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Parental environmental exposure leads to glycometabolic disturbances that affect fertilization of eggs in the silkworm Bombyx mori: the parental transcript legacy

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Abstract

Parental transcript legacy plays an important role in fertilization and development of the early embryo. Parental environmental exposure affects the fertilization of eggs, but the underlying biochemical mechanism is largely unresolved. In this study, the parental environmental effects on fertilization of eggs were explored in the silkworm Bombyx mori (B. mori), an ideal lepidopteran animal model. The results showed that the rate of fertilization decreased after the parents were exposed to a poor environment at 32 °C with continuous illumination for 72 h on days 6–9 of the pupal stage, which is a key period for germ cell maturation. This was likely attributable to lower energy charge values, obstructed nicotinamide adenine dinucleotide (NAD+) regeneration and inactive tricarboxylic acid cycle (TCA), leading to accumulation of large amounts of pyruvic acid and lactic acid. This effect was related to energy metabolism via glycolysis; in particular disruption of pyruvate metabolism. In conclusion, this study showed parental exposure to an abnormal environment during germ cell maturation affected glycolysis and the subsequent fertilization of eggs via the parental transcript legacy in B. mori.

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Abbreviations

25LD:

12-hours light–dark cycles at 25 °C

32LL:

Constant illumination at 32 °C

DEM:

Disorders of energy metabolism

E0:

Eggs from virgin females

E1–E3:

Eggs collected at 1–3 h after oviposition

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 31172264 and 31472149), the National High-Tech R&D Program of China (Program 863) (Grant No. 2011AA100306), the Provincial Key Technology R&D Program of Jiangsu (Project No. BE2011327-1) and the Priority Academic Program Development of Jiangsu Higher Education Institutions. The funders had no role in study design, data collection or analysis, nor the decision to publish or preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare that the experiments comply with the current laws of the country in which they were performed.

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Authors and Affiliations

  1. Department of Applied Biology, School of Biology and Basic Medical Sciences, Soochow University, Suzhou, 215123, China

    H. Tao, H. J. Liu, Y. Q. Cheng, Y. H. Sima & S. Q. Xu

  2. Institute for Cardiovascular Science, Soochow University, Suzhou, 215123, China

    W. M. Yin

  3. National Engineering Laboratory for Modern Silk, Soochow University, Suzhou, 215123, China

    Y. H. Sima & S. Q. Xu

Authors
  1. H. Tao
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  2. H. J. Liu
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  3. Y. Q. Cheng
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  4. Y. H. Sima
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  5. W. M. Yin
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  6. S. Q. Xu
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Corresponding author

Correspondence to S. Q. Xu.

Additional information

Communicated by I. D. Hume.

H. Tao and H.J. Liu contributed equally to this work.

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Tao, H., Liu, H.J., Cheng, Y.Q. et al. Parental environmental exposure leads to glycometabolic disturbances that affect fertilization of eggs in the silkworm Bombyx mori: the parental transcript legacy. J Comp Physiol B 185, 47–55 (2015). https://doi.org/10.1007/s00360-014-0864-6

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  • DOI: https://doi.org/10.1007/s00360-014-0864-6

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