Nutrition-dependent juvenile hormone sensitivity promotes flight-muscle degeneration during the aphid dispersal-reproduction transition.

Abstract

In insects, the loss of flight typically involves a dispersal-reproduction transition, but the underlying molecular mechanisms remain poorly understood. In the parthenogenetic pea aphid Acyrthosiphon pisum, winged females undergo flight-muscle degeneration after flight and feeding on new host plants. Similarly, topical application of a juvenile hormone (JH) mimic to starved aphids also induces flight-muscle degeneration. We found that feeding preferentially upregulated the expression of the JH receptor gene Met and a JH-inducible gene, Kr-h1, in the flight muscles, and, thus, enhanced tissue-specific JH sensitivity and signaling. RNAi-mediated knockdown of Kr-h1 prevented flight-muscle degeneration. Likewise, blocking nutritional signals by pharmacological inhibition of the target of rapamycin complex 1 (TORC1) impaired JH sensitivity of the flight muscles in feeding aphids and subsequently delayed muscle degeneration. RNA-sequencing analysis revealed that enhanced JH signaling inhibited the transcription of genes involved in the tricarboxylic acid cycle, likely resulting in reduction of the energy supply, mitochondrial dysfunction and muscle-fiber breakdown. This study shows that nutrient-dependent hormone sensitivity regulates developmental plasticity in a tissue-specific manner, emphasizing a relatively underappreciated mechanism of hormone sensitivity in modulating hormone signaling.

• Authors: Yu Bai, Xiao-Jin Pei, Ning Ban, Nan Chen, Su-Ning Liu, Sheng Li, Tong-Xian Liu
• Journal: Development (Cambridge, England) (Development) Vol. 149 Issue 15 (08 01 2022) ISSN: 1477-9129 [Electronic] England
• PMID: 35815651 (Publication Type: Journal Article, Research Support, Non-U.S. Gov't)
• Copyright: © 2022. Published by The Company of Biologists Ltd.

Chemical References

• Insect Proteins
• Juvenile Hormones

Topics

• Animals
• Aphids (metabolism)
• Female
• Insect Proteins (metabolism)
• Juvenile Hormones (metabolism)
• Muscles (metabolism)
• Reproduction
• Wings, Animal (metabolism)