Biotic interactions
Recurring themes and expanding scales
Editorial overview
Jane Glazebrook and Jurriaan Ton
Current Opinion in Plant Biology 2007, 10:331–334
1369-5266/$ – see front matter
# 2007 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2007.06.005
Jane Glazebrook
Department of Plant Biology and Center for
Microbial and Plant Genomics, University of
Minnesota, Rm 250 BioSci Center, 1445 Gortner
Avenue, St. Paul, MN 55108, USA
e-mail: [email protected]
Jane Glazebrook’s research interests surround signal
transduction networks that control activation of plant
defense responses, and the nature of responses that
contribute to resistance to particular pathogens.
Works on an Arabidopsis-Pseudomonas syringae
pathosystem are focused on using expression
profiles as detailed phenotypic descriptions of
mutants with defects in defense signaling. Similarities
in profiles are used to construct models of signal
transduction networks controlling activation of
defense responses. Similar work is done using an
Arabidopsis — Alternaria brassicicola pathosystem
in an effort to understand resistance to necrotrophs.
The phytoalexin camalexin is required for resistance
to Alternaria, so some works address the
biosynthesis of this compound and mechanisms that
regulate its production.
Jurriaan Ton
Plant-Microbe Interactions, Institute of
Environmental Biology, Utrecht University,
Wentgebouw, Sorbonnelaan 16, 3584 CA Utrecht,
The Netherlands
e-mail: [email protected]
The research interests of Jurriaan are focused on
priming for defense against pathogens and insects.
After perception of specific environmental stimuli,
plants are capable of enhancing the efficiency of
their innate immune system. Many of these
induced-resistance phenomena are based on a
sensitization, or ‘‘priming’’, of inducible defense
mechanisms. Activation of priming causes an earlier
and stronger defense reaction upon exposure to
biotic stress, and yields protection against a broad
spectrum of pathogens and insects. Elucidating the
molecular and physiological regulations of priming
is the main topic of Jurriaan’s research. This line of
research is focused on the mechanisms by which
priming-inducing signals enhance the capacity of
defense-related signaling pathways in Arabidopsis
and maize. Other areas of research include a series
of field experiments that aim to explore the
ecological relevance of priming. These field trials
may also provide useful information for future
initiatives to exploit priming in agriculture.
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In nature, plants are constantly engaged in a complex dialogue with other
organisms. Because photosynthesis enables plants to convert inorganic
molecules into organic energy, they are an attractive target for potentially
harmful, opportunistic organisms. Consequently, many plant–biotic interactions are hostile, although some organisms have evolved neutral or even
symbiotic strategies to exploit the plant’s photosynthetic energy. The
outcome of these interactions determines how much energy is channeled
directly into the food web that surrounds the plant. The plant’s immune
system plays an important regulatory role in this process, and helps the plant
to shape the composition of its biotic environment.
In recent years, there has been an increasing awareness that multidisciplinary and integrative research is necessary to clarify the complexity of plant–
biotic interactions. In this context, it is not only important to extract relevant
information from the growing pile of ‘‘-omics’’ data, but is also necessary to
extrapolate this molecular and biochemical information to the level of whole
organisms and communities. At the same time, translation of important
discoveries from the field of plant–biotic interactions into useful applications
in sustainable agriculture remains the ultimate goal of many basic research
projects.
This issue of Current Opinion in Plant Biology contains 13 reviews that,
together, illustrate how integrative and multidisciplinary research provides
insights into the biotic ‘‘interactome’’ of plants and possible applications in
agriculture. Some of these reports review the latest discoveries about
molecular processes common to many plant–pathogen interactions. These
recurrent themes include recognition of pathogens by plants, resistance to
pathogen penetration at the cell wall, suppression of plant defense by
pathogens, and the transcriptional regulation of defense-related plant genes.
Other reviews in this issue focus on the consequences of these processes at
expanding biological scales, ranging from molecular recognition to the
ecological impact of plant defense.
Recurring theme 1: plants recognize microbes
Plants are constantly under attack by prospective pathogens, so pathogenrecognition mechanisms are crucial for their survival. Readers of this issue
are probably familiar with the paradigm of gene-for-gene resistance, in
which plant resistance (R) gene products, usually of the nucleotide bindingleucine rich repeat (NB-LRR) class, recognize products of pathogen avirulence genes and trigger a resistance response usually accompanied by
hypersensitive cell death. This concept has evolved in recent years with
the realizations that avirulence genes are actually pathogen effector genes
Current Opinion in Plant Biology 2007, 10:331–334
332 Biotic interactions
that promote virulence in hosts lacking corresponding R
genes and that recognition may not involve direct interaction between R proteins and effectors but rather the
sensing of effector activities by R proteins. R-genemediated resistance was reviewed in previous Biotic
Interactions issues.
In this issue, Bittel and Robatzek describe a distinct
microbe-recognition mechanism that is probably much
older than R gene recognition. Microbes produce molecules that are foreign to plants, so the presence of such
molecules (known as MAMPs, for microbe-associated molecular patterns) indicates the presence of a microbe. Wellstudied examples include bacterial flagellin, elongation
factor Tu (EF-Tu), and lipopolysaccharide (LPS). MAMPs
are recognized through receptor-like kinases in the host
plasma membrane, triggering at least two MAP kinase
cascades leading to transcriptional activation of defense
genes. Some of these receptors are well conserved among
different plant species, while others appear to be quite
specific. Defense responses activated by different MAMPs
receptors are very similar, leading to speculation that
MAMPs signaling converges on a common pathway.
Recurring theme 2: pathogens must penetrate
The first challenge that a successful pathogen must overcome is gaining access to the host tissue. Goggin reminds us
that many viruses are delivered by aphids. Bacterial pathogens that colonize intercellular spaces in leaves enter
through open stomata. Biotrophic fungi and oomycetes
must penetrate plant cell walls in order to elaborate intracellular haustoria through which nutrients are absorbed.
Hardham et al. describe recent work on the importance of
cell wall appositions (CWA) that form at sites of attempted
pathogen penetration. CWAs are constructed through
delivery of materials by specialized vesicles. Callose
synthases build callose deposits that reinforce the CWAs.
Mutations that compromise construction of CWAs by
interfering with vesicle fusion or callose deposition result
in successful penetration by non-adapted fungi that would
otherwise be stopped at the cell wall. Clearly, pathogens
face a difficult situation: they are rapidly recognized by
receptors of MAMPs, and this recognition results in the
activation of a slew of defense responses that may prevent
them from even entering the host. The solution to this
problem is our next recurring theme.
Recurring theme 3: pathogens produce
effectors that inhibit plant defenses
Bacterial pathogens actively transfer dozens of proteins
into host cells through a Type III secretion system.
Consequently, these proteins are often referred to as
‘‘Type III effectors’’. Intensive study of the activities
of these proteins over the past several years has revealed
biochemical activities and/or host target proteins for many
of them. The article by da Cunha et al. provides a
thorough overview of the state of the field. Amazingly,
Current Opinion in Plant Biology 2007, 10:331–334
effectors appear to target almost every imaginable aspect
of plant defense. Some even manage to mimic enzymes
that do not exist in bacteria, such as E3 ubiquitin ligases.
Other dephosphorylate MAP kinases, enter the host
nucleus and affect transcription, or degrade host proteins
through proteolytic activity. Pseudomonas syringae also
produces a small molecule effector, coronatine, that
mimics the action of the plant signaling molecule jasmonic acid, thereby inhibiting salicylic-acid-regulated
defenses and stomatal closure. As da Cunha et al. point
out, the result of all this is that the nature and extent of
plant defense responses that are actually deployed are
what remains of the recognition-induced responses after
pathogen effectors have done their work.
More recently, filamentous pathogens such as oomycetes
and fungi have also been found to produce effectors. Most
of them have a bipartite structure consisting of a domain
required for secretion and another responsible for function. Searches for characteristic motifs in genome
sequences suggest that individual isolates may produce
hundreds of different effectors. These effectors show
evidence of diversifying selection, consistent with roles
in pathogenicity. The article by Kamoun provides a
delightful review of recent work on fungal and oomycete
effectors, with a whimsical organization inspired by lyrics
of popular songs. Do not overlook the playlist provided as
Supplementary material!
Recurring theme 4: all roads lead to WRKYs
Resistance responses triggered by MAMPs recognition, as
well as those triggered by R genes, often involve the
action of WRKY transcription factors. As described by
Eulgem and Somssich, the 72 WRKY factors in Arabidopsis constitute a complex web controlling expression of
defense genes. Some WRKY factors act as transcriptional
repressors, while others are clearly activators. The presence of WRKY biding sites (W boxes) in the promoters of
defense genes suggests that many are regulated by
WRKY factors and that transcription of many WRKY
genes is also regulated by WRKY factors! An unusual
WRKY gene (WRKY52 also known as RRS1) acts as an R
gene against Ralstonia solanacearum. Once viewed as an
oddity, it now seems that this was an important clue for
the function of at least some R proteins, as the barley R
protein Mla has now been found to interact with two
WRKY repressors in plant nuclei.
Expanding scale 1: from recognition to
interacting signaling pathways
In most laboratory studies, plants are exposed to a single
pathogen, at one time, at a specific developmental stage,
and under carefully controlled environmental conditions.
Of course, in natural habitats plants can be exposed to
multiple pathogens or insects simultaneously, at any time
and under a variety of conditions. This situation requires
integration and translation of multiple stress signals into
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Editorial overview Glazebrook and Ton 333
appropriate adaptive responses. Cross-talk between
different defense-related signaling pathways may provide
enough regulatory potential to explain this ‘‘decisionmaking’’ behavior of plants. Over the past few years,
much progress has been made in understanding cross-talk
between salicylic acid-dependent (SA), jasmonic aciddependent (JA) and ethylene (ET)-dependent response
pathways. By contrast, much less is known about the roles
of other hormones in this defense-signaling network, such
as abscisic acid, auxin, gibberellin, and cytokinin. The
review by Seilaniantz et al. provides an overview of the
effects of hormones other than SA, JA, and ET on plant
defense. Recent studies point to fascinating mechanisms
by which these hormones influence plant–pathogen interactions through their effects on SA-dependent or JAdependent signaling pathways. Additional research is
required to discover the molecular signaling nodes where
this cross-talk occurs.
The collection of well-known small molecule signals
already presents a daunting challenge for understanding
how they all interact during biotic interactions. The review
by Farmer and Davoine points out that there are almost
certainly more whose roles are not very clear. In particular,
reactive electrophile species can affect gene expression as
well as other cellular processes by reacting with various
cellular components. There is still plenty of work to do in
defining the molecular players involved in biotic interactions as well as in understanding their functions.
Expanding scale 2: from interacting signaling
pathways to interacting organisms
Interactions between defense signaling pathways are also
thought to mediate the effects of below-ground defense
elicitation on above-ground interactions and vice versa.
Bruce and Pickett review many examples of cross-talk
between below-ground and above-ground interactions
with pathogenic micro-organisms and/or herbivorous
insects, and discuss potential mechanisms behind this
form of systemic communication. While activation of
systemic resistance by pathogens or insects is well documented, Bruce and Pickett raise the possibility that
suppression of defense by pathogens or insects may also
affect the balance between below-ground and aboveground resistances. Interestingly, this latter mechanism
has also been suggested to take place during interactions
with plant-beneficial organisms. In their paper on mycorrhiza-induced resistance, Pozo and Azcón-Aguilar reevaluate the phenomenon by which mycorrhizal fungi
suppress SA-dependent defenses in their hosts. The
authors propose that this suppression mitigates the negative effect by SA on JA-inducible defense reactions.
Consequently, infection by mycorrhizal fungi results in
a local and systemic potentiation of JA-inducible resistance. The hypothesis by Pozo and Azcón-Aguilar is
supported by many examples of mycorrhization boosting
resistance against necrotrophic pathogens and insects,
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and suppressing resistance against certain biotrophic
pathogens that are affected by SA-inducible defense
mechanisms.
The review by Goggin focuses on interactions between
plants and aphids. Plant defense against aphids seems
more similar to pathogen resistance than to insect resistance. For example, many plant varieties contain single
dominant genes that reduce aphid performance, which
are structurally related to R genes that are active against
microbes. Furthermore, susceptible plants attacked by
aphids deploy basal defense strategies that are remarkably similar to those deployed in response to pathogens.
Finally, the fact that many aphid species are limited to
relatively small numbers of host plants suggests comparable mechanisms of non-host resistance. In addition,
Goggin provides fascinating examples of how plant–aphid
interactions affect other organisms. Plants that are under
attack by aphids can attract natural enemies of aphids
through emissions of air-borne volatiles, whereas aphids
have been shown to recruit other organisms to help them
locate and attack their hosts. These examples demonstrate that a single plant–biotic interaction can have farreaching consequences at multiple trophic levels. This
ecological impact is the focus of our next expanding scale.
Expanding scale 3: from individual plants to
ecology
The impact of plant defense goes beyond its direct effect
on the defense-eliciting organism. The review by Kessler
and Halitsche illustrates how activation of plant defense
can influence interactions between organisms at multiple
trophic levels, leading to complex, community-wide
effects on the plant’s living environment. Kessler and
Halitsche provide examples of herbivore-induced
defense mechanisms that influence pollinator behavior
and attract natural enemies of the herbivore. In many
cases, these multitrophic impacts of plant defense are
mediated by plant-derived volatiles. Kessler and
Halitsche also emphasize the importance of field experiments. By using plants that are altered in a specific
defensive trait, crucial information can be obtained about
the ecological impact of the defensive trait, because field
experiments are not biased toward isolated target organisms. Hence, field trials can reveal aspects of plant–biotic
interactions that cannot be discovered in laboratory
environments.
Another powerful strategy to explore the ecological impact
of plant defense is presented in Holub’s review. This lucid
essay on genetic variation in Arabidopsis innate immunity
not only describes different strategies to identify R-genes,
but also illustrates how natural genetic variability can be
used as a tool to explore the ecological relevance of plant
resistance. Indeed, the idea of using a large-scale multidisciplinary approach to map genetic variation onto geographic distributions of Arabidopsis seems a very promising
Current Opinion in Plant Biology 2007, 10:331–334
334 Biotic interactions
way to assess the ecological impact of individual defenserelated genes, thereby expanding the scale of study from
molecular genetics to ecology.
Expanding scale 4: from laboratory studies to
agronomic impact
The knowledge obtained from research into plant–biotic
interactions is essential for designing innovative strategies
for sustainable agriculture. The phenomenon of induced
resistance presents an attractive concept for alternative
strategies in durable agriculture. Induced resistance can
be defined as an increase in the defensive capacity of the
plant, which is triggered by various biotic and abiotic
agents and is effective against a remarkably wide range
of pathogens and insects. Many forms of induced resistance are not based on direct activation of defensive
mechanisms by the resistance-inducing agent, but rather
on a faster and stronger activation of inducible defence
mechanisms once the plant is triggered to respond. This
sensitization of defence is called ‘‘priming’’ and is the
focus of the review by Beckers and Conrath. It is commonly assumed that induction of priming is mediated by
increased amounts of cellular components with important
roles in defense signaling. Theoretically, this enhancement in signaling capacity could act at different steps of
the pathway, ranging from the detection of MAMPS to the
production and delivery of defensive metabolites. As a
Current Opinion in Plant Biology 2007, 10:331–334
corollary, Beckers and Conrath discuss the potential of
priming in modern disease and pest management. Priming
seems an attractive concept for agricultural applications:
primed plants do not suffer from costly defense investments, as their defense arsenal is not activated before
stress exposure. Accordingly, priming for defense protects
plants without harmful trade-offs on commercially important traits, such as growth and fruit set. They conclude that
successful modern plant protection agents should combine
antimicrobial and priming-inducing activities, thus allowing reduced chemical input into the environment while
maintaining effective and sustainable plant protection.
Conclusion
We thank all the authors for their effort in creating this
volume of reviews. It is exciting to see how rapidly the
field of plant–biotic interactions is advancing and expanding into previously unexplored areas. We have enjoyed
compiling this volume and look forward to more exciting
news reported in next year’s edition. Happy reading!
Acknowledgements
Research activities of JG are supported by grants from the National Science
Foundation Arabidopsis 2010 program (IOS - 0419648) and the Department
of Energy Biosciences program (DE-FG02-05ER15670). Research of JT is
supported by a personal VENI grant from NWO, the Dutch Organization
for Scientific Research (no. 863.04.019). We also thank Kees van Loon for
helpful comments on parts of this manuscript.
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