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      Nitric oxide in fungi: is there NO light at the end of the tunnel?

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          Abstract

          Nitric oxide (NO) is a remarkable gaseous molecule with multiple and important roles in different organisms, including fungi. However, the study of the biology of NO in fungi has been hindered by the lack of a complete knowledge on the different metabolic routes that allow a proper NO balance, and the regulation of these routes. Fungi have developed NO detoxification mechanisms to combat nitrosative stress, which have been mainly characterized by their connection to pathogenesis or nitrogen metabolism. However, the progress on the studies of NO anabolic routes in fungi has been hampered by efforts to disrupt candidate genes that gave no conclusive data until recently. This review summarizes the different roles of NO in fungal biology and pathogenesis, with an emphasis on the alternatives to explain fungal NO production and the recent findings on the involvement of nitrate reductase in the synthesis of NO and its regulation during fungal development.

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          Most cited references51

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          Nitric oxide functions as a signal in plant disease resistance.

          Recognition of an avirulent pathogen triggers the rapid production of the reactive oxygen intermediates superoxide (O2-) and hydrogen peroxide (H2O2). This oxidative burst drives crosslinking of the cell wall, induces several plant genes involved in cellular protection and defence, and is necessary for the initiation of host cell death in the hypersensitive disease-resistance response. However, this burst is not enough to support a strong disease-resistance response. Here we show that nitric oxide, which acts as a signal in the immune, nervous and vascular systems, potentiates the induction of hypersensitive cell death in soybean cells by reactive oxygen intermediates and functions independently of such intermediates to induce genes for the synthesis of protective natural products. Moreover, inhibitors of nitric oxide synthesis compromise the hypersensitive disease-resistance response of Arabidopsis leaves to Pseudomonas syringae, promoting disease and bacterial growth. We conclude that nitric oxide plays a key role in disease resistance in plants.
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            Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates.

            Phagocytosis and mechanisms of killing of Aspergillus fumigatus conidia by murine alveolar macrophages (AM), which are the main phagocytic cells of the innate immunity of the lung, were investigated. Engulfment of conidia by murine AM lasts 2 h. Killing of A. fumigatus conidia by AM begins after 6 h of phagocytosis. Swelling of the conidia inside the AM is a prerequisite for killing of conidia. The contributions of NADPH oxidase and inducible nitric oxide synthase to the conidicidal activity of AM were studied using AM from OF1, wild-type and congenic p47phox(-/-) 129Sv, and wild-type and congenic iNOS(-/-) C57BL/6 mice. AM from p47phox(-/-) mice were unable to kill A. fumigatus conidia. Inhibitors of NADPH oxidase that decreased the production of reactive oxidant intermediates inhibited the killing of A. fumigatus without altering the phagocytosis rate. In contrast to NADPH oxidase, nitric oxide synthase does not play a role in killing of conidia. Corticosteroids did not alter the internalization of conidia by AM but did inhibit the production of reactive oxidant intermediates and the killing of A. fumigatus conidia by AM. Impairment of production of reactive oxidant intermediates by corticosteroids is responsible for the development of invasive aspergillosis in immunosuppressed mice.
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              Nitrogen regulation in Saccharomyces cerevisiae.

              Yeast cells can respond to growth on relatively poor nitrogen sources by increasing expression of the enzymes for the synthesis of glutamate and glutamine and by increasing the activities of permeases responsible for the uptake of amino acids for use as a source of nitrogen. These general responses to the quality of nitrogen source in the growth medium are collectively termed nitrogen regulation. In this review, we discuss the historical foundations of the study of nitrogen regulation as well as the current understanding of the regulatory networks that underlie nitrogen regulation. One focus of the review is the array of four GATA type transcription factors which are responsible for the regulation the expression of nitrogen-regulated genes. They are the activators Gln3p and Nil1p and their antagonists Nil2p and Dal80p. Our discussion includes consideration of the DNA elements which are the targets of the transcription factors and of the regulated translocation of Gln3p and Nil1p from the cytoplasm to the nucleus. A second focus of the review is the nitrogen regulation of the general amino acid permease, Gap1p, and the proline permease, Put4p, by ubiquitin mediated intracellular protein sorting in the secretory and endosomal pathways.
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                Author and article information

                Contributors
                davidc@us.es
                Journal
                Curr Genet
                Curr. Genet
                Current Genetics
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0172-8083
                1432-0983
                17 February 2016
                17 February 2016
                2016
                : 62
                : 513-518
                Affiliations
                [ ]Department of Genetics, Faculty of Biology, University of Sevilla, Seville, Spain
                [ ]Division of Microbial Genetics and Pathogen Interactions, Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences (BOKU), Bioresources Campus Tulln, Vienna, Austria
                [ ]Department of Food Science, Institute of Agrochemistry and Food Technology (IATA), CSIC, Valencia, Spain
                Author notes

                Communicated by M. Kupiec.

                Author information
                http://orcid.org/0000-0002-7293-7332
                Article
                574
                10.1007/s00294-016-0574-6
                4929157
                26886232
                dfb7030c-fea6-486f-8540-b4e63923eaf6
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 28 January 2016
                : 31 January 2016
                : 2 February 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002428, Austrian Science Fund;
                Award ID: M01693-B22
                Funded by: n(f + b) Lower Austria Science Fund
                Award ID: LS12-009
                Categories
                Review
                Custom metadata
                © Springer-Verlag Berlin Heidelberg 2016

                Genetics
                nitric oxide,aspergillus,fungal pathogens,nitrate reductase,flavohemoglobin,development
                Genetics
                nitric oxide, aspergillus, fungal pathogens, nitrate reductase, flavohemoglobin, development

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