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The Entomopathogenic Fungal Endophytes Purpureocillium lilacinum (Formerly Paecilomyces lilacinus) and Beauveria bassiana Negatively Affect Cotton Aphid Reproduction under Both Greenhouse and Field Conditions

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      The effects of two entomopathogenic fungal endophytes, Beauveria bassiana and Purpureocillium lilacinum (formerly Paecilomyces lilacinus), were assessed on the reproduction of cotton aphid, Aphis gossypii Glover (Homoptera:Aphididae), through in planta feeding trials. In replicate greenhouse and field trials, cotton plants ( Gossypium hirsutum) were inoculated as seed treatments with two concentrations of B. bassiana or P. lilacinum conidia. Positive colonization of cotton by the endophytes was confirmed through potato dextrose agar (PDA) media plating and PCR analysis. Inoculation and colonization of cotton by either B. bassiana or P. lilacinum negatively affected aphid reproduction over periods of seven and 14 days in a series of greenhouse trials. Field trials were conducted in the summers of 2012 and 2013 in which cotton plants inoculated as seed treatments with B. bassiana and P. lilacinum were exposed to cotton aphids for 14 days. There was a significant overall effect of endophyte treatment on the number of cotton aphids per plant. Plants inoculated with B. bassiana had significantly lower numbers of aphids across both years. The number of aphids on plants inoculated with P. lilacinum exhibited a similar, but non-significant, reduction in numbers relative to control plants. We also tested the pathogenicity of both P. lilacinum and B. bassiana strains used in the experiments against cotton aphids in a survival experiment where 60% and 57% of treated aphids, respectively, died from infection over seven days versus 10% mortality among control insects. Our results demonstrate (i) the successful establishment of P. lilacinum and B. bassiana as endophytes in cotton via seed inoculation, (ii) subsequent negative effects of the presence of both target endophytes on cotton aphid reproduction using whole plant assays, and (iii) that the P. lilacinum strain used is both endophytic and pathogenic to cotton aphids. Our results illustrate the potential of using these endophytes for the biological control of aphids and other herbivores under greenhouse and field conditions.

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      The endophytic continuum.

      In spite of the term 'endophyte' being employed for all organisms that inhabit plants, mycologists have come to use the term 'fungal endophyte' for fungi that inhabit plants without causing visible disease symptoms. The term refers only to fungi at the moment of detection without regard for the future status of the interaction. This paper is a review of literature on non-balansiaceous fungi involved in asymptomatic colonisations of plants. These fungal endophytes represent a continuum of fungi with respect to physiological status, infection modus, colonisation pattern, secondary metabolism, life-history strategy, and developmental and evolutionary stages, but also with respect to the fungal and host taxa involved in the symbioses. We hypothesize that there are no neutral interactions, but rather that endophyte-host interactions involve a balance of antagonisms, irrespective of the plant organ infected. There is always at least a degree of virulence on the part of the fungus enabling infection, whereas defence of the plant host limits development of fungal invaders and disease. It is also hypothesized that the endophytes, in contrast to known pathogens, generally have far greater phenotypic plasticity and thus more options than pathogens: infection, local but also extensive colonisation, latency, virulence, pathogenity and (or) saprophytism. This phenotypic plasticity is a motor of evolution.
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        Hidden fungi, emergent properties: endophytes and microbiomes.

        Endophytes are microorganisms that live within plant tissues without causing symptoms of disease. They are important components of plant microbiomes. Endophytes interact with, and overlap in function with, other core microbial groups that colonize plant tissues, e.g., mycorrhizal fungi, pathogens, epiphytes, and saprotrophs. Some fungal endophytes affect plant growth and plant responses to pathogens, herbivores, and environmental change; others produce useful or interesting secondary metabolites. Here, we focus on new techniques and approaches that can provide an integrative understanding of the role of fungal endophytes in the plant microbiome. Clavicipitaceous endophytes of grasses are not considered because they have unique properties distinct from other endophytes. Hidden from view and often overlooked, endophytes are emerging as their diversity, importance for plant growth and survival, and interactions with other organisms are revealed. Copyright © 2011 by Annual Reviews. All rights reserved.
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          Symbioses of grasses with seedborne fungal endophytes.

          Grasses (family Poaceae) and fungi of the family Clavicipitaceae have a long history of symbiosis ranging in a continuum from mutualisms to antagonisms. This continuum is particularly evident among symbioses involving the fungal genus Epichloe (asexual forms = Neotyphodium spp.). In the more mutualistic symbiota, the epichloe endophytes are vertically transmitted via host seeds, and in the more antagonistic symbiota they spread contagiously and suppress host seed set. The endophytes gain shelter, nutrition, and dissemination via host propagules, and can contribute an array of host fitness enhancements including protection against insect and vertebrate herbivores and root nematodes, enhancements of drought tolerance and nutrient status, and improved growth particularly of the root. In some systems, such as the tall fescue N. coenophialum symbioses, the plant may depend on the endophyte under many natural conditions. Recent advances in endophyte molecular biology promise to shed light on the mechanisms of the symbioses and host benefits.

            Author and article information

            [1 ]Department of Entomology, Texas A&M University, College Station, Texas, United States of America
            [2 ]Department of Immunology and Microbiology, Autonomous University of Nuevo Leon, San Nicolás de los Garza, Nuevo Leon, Mexico
            University College Dublin, Ireland
            Author notes

            Competing Interests: This study was funded in part by a grant from the Cotton Incorporated Core Program (#12-387) to GAS. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

            Conceived and designed the experiments: DCL KZS GAS. Performed the experiments: DCL. Analyzed the data: DCL GAS. Contributed reagents/materials/analysis tools: DCL GAS KZS MJER. Wrote the paper: DCL GAS.

            Role: Editor
            PLoS One
            PLoS ONE
            PLoS ONE
            Public Library of Science (San Francisco, USA )
            5 August 2014
            : 9
            : 8
            25093505 4122372 PONE-D-14-07138 10.1371/journal.pone.0103891

            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.

            Pages: 8
            The work was supported by Cotton Incorporated Grant and Good Neighbor Scholarship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
            Research Article
            Biology and Life Sciences
            Pest Control
            Plant Science



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