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      Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities

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          Abstract

          Trees can communicate with each other through networks in soil. Much like social networks or neural networks, the fungal mycelia of mycorrhizas allow signals to be sent between trees in a forest. These mycorrhizal networks are effectively an information highway, with recent studies demonstrating the exchange of nutritional resources, defence signals and allelochemicals. Sensing and responding to networked signals elicits complex behavioural responses in plants. This ability to communicate ('tree talk') is a foundational process in forest ecosystems.

          Abstract

          Adaptive behaviour of plants, including rapid changes in physiology, gene regulation and defence response, can be altered when linked to neighbouring plants by a mycorrhizal network (MN). Mechanisms underlying the behavioural changes include mycorrhizal fungal colonization by the MN or interplant communication via transfer of nutrients, defence signals or allelochemicals. We focus this review on our new findings in ectomycorrhizal ecosystems, and also review recent advances in arbuscular mycorrhizal systems. We have found that the behavioural changes in ectomycorrhizal plants depend on environmental cues, the identity of the plant neighbour and the characteristics of the MN. The hierarchical integration of this phenomenon with other biological networks at broader scales in forest ecosystems, and the consequences we have observed when it is interrupted, indicate that underground ‘tree talk’ is a foundational process in the complex adaptive nature of forest ecosystems.

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          Most cited references37

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          Diversity and productivity in a long-term grassland experiment.

          Plant diversity and niche complementarity had progressively stronger effects on ecosystem functioning during a 7-year experiment, with 16-species plots attaining 2.7 times greater biomass than monocultures. Diversity effects were neither transients nor explained solely by a few productive or unviable species. Rather, many higher-diversity plots outperformed the best monoculture. These results help resolve debate over biodiversity and ecosystem functioning, show effects at higher than expected diversity levels, and demonstrate, for these ecosystems, that even the best-chosen monocultures cannot achieve greater productivity or carbon stores than higher-diversity sites.
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            Explaining evolution of plant communication by airborne signals.

            In spite of initial doubts about the reality of 'talking trees', plant resistance expression mediated by volatile compounds that come from neighboring plants is now well described. Airborne signals usually improve the resistance of the receiver, but without obvious benefits for the emitter, thus making the evolutionary explanation of this phenomenon problematic. Here, we discuss four possible non-exclusive explanations involving the role of volatiles: in direct defense, as within-plant signals, as traits that synergistically interact with other defenses, and as cues among kin. Unfortunately, there is a lack of knowledge on the fitness consequences of plant communication for both emitter and receiver. This information is crucial to understanding the ecology and evolution of plant communication via airborne cues.
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              The molecular revolution in ectomycorrhizal ecology: peeking into the black-box.

              Molecular tools have now been applied for the past 5 years to dissect ectomycorrhizal (EM) community structure, and they have propelled a resurgence in interest in the field. Results from these studies have revealed that: (i) EM communities are impressively diverse and are patchily distributed at a fine scale below ground; (ii) there is a poor correspondence between fungi that appear dominant as sporocarps vs. those that appear dominant on roots; (iii) members of Russulaceae, Thelephoraceae, and/or non-thelephoroid resupinates are among the most abundant EM taxa in ecosystems sampled to date; (iv) dissimilar plants are associated with many of the same EM species when their roots intermingle--this occurs on a small enough spatial scale that fungal individuals are likely to be shared by dissimilar plants; and (v) mycoheterotrophic plants have highly specific fungal associations. Although, these results have been impressive, they have been tempered by sampling difficulties and limited by the taxonomic resolution of restriction fragment length polymorphism methods. Minor modifications of the sampling schemes, and more use of direct sequencing, has the potential to solve these problems. Use of additional methods, such as in situ hybridization to ribosomal RNA or hybridization coupled to microarrays, are necessary to open up the analysis of the mycelial component of community structure.
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                Author and article information

                Journal
                AoB Plants
                AoB Plants
                aobpla
                aobpla
                AoB Plants
                Oxford University Press
                2041-2851
                2015
                15 May 2015
                : 7
                : plv050
                Affiliations
                Department of Forest and Conservation Sciences, University of British Columbia , Vancouver, BC, Canada, V6T 1Z4
                Author notes
                [* ]Corresponding author's e-mail address: suzanne.simard@ 123456ubc.ca

                Associate Editor: James F. Cahill

                Article
                plv050
                10.1093/aobpla/plv050
                4497361
                25979966
                db493b2c-b009-4b80-bfc3-48c92b50ab8d
                Published by Oxford University Press on behalf of the Annals of Botany Company.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 4 December 2014
                : 26 March 2015
                Page count
                Pages: 13
                Funding
                Funded by: NSERC CGS-D
                Categories
                1026
                1009
                1024
                1049
                1057
                Invited Reviews
                SPECIAL ISSUE: Using Ideas from Behavioural Ecology to Understand Plants

                Plant science & Botany
                complex adaptive systems,ectomycorrhiza,forests,mycorrhizal networks,plant behaviour,plant communication

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