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Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males
The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. However, irradiation in normal atmospheric conditions can be damaging for males, because irradiation generates substantial biological oxidative stress that, combined with do...
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description | The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. However, irradiation in normal atmospheric conditions can be damaging for males, because irradiation generates substantial biological oxidative stress that, combined with domestication and mass-rearing conditions, may reduce sterile male sexual competitiveness and quality. In this study, biological oxidative stress and antioxidant capacity were experimentally manipulated in
Anastrepha suspensa
using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate their role in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited only a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs. |
doi_str_mv | 10.1038/s41598-021-99594-1 |
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Anastrepha suspensa
using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate their role in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited only a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-021-99594-1</identifier><identifier>PMID: 34642368</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/158 ; 631/181 ; 631/208 ; 631/601 ; 631/61 ; Animal reproduction ; Animals ; Animals, Genetically Modified ; Antioxidants ; Atmospheric conditions ; Competitiveness ; Domestication ; Hormesis ; Humanities and Social Sciences ; Hypoxia ; Infertility, Male - etiology ; Insect Control - methods ; Insect Proteins - genetics ; Insect Proteins - metabolism ; Insects ; Ionizing radiation ; Irradiation ; Lek behavior ; Male ; Male sterility ; Males ; Mass rearing ; Mating ; Mitochondria ; multidisciplinary ; Mutation ; Oxidative Stress ; Oxygen ; Oxygen - metabolism ; Pest control ; Science ; Science (multidisciplinary) ; Sexual behavior ; Sexual Behavior, Animal - physiology ; Sexual Behavior, Animal - radiation effects ; Sterilized organisms ; Superoxide dismutase ; Superoxide Dismutase - genetics ; Superoxide Dismutase - metabolism ; Tephritidae - enzymology ; Tephritidae - physiology ; Tephritidae - radiation effects</subject><ispartof>Scientific reports, 2021-10, Vol.11 (1), p.20182-15, Article 20182</ispartof><rights>The Author(s) 2021</rights><rights>2021. The Author(s).</rights><rights>The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-5cee1b95f86f9646cacf2f377be4feb6569d52085644166ebd59545c52ac61b93</citedby><cites>FETCH-LOGICAL-c540t-5cee1b95f86f9646cacf2f377be4feb6569d52085644166ebd59545c52ac61b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2581099026/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2581099026?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34642368$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dias, Vanessa S.</creatorcontrib><creatorcontrib>Cáceres, Carlos</creatorcontrib><creatorcontrib>Parker, Andrew G.</creatorcontrib><creatorcontrib>Pereira, Rui</creatorcontrib><creatorcontrib>Demirbas-Uzel, Güler</creatorcontrib><creatorcontrib>Abd-Alla, Adly M. M.</creatorcontrib><creatorcontrib>Teets, Nicholas M.</creatorcontrib><creatorcontrib>Schetelig, Marc F.</creatorcontrib><creatorcontrib>Handler, Alfred M.</creatorcontrib><creatorcontrib>Hahn, Daniel A.</creatorcontrib><title>Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. However, irradiation in normal atmospheric conditions can be damaging for males, because irradiation generates substantial biological oxidative stress that, combined with domestication and mass-rearing conditions, may reduce sterile male sexual competitiveness and quality. In this study, biological oxidative stress and antioxidant capacity were experimentally manipulated in
Anastrepha suspensa
using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate their role in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited only a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs.</description><subject>631/158</subject><subject>631/181</subject><subject>631/208</subject><subject>631/601</subject><subject>631/61</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Antioxidants</subject><subject>Atmospheric conditions</subject><subject>Competitiveness</subject><subject>Domestication</subject><subject>Hormesis</subject><subject>Humanities and Social Sciences</subject><subject>Hypoxia</subject><subject>Infertility, Male - etiology</subject><subject>Insect Control - methods</subject><subject>Insect Proteins - genetics</subject><subject>Insect Proteins - metabolism</subject><subject>Insects</subject><subject>Ionizing radiation</subject><subject>Irradiation</subject><subject>Lek behavior</subject><subject>Male</subject><subject>Male sterility</subject><subject>Males</subject><subject>Mass rearing</subject><subject>Mating</subject><subject>Mitochondria</subject><subject>multidisciplinary</subject><subject>Mutation</subject><subject>Oxidative Stress</subject><subject>Oxygen</subject><subject>Oxygen - metabolism</subject><subject>Pest control</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sexual behavior</subject><subject>Sexual Behavior, Animal - physiology</subject><subject>Sexual Behavior, Animal - radiation effects</subject><subject>Sterilized organisms</subject><subject>Superoxide dismutase</subject><subject>Superoxide Dismutase - genetics</subject><subject>Superoxide Dismutase - metabolism</subject><subject>Tephritidae - enzymology</subject><subject>Tephritidae - physiology</subject><subject>Tephritidae - radiation effects</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9kk1vFSEUhidGY5vaP-DCkLgeBQa4w8bENFab1LjRNWHgMJebGbgCU2__gr9a2unnRjYQzvs-h4-3ad4S_IHgrv-YGeGybzElrZRcspa8aI4pZrylHaUvn6yPmtOcd7gOTiUj8nVz1DHBaCf64-bvd1-i2cZgk9cTysseUjx4C8j6PC9FZ0DxChIc9gly9jEgHSya4h8UD9cjBGSq15da8GFE25hmyD4jP-9T9aGyBVSRru7rYCrLIZ-Stl4XsCgXSH4CNOsJ8pvmldNThtO7-aT5df7l59m39vLH14uzz5et4QyXlhsAMkjueuGkYMJo46jrNpsBmINBcCEtp7jngjEiBAyWS8644VQbUY3dSXOxcm3UO7VPftbpWkXt1e1GTKPSqXgzgSKygtlGWltfzlEhmXYAvZVUa91pXFmfVtZ-GWawBkJJenoGfV4JfqvGeKV6TghmpALe3wFS_L1ALmoXlxTq_RXlPcFSYiqqiq4qk2LOCdxDB4LVTRzUGgdV46Bu46Bu0O-enu3Bcv_5VdCtglxLYYT02Ps_2H8QisWS</recordid><startdate>20211012</startdate><enddate>20211012</enddate><creator>Dias, Vanessa S.</creator><creator>Cáceres, Carlos</creator><creator>Parker, Andrew G.</creator><creator>Pereira, Rui</creator><creator>Demirbas-Uzel, Güler</creator><creator>Abd-Alla, Adly M. 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M.</au><au>Teets, Nicholas M.</au><au>Schetelig, Marc F.</au><au>Handler, Alfred M.</au><au>Hahn, Daniel A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males</atitle><jtitle>Scientific reports</jtitle><stitle>Sci Rep</stitle><addtitle>Sci Rep</addtitle><date>2021-10-12</date><risdate>2021</risdate><volume>11</volume><issue>1</issue><spage>20182</spage><epage>15</epage><pages>20182-15</pages><artnum>20182</artnum><issn>2045-2322</issn><eissn>2045-2322</eissn><abstract>The Sterile Insect Technique (SIT) is a successful autocidal control method that uses ionizing radiation to sterilize insects. However, irradiation in normal atmospheric conditions can be damaging for males, because irradiation generates substantial biological oxidative stress that, combined with domestication and mass-rearing conditions, may reduce sterile male sexual competitiveness and quality. In this study, biological oxidative stress and antioxidant capacity were experimentally manipulated in
Anastrepha suspensa
using a combination of low-oxygen conditions and transgenic overexpression of mitochondrial superoxide dismutase (SOD2) to evaluate their role in the sexual behavior and quality of irradiated males. Our results showed that SOD2 overexpression enhances irradiated insect quality and improves male competitiveness in leks. However, the improvements in mating performance were modest, as normoxia-irradiated SOD2 males exhibited only a 22% improvement in mating success compared to normoxia-irradiated wild type males. Additionally, SOD2 overexpression did not synergistically improve the mating success of males irradiated in either hypoxia or severe hypoxia. Short-term hypoxic and severe-hypoxic conditioning hormesis, per se, increased antioxidant capacity and enhanced sexual competitiveness of irradiated males relative to non-irradiated males in leks. Our study provides valuable new information that antioxidant enzymes, particularly SOD2, have potential to improve the quality and lekking performance of sterile males used in SIT programs.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>34642368</pmid><doi>10.1038/s41598-021-99594-1</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | 631/158 631/181 631/208 631/601 631/61 Animal reproduction Animals Animals, Genetically Modified Antioxidants Atmospheric conditions Competitiveness Domestication Hormesis Humanities and Social Sciences Hypoxia Infertility, Male - etiology Insect Control - methods Insect Proteins - genetics Insect Proteins - metabolism Insects Ionizing radiation Irradiation Lek behavior Male Male sterility Males Mass rearing Mating Mitochondria multidisciplinary Mutation Oxidative Stress Oxygen Oxygen - metabolism Pest control Science Science (multidisciplinary) Sexual behavior Sexual Behavior, Animal - physiology Sexual Behavior, Animal - radiation effects Sterilized organisms Superoxide dismutase Superoxide Dismutase - genetics Superoxide Dismutase - metabolism Tephritidae - enzymology Tephritidae - physiology Tephritidae - radiation effects |
title | Mitochondrial superoxide dismutase overexpression and low oxygen conditioning hormesis improve the performance of irradiated sterile males |
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