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Background <p>Spermatogenesis is a highly complex developmental process requiring coordinated expression of a large fraction of the genome, and the testis displays one of the highest proportions of tissue-specific proteins across animal species. However, proteomic data capturing testis development over time remain limited, particularly in non-model organisms. In <i>Nasonia vitripennis</i>, spermatogenesis occurs as a single synchronized wave during pupal development, providing a valuable framework to investigate stage-specific protein dynamics underlying testis differentiation.</p> Results <p>We quantified protein abundance in heads, legs, and testes across four successive pupal stages (white, red-eyed white, bicolor, and black pupae), identifying 3,130 proteins. A large ubiquitous core proteome (69.4%) was detected alongside clear tissue- and stage-specific expression patterns. The testis showed the earliest proteomic divergence between early and late pupal stages, indicating an earlier onset of differentiation compared to heads and legs. Clustering of protein abundance trajectories revealed sequential molecular programs associated with cytoskeletal remodeling, meiotic processes, and spermiogenesis, highlighting both conserved pathways and lineage-specific features. Among 175 proteins showing at least a two-fold change in abundance during testis development, 11 were uncharacterized. Four of these belong to a novel family of six-bladed β-propeller–like proteins identified by three-dimensional structure prediction and showing similarity to exo-α-sialidases.</p> Conclusions <p>These findings provide a comprehensive view of proteome dynamics during synchronized spermatogenesis in <i>N. vitripennis</i> and reveal candidate proteins potentially involved in testis differentiation. The identification of Hymenoptera-specific β-propeller–like proteins related to sialidases suggests roles in glycan processing, sperm surface modification, and reproductive function, opening new perspectives for understanding the evolution and specialization of reproductive proteins.</p>

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Dynamic proteomics of Nasonia vitripennis pupal development reveals testis-specific regulation of new proteins (orphans) likely related to exo-α-sialidases

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年5月21日

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  • Charlotte Lécureuil,
  • Christine Almunia,
  • Vanessa Guérin,
  • Jean Armengaud,
  • Thierry Moreau,
  • Sophie Fouchécourt

摘要

Background

Spermatogenesis is a highly complex developmental process requiring coordinated expression of a large fraction of the genome, and the testis displays one of the highest proportions of tissue-specific proteins across animal species. However, proteomic data capturing testis development over time remain limited, particularly in non-model organisms. In Nasonia vitripennis, spermatogenesis occurs as a single synchronized wave during pupal development, providing a valuable framework to investigate stage-specific protein dynamics underlying testis differentiation.

Results

We quantified protein abundance in heads, legs, and testes across four successive pupal stages (white, red-eyed white, bicolor, and black pupae), identifying 3,130 proteins. A large ubiquitous core proteome (69.4%) was detected alongside clear tissue- and stage-specific expression patterns. The testis showed the earliest proteomic divergence between early and late pupal stages, indicating an earlier onset of differentiation compared to heads and legs. Clustering of protein abundance trajectories revealed sequential molecular programs associated with cytoskeletal remodeling, meiotic processes, and spermiogenesis, highlighting both conserved pathways and lineage-specific features. Among 175 proteins showing at least a two-fold change in abundance during testis development, 11 were uncharacterized. Four of these belong to a novel family of six-bladed β-propeller–like proteins identified by three-dimensional structure prediction and showing similarity to exo-α-sialidases.

Conclusions

These findings provide a comprehensive view of proteome dynamics during synchronized spermatogenesis in N. vitripennis and reveal candidate proteins potentially involved in testis differentiation. The identification of Hymenoptera-specific β-propeller–like proteins related to sialidases suggests roles in glycan processing, sperm surface modification, and reproductive function, opening new perspectives for understanding the evolution and specialization of reproductive proteins.