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      An Invasive Plant Promotes Its Arbuscular Mycorrhizal Symbioses and Competitiveness through Its Secondary Metabolites: Indirect Evidence from Activated Carbon

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          Abstract

          Secondary metabolites released by invasive plants can increase their competitive ability by affecting native plants, herbivores, and pathogens at the invaded land. Whether these secondary metabolites affect the invasive plant itself, directly or indirectly through microorganisms, however, has not been well documented. Here we tested whether activated carbon (AC), a well-known absorbent for secondary metabolites, affect arbuscular mycorrhizal (AM) symbioses and competitive ability in an invasive plant. We conducted three experiments (experiments 1–3) with the invasive forb Solidago canadensis and the native Kummerowia striata. Experiment 1 determined whether AC altered soil properties, levels of the main secondary metabolites in the soil, plant growth, and AMF communities associated with S. canadensis and K. striata. Experiment 2 determined whether AC affected colonization of S. canadensis by five AMF, which were added to sterilized soil. Experiment 3 determined the competitive ability of S. canadensis in the presence and absence of AMF and AC. In experiment 1, AC greatly decreased the concentrations of the main secondary metabolites in soil, and the changes in concentrations were closely related with the changes of AMF in S. canadensis roots. In experiment 2, AC inhibited the AMF Glomus versiforme and G. geosporum but promoted G. mosseae and G. diaphanum in the soil and also in S. canadensis roots. In experiment 3, AC reduced S. canadensis competitive ability in the presence but not in the absence of AMF. Our results provided indirect evidence that the secondary metabolites (which can be absorbed by AC) of the invasive plant S. canadensis may promote S. canadensis competitiveness by enhancing its own AMF symbionts.

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          Most cited references14

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          Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.

          Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
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            The role of polyphenols in terrestrial ecosystem nutrient cycling.

            Interspecific variation in polyphenol production by plants has been interpreted in terms of defense against herbivores. Several recent lines of evidence suggest that polyphenols also influence the pools and fluxes of inorganic and organic soil nutrients. Such effects could have far-ranging consequences for nutrient competition among and between plants and microbes, and for ecosystem nutrient cycling and retention. The significance of polyphenols for nutrient cycling and plant productivity is still uncertain, but it could provide an alternative or complementary explanation for the variability in polyphenol production by plants.
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              Invasive plants versus their new and old neighbors: a mechanism for exotic invasion.

              Invading exotic plants are thought to succeed primarily because they have escaped their natural enemies, not because of novel interactions with their new neighbors. However, we find that Centaurea diffusa, a noxious weed in North America, has much stronger negative effects on grass species from North America than on closely related grass species from communities to which Centaurea is native. Centaurea's advantage against North American species appears to be due to differences in the effects of its root exudates and how these root exudates affect competition for resources. Our results may help to explain why some exotic species so successfully invade natural plant communities.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                9 May 2014
                : 9
                : 5
                : e97163
                Affiliations
                [1 ]College of Life Sciences, Zhejiang University, Hangzhou, China
                [2 ]Department of Plant Pathology, North Carolina State University, Raleigh, North Carolina, United States of America
                [3 ]Singapore University of Technology and Design, Singapore, Singapore
                University of Tartu, Estonia
                Author notes

                Competing Interests: The authors confirm that co-author Dr. Shuijin Hu currently serves as an editor of PLOS ONE. This does not alter the authors’ adherence to PLOS ONE Editorial policies and criteria.

                Conceived and designed the experiments: XC SH. Performed the experiments: YY JT DL. Analyzed the data: YY JWHY. Contributed reagents/materials/analysis tools: YY JT DL. Wrote the paper: YY XC SH.

                Article
                PONE-D-13-54270
                10.1371/journal.pone.0097163
                4016281
                24817325
                26639d36-4cb4-4944-9608-55ec36bd0970
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 4 January 2014
                : 15 April 2014
                Page count
                Pages: 9
                Funding
                This study was supported by the Zhejiang Provincial Natural Science Foundation of China (No. Z5090089) and the Research Fund for the Doctoral Program of Higher Education of China (RFDP, No. 20110101110077). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Ecology and Environmental Sciences
                Soil Science
                Soil Ecology

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                Uncategorized

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