Trends in Plant Science
Volume 12, Issue 12, December 2007, Pages 564-569
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Review
Plant interactions with microbes and insects: from molecular mechanisms to ecology

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Plants are members of complex communities and interact both with antagonists and beneficial organisms. An important question in plant defense-signaling research is how plants integrate signals induced by pathogens, beneficial microbes and insects into the most appropriate adaptive response. Molecular and genomic tools are now being used to uncover the complexity of the induced defense signaling networks that have evolved during the arms races between plants and their attackers. Molecular biologists and ecologists are joining forces to place molecular mechanisms of plant defense into an ecological perspective. Here, we review our current understanding of the molecular mechanisms of induced plant defense and their potential ecological relevance in nature.

Section snippets

Plants interact with friends and foes

Plants are abundantly present on Earth and are at the basis of most food webs. Each of the ∼300 000 plant species is attacked by a multitude of other organisms, which includes insects and pathogens. For instance, the number of insect species is estimated to be in the order of six million, half of which are herbivorous [1]. The diversity of pathogenic microbes is less well characterized but their threat to plants is equally renowned [2]. In addition to parasitic interactions, beneficial

Molecular biology meets nature

Studies on the mechanisms of plant defense responses usually consider individual plant–attacker interactions under a limited set of abiotic conditions. Because plant defense mechanisms have evolved during the co-evolutionary arms race between plants and their attackers and come with costs in addition to benefits 1, 10, 12, insights into their significance for plant fitness should ideally come from ecological studies. Recently, a meta-analysis of plant performance during the interaction with

Defense signaling networks

The use of model plant systems, such as Arabidopsis, and various plant genomics approaches has expanded our understanding of the molecular mechanisms by which plants tailor their responses to parasites, herbivores and beneficial organisms. The plant hormones salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) emerged as key players in the regulation of signaling networks involved in these responses 21, 23, 24, 25. Other plant hormones, including abscisic acid [26], brassinosteroids [27]

Fine-tuning of defense

A major focus in plant defense signaling research is to uncover key mechanisms by which plants tailor their responses to attackers and mutualists, and to investigate how plants cope with simultaneous interactions with multiple aggressors. The regulatory potential of the so-called ‘signal signature’ has an important role in the fine-tuning of the plant's defense response [35]. In Arabidopsis, the production of the defense signals SA, JA and ET has been shown to vary depending on the type of

Molecular players in pathway crosstalk

There is ample evidence that SA, JA and ET pathways interact, either positively or negatively 37, 38, 39. Global expression profiling of pathogen-infected Arabidopsis wild type and signaling mutants highlighted substantial crosstalk between the SA, JA and ET signaling pathways [40]. In some cases, the simultaneous activation of multiple defense pathways results in enhanced levels of induced resistance, whereas in other cases antagonistic effects on pathogen and insect resistance have been

Decoy of plant defenses

Crosstalk between defense pathways is thought to provide the plant with a powerful regulatory potential, which helps it to prioritize and ‘decide’ which defensive strategy to follow, depending on the type of attacker. Yet, it seems that attackers and beneficial organisms have also evolved to manipulate plants for their own benefit by shutting down induced defenses by modulating the signaling network 3, 46, 47. An example is the response of Arabidopsis to silverleaf whitefly (Bemisia tabaci)

Priming for enhanced defense

Differential signal signatures, pathway crosstalk and attacker-mediated suppression of host defense signaling are major molecular mechanisms by which the defense response of the plant is shaped. Priming for enhanced defense adds another layer of complexity to the way by which plants can adapt to their biotic environment. The primed state can be induced biologically by beneficial rhizobacteria [14], mycorrhizal fungi [7], pathogens [54] and insect herbivores 34, 55, but also chemically, for

Molecular ecology: beyond Arabidopsis

Ecologists have provided ample data on plant–microbe and plant–insect interactions. For instance, mycorrhizae have been shown to affect interactions between plants and pollinators, herbivorous insects and their parasitic wasps 66, 67, 68. Conversely, herbivory can influence mycorrhizal colonization of plants. However, in most cases, the underlying mechanisms, in terms of signal transduction and gene expression, have yet to be investigated. Research on Arabidopsis has contributed to our

Concluding remarks and future perspectives

The reductionist approach taken in plant defense research has resulted in profound insight into the complexity of plant defense responses. The wealth of Arabidopsis mutants that are available has resulted in important progress in our understanding of how plants interact with individual microbe or arthropod species. This knowledge is now being further developed to address interactions between Arabidopsis and two or more species, including pathogenic and beneficial microbes and herbivorous and

Acknowledgements

We apologize to all our colleagues whose work could not be reviewed here because of space limitations. Our laboratories have been financially supported (grants 811.36.004, 865.03.002 and 865.04.002) by the Earth and Life Sciences Foundation (ALW), which is subsidized by the Netherlands Organization for Scientific Research (NWO).

References (82)

  • R.K. Cameron

    Accumulation of salicylic acid and PR gene transcripts in relation to the systemic acquired resistance (SAR) response by Pseudomonas syringae pv. tomato in Arabidopsis

    Physiol. Mol. Plant Pathol.

    (1999)
  • U. Conrath

    Priming in plant-pathogen interactions

    Trends Plant Sci.

    (2002)
  • M.E. Schranz

    Comparative genomics in the Brassicaceae: a family-wide perspective

    Curr. Opin. Plant Biol.

    (2007)
  • M.J. Harrison

    Signaling in the arbuscular mycorrhizal symbiosis

    Annu. Rev. Microbiol.

    (2005)
  • L.C. Van Loon

    Systemic resistance induced by rhizosphere bacteria

    Annu. Rev. Phytopathol.

    (1998)
  • M.J. Pozo

    Jasmonates – signals in plant–microbe interactions

    J. Plant Growth Regul.

    (2004)
  • D. Kessler et al.

    Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata

    Plant J.

    (2007)
  • A. Kessler et al.

    Plant responses to insect herbivory: The emerging molecular analysis

    Annu. Rev. Plant Biol.

    (2002)
  • J.D.G. Jones et al.

    The plant immune system

    Nature

    (2006)
  • M. De Vos

    Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack

    Mol. Plant–Microbe Interact.

    (2005)
  • B.W. Verhagen

    The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis

    Mol. Plant–Microbe Interact.

    (2004)
  • L.A. Kempema

    Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids

    Plant Physiol.

    (2007)
  • P. Reymond

    A conserved transcriptional pattern in response to a specialist and a generalist herbivore

    Plant Cell

    (2004)
  • L. Sanchez

    Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula

    Plant Physiol.

    (2005)
  • W.F. Morris

    Direct and interactive effects of enemies and mutualists on plant performance: A meta-analysis

    Ecology

    (2007)
  • E.B. Holub

    The Arms race is ancient history in Arabidopsis, the wildflower

    Nat. Rev. Genet.

    (2001)
  • R.M.P. Van Poecke et al.

    Indirect defence of plants against herbivores: using Arabidopsis thaliana as a model plant

    Plant Biol.

    (2004)
  • A. Kessler

    Silencing the jasmonate cascade: induced plant defenses and insect populations

    Science

    (2004)
  • W.E. Durrant et al.

    Systemic acquired resistance

    Annu. Rev. Phytopathol.

    (2004)
  • C.C. Von Dahl et al.

    Deciphering the role of ethylene in plant–herbivore interactions

    J. Plant Growth Regul.

    (2007)
  • H. Nakashita

    Brassinosteroid functions in a broad range of disease resistance in tobacco and rice

    Plant J.

    (2003)
  • L. Navarro

    A plant miRNA contributes to antibacterial resistance by repressing auxin signaling

    Science

    (2006)
  • J.S. Thaler

    The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles

    Plant Physiol.

    (2004)
  • J. Glazebrook

    Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens

    Annu. Rev. Phytopathol.

    (2005)
  • B. Hause et al.

    Molecular and cell biology of arbuscular mycorrhizal symbiosis

    Planta

    (2005)
  • J. Ton

    Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis

    Mol. Plant–Microbe Interact.

    (2002)
  • M. De Vos

    Herbivore-induced resistance against microbial pathogens in Arabidopsis

    Plant Physiol.

    (2006)
  • L.A.J. Mur

    The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death

    Plant Physiol.

    (2006)
  • G.J.M. Beckers et al.

    Fine-tuning plant defence signalling: salicylate versus jasmonate

    Plant Biol.

    (2006)
  • Cited by (0)

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