Duplication of a conserved mitochondrial enzyme gene arms parasitoid wasps with venom cytotoxicity and oogenesis regulation

J Jiqiang Song (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) Z Zihan Qi (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) C Chun He (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) G Guilin Luo (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) B Bo Yuan S Shan Xiao (Ningbo Academy of Agricultural Science) Y Yi Yang F Fang Wang G Gongyin Ye (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) Q Qi Fang (State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University) Z Zhichao Yan (Department of Entomology, Nanjing Agricultural University)

Abstract

Gene duplication, followed by neofunctionalization, is a key mechanism driving the emergence of evolutionary novelties. Despite its significance, the molecular and functional processes underlying this phenomenon remain incompletely understood. By tracing the evolutionary history of cysteine-S-conjugate beta-lyase genes within the kynurenine aminotransferase family, we identified a gene duplication event in parasitoid wasps of the Chalcidoidea superfamily. Notably, a single-copy, highly conserved mitochondria-localized physiological gene underwent a significant duplication, resulting in one copy being recruited into the venom system and acquired cytotoxicity against wasps' hosts. Through this neofunctionalization process, we observed several key evolutionary changes, including loss of ancestral mitochondrial localization and enzyme activity, acquisition of a secretory signal peptide, shift in expression pattern, positive selection, and the establishment of evolutionary acquired protein–protein interactions. Additionally, we found that another duplicate copy was specialized in wasps' ovary and repurposed for oogenesis regulation. Our study offers a detailed insight into the genetic and molecular mechanisms that drive functional diversification during the evolution of gene families.

Article Details

Volume / Issue Vol. 122, Issue 39
Published September 30, 2025
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (11)

J

Jiqiang Song

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

Z

Zihan Qi

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

C

Chun He

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

G

Guilin Luo

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

B

Bo Yuan

S

Shan Xiao

Ningbo Academy of Agricultural Science

Y

Yi Yang

F

Fang Wang

G

Gongyin Ye

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

Q

Qi Fang

State Key Laboratory of Rice Biology and Breeding and Ministry of Agriculture and Rural Affairs Key Laboratory of Molecular Biology of Crop Pathogens and Insect Pests and Zhejiang Key Laboratory of Biology and Ecological Regulation of Crop Pathogens and Insects, Institute of Insect Sciences, College of Agriculture and Biotechnology, Zhejiang University

Z

Zhichao Yan

Department of Entomology, Nanjing Agricultural University