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      Modified Atmosphere Does Not Reduce the Efficacy of Phytosanitary Irradiation Doses Recommended for Tephritid Fruit Flies

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          Abstract

          Phytosanitary irradiation (PI) has been successfully used to disinfest fresh commodities and facilitate international agricultural trade. Critical aspects that may reduce PI efficacy must be considered to ensure the consistency and effectiveness of approved treatment schedules. One factor that can potentially reduce PI efficacy is irradiation under low oxygen conditions. This factor is particularly important because storage and packaging of horticultural commodities under low oxygen levels constitute practices widely used to preserve their quality and extend their shelf life. Hence, international organizations and regulatory agencies have considered the uncertainties regarding the efficacy of PI doses for insects infesting fresh commodities stored under low oxygen levels as a rationale for restricting PI application under modified atmosphere. Our research examines the extent to which low oxygen treatments can reduce the efficacy of phytosanitary irradiation for tephritids naturally infesting fruits. The effects of normoxia (21% O 2), hypoxia (~5% O 2), and severe hypoxia (< 0.5% O 2) on radiation sensitivity of third instars of Anastrepha fraterculus (sensu lato), A. ludens (Loew), Bactrocera dorsalis (Hendel), and Ceratitis capitata (Wiedemann) were evaluated and compared at several gamma radiation doses. Our findings suggest that, compared to normoxia, hypoxic and severe-hypoxic conditioning before and during irradiation can increase adult emergence and contribute to advancement of larval development of tephritid fruit flies only at low radiation doses that are not used as phytosanitary treatments. With phytosanitary irradiation doses approved internationally for several tephritids, low oxygen treatments applied before and during irradiation did not increase the emergence rates of any fruit fly species evaluated, and all treated insects died as coarctate larvae. Thus, the findings of our research support a re-evaluation of restrictions related to phytosanitary irradiation application under modified atmospheres targeting tephritid fruit flies.

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          Cellular mechanism of oxygen sensing.

          O2 sensing is a fundamental biological process necessary for adaptation of living organisms to variable habitats and physiological situations. Cellular responses to hypoxia can be acute or chronic. Acute responses rely mainly on O2-regulated ion channels, which mediate adaptive changes in cell excitability, contractility, and secretory activity. Chronic responses depend on the modulation of hypoxia-inducible transcription factors, which determine the expression of numerous genes encoding enzymes, transporters and growth factors. O2-regulated ion channels and transcription factors are part of a widely operating signaling system that helps provide sufficient O2 to the tissues and protect the cells against damage due to O2 deficiency. Despite recent advances in the molecular characterization of O2-regulated ion channels and hypoxia-inducible factors, several unanswered questions remain regarding the nature of the O2 sensor molecules and the mechanisms of interaction between the sensors and the effectors. Current models of O2 sensing are based on either a heme protein capable of reversibly binding O2 or the production of oxygen reactive species by NAD(P)H oxidases and mitochondria. Complete molecular characterization of the hypoxia signaling pathways will help elucidate the differential sensitivity to hypoxia of the various cell types and the gradation of the cellular responses to variable levels of PO2. A deeper understanding of the cellular mechanisms of O2 sensing will facilitate the development of new pharmacological tools effective in the treatment of diseases such as stroke or myocardial ischemia caused by localized deficits of O2.
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            Preparation for oxidative stress under hypoxia and metabolic depression: Revisiting the proposal two decades later.

            Organisms that tolerate wide variations in oxygen availability, especially to hypoxia, usually face harsh environmental conditions during their lives. Such conditions include, for example, lack of food and/or water, low or high temperatures, and reduced oxygen availability. In contrast to an expected strong suppression of protein synthesis, a great number of these animals present increased levels of antioxidant defenses during oxygen deprivation. These observations have puzzled researchers for more than 20 years. Initially, two predominant ideas seemed to be irreconcilable: on one hand, hypoxia would decrease reactive oxygen species (ROS) production, while on the other the induction of antioxidant enzymes would require the overproduction of ROS. This induction of antioxidant enzymes during hypoxia was viewed as a way to prepare animals for oxidative damage that may happen ultimately during reoxygenation. The term "preparation for oxidative stress" (POS) was coined in 1998 based on such premise. However, there are many cases of increased oxidative damage in several hypoxia-tolerant organisms under hypoxia. In addition, over the years, the idea of an assured decrease in ROS formation under hypoxia was challenged. Instead, several findings indicate that the production of ROS actually increases in response to hypoxia. Recently, it became possible to provide a comprehensive explanation for the induction of antioxidant enzymes under hypoxia. The supporting evidence and the limitations of the POS idea are extensively explored in this review as we discuss results from research on estivation and situations of low oxygen stress, such as hypoxia, freezing exposure, severe dehydration, and air exposure of water-breathing animals. We propose that, under some level of oxygen deprivation, ROS are overproduced and induce changes leading to hypoxic biochemical responses. These responses would occur mainly through the activation of specific transcription factors (FoxO, Nrf2, HIF-1, NF-κB, and p53) and post translational mechanisms, both mechanisms leading to enhanced antioxidant defenses. Moreover, reactive nitrogen species are candidate modulators of ROS generation in this scenario. We conclude by drawing out the future perspectives in this field of research, and how advances in the knowledge of the mechanisms involved in the POS strategy will offer new and innovative study scenarios of biological and physiological cellular responses to environmental stress.
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              Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa.

              Most organisms are repeatedly exposed to oxidative stress from multiple sources throughout their lifetimes, potentially affecting all aspects of organismal performance. Here we test whether exposure to a conditioning bout of anoxia early in adulthood induces a hormetic response that confers resistance to oxidative stress and enhances male sexual performance later in life in the Caribbean fruit fly, Anastrepha suspensa. Anoxic conditioning of adults prior to emergence led to an increase in antioxidant capacity driven by mitochondrial superoxide dismutase and glutathione peroxidase. When exposed to gamma irradiation, a strong oxidative stressor, males that received anoxic conditioning had lower lipid and protein oxidative damage at sexual maturity. Anoxia conditioning led to greater male sexual competitiveness compared with unconditioned males when both were irradiated, although there was no effect of anoxia conditioning on mating competitiveness in unirradiated males. Anoxia also led to higher adult emergence rates and greater flight ability in irradiation-stressed flies while preserving sterility. Thus, hormetic treatments that increased antioxidant enzyme activity also improved male performance after irradiation, suggesting that antioxidant enzymes play an important role in mediating the relationship between oxidative stress and sexual selection. Furthermore, our work has important applied implications for the sterile insect technique (SIT), an environmentally friendly method of insect pest control where males are sterilized by irradiation and deployed in the field to disrupt pest populations via mating. We suggest that hormetic treatments specifically designed to enhance antioxidant activity may produce more sexually competitive sterile males, thus improving the efficacy and economy of SIT programs.
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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                15 June 2020
                June 2020
                : 11
                : 6
                : 371
                Affiliations
                [1 ]Insect Pest Control Laboratory, Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, IAEA, Wagramer Strasse 5, 1400 Vienna, Austria; oyamaba@ 123456gmail.com (O.Y.M.-B.); nickvahurt312013@ 123456gmail.com (N.V.H.); amandaascardoso@ 123456gmail.com (A.A.S.C.); a.g.parker@ 123456protonmail.com (A.G.P.); lax.caravantes@ 123456gmail.com (L.A.C.); cam1lo.11194@ 123456gmail.com (C.R.); alexandressa2@ 123456live.com (A.S.A.); F.Maxwell@ 123456iaea.org (F.M.); C.E.Caceres-Barrios@ 123456iaea.org (C.E.C.-B.); M.Vreysen@ 123456iaea.org (M.J.B.V.)
                [2 ]Phytosanitation, 3917 Estancia Drive, Oceanside, CA 92058, USA
                [3 ]USDA, APHIS, PPQ, Science and Technology, Otis Laboratory 1398 W. Truck Rd., Buzzards Bay, MA 02542, USA; scott.w.myers@ 123456usda.gov
                Author notes
                [* ]Correspondence: V.Dias-De-Castro@ 123456iaea.org (V.S.D.); n5551212@ 123456yahoo.com (G.J.H.)
                [†]

                These authors contributed equally to the work.

                Author information
                https://orcid.org/0000-0001-9904-2849
                https://orcid.org/0000-0002-0708-7618
                https://orcid.org/0000-0002-2530-6001
                https://orcid.org/0000-0001-8187-1278
                https://orcid.org/0000-0003-0230-3956
                Article
                insects-11-00371
                10.3390/insects11060371
                7348963
                32549285
                5f5ac2e8-8feb-4c37-9516-1c30b19c3df6
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 18 May 2020
                : 10 June 2020
                Categories
                Article

                hypoxia,normoxia,phytosanitation,oxygen effect,radiotolerance,radiation sensitivity,radioprotection,radioresistance

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