Peroxiredoxin 1 transfer during mating protects eupyrene sperm against oxdative stress in Grapholita molesta

BACKGROUND: Each Grapholita molesta female only copulates once during its lifetime and thus must maintain the viability of stored eupyrene sperm for male reproductive success. The male ejaculate comprises abundant accessory gland proteins produced by the male accessory gland (AG), and many of which are major effectors for sperm storage and maintenance.

RESULTS: Here, we reported that an antioxidant protein, peroxiredoxin 1 (GmolPrx1), secreted by the male AG, is essential for protecting eupyrene sperm from oxidative stress and maintaining their quality during storage in the female bursa copulatrix (BC). Our data showed that GmolPrx1 is highly expressed in the AG of sexually mature males. The GmolPrx1 protein is localized to the cytoplasm of AG cells and delivered to the female BC during mating. Knockdown of GmolPrx1 strongly decreased the fertility of mated females. Additionally, we evaluated oxidative status in the spermatophore of females and found that the content of hydrogen peroxide increased significantly after mating with GmolPrx1 knockdown males. Finally, the quality assessment of eupyrene sperm demonstrated that the plasma membrane integrity, acrosome integrity, and DNA integrity were all severely impaired in the spermatophore of females after mating with GmolPrx1 knockdown males, which may contribute to the fertility decline in males.

CONCLUSION: Our current data demonstrated that activities of eupyrene sperm stored in females can be significantly impaired by enhanced oxidative stress through knocking down of GmolPrx1 in males. Our finding thus may further lay new foundations for the control of G. molesta through suppressing their populations by manipulating male reproductive genes.

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Work Title Peroxiredoxin 1 transfer during mating protects eupyrene sperm against oxdative stress in Grapholita molesta
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Open Access
Creators
  1. Jie Cheng
  2. Lin Zhu
  3. Fang Zhu
  4. Peng Zhao
  5. Qiong-Xi Li
  6. Zi-Hang Lu
  7. Song-Dou Zhang
  8. Zhen Li
  9. Xiao-Xia Liu
Keyword
  1. Oriental fruit moth
  2. Peroxiredoxin 1
  3. Mating
  4. Fertility
  5. Oxidative stress
  6. Sperm quality
License In Copyright (Rights Reserved)
Work Type Article
Publisher
  1. Pest Management Science
Publication Date March 16, 2023
Publisher Identifier (DOI)
  1. https://doi.org/10.1002/ps.7458
Deposited March 18, 2024

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Version 1
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  • Created
  • Added 2023-PMS-Cheng-Peroxiredoxin_1_transfer_during_mating_protects_eupyrene_sperm_against_oxdative_stress.pdf
  • Added Creator Jie Cheng
  • Added Creator Lin Zhu
  • Added Creator Fang Zhu
  • Added Creator Peng Zhao
  • Added Creator Qiong Xi Li
  • Added Creator Zi Hang Lu
  • Added Creator Song Dou Zhang
  • Added Creator Zhen Li
  • Added Creator Xiao Xia Liu
  • Published
  • Updated Keyword, Description, Publication Date Show Changes
    Keyword
    • Oriental fruit moth, Peroxiredoxin 1, Mating, Fertility, Oxidative stress, Sperm quality
    Description
    • <p>BACKGROUND: Each Grapholita molesta female only copulates once during its lifetime and thus must maintain the viability of stored eupyrene sperm for male reproductive success. The male ejaculate comprises abundant accessory gland proteins produced by the male accessory gland (AG), and many of which are major effectors for sperm storage and maintenance. RESULTS: Here, we reported that an antioxidant protein, peroxiredoxin 1 (GmolPrx1), secreted by the male AG, is essential for protecting eupyrene sperm from oxidative stress and maintaining their quality during storage in the female bursa copulatrix (BC). Our data showed that GmolPrx1 is highly expressed in the AG of sexually mature males. The GmolPrx1 protein is localized to the cytoplasm of AG cells and delivered to the female BC during mating. Knockdown of GmolPrx1 strongly decreased the fertility of mated females. Additionally, we evaluated oxidative status in the spermatophore of females and found that the content of hydrogen peroxide increased significantly after mating with GmolPrx1 knockdown males. Finally, the quality assessment of eupyrene sperm demonstrated that the plasma membrane integrity, acrosome integrity, and DNA integrity were all severely impaired in the spermatophore of females after mating with GmolPrx1 knockdown males, which may contribute to the fertility decline in males. CONCLUSION: Our current data demonstrated that activities of eupyrene sperm stored in females can be significantly impaired by enhanced oxidative stress through knocking down of GmolPrx1 in males. Our finding thus may further lay new foundations for the control of G. molesta through suppressing their populations by manipulating male reproductive genes.</p>
    • <p>BACKGROUND: Each _Grapholita molesta_ female only copulates once during its lifetime and thus must maintain the viability of stored eupyrene sperm for male reproductive success. The male ejaculate comprises abundant accessory gland proteins produced by the male accessory gland (AG), and many of which are major effectors for sperm storage and maintenance.
    • RESULTS: Here, we reported that an antioxidant protein, peroxiredoxin 1 (GmolPrx1), secreted by the male AG, is essential for protecting eupyrene sperm from oxidative stress and maintaining their quality during storage in the female bursa copulatrix (BC). Our data showed that GmolPrx1 is highly expressed in the AG of sexually mature males. The GmolPrx1 protein is localized to the cytoplasm of AG cells and delivered to the female BC during mating. Knockdown of _GmolPrx1_ strongly decreased the fertility of mated females. Additionally, we evaluated oxidative status in the spermatophore of females and found that the content of hydrogen peroxide increased significantly after mating with _GmolPrx1_ knockdown males. Finally, the quality assessment of eupyrene sperm demonstrated that the plasma membrane integrity, acrosome integrity, and DNA integrity were all severely impaired in the spermatophore of females after mating with _GmolPrx1_ knockdown males, which may contribute to the fertility decline in males.
    • CONCLUSION: Our current data demonstrated that activities of eupyrene sperm stored in females can be significantly impaired by enhanced oxidative stress through knocking down of _GmolPrx1_ in males. Our finding thus may further lay new foundations for the control of _G. molesta_ through suppressing their populations by manipulating male reproductive genes.</p>
    Publication Date
    • 2023-08-01
    • 2023-03-16
  • Renamed Creator Qiong-Xi Li Show Changes
    • Qiong Xi Li
    • Qiong-Xi Li
  • Renamed Creator Zi-Hang Lu Show Changes
    • Zi Hang Lu
    • Zi-Hang Lu
  • Renamed Creator Song-Dou Zhang Show Changes
    • Song Dou Zhang
    • Song-Dou Zhang
  • Renamed Creator Xiao-Xia Liu Show Changes
    • Xiao Xia Liu
    • Xiao-Xia Liu
  • Updated