Biotic interactions: Recurring themes and expanding scales

Biotic interactionsRecurring themes and expanding scalesEditorial overviewJane 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 inter-

actions 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 multidisciplin-

ary 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 microbesPlants are constantly under attack by prospective pathogens, so pathogen-

recognition 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 binding-

leucine rich repeat (NB-LRR) class, recognize products of pathogen aviru-

lence 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


http://dx.doi.org/10.1016/j.pbi.2007.06.005

mailto:[email protected]

mailto:[email protected]

332 Biotic interactions

that promote virulence in hosts lacking corresponding Rgenes and that recognition may not involve direct inter-

action between R proteins and effectors but rather the

sensing of effector activities by R proteins. R-gene-

mediated 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 mol-

ecules that are foreign to plants, so the presence of such

molecules (known as MAMPs, for microbe-associated mol-

ecular patterns) indicates the presence of a microbe. Well-

studied 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 penetrateThe first challenge that a successful pathogen must over-

come is gaining access to the host tissue. Goggin reminds us

that many viruses are delivered by aphids. Bacterial patho-

gens that colonize intercellular spaces in leaves enter

through open stomata. Biotrophic fungi and oomycetes

must penetrate plant cell walls in order to elaborate intra-

cellular 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 produceeffectors that inhibit plant defensesBacterial 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,


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 jasmo-

nic 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 func-

tion. 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 WRKYsResistance 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 Arabi-

dopsis constitute a complex web controlling expression of

defense genes. Some WRKY factors act as transcriptional

repressors, while others are clearly activators. The pre-

sence 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 Rgene 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 tointeracting signaling pathwaysIn 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









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 ‘‘decision-

making’’ behavior of plants. Over the past few years,

much progress has been made in understanding cross-talk

between salicylic acid-dependent (SA), jasmonic acid-

dependent (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 inter-

actions through their effects on SA-dependent or JA-

dependent 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 inter-

actions as well as in understanding their functions.

Expanding scale 2: from interacting signalingpathways to interacting organismsInteractions 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 docu-

mented, Bruce and Pickett raise the possibility that

suppression of defense by pathogens or insects may also

affect the balance between below-ground and above-

ground resistances. Interestingly, this latter mechanism

has also been suggested to take place during interactions

with plant-beneficial organisms. In their paper on mycor-

rhiza-induced resistance, Pozo and Azcon-Aguilar re-

evaluate the phenomenon by which mycorrhizal fungi

suppress SA-dependent defenses in their hosts. The

authors propose that this suppression mitigates the nega-

tive effect by SA on JA-inducible defense reactions.

Consequently, infection by mycorrhizal fungi results in

a local and systemic potentiation of JA-inducible resist-

ance. The hypothesis by Pozo and Azcon-Aguilar is

supported by many examples of mycorrhization boosting

resistance against necrotrophic pathogens and insects,


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 resist-

ance. 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 remark-

ably 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 compar-

able 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 demon-

strate that a single plant–biotic interaction can have far-

reaching consequences at multiple trophic levels. This

ecological impact is the focus of our next expanding scale.

Expanding scale 3: from individual plants toecologyThe 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 exper-

iments. 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 organ-

isms. 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 multi-

disciplinary approach to map genetic variation onto geo-

graphic distributions of Arabidopsis seems a very promising

















334 Biotic interactions

way to assess the ecological impact of individual defense-

related genes, thereby expanding the scale of study from

molecular genetics to ecology.

Expanding scale 4: from laboratory studies toagronomic impactThe 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 resist-

ance 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 com-

monly assumed that induction of priming is mediated by

increased amounts of cellular components with important

roles in defense signaling. Theoretically, this enhance-

ment 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


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 invest-

ments, as their defense arsenal is not activated before

stress exposure. Accordingly, priming for defense protects

plants without harmful trade-offs on commercially import-

ant traits, such as growth and fruit set. They conclude that

successful modern plant protection agents should combine

antimicrobial and priming-inducing activities, thus allow-

ing reduced chemical input into the environment while

maintaining effective and sustainable plant protection.

ConclusionWe 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 expand-

ing 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!

AcknowledgementsResearch activities of JG are supported by grants from the National ScienceFoundation Arabidopsis 2010 program (IOS - 0419648) and the Departmentof Energy Biosciences program (DE-FG02-05ER15670). Research of JT issupported by a personal VENI grant from NWO, the Dutch Organizationfor Scientific Research (no. 863.04.019). We also thank Kees van Loon forhelpful comments on parts of this manuscript.




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Biotic interactions: Recurring themes and expanding scales