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      The caterpillar fungus, Ophiocordyceps sinensis, genome provides insights into highland adaptation of fungal pathogenicity

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          Abstract

          To understand the potential genetic basis of highland adaptation of fungal pathogenicity, we present here the ~116 Mb de novo assembled high-quality genome of Ophiocordyceps sinensis endemic to the Qinghai-Tibetan Plateau. Compared with other plain-dwelling fungi, we find about 3.4-fold inflation of the O. sinensis genome due to a rapid amplification of long terminal repeat retrotransposons that occurred ~38 million years ago in concert with the uplift of the plateau. We also observe massive removal of thousands of genes related to the transport process and energy metabolism. O. sinensis displays considerable lineage-specific expansion of gene families functionally enriched in the adaptability of low-temperature of cold tolerance, fungal pathogenicity and specialized host infection. We detect signals of positive selection for genes involved in peroxidase and hypoxia to enable its highland adaptation. Resequencing and analyzing 31 whole genomes of O. sinensis, representing nearly all of its geographic range, exhibits latitude-based population divergence and nature selection for population inhabitation towards higher altitudes on the Qinghai-Tibetan Plateau.

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          Life with 6000 Genes

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            Action on the Surface: Entomopathogenic Fungi versus the Insect Cuticle

            Infections mediated by broad host range entomopathogenic fungi represent seminal observations that led to one of the first germ theories of disease and are a classic example of a co-evolutionary arms race between a pathogen and target hosts. These fungi are able to parasitize susceptible hosts via direct penetration of the cuticle with the initial and potentially determining interaction occurring between the fungal spore and the insect epicuticle. Entomogenous fungi have evolved mechanisms for adhesion and recognition of host surface cues that help direct an adaptive response that includes the production of: (a) hydrolytic, assimilatory, and/or detoxifying enzymes including lipase/esterases, catalases, cytochrome P450s, proteases, and chitinases; (b) specialized infectious structures, e.g., appressoria or penetrant tubes; and (c) secondary and other metabolites that facilitate infection. Aside from immune responses, insects have evolved a number of mechanisms to keep pathogens at bay that include: (a) the production of (epi) cuticular antimicrobial lipids, proteins, and metabolites; (b) shedding of the cuticle during development; and (c) behavioral-environmental adaptations such as induced fever, burrowing, and grooming, as well as potentially enlisting the help of other microbes, all intended to stop the pathogen before it can breach the cuticle. Virulence and host-defense can be considered to be under constant reciprocal selective pressure, and the action on the surface likely contributes to phenomena such as strain variation, host range, and the increased virulence often noted once a (low) virulent strain is “passaged” through an insect host. Since the cuticle represents the first point of contact and barrier between the fungus and the insect, the “action on the surface” may represent the defining interactions that ultimately can lead either to successful mycosis by the pathogen or successful defense by the host. Knowledge concerning the molecular mechanisms underlying this interaction can shed light on the ecology and evolution of virulence and can be used for rational design strategies at increasing the effectiveness of entomopathogenic fungi for pest control in field applications.
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              Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana

              The ascomycete fungus Beauveria bassiana is a pathogen of hundreds of insect species and is commercially produced as an environmentally friendly mycoinsecticide. We sequenced the genome of B. bassiana and a phylogenomic analysis confirmed that ascomycete entomopathogenicity is polyphyletic, but also revealed convergent evolution to insect pathogenicity. We also found many species-specific virulence genes and gene family expansions and contractions that correlate with host ranges and pathogenic strategies. These include B. bassiana having many more bacterial-like toxins (suggesting an unsuspected potential for oral toxicity) and effector-type proteins. The genome also revealed that B. bassiana resembles the closely related Cordyceps militaris in being heterothallic, although its sexual stage is rarely observed. A high throughput RNA-seq transcriptomic analysis revealed that B. bassiana could sense and adapt to different environmental niches by activating well-defined gene sets. The information from this study will facilitate further development of B. bassiana as a cost-effective mycoinsecticide.
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                Author and article information

                Contributors
                Lgaogenomics@163.com
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                11 May 2017
                11 May 2017
                2017
                : 7
                : 1806
                Affiliations
                [1 ]ISNI 0000 0004 1764 155X, GRID grid.458460.b, Plant Germplasm and Genomics Center, Germplasm Bank of Wild Species in Southwestern China, , Kunming Institute of Botany, the Chinese Academy of Sciences, ; Kunming, 650204 China
                [2 ]ISNI 0000 0000 9546 5767, GRID grid.20561.30, Institution of Genomics and Bioinformatics, , South China Agricultural University, ; Guangzhou, 510642 China
                [3 ]ISNI 0000 0004 1797 8419, GRID grid.410726.6, , University of the Chinese Academy of Sciences, ; Beijing, 100039 China
                [4 ]ISNI 0000000119573309, GRID grid.9227.e, Xishuangbanna Tropical Botanical Garden, , The Chinese Academy of Sciences, ; Menglun, 666303 China
                [5 ]ISNI 0000 0001 0561 6611, GRID grid.135769.f, Agrobiological Gene Research Center, , Guangdong Academy of Agricultural Sciences, ; Guangzhou, 510640 China
                [6 ]Marcogene Inc., Seoul, 08511 South Korea
                [7 ]ISNI 0000000119573309, GRID grid.9227.e, Center for Computational Genomics, Beijing Institute of Genomics, , The Chinese Academy of Sciences, ; Beijing, 100101 China
                [8 ]ISNI 0000000122986657, GRID grid.34477.33, Department of Genome Sciences, , University of Washington School of Medicine, ; Seattle, WA 98195 USA
                [9 ]ISNI 0000000122986657, GRID grid.34477.33, Howard Hughes Medical Institute, , University of Washington, ; Seattle, WA 98195 USA
                Article
                1869
                10.1038/s41598-017-01869-z
                5432009
                28496210
                5f0ad6f8-8a66-417a-a36f-fcc2f55a21f1
                © The Author(s) 2017

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 2 December 2016
                : 31 March 2017
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