Unraveling mycorrhiza-induced resistance

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Arbuscular mycorrhizal symbioses have a significant impact on plant interactions with other organisms. Increased resistance to soil-borne pathogens has been widely described in mycorrhizal plants. By contrast, effects on shoot diseases largely rely on the lifestyle and challenge strategy of the attacker. Among the potential mechanisms involved in the resistance of mycorrhizal systems, the induction of plant defenses is the most controversial. During mycorrhiza formation, modulation of plant defense responses occurs, potentially through cross-talk between salicylic acid and jasmonate dependent signaling pathways. This modulation may impact plant responses to potential enemies by priming the tissues for a more efficient activation of defense mechanisms.

Introduction

For more than 400 million years plants have established a mutualistic association known as arbuscular mycorrhizas (AM) with certain soil fungi. Nowadays, about 80% of all terrestrial plants, including most agricultural, horticultural, and hardwood crop species are able to establish this mutualistic association. Arbuscular mycorrhiza forming fungi (AMF) are obligate biotrophs because they rely on their host plant to proliferate and survive. The establishment of the symbiosis requires a co-ordinated developmental program that has been the focus of several recent reviews [1, 2, 3]. The benefits of the AM symbiosis on plant fitness are largely known, including a better mineral nutrition and increased ability to overcome biotic and abiotic stresses.

A growing body of evidence supports the overlap in plant responses to different stresses, regulated through a sophisticated signaling network [4]. Synergism and antagonism between signaling pathways provide a cost-efficient regulatory potential for fine-tuning the appropriate defense mechanism. This review summarizes the data on AM-induced protection against biotic stress and the possible mechanisms involved, with special emphasis on the role of plant defense responses. We try to integrate current models on regulation of plant responses during mutualistic and pathogenic interactions to explain the spectrum of effectiveness of mycorrhiza-induced resistance (MIR).

Section snippets

Impact of mycorrhizal symbiosis on plant resistance to biotic stress

Alleviation of damage caused by soil-borne pathogens has been widely reported in mycorrhizal plants. Most studies on protection by AM deal with the reduction of incidence and/or severity of soil-borne diseases mainly root rot or wilting caused by fungi such as Rhizoctonia, Fusarium, or Verticillium, and root rot caused by oomycetes including Phytophthora, Pythium, and Aphanomyces. These studies have been compiled in a comprehensive review by Whipps [5]. A reduction in the deleterious effects by

Mechanisms of mycorrhiza-induced resistance

Different mechanisms have been shown to play a role in plant protection by AMF, namely, improved plant nutrition, damage compensation, competition for colonization sites or photosynthates, changes in the root system, changes in rhizosphere microbial populations, and activation of plant defense mechanisms. Several mechanisms can be operative simultaneously, with contributions depending on environmental conditions, timing of the interaction, and partners involved [5, 8]. The requirement of a

Mycorrhiza-induced priming for defense

Defense responses are vital but costly for the plant. A rapid and strong activation of defense mechanisms is crucial for success in controlling attackers. Accordingly, preconditioning of plant tissues for a more effective activation of defenses is a plausible strategy [24••]. This phenomenon, known as priming, is the focus of the review by Uwe Conrath in this issue.

Priming seems to be the main mechanism operating in MIR. The lack of systemic activation of cellular or biochemical defense

Signaling pathways involved

The establishment of mutualistic associations involves mutual recognition and a high degree of co-ordination based on a continuous molecular dialogue between both symbionts [1, 2]. Advances in our knowledge about plant–microbe signaling are unraveling mechanisms regulating biotic interactions. For example, the identification of strigolactones, known to stimulate seed germination of parasitic plants, as host recognition compounds for AMF [28] has uncovered a possible mechanism mediating the

Conclusions

Aboveground and belowground communities can be powerful mutual drivers, with both positive and negative feedbacks affecting biodiversity and functioning of the ecosystem [50, 51]. Mycorrhizal symbioses have an important impact on plant interactions with pathogens and insects. The association leads generally to a reduction of damage caused by soil-borne pathogens, but effects on shoot-targeting organisms depend greatly on the attacker lifestyle. MIR in aboveground tissues seems effective against

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We apologize to our colleagues whose work has not been included because of space limitations. We thank J. Perez-Tienda ([email protected]) for drawing the figures and V. Gianinazzi-Pearson, A. Gange, and J.M. García-Garrido for comments on the manuscript. Our research on MIR was financed by grant ERG 014770 from the Marie Curie Program (EU) and grant AGL2006-08029 from the Spanish Ministry of Science and Technology. MJP is supported by a “Ramón y Cajal” research contract (RYC2003-5375).

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