Chitinase inhibition induces transcriptional dysregulation altering ecdysteroid-mediated control of Spodoptera frugiperda development

Ranjit S Barbole; Shivani Sharma; Yogita Patil; Ashok P Giri; Rakesh S Joshi

doi:10.1016/j.isci.2024.109280

Chitinase inhibition induces transcriptional dysregulation altering ecdysteroid-mediated control of Spodoptera frugiperda development

iScience. 2024 Feb 20;27(3):109280. doi: 10.1016/j.isci.2024.109280. eCollection 2024 Mar 15.

Authors

Ranjit S Barbole^{1

2}, Shivani Sharma¹, Yogita Patil^{1

2}, Ashok P Giri^{1

2}, Rakesh S Joshi^{1

2}

Affiliations

¹ Biochemical Sciences Division, CSIR-National Chemical Laboratory, Dr. Homi Bhabha Road, Pune 411008, Maharashtra, India.
² Academy of Scientific and Innovative Research (AcSIR), Ghaziabad 201002, Uttar Pradesh, India.

Abstract

Chitinases and ecdysteroid hormones are vital for insect development. Crosstalk between chitin and ecdysteroid metabolism regulation is enigmatic. Here, we examined chitinase inhibition effect on Spodoptera frugiperda ecdysteroid metabolism. In vitro studies suggested that berberine inhibits S. frugiperda chitinase 5 (SfCht5). The Berberine feeding resulted in defective S. frugiperda development. Berberine-fed insects showed higher SfCht5 and Chitinase 7 expression and cumulative chitinase activity. Chitinase inhibition led to overexpression of chitinases, ecdysteroid biosynthesis, and responsive genes. SfCht5 silencing and overexpression resulted in ecdysone receptor deregulation. Transcription factors, like Broad Complex Z4, regulate the ecdysteroid metabolism and showed high expression upon berberine ingestion. Broad Complex Z4 binding in 5' UTR of Ecdysone receptor, SfCht5, Chitinase 7, Phantom, Neverland, and other ecdysteroid biosynthesis genes might lead to their upregulation in berberine-fed insects. As a result, berberine-fed insects showed ecdysone overaccumulation. These findings underscore chitinase activity's impact on ecdysone biosynthesis and its transcriptional crosstalk.

Keywords: Biological sciences; Microbial metabolism.