factor in increasing years and have, since then, developed
species diversity in both herbivores and myriads of relationships. The extraordinary
hosts (HARBORNE, 1988). On the basis radiation of flowering plants for example
of this long-standing relationship, it is not was clearly the impact of a coevolutionary
surprising that the strategies employed by interaction with pollinating insects
plants that attempt to resist or evade their (REGAL, 1977). In the Cretaceous, about
insect herbivores are very diverse. 100 million years ago, when the first
widely foraging seed dispersers came into
Plant defence reactions existence (initially birds), insect pollination
The spectrum of defensive mechanisms allowed flowering plants to produce out-
that plants have evolved against herbi-crossed offspring with conspecifics, even
vores has been classified as direct (bot-when they were patchy and widely dis-
tom-up) or indirect defences (top-down). persed. Plants offered nectar to insects,
Direct defences prevent herbivores from thus creating new niches for nectivores
feeding via physical barriers, such as with this diversification in turn creating new
spines, thorns, trichomes, and waxes or evolutionary possibilities for the plants. A
chemically, via the production of toxins or permanent reciprocal selection pressure
anti-digestive and anti-nutritive com-between pairs of single or multiple species
2 General introduction


pounds. Additionally, plants may express their defence response to the particular
traits that facilitate top-down control over herbivore as has been shown on the level
the herbivore population by attracting of transcriptional responses (VOELCKEL
natural enemies of the herbivore that indi- & BALDWIN, 2004), signal molecules (e.g.
rectly defend them against their attackers jasmonic acid: HALITSCHKE et al., 2001;
(i.e. indirect defences, see Box 1). Direct SCHITTKO et al., 2000; ethylene: KAHL et
and indirect defences can be expressed al., 2000) and defence-related metabolites
constitutively (i.e. permanently) or be such as e.g. nicotine (WINZ & BALDWIN,
induced upon mechanical wounding or 2001), proteinase inhibitors (STOUT et al.,
herbivore damage. 1994; TAMAYO et al., 2000), as well as
Defence responses channel re- volatile organic compounds (VOCs) (DE
sources from vegetative and reproductive MORAES et al., 1998; TAKABAYASHI et
growth into protective mechanisms. There- al., 1995). Elicitation and orchestration of
fore, the plant must attain a balance to such complex biochemical and physio-
ensure survival from immediate and sub- logical responses requires at first the re-
sequent attacks without sacrificing plant cognition of the currently feeding herbivore
vitality and reproduction. The finding that via physical and chemical signals which
many direct and indirect defences are activate subsequent signal transduction
inducible suggests that these defences cascades and finally up-regulate defence-
may incur costs to the plant. Fitness costs related genes.
can arise directly from ‘internal’ mecha-
nisms such as allocation costs, genetic Herbivore recognition and signal
costs and autotoxicity costs (i.e. the resis- transduction
tance trait itself is toxic to the plant) or The study of how plants recognize an
indirectly from ecological interactions with attacking insect herbivore has mainly
mutualists or antagonistic species (HEIL & focused on the emission of induced vola-
BALDWIN, 2002; STRAUSS et al., 2002). tiles. Here it could be shown that the sig-
These costs have been discussed as a nals generated by the herbivore are first
driving force for the evolution of induced the mechanical damage that is inflicted,
resistance (HEIL, 2001; HEIL & BALD- and second the chemical compounds of
WIN, 2002). the herbivore’s oral secretions which are
In order to minimize costs associated introduced at the site of wounding.
with induced resistance, plants must be Mechanical damage triggers the re-
able to identify their attacker to mount the lease of several VOCs. Immediately after
most efficacious defence strategy. Indeed wounding, the so-called green-leaf odours
it has been shown that plants may tailor are released (i.e. saturated and un-