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      Male Selenoprotein F-Like (SPF-L) Influences Female Reproduction and Population Growth in Nilaparvata lugens (Hemiptera: Delphacidae)

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          Abstract

          Selenoproteins serve in anti-oxidant and cellular redox functions in almost all organisms. A recent study characterized a selenoprotein F-like (SPF-L) in the brown plant hopper’s (BPH), Nilaparvata lugens, male accessory glands (MAGs), raised the question of whether the SPF-L is associated with female fecundity. In this study, SPF-L mRNA was found to be enriched in the internal reproductive organ (IRO) of virgin males, also expressed relatively stably in virgin males and females, and dietary dsSPF-L-treatments led to reduced MAG protein and Arginine content. Knockdown of NlSPF-L in unmated males did not influence juvenile hormone (JH) III and ecdysteroid titers, however, dsSPF-L-treated mated males had increased JH III titer, and reduced ecdysteroid titer compared to controls. After mating with dsSPF-L-treated males, female partners had reduced fat body and ovary soluble proteins and JH III tier and vitellogenin (Vg) mRNA levels, but no alterations in ecdysteroid titer, body weight or longevity. The experimental females had prolonged pre-oviposition periods and they laid fewer eggs, which suffered reduced hatching rates and population growth index (PGI). Such mating also led to impaired IRO development in males and females, which was confirmed by immunofluorescence staining. We infer that SPF-L affects reproductive success of males and their partners.

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          Most cited references39

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          Male accessory gland secretions: modulators of female reproductive physiology and behavior.

          Secretions of male accessory glands contain a variety of bioactive molecules. When transferred during mating, these molecules exert wide-ranging effects on female reproductive activity and they improve the male's chances of siring a significant proportion of the female's offspring. The accessory gland secretions may affect virtually all aspects of the female's reproductive activity. The secretions may render her unwilling or unable to remate for some time, facilitating sperm storage and ensuring that any eggs laid will be fertilized by that male's sperm. They may stimulate an increase in the number and rate of development of eggs and modulate ovulation and/or oviposition. Antimicrobial agents in the secretions ensure that the female reproductive tract is a hospitable environment during sperm transfer. In a few species the secretions include noxious chemicals. These are sequestered by developing eggs that are thereby protected from predators and pathogens when laid.
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            Complexity of seminal fluid: a review

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              Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster.

              Mating elicits two major changes in the reproductive behavior of many insect females. The egg-laying rate increases and the readiness to accept males (receptivity) is reduced. These postmating responses last approximately 1 week in Drosophila melanogaster. Males that do not transfer sperm but transfer seminal fluid during mating induce a short-term response of 1 day. The long-term response of 1 week requires the presence of sperm (sperm effect). Hence, sperm is essential for the long-term persistence of the postmating responses. Three seminal fluid peptides elicit postmating responses: ovulin, sex-peptide (SP), and DUP99B. Using the technique of targeted mutagenesis by homologous recombination, we have produced males with mutant SP genes. Here, we report that males lacking functional SP elicit only a weak short-term response. However, these males do transfer sperm. Thus, (i) SP is the major agent eliciting the short-term and the long-term postmating responses and (ii) sperm is merely the carrier for SP. The second conclusion is supported by the finding that SP binds to sperm. The 36-aa-encoding SP gene is the first small Drosophila gene knocked out with the method of homologous recombination.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                25 September 2019
                2019
                : 10
                : 1196
                Affiliations
                [1] 1School of Horticulture and Plant Protection, Yangzhou University , Yangzhou, China
                [2] 2Biological Control of Insects Research Laboratory, USDA/Agricultural Research Service , Columbia, MO, United States
                [3] 3Division of Plant Sciences, University of Missouri , Columbia, MO, United States
                Author notes

                Edited by: Senthil-Nathan Sengottayan, Manonmaniam Sundaranar University, India

                Reviewed by: Pin-Jun Wan, China National Rice Research Institute (CAAS), China; Kai Lu, Fujian Agriculture and Forestry University, China

                *Correspondence: LinQuan Ge, lqge@ 123456yzu.edu.cn

                Co-first authors

                This article was submitted to Invertebrate Physiology, a section of the journal Frontiers in Physiology

                Article
                10.3389/fphys.2019.01196
                6773838
                56f02c90-2b54-47b5-8879-33bc76209edd
                Copyright © 2019 Ge, Zhou, Gu, Wu, Zhou, Zheng, Stanley and Song.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 22 June 2019
                : 03 September 2019
                Page count
                Figures: 11, Tables: 2, Equations: 0, References: 45, Pages: 17, Words: 0
                Categories
                Physiology
                Original Research

                Anatomy & Physiology
                nilaparvata lugens,selenoprotein,seminal fluids,mating,fecundity
                Anatomy & Physiology
                nilaparvata lugens, selenoprotein, seminal fluids, mating, fecundity

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