Trends in Plant Science
ReviewPlant interactions with microbes and insects: from molecular mechanisms to ecology
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).
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