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The Role of Dark Septate Endophytic Fungal Isolates in the Accumulation of Cesium by Chinese Cabbage and Tomato Plants under Contaminated Environments

1,*, 2, 2

PLoS ONE

Public Library of Science

4190073

10.1371/journal.pone.0109233

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      Abstract

      Following the 2011 Fukushima Daiichi Nuclear Power Plant accident, the preservation of the food chain from radionuclides contamination has become of crucial importance. The potential of Dark septate endophytic fungi in the management of Cs accumulation in plants under contaminated environments was investigated using Chinese cabbage and tomato plants. Four endophytic fungal isolates of different species, i.e. Pseudosigmoidea ibarakiensis I.4-2-1, Veronaeopsis simplex Y34, Helminthosporium velutinum 41-1, and as yet unidentified taxon 312-6 were tested In Vitro in two levels of Cs (5ppm and 10ppm). On the plant growth, the inoculation of the selected DSEs to both Chinese cabbage and tomato resulted in an increased biomass of up to 82% and 122%, respectively compared to control (non-inoculated) plants. With regards to the Cs accumulation, it varied with the host plant considered. In Chinese cabbage, DSEs inoculation caused higher Cs accumulation in above ground plant parts, whereas in tomato, Cs accumulation decreased significantly with three of the isolates tested, i.e., V. simplex Y34, P. ibarakiensis I.4-2-1, and the as yet unidentified taxon 312-6 suggesting low-risk transfer on the above ground plants parts as a result of high and negative plant reactions rather than high and positive reactions as it is the case with Chinese cabbage. These results suggested that DSEs can be recommended for use with Chinese cabbage to enhance phytoremediation of Cs in surrounding contaminated areas. With tomato, DSEs can be recommended for decreasing the accumulation of Cs in plants under contaminated environments.

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      Most cited references 20

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      Cesium-137 deposition and contamination of Japanese soils due to the Fukushima nuclear accident.

      The largest concern on the cesium-137 ((137)Cs) deposition and its soil contamination due to the emission from the Fukushima Daiichi Nuclear Power Plant (NPP) showed up after a massive quake on March 11, 2011. Cesium-137 ((137)Cs) with a half-life of 30.1 y causes the largest concerns because of its deleterious effect on agriculture and stock farming, and, thus, human life for decades. Removal of (137)Cs contaminated soils or land use limitations in areas where removal is not possible is, therefore, an urgent issue. A challenge lies in the fact that estimates of (137)Cs emissions from the Fukushima NPP are extremely uncertain, therefore, the distribution of (137)Cs in the environment is poorly constrained. Here, we estimate total (137)Cs deposition by integrating daily observations of (137)Cs deposition in each prefecture in Japan with relative deposition distribution patterns from a Lagrangian particle dispersion model, FLEXPART. We show that (137)Cs strongly contaminated the soils in large areas of eastern and northeastern Japan, whereas western Japan was sheltered by mountain ranges. The soils around Fukushima NPP and neighboring prefectures have been extensively contaminated with depositions of more than 100,000 and 10,000 MBq km(-2), respectively. Total (137)Cs depositions over two domains: (i) the Japan Islands and the surrounding ocean (130-150 °E and 30-46 °N) and, (ii) the Japan Islands, were estimated to be approximately 6.7 and 1.3 PBq, [corrected] respectively.We hope our (137)Cs deposition maps will help to coordinate decontamination efforts and plan regulatory measures in Japan.
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        Stress tolerance in plants via habitat-adapted symbiosis.

        We demonstrate that native grass species from coastal and geothermal habitats require symbiotic fungal endophytes for salt and heat tolerance, respectively. Symbiotically conferred stress tolerance is a habitat-specific phenomenon with geothermal endophytes conferring heat but not salt tolerance, and coastal endophytes conferring salt but not heat tolerance. The same fungal species isolated from plants in habitats devoid of salt or heat stress did not confer these stress tolerances. Moreover, fungal endophytes from agricultural crops conferred disease resistance and not salt or heat tolerance. We define habitat-specific, symbiotically-conferred stress tolerance as habitat-adapted symbiosis and hypothesize that it is responsible for the establishment of plants in high-stress habitats. The agricultural, coastal and geothermal plant endophytes also colonized tomato (a model eudicot) and conferred disease, salt and heat tolerance, respectively. In addition, the coastal plant endophyte colonized rice (a model monocot) and conferred salt tolerance. These endophytes have a broad host range encompassing both monocots and eudicots. Interestingly, the endophytes also conferred drought tolerance to plants regardless of the habitat of origin. Abiotic stress tolerance correlated either with a decrease in water consumption or reactive oxygen sensitivity/generation but not to increased osmolyte production. The ability of fungal endophytes to confer stress tolerance to plants may provide a novel strategy for mitigating the impacts of global climate change on agricultural and native plant communities.
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          Ionizing Radiation Changes the Electronic Properties of Melanin and Enhances the Growth of Melanized Fungi

          Background Melanin pigments are ubiquitous in nature. Melanized microorganisms are often the dominating species in certain extreme environments, such as soils contaminated with radionuclides, suggesting that the presence of melanin is beneficial in their life cycle. We hypothesized that ionizing radiation could change the electronic properties of melanin and might enhance the growth of melanized microorganisms. Methodology/Principal Findings Ionizing irradiation changed the electron spin resonance (ESR) signal of melanin, consistent with changes in electronic structure. Irradiated melanin manifested a 4-fold increase in its capacity to reduce NADH relative to non-irradiated melanin. HPLC analysis of melanin from fungi grown on different substrates revealed chemical complexity, dependence of melanin composition on the growth substrate and possible influence of melanin composition on its interaction with ionizing radiation. XTT/MTT assays showed increased metabolic activity of melanized C. neoformans cells relative to non-melanized cells, and exposure to ionizing radiation enhanced the electron-transfer properties of melanin in melanized cells. Melanized Wangiella dermatitidis and Cryptococcus neoformans cells exposed to ionizing radiation approximately 500 times higher than background grew significantly faster as indicated by higher CFUs, more dry weight biomass and 3-fold greater incorporation of 14C-acetate than non-irradiated melanized cells or irradiated albino mutants. In addition, radiation enhanced the growth of melanized Cladosporium sphaerospermum cells under limited nutrients conditions. Conclusions/Significance Exposure of melanin to ionizing radiation, and possibly other forms of electromagnetic radiation, changes its electronic properties. Melanized fungal cells manifested increased growth relative to non-melanized cells after exposure to ionizing radiation, raising intriguing questions about a potential role for melanin in energy capture and utilization.
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            Author and article information

            Affiliations
            [1]Direction de la Protection des Végétaux, Ministère de l’Agriculture et de l’Equipement Rural, Thiaroye, Dakar, Sénégal
            [2]College of Agriculture, Ibaraki University, Ami-machi, Ibaraki, Japan
            NERC Centre for Ecology & Hydrology, United Kingdom
            Author notes

            Competing Interests: The authors have declared that no competing interests exist.

            Conceived and designed the experiments: KN OD. Performed the experiments: KN OD. Analyzed the data: KN OD NS. Contributed reagents/materials/analysis tools: KN OD NS. Wrote the paper: KN OD NS. Performed the XRF analysis and analyzed the data: NS.

            Contributors
            Role: Editor
            Journal
            PLoS One
            PLoS ONE
            plos
            plosone
            PLoS ONE
            Public Library of Science (San Francisco, USA)
            1932-6203
            2014
            8 October 2014
            : 9
            : 10
            Andrew C. Singer (Editor)

            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.

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            Pages: 6
            Funding
            Funding : This work was supported by a Grant-in-Aid for Scientific Research (B) (No. 23380190) from the Japan Society for the Promotion of Science (to K. N.). http://www.jsps.go.jp/english/e-grants/. 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
            Agriculture
            Ecology
            Chemical Ecology
            Custom metadata
            The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.
            ScienceOpen disciplines:

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