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      Phosphorus and Nitrogen Regulate Arbuscular Mycorrhizal Symbiosis in Petunia hybrida

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          Abstract

          Phosphorus and nitrogen are essential nutrient elements that are needed by plants in large amounts. The arbuscular mycorrhizal symbiosis between plants and soil fungi improves phosphorus and nitrogen acquisition under limiting conditions. On the other hand, these nutrients influence root colonization by mycorrhizal fungi and symbiotic functioning. This represents a feedback mechanism that allows plants to control the fungal symbiont depending on nutrient requirements and supply. Elevated phosphorus supply has previously been shown to exert strong inhibition of arbuscular mycorrhizal development. Here, we address to what extent inhibition by phosphorus is influenced by other nutritional pathways in the interaction between Petunia hybrida and R. irregularis. We show that phosphorus and nitrogen are the major nutritional determinants of the interaction. Interestingly, the symbiosis-promoting effect of nitrogen starvation dominantly overruled the suppressive effect of high phosphorus nutrition onto arbuscular mycorrhiza, suggesting that plants promote the symbiosis as long as they are limited by one of the two major nutrients. Our results also show that in a given pair of symbiotic partners ( Petunia hybrida and R. irregularis), the entire range from mutually symbiotic to parasitic can be observed depending on the nutritional conditions. Taken together, these results reveal complex nutritional feedback mechanisms in the control of root colonization by arbuscular mycorrhizal fungi.

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          Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems.

          The cycles of the key nutrient elements nitrogen (N) and phosphorus (P) have been massively altered by anthropogenic activities. Thus, it is essential to understand how photosynthetic production across diverse ecosystems is, or is not, limited by N and P. Via a large-scale meta-analysis of experimental enrichments, we show that P limitation is equally strong across these major habitats and that N and P limitation are equivalent within both terrestrial and freshwater systems. Furthermore, simultaneous N and P enrichment produces strongly positive synergistic responses in all three environments. Thus, contrary to some prevailing paradigms, freshwater, marine and terrestrial ecosystems are surprisingly similar in terms of N and P limitation.
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            How do plants respond to nutrient shortage by biomass allocation?

            Plants constantly sense the changes in their environment; when mineral elements are scarce, they often allocate a greater proportion of their biomass to the root system. This acclimatory response is a consequence of metabolic changes in the shoot and an adjustment of carbohydrate transport to the root. It has long been known that deficiencies of essential macronutrients (nitrogen, phosphorus, potassium and magnesium) result in an accumulation of carbohydrates in leaves and roots, and modify the shoot-to-root biomass ratio. Here, we present an update on the effects of mineral deficiencies on the expression of genes involved in primary metabolism in the shoot, the evidence for increased carbohydrate concentrations and altered biomass allocation between shoot and root, and the consequences of these changes on the growth and morphology of the plant root system.
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              Nitrogen transfer in the arbuscular mycorrhizal symbiosis.

              Most land plants are symbiotic with arbuscular mycorrhizal fungi (AMF), which take up mineral nutrients from the soil and exchange them with plants for photosynthetically fixed carbon. This exchange is a significant factor in global nutrient cycles as well as in the ecology, evolution and physiology of plants. Despite its importance as a nutrient, very little is known about how AMF take up nitrogen and transfer it to their host plants. Here we report the results of stable isotope labelling experiments showing that inorganic nitrogen taken up by the fungus outside the roots is incorporated into amino acids, translocated from the extraradical to the intraradical mycelium as arginine, but transferred to the plant without carbon. Consistent with this mechanism, the genes of primary nitrogen assimilation are preferentially expressed in the extraradical tissues, whereas genes associated with arginine breakdown are more highly expressed in the intraradical mycelium. Strong changes in the expression of these genes in response to nitrogen availability and form also support the operation of this novel metabolic pathway in the arbuscular mycorrhizal symbiosis.
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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
                7 March 2014
                : 9
                : 3
                : e90841
                Affiliations
                [1 ]Dept. of Biology, University of Fribourg, Fribourg, Switzerland
                [2 ]Institute of Plant Science, University of Bern, Bern, Switzerland
                Radboud University Medical Centre, NCMLS, Netherlands
                Author notes

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

                Conceived and designed the experiments: DR EN FBS UF. Performed the experiments: DR EN FBS UF. Analyzed the data: DR EN FBS UF. Contributed reagents/materials/analysis tools: DR UF. Wrote the paper: DR EN FBS UF.

                [¤]

                Current address: Plant Pathology Dept., University of Minnesota, St. Paul, Minnesota, United States of America

                Article
                PONE-D-13-40397
                10.1371/journal.pone.0090841
                3946601
                24608923
                9fd97e71-b13c-4f65-b6da-2b970441daef
                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
                : 1 October 2013
                : 6 February 2014
                Page count
                Pages: 14
                Funding
                This work was supported by a grant from the National Centre of Competence in Research (NCCR) “Plant Survival”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Agriculture
                Sustainable Agriculture
                Biology
                Microbiology
                Mycology
                Fungi
                Plant Science
                Botany
                Mycology
                Fungi
                Plants
                Flowering Plants
                Vascular Plants
                Plant Microbiology
                Plant Physiology

                Uncategorized
                Uncategorized

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