Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold

Abstract Nearly 10,000 plant species are represented by RNA-seq datasets in the NCBI sequence read archive, which are difficult to search in unassembled format due to database size. Here, we optimize RNA-seq assembly to transform most of this public RNA-seq data to a searchable database for biosynth...

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Main Authors: Xiaofeng Wang, Khadija Shafiq, Derrick A. Ousley, Desnor N. Chigumba, Dulciana Davis, Kali M. McDonough, Lisa S. Mydy, Jonathan Z. Sexton, Roland D. Kersten
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59428-4
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author Xiaofeng Wang
Khadija Shafiq
Derrick A. Ousley
Desnor N. Chigumba
Dulciana Davis
Kali M. McDonough
Lisa S. Mydy
Jonathan Z. Sexton
Roland D. Kersten
author_facet Xiaofeng Wang
Khadija Shafiq
Derrick A. Ousley
Desnor N. Chigumba
Dulciana Davis
Kali M. McDonough
Lisa S. Mydy
Jonathan Z. Sexton
Roland D. Kersten
author_sort Xiaofeng Wang
collection DOAJ
description Abstract Nearly 10,000 plant species are represented by RNA-seq datasets in the NCBI sequence read archive, which are difficult to search in unassembled format due to database size. Here, we optimize RNA-seq assembly to transform most of this public RNA-seq data to a searchable database for biosynthetic gene discovery. We test our transcriptome mining pipeline towards the diversification of moroidins, which are plant ribosomally-synthesized and posttranslationally-modified peptides (RiPPs) biosynthesized from copper-dependent peptide cyclases. Moroidins are bicyclic compounds with a conserved stephanotic acid scaffold, which becomes cytotoxic to non-small cell lung adenocarcinoma cells with an additional C-terminal macrocycle. We discover moroidin analogs with second ring structures diversified at the crosslink and the non-crosslinked residues including a moroidin analog from water chickweed, which exhibits higher cytotoxicity against lung adenocarcinoma cells than moroidin. Our study expands stephanotic acid-type peptides to grasses, Lowiaceae, mints, pinks, and spurges while demonstrating that large-scale transcriptome mining can broaden the medicinal chemistry toolbox for chemical and biological exploration of eukaryotic RiPP lead structures.
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spelling doaj-art-edb976804d364e47b9e37b5f7c49bd402025-08-20T02:15:11ZengNature PortfolioNature Communications2041-17232025-05-0116111810.1038/s41467-025-59428-4Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffoldXiaofeng Wang0Khadija Shafiq1Derrick A. Ousley2Desnor N. Chigumba3Dulciana Davis4Kali M. McDonough5Lisa S. Mydy6Jonathan Z. Sexton7Roland D. Kersten8Department of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganDepartment of Medicinal Chemistry, University of MichiganAbstract Nearly 10,000 plant species are represented by RNA-seq datasets in the NCBI sequence read archive, which are difficult to search in unassembled format due to database size. Here, we optimize RNA-seq assembly to transform most of this public RNA-seq data to a searchable database for biosynthetic gene discovery. We test our transcriptome mining pipeline towards the diversification of moroidins, which are plant ribosomally-synthesized and posttranslationally-modified peptides (RiPPs) biosynthesized from copper-dependent peptide cyclases. Moroidins are bicyclic compounds with a conserved stephanotic acid scaffold, which becomes cytotoxic to non-small cell lung adenocarcinoma cells with an additional C-terminal macrocycle. We discover moroidin analogs with second ring structures diversified at the crosslink and the non-crosslinked residues including a moroidin analog from water chickweed, which exhibits higher cytotoxicity against lung adenocarcinoma cells than moroidin. Our study expands stephanotic acid-type peptides to grasses, Lowiaceae, mints, pinks, and spurges while demonstrating that large-scale transcriptome mining can broaden the medicinal chemistry toolbox for chemical and biological exploration of eukaryotic RiPP lead structures.https://doi.org/10.1038/s41467-025-59428-4
spellingShingle Xiaofeng Wang
Khadija Shafiq
Derrick A. Ousley
Desnor N. Chigumba
Dulciana Davis
Kali M. McDonough
Lisa S. Mydy
Jonathan Z. Sexton
Roland D. Kersten
Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
Nature Communications
title Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
title_full Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
title_fullStr Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
title_full_unstemmed Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
title_short Large-scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
title_sort large scale transcriptome mining enables macrocyclic diversification and improved bioactivity of the stephanotic acid scaffold
url https://doi.org/10.1038/s41467-025-59428-4
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