Fungal pathogen promotes caterpillar feeding and weight gain using a host-like trehalase

Peiqing Zhao; Jianfeng Lin; Dehong Yang; Weihan Peng; Xuewen Wang; Yongping Huang; Chengshu Wang

doi:10.1016/j.cub.2025.06.002

Fungal pathogen promotes caterpillar feeding and weight gain using a host-like trehalase

Curr Biol. 2025 Jun 24:S0960-9822(25)00690-6. doi: 10.1016/j.cub.2025.06.002. Online ahead of print.

Authors

Peiqing Zhao¹, Jianfeng Lin¹, Dehong Yang², Weihan Peng¹, Xuewen Wang¹, Yongping Huang³, Chengshu Wang⁴

Affiliations

¹ Key Laboratory of Insect Developmental and Evolutionary Biology, State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China.
² Key Laboratory of Insect Developmental and Evolutionary Biology, State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China; School of Environmental Science and Engineering, Shanghai Jiao Tong University, Shanghai 200240, China.
³ School of Environmental Science and Engineering, Shanghai Jiao Tong University, Shanghai 200240, China.
⁴ Key Laboratory of Insect Developmental and Evolutionary Biology, State Key Laboratory of Plant Trait Design, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai 200032, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China; School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China. Electronic address: wangcs@sippe.ac.cn.

PMID: 40580961
DOI: 10.1016/j.cub.2025.06.002

Abstract

Parasite-mediated extended phenotypes in hosts are of particular interest in biology. However, few parasite genes have been characterized for their selfish role in altering host behaviors to benefit parasite transmission or reproduction. The entomopathogenic fungus Cordyceps militaris infects caterpillar larvae without killing them until after pupation. Here, we report that fungal infection of silkworm larvae induces increased feeding and weight gain, which is manifested by starvation-like responses, including the constant upregulation of the orexigenic peptide HemaP and a sharp reduction in hemolymph trehalose levels. Engineered fungal strains overexpressing HemaP further enhance silkworms' excessive feeding and weight gain. Disruption of HemaP in silkworms reduced trehalose production and pupal weight, thereby decreasing fungal fruiting body formation on mutant pupae. Consistent with the depletion of blood sugars, an insect-like trehalase gene was upregulated in fungal cells growing within insect body cavities, and deleting this gene in C. militaris abolished fungal ability to promote weight gain in silkworms after infection. Our data shed light on a previously unsuspected extended phenotype: fungal promotion of insect feeding through the function of a host-like gene, ultimately benefiting fungal reproduction.

Keywords: Cordyceps militaris; extended phenotype; hyperphagia; orexigenic peptide; silkworm; trehalase; trehalose.