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The Layers of Plant Responses
to Insect Herbivores
Meredith C. Schuman
∗
and Ian T. Baldwin*
Department of Molecular Ecology, Max Planck Institute for Chemical Ecology, 07745 Jena,
Germany; email: mschuman@ice.mpg.de, baldwin@ice.mpg.de
German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig,
04103 Leipzig, Germany
Annu. Rev. Entomol. 2016. 61:373–94
The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev-ento-010715-023851
Copyright
c
2016 by Annual Reviews.
All rights reserved
∗
Corresponding authors
Keywords
levels of analysis, Tinbergen’s four questions, plant defense theory,
herbivore-associated elicitors, plant-insect interactions
Abstract
Plants collectively produce hundreds of thousands of specialized metabolites
that are not required for growth or development. Each species has a qual-
itatively unique profile, with variation among individuals, growth stages,
and tissues. By the 1950s, entomologists began to recognize the supreme
importance of these metabolites in shaping insect herbivore communities.
Plant defense theories arose to address observed patterns of variation, but
provided few testable hypotheses because they did not distinguish clearly
among proximate and ultimate causes. Molecular plant-insect interaction
research has since revealed the sophistication of plant metabolic, develop-
mental, and signaling networks. This understanding at the molecular level,
rather than theoretical predictions, has driven the development of new hy-
potheses and tools and pushed the field forward. We reflect on the utility
of the functional perspective provided by the optimal defense theory, and
propose a conceptual model of plant defense as a series of layers each at a
different level of analysis, illustrated by advances in the molecular ecology
of plant-insect interactions.
373
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Molecular chemical
ecology: the field
investigating the
evolution of ecological
interactions, and the
functional traits and
molecular and
chemical mechanisms
mediating these
interactions
Levels of analysis:
explanatory levels of
proximate and
ultimate causation
INTRODUCTION
Most plant species are sessile and, during a large portion of their life histories, literally rooted to
the ground. They must either adapt themselves to their environment or adapt their environment
to their needs. It is therefore not surprising that plants are among nature’s most accomplished
chemists, producing a cornucopia of secondary, or specialized, metabolites with which they
manipulate the physiology and behavior of insects and other organisms. In contrast to primary, or
general, metabolites commonly required for cell growth (77), which include most carbohydrates,
amino acids, and fatty acids, specialized metabolites such as alkaloids are by definition unevenly
distributed, both across phylogenetic groups and among individuals within a species (e.g., 9, 32,
40, 44, 48, 63, 75, 87, 113). Of course animals and microbes also produce specialized metabolites,
e.g., defensive glandular exudates or antibiotics; and in the animal kingdom there are many
examples of co-opting, or sequestering specialized metabolites or their precursors, usually from
food and thus often from plants (reviewed in 9, 53). This complex chemical web of life is the
subject of molecular chemical ecology, which originated in studies revealing that phytochemicals
can determine the occurrence and outcome of plant-herbivore interactions (reviewed in 40, 51).
Many early chemical ecologists were zoologists who were interested in the distribution and
evolution of specialized plant metabolites because of the apparent consequences for distribution
and evolution of insect herbivores (32, 40) (Figure 1, 1950s–1960s). The theories that emerged
(Figure 1, 1970s–1990s) posited that plants encounter trade-offs between the costs of producing
these metabolites, in the face of limited resources and coevolving herbivores, and their benefits
via reduced herbivore pressure on plant fitness (9, 123). However, the physiological mechanism
through which a trait occurs does not reveal its function, just as function does not dictate a
mechanism—although each may hint at a reasonable range of possibilities for the other. The
hypotheses derived from these theories were thus frequently neither testable nor mutually exclusive
(8, 9, 123).
In 1988, Sherman (118, p. 616) addressed other, similar instances of “talk[ing] past each other”
in biology, building on earlier work by Tinbergen (130) and Mayr (84) to point out that there are
four levels at which biological phenomena can be understood: (a) Ontogenetic mechanisms and
(b) physiological or cognitive processes determine how a phenomenon happens; while (c) evo-
lutionary trajectories and (d ) ecological pressures determine why it happens that way, or at all
(Figure 1). Biological phenomena can, and ideally should, be understood at all four levels, but
hypotheses may only compete and be tested within a level (118). For example, “increased produc-
tion of specialized compound A entails a reduction in growth” and “the function of compound A
is to defend plants attacked by insect herbivores” are not competing hypotheses. One, both, or
neither may be true, and different types of data must be generated to test each: comparing growth
of plants differing only in their production of compound A in the first case; and comparing fitness
of plants under herbivore attack differing only in their production of compound A in the second
case.
Classical plant defense theories and their insights and shortcomings have been thoroughly
reviewed elsewhere (e.g., 8, 9, 20, 39, 101, 123). Here, we focus on how the utility of these
theories has been limited by their failure to cleanly separate biological levels of analysis; this is
both a universal problem in biology (84, 118) and a topic that has rarely been handled (but see
8). From this point of view, we critically discuss the optimal defense framework and the idea of
growth-defense trade-offs, which are perhaps the most useful of the body of classical plant defense
theories (8, 9, 123). We then provide a synthetic overview of the advances in molecular physiology,
which, in the absence of clear guidance from theory, have driven the field forward (8, 9). Finally,
we offer a perspective on maintaining clear divisions of hypotheses by level of analysis as key
374 Schuman
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Coevolution
(Ehrlich & Raven 1964)
Apparency
(Feeney 1976)
Growth:dierentiation balance
(Loomis 1932, 1953; Herms & Mattson 1992)
Spatially varying selection
(Gloss 2013)
Community genetics
(Whitham et al. 2006, Wymore et al. 2011)
Carbon:nutrient balance
(Bryant et al. 1983, Tuomi et al. 1988)
Growth rate/resource availability
(Coley 1985a,b; Coley et al. 1985)
Physiological
mechanisms
Ontogenetic
processes
Evolutionary
origins
Functional
consequences
Why is there natural variation
in plant specialized metabolism?
How are plant specialized metabolites
distributed in nature?
Raison d’être
(Fraenkl 1959)
1950
1960
1970
1980
1990
2000
2010
Optimal defense
(McKey 1974, 1979; Rhoades 1979; Rhoades & Cates 1976)
Figure 1
Several hypotheses from different theoretical frameworks have been put forth over six decades to explain
how and why observed variation in specialized plant metabolites exists. None of these frameworks attempts
to cleanly integrate the levels of analysis at which biological hypotheses can be formulated (8, 118). Because
the frameworks address different levels of how or why (and some blend multiple levels), they generally do
not provide alternative hypotheses but rather different, to an extent complementary, points of view.
discoveries in molecular physiology are extrapolated to the level of ecological interactions, in an
attempt to avoid similar problems of unfalsifiability and talking past each other in the future.
Plant Defense Theory: What Level Are We On?
Figure 1 portrays key concepts and frameworks in classical plant defense theory as well as selected
newer frameworks in terms of how they address, or mix, levels of analysis. In 1959, Fraenkel (40)
argued that plant secondary metabolites evolved primarily under ecological pressure to thwart
herbivores, while herbivores in turn evolved to avoid, detoxify, or sequester these metabolites or
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Layers of Plant Responses to Insect Herbivores 375
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Defense trait: a trait
that increases a plant’s
Darwinian fitness
under stress such as
herbivory
OD: optimal defense
CNB: carbon:nutrient
balance
GR/RA: growth
rate/resource
availability
GDB:
growth:differentiation
balance
Indirect defense:
plant defense trait that
indirectly affects
herbivores by
attracting their
enemies through
provision of resources
or information
even use them to identify suitable host plants. Five years later, Ehrlich & Raven (32) proposed that
coevolution between plant defense and herbivore counteradaptations could explain the diversity
of plants and their herbivores: Plants evolve new defense traits in response to herbivore pressure,
the resulting reduction in pressure permits a radiation in plant diversity, and that radiation creates
new host plants to which herbivores then adapt (adapt-and-radiate coevolution; 123, 129). Fox (39)
later proposed that ephemeral plants interacting with a few, primarily specialized herbivores may
undergo stepwise coevolution in a true evolutionary arms race, while more persistent plant species
may undergo diffuse coevolution, developing a complex suite of defense traits to hedge against
fitness loss to a large, complex, and variable herbivore community. Usually plant defense traits
are taken to refer to specialized plant metabolites, but a robust definition of defense incorporates
other fitness-enhancing responses (discussed below). Coevolutionary hypotheses are difficult to
test because the phylogenetic distribution of traits cannot be predicted from their ecological
functions, or vice versa. However, Fraenkel’s (40) and Erlich & Raven’s theses (32) stimulated
entomologists to ask why, and how, plant defenses are distributed as they are in nature, and how
this distribution has influenced the evolution, behavior, and physiology of insect herbivores.
Perhaps the most successful of these theories has been the optimal defense (OD) theory (85,
86, 102, 103), which has provided testable functional hypotheses. By quantifying plant defense
in the currency of Darwinian fitness, OD provides a link to evolutionary theory (9, 25, 30). This
is not true of carbon:nutrient balance (CNB) theory (15, 133), growth rate/resource availability
(GR/RA) theory (21–23), or growth:differentiation balance (GDB) theory (58, 76, 77), none of
which addresses functional questions (97, 123). The two main hypotheses of OD are (a) defenses
evolve and are allocated to maximize individual inclusive fitness, and (b) defenses have a fitness
cost because they divert resources from other processes, mainly growth and reproduction (102,
123). The first hypothesis is rather the assumption that most traits are adaptive, positing that any
pattern of defense is possible as long as it is adaptive (85, 86, 102, 123). The second hypothesis is
falsifiable (if imprecisely worded; see 34) and produced several subhypotheses. (a) The allocation
hypothesis states that within a plant, tissues are defended in direct proportion to their fitness
value and risk of predation, and in inverse proportion to the cost of allocation. (b) The plasticity
hypothesis states that defenses decrease in the absence of enemies and increase in their presence.
(c) The stress hypothesis states that individuals are less defended when under additional stresses
because they cannot afford to allocate as many resources to defense against herbivores (36, 102,
103, 123).
The hypotheses of OD theory are compatible with apparency theory (36), and the concept of
apparency is implicit in the allocation hypothesis (risk of predation) and the plasticity hypothesis
(presence of enemies) (103, 123). Apparency theory (36) predicts that defenses evolve in direct
proportion to predation risk and inverse proportion to fitness cost. It has largely been criticized
as impractical: Although Feeney (36) defined apparency as the quality of being predictable in time
and space, to quantify the apparency of a host plant or tissue, one must understand the prediction
mechanism used by its herbivores, and thus apparency may be a quality of an interaction and
not of a plant per se (39, 123). However, apparency theory has been remarkably useful to our
understanding of the widespread phenomenon of indirect defenses, which function by increasing
the apparency of herbivores to their enemies (68). The apparency and OD theories have together
provided a handful of testable hypotheses posed at a functional level of analysis. Thus, among the
classical plant defense theories, these likely have the most empirical support (reviewed in 89, 123).
Nevertheless, the trade-off concept invoked by both OD and apparency theories may encourage
researchers to confuse physiological mechanism with functional roles.
As an illustration, evidence for the stress hypothesis of OD is mixed: Plants subjected to non-
herbivory stresses such as drought are predicted to be less well defended, but often are not, and
376 Schuman
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SVS: spatially varying
selection
sometimes appear to be better defended (52). Admittedly, this literature is obfuscated by the chal-
lenge of stressing plants without stressing herbivores, as well as imprecise definitions of stress
(73). Nevertheless, the mixed evidence is consistent with observations indicating that plant de-
fense traits may have multiple functions, and that the expression of these traits, as well as their
fitness consequences, depends on multiple ecological factors in addition to herbivore pressure (28,
36, 39). Patterns of plant defense are likely better understood as positions on a changing fitness
landscape, rather than as solutions to an optimization problem (87, 98).
Similarly, observed plant phenotypes may not be best explained mechanistically by a trade-off
between defense traits and growth and development. Plants excel at coordinating their metabolism
interactively with their biotic and abiotic environments, both responding to their environment
and changing it, to avoid situations in which resource availability would constrain their options
(see, e.g., 28, 48, 74, 87, 98, 111, 145). The extent to which any defense trait limits growth and
development depends on the interaction of multiple physiologically and ontogenetically regulated
processes, each of which individually contributes to, but does not solely determine, the observed
growth and defense phenotype. Each of these mechanisms involves some clearly defined trade-off
at the level of, e.g., cell expansion or proliferation versus differentiation, allocation of nutrients,
substrate channeling, or protein stability; but they may interact to buffer potential trade-offs at the
ecological or functional level (74, 76, 77). In the end, the fitness costs and benefits of any trait, and
whether it supports or competes with other traits’ contribution to plant fitness, depend on current
(ecological) and historical (evolutionary) pressures (Figure 2) (6, 88). Despite other failings, GDB
theory recognizes that physiological trade-offs at a cellular level do not equate to trade-offs at an
ecological level (74): It predicts, for example, that high levels of nutrients and light will result in
high rates of both growth and defense (123).
Functional population genetics approaches have now been added to the defense theory
repertoire (Figure 1, 2000 onward). Spatially varying selection (SVS) theory (44) draws a direct
connection between the environment-dependent Darwinian fitness consequences of genetically
controlled defense traits and traits’ predicted frequency in a population, but it does not consider
ecological functions or physiological mechanisms of these traits. Similarly, community genetics
theory (145) proposes equations derived from population genetics that can be used to scale up
from the function of a genetic trait in an individual to its effects in ecological communities. But
although it considers ecological mechanisms cleanly divided into evolutionary and functional
levels, this approach neglects physiological mechanisms of traits. Thus, neither approach provides
a full biological picture, but each offers insights into how ecological contexts might be explicitly
integrated into updated plant defense theory.
This is important because the role of ecological context in determining phenotypes is poorly
understood, most obviously in the case of biological invasions, in which a species out of context
dominates its new community. For over two decades, ecologists have sought with little success
phenotypic markers of invasiveness (136). Feeney (36) suggested that weediness of invasive plants
might be connected to their unapparency in a novel environment, and in 1995, Blossey & Notzold
(10) proposed that invasive species evolve increased competitive ability (EICA) when resources
are not allocated to defense. Data have not supported this hypothesis, which has misled its field
for twenty years (37).
Where Do Trade-Offs Occur, and How Do They Relate to Function?
The simple trade-off between growth and defense invoked in classical plant defense theories
such as OD has been supplanted by an increasingly detailed picture portraying a sophisticated
reconfiguration of metabolism in attacked plants, revealed by molecular chemical studies (see,
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Layers of Plant Responses to Insect Herbivores 377
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a Cellular physiology
b Regulatory feedback loops c Metabolic reconguration
PS II
H
2
O CO
2
(CHOH)
n
O
2
ETC
PS I
NADPH
ATP
ADP
NADP
+
G3P
RuBP 3PG
Sucrose
(export)
Amino acids,
fatty acids
Starch
(storage)
Chloroplast
Abiotic stress
Biotic stress
Mutations
Development
Unfolded proteins
UPR genes
Ub
ATP depletion
Vigorous protein synthesis
Aberration of Ca
2+
or redox homeostasis
Inhibition of protein modication
Inhibition of protein transfer to Golgi apparatus
ERAD
stimulate
promote
restore
prevent
relieve
Nucleus
ER
Interlocked
feedback loops
Diurnal and
other
external cues
Metabolite
accumulation
ZT 0 12 24 36 48 0 12 24 36 48 0 12 24 36 48
1° metabolites Intermediates 2° metabolites
Herbivores
Herbivores
Mycorrhizae
Systemic
HIPVs
HIPVs
Plant pathogens
Competitor
or parasitic plant
Entomopathogenic
nematode
Carnivores
Pollinators
Endophytes
26s
d Ecological phenotypes
378 Schuman
·
Baldwin
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e.g., 8, 9, 12, 54, 94, 110, 122, 125, 147). The individual physiological and ontogenetic trade-offs
that contribute to this complex network differ by how much they influence fitness trade-offs at the
ecological level. A few master switches regulate many components, and in many cases, molecular
interaction studies have already implicated these key players (e.g., 16, 17, 33, 38, 50, 96, 104, 116,
117, 128, 132, 150). However, even when measuring effects of master regulators, the magnitude
and even direction of a growth-defense trade-off are likely to depend strongly on environmental
variables. Furthermore, traits that attract enemies of herbivores, transport and storage mechanisms
that make nutrients inaccessible, and even phenological shifts that confer herbivore avoidance are
part of the network regulated by herbivory, and must be considered as components of defense,
alongside toxic, repellent, and antinutritive secondary metabolites (8, 36, 64, 69, 112, 114, 115).
Defense traits are any traits that defend plant fitness in the face of stress, and the more ecologically
realistic the environment, the more robust the demonstration of defensive function (64, 74). As
has been discussed elsewhere (e.g., 9, 20), it is often difficult to establish ecologically realistic assays
and to measure fitness consequences, but challenges encountered when measuring the right thing
cannot be remedied by measuring the wrong thing. We would argue that suitable compromises
can be found, so long as these are also clearly defined and their shortcomings acknowledged (e.g.,
74, 112).
In fact, we still know astonishingly little about what plants must do in order to grow, defend,
reproduce, and keep fit in their native ecologies (Figure 2). Although plants are autotrophic
organisms, harnessing energy from sunlight and water, fixing carbon from the air, and taking up
mineral nutrients from the soil, they also must operate as heterotrophs, metabolizing their fixed
carbon and nutrients to form a plethora of other metabolites in a system of precisely coordinated
metabolic networks (126). The circadian clock plays a crucial role in regulating these processes,
for example, preparing the photosynthetic machinery just before daylight and allowing plants to
pace the metabolism of starch during the night (31).
The next section provides an updated overview on the molecular mechanisms of plant de-
fense responses that points out where trade-offs take place, and describes how a multitude of
physiological and ontogenetic events are integrated into observed phenotypes, i.e., to incorporate
mechanistic, functional, and evolutionary levels of analysis into an integrated understanding with-
out confounding these levels. We continue to take a phytocentric view (8) because this reflects our
expertise and because we believe that entomologists benefit from an accurate understanding of
plants just as plant scientists benefit from understanding insect herbivores (32, 40). Furthermore,
we assume that plants and their herbivores are strategic players in a set of games that play out in
ecological time, with consequences for evolutionary trajectories (87, 98). The view we present dif-
fers from descriptions of plant defense syndromes (2), which acknowledge the interdependency of
defense- and growth-related traits but have not integrated physiological and ecological plasticity.
←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Figure 2
An overview of the physiological constraints plants face as photosynthetic organisms when responding to attack from, and manipulating
the behavior of heterotrophs: coordination of the light and dark reactions of photosynthesis with (a) subcellular physiology of general
and specialized metabolism via the (b) circadian clock, and the resulting (c) chemical and (d ) ecological phenotypic parameters that we
can measure. Arrows in panel c indicate the timing of an herbivore induction event either at midday (left arrow)ormidnight
(right arrow). Abbreviations: ER, endoplasmic reticulum; ERAD, ER-associated degradation; ETC, electron transport chain; HIPVs,
herbivore-induced plant volatiles; PSI/II, photosystem I/II; Ub, ubiquitin; UPR, unfolded protein response; ZT, Zeitgeber time (e.g.,
time since dawn on the first day of the experiment). Images in panel a are modified from References 92 (left) and 151 (right), image in
panel b is modified from Reference 50, and images in panel d are modified from Reference 28. Conceptual graphs in panel c arose from
discussions with D. Li (75).
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Layers of Plant Responses to Insect Herbivores 379
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HAE:
herbivore-associated
elicitor
FAC: fatty
acid–amino acid
conjugate
THE LAYERS OF PLANT DEFENSE RESPONSES TO HERBIVORES
Plant defense responses to herbivores can be understood at any of several layers, from genetic
structure through ecological influence (Table 1). These layers are separate but not independent:
Each emerges from layers below it, and receives feedback from layers above it, but each layer
represents a different level of analysis (118). Genetic programming, ontogeny, and environmental
factors have all been considered, if not cleanly separated, in plant defense theory. We focus on
the molecular physiology of plant responses to insect herbivores, an area in which advances in
knowledge have led to an updated experimental and theoretical understanding of plant defense
against herbivores. This layer can be divided into (a) perception of herbivores, (b) early signaling
responses, (c) hormone-mediated signaling, (d ) reconfiguration of metabolism, and (e) changes to
phenology. The transcriptional layer of regulation that connects hormonal signaling to phenotypic
changes has been reviewed (54) and so we do not repeat it here.
Perception of Insect Herbivores
Specificity in response to herbivores begins with plants’ perception of damage patterns and
herbivore-associated elicitors (HAEs) in amounts as little as femtomolar concentrations (see side-
bar, PAMP Envy) (reviewed in 12, 33, 60, 93, 147). Plants respond to characteristic spatiotemporal
patterns of damage (60, 95) and furthermore can perceive damage to the leaf surface and trichomes
when herbivores land or walk (reviewed in 33, 59). Plants seem to count the number of herbivore-
associated damage events, and the dynamics of the signaling response to each individual event
determine the characteristics of the response to repeated events (reviewed in 41). However, the
HAEs found in secretions and fluids from herbivores are essential for many components of plant
responses (reviewed in 12, 59, 60, 93, 147).
The first HAEs were discovered in the 1980s and 1990s (reviewed in 12). HAEs may be digested
plant molecules such as inceptins, proteolytic products of the plant chloroplastic ATP synthase γ-
subunit found in Spodoptera frugiperda (fall armyworm) oral secretions (108); or herbivore-derived
molecules thought to be essential for metabolism, such as fatty acid–amino acid conjugates (FACs),
which are probably required for nitrogen metabolism in Lepidoptera (151). The first fully charac-
terized HAE was the hydroxyl FAC volicitin [N-(17-hydroxylinolenoyl)-
L-glutamine], identified
as the plant-volatile-inducing factor in Spodoptera exigua (beet armyworm) oral secretions (3). Data
support the existence of a membrane-bound volicitin receptor that is upregulated by herbivory
(131), but the protein has not been identified; however, a lectin receptor kinase gene (LecRK1)
that is rapidly, transcriptionally upregulated in response to the FAC N-linolenoyl-glutamate from
Manduca sexta (tobacco hornworm) was identified in Nicotiana attenuata (coyote tobacco) (42). Oral
secretions from eight different lepidopteran species furthermore formed ion-permeable channels
in artificial membranes, although FACs alone were unable to form stable channels (82).
Plants may further metabolize HAEs as in the case of N-linolenoyl-glutamate from M. sexta,
which is rapidly oxidized by a lipoxygenase upon application to N. attenuata leaves (139). This may
be one mechanism endowing specificity of plant responses to herbivores. Plant species respond
differently to the same HAEs as measured, e.g., by phytohormone production (109), or they may
not respond at all to specific HAEs (121). Within plant species, the magnitude and quality of
response to the same HAEs vary: In N. attenuata, a genotype native to Arizona had a reduced
signaling and metabolic response to M. sexta oral secretions compared with a genotype from Utah
(149), and neighboring plants from single populations in Utah displayed differences of a similar
magnitude (63, 113).
380 Schuman
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Table 1 Layers of plant defense against herbivores, corresponding levels of analysis, and examples of observed phenomena
and testable hypotheses. Levels of analysis are from Sherman (118)
Layer Level of analysis Phenomena Example hypotheses
Ontogenetic changes Ontogeny (proximate) Changes in tissue-specific
hormonal signaling over life
stages
Flowering shuts down herbivore-elicited
ethylene signaling.
Tissue- and life-stage-specific
accumulation of metabolites
Herbivore-induced vegetative volatile
emission is downregulated when flowers
open.
Stage-specific growth and
differentiation patterns
Sensitivity to herbivore induction as
measured by production of hormones,
transcripts, or metabolites differs with
growth stage.
Changes in phenology Senescence processes are induced by
herbivory.
Flower opening time is changed by
herbivory.
Physiological changes Physiology (proximate) Perception of herbivory Transmembrane receptor proteins detect
FACs.
Early signaling events The waveform of [Ca
2+
]
cyt
fluctuations
determines the identity of the protein
messenger activated by Ca
2+
.
Phytohormone signaling JAs other than JA-Ile also bind specific
SCF
COI1
-InsP
5
-JAZ complexes to
release inhibition of JA-upregulated
genes.
Reconfiguration of metabolism Systemically transported specialized
metabolites accumulate in proportion to
tissue sink strength.
Changes in growth rate Different herbivore elicitors result in
different magnitudes of reduced growth
rates within a plant genotype.
Genetic and epigenetic
architecture
Evolution (ultimate) Inter- and intrapopulation
variation in defense gene alleles
The frequency of a defensive gene in a
plant population is proportional to risk
of herbivory by a susceptible herbivore.
Epigenetic signatures of
herbivory
Herbivory in the current generation of
plants causes a predictable epigenetic
signature in the next generation.
Ecological interactions
and realized phenotype
Function (ultimate) Defensive functions of specialized
metabolites
WT accumulation patterns of specialized
metabolites increase plant fitness under
herbivory.
Resistance function of specialized
metabolites
WT accumulation patterns of specialized
metabolites reduce herbivore damage.
Fitness costs of producing
specialized metabolites
WT accumulation patterns of specialized
metabolites reduce plant fitness in the
absence of herbivore attack.
Abbreviations: FAC, fatty acid–amino acid conjugate; JA, jasmonate; WT, wild type.
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Layers of Plant Responses to Insect Herbivores 381
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PAMP ENVY
The perception mechanisms for characteristic microbe- or pathogen-associated molecular patterns (MAMPs/
PAMPs) and effectors from pathogenic microbes is well understood, having produced the gene-for-gene and guard
hypotheses for which there is extensive experimental support (62). This has produced a phenomenon that could
be called PAMP envy in which every review of HAEs must begin with a summary of how similar HAEs are to
MAMPS, PAMPS, and effectors, yet how relatively little is yet known about HAE perception. This sorry state
of affairs is a consequence of where the two fields started: The chemical ecology of plant-insect interactions was
developed by zoologists, phytochemists, and plant physiologists, and plant pathology investigations were begun by
molecular biologists and geneticists. Plant-insect interaction research generally has a better understanding of the
mechanisms, in particular the specific chemistries by which plants and sometimes ecological communities shape
interactions, whereas plant pathologists have a more epidemiological understanding: Some genotypes are more
resistant than others, but the organism-level mechanism and context dependence of resistance are often not known.
An exception is the field of ecological immunology, which attempts to synthesize the cellular, immunological level
with the community-based, ecological level of an organism’s responses to pathogens (83).
MAPK:
mitogen-activated
protein kinase
ROS: reactive oxygen
species
JA: jasmonate
Early Signaling Response
Upon feeding damage or wounding and application of regurgitant, a membrane potential (V
m
)
depolarization at the feeding site spreads isotropically through the leaf in minutes, as first charac-
terizedindetailforPhaseolus lunatus (Lima bean) damaged by Spodoptera littoralis (Egyptian cotton
leafworm) (81). This is rapidly followed by influx of Ca
2+
at the feeding site, which could also be
stimulated in P. lunatus by wounding and application of volicitin or the detergent sodium dodecyl
sulfate (SDS) (81). Within minutes of feeding damage, elevated mitogen-activated protein kinase
(MAPK) activity can be detected proximate to the feeding site and in remote locations within
the damaged leaf, although the distribution of MAPK activity in N. attenuata was constrained by
vasculature and vascular flow (148). MAPK activation occurs both up- and downstream of calcium
signaling (reviewed in 147), and calcium signaling appears to occur both up- and downstream of
reactive oxygen species (ROS) signaling, which is also associated with herbivory but not with me-
chanical damage; as in pathogen attack, induced ROS production is likely controlled by NADPH
oxidases (reviewed in 12, 147).
ROS production, calcium signaling, and MAPK signaling are essential components of responses
to a plethora of biotic and abiotic stresses and cues. Thus, the integration of other environmental
or stress-related signals likely occurs during the early signaling response to herbivores, but the
mechanism of signal integration at this stage is not well understood (reviewed in 12, 147). MAPKs
initiate signaling cascades, resulting in activation of transcription factors and phytohormone-
mediated signaling (reviewed in 147), and signal integration via phytohormone interactions has
been more closely investigated. Interestingly, herbivory-induced MAPK activity patterns corre-
spond to patterns of jasmonate ( JA) stress hormone accumulation in N. attenuata leaves (127, 148).
Hormonal Signaling Response
Most herbivore resistance traits are induced by JAs (reviewed in 60, 147), and JAs were shown to
negatively regulate tolerance of herbivory in N. attenuata (80). JAs are synthesized in plastids and
peroxisomes from linolenic acid cleaved from plastidial membranes by glycerolipase (GLA) and
peroxidated by lipoxygenase (13). cis-(+)-12-Oxo-phytodienoic acid (OPDA), which is synthe-
sized in the plastid, may be the first active hormone in the pathway and is stored, for example, as
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arabidopsides for rapid release upon wounding in Arabidopsis thaliana (mouse-ear cress) (reviewed
in 26). The 18-carbon OPDA is transported to the peroxisome, where it is converted to the
12-carbon (+)-7-iso-jasmonic acid, which may be methylated, hydroxylated, or conjugated to
amino acids or sugars to form active and inactive JAs that may be modified further (reviewed in
60, 143, 144).
The conjugate (+)-7-iso-jasmonoyl-
L-isoleucine ( JA-Ile) is thought to be the primary active
form (38); however, JA signaling, but not JA-Ile, is required in Solanum nigrum (black nightshade)
for resistance against herbivores (138); and JA-Ile is not required for JA-induced volatile emission
in A. thaliana (137). JA-Ile is perceived by the Skp/Cullin/F-box SCF
COI1
E3 ubiquitin ligase
complex (65, 150) interacting with inositol pentakisphosphate (InsP
5
) (117) and one or more
jasmonate ZIM-domain ( JAZ) proteins (17, 128): Different SCF
COI1
-InsP
5
-JAZ complexes may
have altered binding specificities (19, 117). Fifteen JAZ/TIFY proteins in A. thaliana have been
characterized to date (reviewed in 66), and similar numbers were reported in other plant species
(99). The JAZ/TIFY proteins can form complexes with each other and with the JA-regulated
transcription factor MYC2 as well as with proteins involved in other hormone signaling pathways
(reviewed in 67, 104). In a mechanism similar to auxin and gibberellin signaling, when levels of
active JAs are low, JAZ proteins bind to and repress JA-regulated transcription factors; when JA
levels are high, the activated SCF
COI1
-InsP
5
-JAZ complex labels JAZ for degradation, activating
gene transcription (reviewed in 104). Alternative splicing of JAZ may tune sensitivity by producing
variants with reduced affinity for the SCF
COI1
receptor complex (18).
JAs interact extensively with other plant hormones and function in growth and fertility as well
as defense (reviewed in 143, 144, 147). The interaction of JAs with other hormones permits in-
tegration of multiple stress and developmental signals (reviewed in 33, 104). Ethylene modifies
JA-mediated responses, and auxins and the pathogen defense hormone salicylic acid suppress the
action of JAs, whereas interactions between JAs and gibberellins (57), cytokinins (106, 107), ab-
scisic acid, and nitric oxide are less well understood (reviewed in 33, 104). Herbivores, similar to
pathogens, can manipulate these hormone interactions to their own advantage, often by inducing
salicylic acid accumulation to repress JA-mediated responses (reviewed in 104). Some herbivores
and pathogens manipulate cytokinins to change the sink strength and nutritional quality of dam-
aged tissues: Agrobacterium tumefaciens and galling herbivores use cytokinins to create local sinks
in plants, and leafminers form green islands in senescent leaves (reviewed in 33, 43); and more
mobile herbivores such as M. sexta and Tupiocoris notatus (tobacco suckfly) may also manipulate
cytokinin signaling (105, 107). Cytokinins from herbivores are often produced by symbiotic mi-
crobes (reviewed in 43).
Systemic signaling via the vascular system induces defenseproduction in remote plant parts after
attack, similar to the phenomenon of induced systemic resistance after pathogen attack (reviewed
in 35, 60, 147). Classical grafting experiments in Solanum lycopersicum (tomato) indicated that JA
biosynthesis was necessary to produce a long-distance wounding signal, while JA perception was
required for its perception in distal leaves, and a JA-derived phloem-mobile signal was proposed
(reviewed in 60). Within minutes of wounding, electrical signals spread to systemic tissue via
vascular connections and glutamate receptor-like (GLR) ion channels (35, 96, 147). In A. thaliana,
a lipoxygenase expressed in cells adjacent to xylem is responsible for synthesizing JAs in systemic
tissue (16, 35). It is now thought that systemic JA biosynthesis in A. thaliana is triggered similarly
to JA biosynthesis in distal regions of a wounded leaf: by V
m
depolarization and/or Ca
2+
flux
transmitted by GLRs and resulting downstream signaling events; however, systemic (between-
leaf) signaling is suggested to also involve temporary changes in xylem pressure (35, 81).
The take-home message of the advances in systemic signaling research is that when an herbivore
attacks a plant, the entire plant recognizes and responds to this attack at some level, even if
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Layers of Plant Responses to Insect Herbivores 383
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Specialized
metabolism:
metabolic pathways
and products that are
not strictly required
for growth and
production of new
cells; also called
secondary metabolism
Direct defense: plant
defense trait that
directly affects the
ability of an herbivore
to assimilate plant
tissue, e.g., via a
repellent, toxic, or
antidigestive
mechanism
some responses are highly localized to the attacked tissues. In some plants, priming of systemic
defense responses by perception of herbivore-induced volatiles may be a mechanism to avoid
vascular constraints on systemic perception of damage (55). The arena of the induced responses is
potentially extended to neighboring plants sufficiently close and sensitive to emitted volatiles or
that share mycorrhizal connections (7, 55).
Reconfiguration of Metabolism
Herbivory induces extensive changes to both general and specialized metabolism via a transcrip-
tional reconfiguration specific to each herbivore (reviewed in 54, 114). This reconfiguration can
be interpreted as a downregulation of growth and an upregulation of defense in the trade-off
framework. Alternatively, it can be understood as the coordinated reconfiguration of metabolism
to prevent the allocation of energy and nutrients to herbivore fitness, rather than to plant fit-
ness (Figure 2, Table 1). These interpretations are not incompatible, but the second suggests
specific hypotheses that are closely connected to known mechanisms of plant physiology and
plant-herbivore interactions, and is therefore more useful.
One option for plants to avoid converting their fitness to herbivore fitness is of course to avoid
attack, and one way to do this is to “smell bad.” Plant volatiles comprise thousands of structures,
and volatile blends are specific to particular stress events and even configurations of herbivores
and their parasitization status (28, 100, 119). Volatiles may increase the foraging efficiency of
predators and parasitoids of herbivores or prevent herbivores from ovipositing, but herbivores
may use the same compounds as cues to locate host plants (reviewed in 28). However, in different
ratios, these compounds become more attractive to predators and deterrent to herbivores (4, 5). A
volatile blend may comprise the emission from multiple plants, meaning that volatile emission of
close neighbors can determine a plant’s attractiveness to herbivores and predators (111). There is
evidence that plants can detect neighbors’ volatiles (reviewed in 28, 55), and one yet unexplored
function of plants’ sense of smell may be that they adjust their own volatile emission to what the
neighbor is producing. Plant volatiles are a double-edged sword.
Once a plant is attacked, the goal of retaining energy and nutrients for plant fitness can be
achieved in two ways: by channeling metabolism toward synthesis of secondary metabolites, in-
cluding direct and indirect defenses, ideally selected for effectiveness against the attacking her-
bivore; and by enacting tolerance mechanisms to mobilize nutrients away from the attack site
and store them in inaccessible forms for later remobilization. The ever-expanding list of known
specialized plant metabolites has been reviewed by many others (e.g., 8, 36, 40, 78, 86, 94) and, in
addition to more classical examples of plant volatiles, toxins, and digestibility reducers, includes
compounds closer to general metabolism such as diterpene glycosides (56, 120) and antinutritive
amino acids (1). The discovery that JA signaling dramatically regulates leaf sugar levels (79), in
addition to regulating specialized metabolites, underscores how everything in metabolism can be
recruited to enhance defense.
Herbivore assimilation rates depend on the composition of nutritive and antinutritive metabo-
lites rather than on the absolute amounts of either: This key insight explained differences in
mechanism as well as consequences for digestibility-reducing defenses versus toxic direct defenses
proposed by OD and apparency theories (36, 39), and it explains why defense theories such as
CNB, RA/GR, and GDB, which at most predict total amounts of secondary metabolites, are not
useful. Herbivore consumption rates depend on palatability, which may reflect tissue nutritional
quality, but are more likely determined by specific metabolites acting as phagostimulants that may
also be important for host location (14, 40, 141), such as the six-carbon green leaf volatiles (46,
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Specialist herbivore:
herbivore that feeds on
a restricted set of
plants
47, 90). When it comes to understanding the chemical underpinnings of defense, the devil lies in
the chemical details: Composition matters more than total amounts.
The composition of metabolites in tissues can be altered not only by induction of specialized
metabolite production and the reallocation of standing pools of antinutritive metabolites, but also
by the reallocation of nutritive metabolites through senescence or other processes (discussed in
23, 88, 89, 105). Changes induced by the shoot herbivore M. sexta in the expression of the SnRK1
subunit GAL83 increased carbon partitioning to N. attenuata roots, reducing loss of energy to
herbivory and permitting later remobilization of more carbon from roots for seed production
(115). Interestingly, members of the SnRK1 family are involved in regulating plant developmental
transitions based on carbon availability and thus may provide a link between growth and defense
(132). The ability of plants to reallocate nutritive metabolites will depend on the sink strength
of the attacked tissue, which may explain why some (perhaps many) herbivores and pathogens
manipulate cytokinin signaling (43, 107).
Particular feeding patterns may also allow herbivores to avoid induced responses in their host
plants, akin to the laticifer-cutting behavior employed by herbivores feeding on latex-producing
plants (2). By contrast, plant metabolites may manipulate herbivore behavior and susceptibility to
attack. For example, ingestion of trypsin protease inhibitors has a small effect on the growth of the
specialist herbivore M. sexta, but a large effect on its ability to defend against predator attack (112),
thus potentially rendering larvae more susceptible to plant indirect defense, although perhaps also
rendering them less nutritious prey. Toxic metabolites such as the eponymous alkaloid nicotine
in N. attenuata may determine the potential predator community, selecting for predators that can
avoid ingesting, or that can detoxify, nicotine (72). For the generalist S. exigua, consumption of
N. attenuata tissue is limited by its capacity to detoxify nicotine, which is much less than the capacity
of the nicotine-adapted M. sexta;thisrendersS. exigua more susceptible to digestibility-reducing
protease inhibitors because it cannot compensate by consuming more tissue (124).
The plant circadian clock has been proposed to synchronize the expression of defense traits
with herbivore activity (45, 61). However, a key insight from plant defense theory—and one that
has proven robust—is that herbivore populations vary with plant chemistry and life history, and
any individual plant species is likely to face attack from an herbivore community that varies in time,
composition, or both (36, 39). Just as herbivores differ in their ability to cope with plant defense
traits, they also differ in the timing of their activity (32, 61). The internal clock tunes sensitivity to
diurnally predictable stress factors, but herbivory often does not fit into that category, in contrast
to events such as drought stress and pathogen attack, which strongly depend on diurnal changes
in abiotic factors such as humidity (61, 116, 142). Thus, the role of the clock in defense against
herbivory is likely to be more complex than simple rhythmic control of secondary metabolism. For
example, clock regulation of metabolic flux may result in differences in the temporal accumulation
of defense metabolites when plants are attacked at different times of day (Figure 2b) (75). Stress
factors may even disrupt the clock (116, 142).
Phenology and Timing
OD theory predicts that changes in phenology to reduce apparency could be an aspect of plant
defense responses; however, it envisioned these changes over evolutionary and not ecological
time (36, 102, 103). More recent studies have shown that growth rate, allocation of resources,
flowering time, and even flower phenology are altered in ecological time in response to herbivory
(69, 115, 116; and see references in 48, 123). For N. attenuata, the specialist herbivore M. sexta is
also an important pollinator. When attacked by M. sexta larvae, the plant changes flowering time
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Layers of Plant Responses to Insect Herbivores 385
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from nighttime to morning, thereby switching to likely less effective hummingbird pollination
but avoiding further oviposition (69). Leaf removal and elicitation with methyl jasmonate can
alter flowering time in competing plants (134); perhaps plants genetically programmed with an
earlier flowering time, though likely to be smaller and set less seed, are more likely to successfully
distribute seed in seasons with high herbivory pressure, thus stabilizing variation in flowering time
in populations.
In A. thaliana, natural variation in the sequence of pseudo response regulator (PRR) genes
that link external inputs to the internal clock can enhance fitness (91). Variation in the expression
of the light-signaling gene gigantea (GI) under long-day conditions is widespread and has been
proposed to cause conditional variation in the temporal dynamics of diurnally regulated gene
expression, which may permit temporal variation in phenotypes while avoiding pleiotropic effects
from disrupting the clock (27). Such differences in timing could be mimicked using transgenic
plants expressing clock genes under the control of an inducible promoter (105). Sensitivity of
plants to herbivores and production of defense metabolites may furthermore fluctuate throughout
the day as a result of regulation by the plant circadian clock (reviewed in 116, 146) and also depends
strongly on plant developmental stage (11, 29, 49, 71, 135), the progression of which is determined
by the clock interacting with environmental cues (24).
CONCLUSIONS AND FUTURE DIRECTIONS
Plants tailor their defense responses to different herbivores on the basis of HAEs and patterns of
damage from, e.g., feeding or oviposition (reviewed in 12, 33, 60, 93). Different plant species re-
spond differently to the same HAEs (109). Within a species, the magnitude and quality of response
to an herbivore, as measured by activation of signal transduction components and accumulation
of stress hormones, may vary greatly (113, 149), as may the resulting profile of defense metabo-
lites (70; reviewed in 28, 147). What causes this variation? This question can be answered at four
different levels of analysis (Figure 1).
Ontogenetic changes cause large changes in the hormonal and metabolic response to her-
bivory. For example, new buds on an oak (Quercus robur) will not produce tannins, although the
surrounding leaves do (36), and although M. sexta feeding on N. attenuata produces a burst of
ethylene on rosette-stage plants, this burst disappears with the first flower, along with some of the
plant’s inducible defenses, representing a switch from inducible to constitutive metabolite deploy-
ment with the transition to reproductive growth (29)—at least for plants in pots. Mechanistically,
different individuals and species have an array of stages in their signaling response to an herbivore
that may be tuned toward higher or lower sensitivity, for example, by mutations in cis-regulatory
DNA elements that control the transcription of regulatory genes, or by mutations in the alterna-
tive splicing of JAZ genes and other regulators. At the evolutionary level, balancing selection for
two or more alleles of such mutated genes may exist owing to unpredictable or cycling herbivore
populations, for example, or plant populations may undergo purifying selection for one allele or
another (44). Finally, at the functional level, the effect of any one defense trait on the individual’s
inclusive fitness will be determined by a changing and interactive Darwinian fitness landscape,
meaning that plasticity and honed powers of perception are likely very important, but, as assumed
by OD, otherwise anything goes, as long as it is adaptive (98, 102).
Often the evolutionary success of a genotype is determined by its relative advantages compared
with those of its neighbors: Can it grow faster, produce more seed, and defend better (87)? How-
ever, there are important examples, such as the survival of seeds in the seed bank, in which fitness
differences approach categorical distinctions rather than small relative advantages: Is the seed resis-
tant to microbial attack or not? The layered view of plant defense permits separate consideration of
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physiological, ontogenetic, ecological, and evolutionary phenomena while recognizing that each
layer contains emergent properties from the one(s) below it, and that both diurnal timing and on-
togenetic processes are important modifiers of plant responses to the environment. The resulting
integrated concept relies on the definition of defense as a set of ecological context-dependent
responses that increase plant fitness in the face of herbivore attack. We note that this definition of
plant defense is compatible with the concept from ecological immunology of adaptive responses
to pathogens (83), and consistent with the attempt to scale up from genes to ecosystems embodied
in the community genetics approach (145).
SUMMARY POINTS
1. Plant defense theory emerged from efforts to understand the distribution of specialized
plant metabolites in nature, and the role of these metabolites in structuring ecological
communities. However, progress was stymied because the theories frequently posited
hypotheses posed at different levels of analysis, which made them impossible to rigorously
test.
2. Plant defense phenotypes emerge from the coordination of subcellular and whole-
organism physiological processes, and the trade-offs involved are more complex than
balancing an account with photosynthetic carbon fixation and nutrient uptake on the
one side, and growth and secondary metabolite production on the other.
3. Plant defenses are configured in response to particular attackers via recognition of specific
elicitors and patterns of damage, leading to tailored reconfiguration of metabolism that
extends to the entire plant for some responses.
4. Specialized plant metabolites are an essential component of plant defense responses,
which also include physical barriers, tolerance mechanisms, repellent traits, spatiotem-
poral escape, and any other traits that increase fitness under herbivore attack.
5. Plant defense responses and their fitness outcomes are shaped by interactions of plants
with their ecological communities and their abiotic environment, likely in that order.
FUTURE ISSUES
1. What are the receptors of HAEs? How can they be identified? Can we learn from
plant-pathogen interaction research methods, which have identified multiple receptors
of MAMPS and PAMPS and targets of effectors?
2. To what extent is there specificity in the early signaling response to different attackers?
How is it shaped by the perception of other stress factors? How do early signaling
responses produce tailored phytohormone signaling?
3. How is specificity encoded at the level of phytohormone signaling? What is the signifi-
cance of the several JAZ/TIFY proteins and their interactions with each other and other
proteins? What role do JAs other than JA-Ile play? How are multiple hormone signaling
pathways integrated? How are they manipulated by herbivores?
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Layers of Plant Responses to Insect Herbivores 387
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4. What are the roles of general and specialized metabolism in determining nutritional
quality and palatability for more or less specialized insect herbivores? How do direct and
indirect defense strategies interact? How is this metabolic reconfiguration constrained
by ontogeny? What are the cellular constraints on launching induced defenses?
5. How do the phenotypes of neighbors alter a plant’s own realized phenotype and fitness
landscape? What are the consequences for biodiversity and ecosystem function?
6. How can we use this knowledge to address pressing practical concerns such as biological
invasions and agricultural sustainability?
7. Can we avoid hypothesis conflation, unfalsifiability, and “talking past each other” in the
future by applying Sherman’s levels of analysis and conceptual frameworks based on these
levels, such as the concept of plant defense as a series of layers?
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
The authors thank C. Diezel for assistance with panels a and b of Figure 2; N. Whiteman for dis-
cussion about functional population genetics and plant defense theory; A. Steppke, M. Berenbaum,
and three anonymous reviewers for comments that improved the concept, focus, and precision of
the manuscript; an ERC Advanced Grant (no. 293926) to I.T.B; the German Centre for Integra-
tive Biodiversity Research (iDiv) Halle-Jena-Leipzig funded by the German Research Foundation
(FZT 118); and the Max Planck Society for funding.
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