Integrative analysis of microRNAs and mRNAs reveals the regulatory networks of triterpenoid saponin metabolism in Soapberry (Sapindus mukorossi Gaertn.)

Yuanyuan Xu; Yuanyuan Xu; Yuanyuan Xu; Jiming Liu; Jiming Liu; Jiming Liu; Xiangqin Ji; Guochun Zhao; Guochun Zhao; Guochun Zhao; Tianyun Zhao; Tianyun Zhao; Tianyun Zhao; Xin Wang; Xin Wang; Xin Wang; Lixian Wang; Lixian Wang; Lixian Wang; Shilun Gao; Shilun Gao; Shilun Gao; Yingying Hao; Yingying Hao; Yingying Hao; Yuhan Gao; Yuhan Gao; Yuhan Gao; Yuan Gao; Xuehuang Weng; Liming Jia; Liming Jia; Liming Jia; Zhong Chen; Zhong Chen; Zhong Chen; Zhong Chen

doi:10.3389/fpls.2022.1037784

Frontiers in Plant Science (Jan 2023)

Integrative analysis of microRNAs and mRNAs reveals the regulatory networks of triterpenoid saponin metabolism in Soapberry (Sapindus mukorossi Gaertn.)

Yuanyuan Xu,
Yuanyuan Xu,
Yuanyuan Xu,
Jiming Liu,
Jiming Liu,
Jiming Liu,
Xiangqin Ji,
Guochun Zhao,
Guochun Zhao,
Guochun Zhao,
Tianyun Zhao,
Tianyun Zhao,
Tianyun Zhao,
Xin Wang,
Xin Wang,
Xin Wang,
Lixian Wang,
Lixian Wang,
Lixian Wang,
Shilun Gao,
Shilun Gao,
Shilun Gao,
Yingying Hao,
Yingying Hao,
Yingying Hao,
Yuhan Gao,
Yuhan Gao,
Yuhan Gao,
Yuan Gao,
Xuehuang Weng,
Liming Jia,
Liming Jia,
Liming Jia,
Zhong Chen,
Zhong Chen,
Zhong Chen,
Zhong Chen

Affiliations

Yuanyuan Xu: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Yuanyuan Xu: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Yuanyuan Xu: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Jiming Liu: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Jiming Liu: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Jiming Liu: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Xiangqin Ji: Bioinformatics Analysis Department, Hangzhou KaiTai Biotechnology Co., Ltd, Hangzhou, Zhejiang, China
Guochun Zhao: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Guochun Zhao: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Guochun Zhao: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Tianyun Zhao: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Tianyun Zhao: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Tianyun Zhao: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Xin Wang: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Xin Wang: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Xin Wang: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Lixian Wang: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Lixian Wang: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Lixian Wang: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Shilun Gao: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Shilun Gao: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Shilun Gao: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Yingying Hao: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Yingying Hao: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Yingying Hao: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Yuhan Gao: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Yuhan Gao: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Yuhan Gao: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Yuan Gao: Planning and Design Institute of Forest Products Industry, National Forestry and Grassland Administration, Beijing, China
Xuehuang Weng: Research and Development Department, Yuanhua Forestry Biological Technology Co., Ltd., Sanming, Fujian, China
Liming Jia: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Liming Jia: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Liming Jia: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Zhong Chen: Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China
Zhong Chen: National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China
Zhong Chen: National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China
Zhong Chen: Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China

DOI: https://doi.org/10.3389/fpls.2022.1037784
Journal volume & issue: Vol. 13

Abstract

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Triterpenoid saponin are important secondary metabolites and bioactive constituents of soapberry (Sapindus mukorossi Gaertn.) and are widely used in medicine and toiletry products. However, little is known about the roles of miRNAs in the regulation of triterpenoid saponin biosynthesis in soapberry. In this study, a total of 3036 miRNAs were identified, of which 1372 miRNAs were differentially expressed at different stages of pericarp development. Important KEGG pathways, such as terpenoid backbone biosynthesis, sesquiterpenoid and triterpenoid biosynthesis, and basal transcription factors were highlighted, as well the roles of some key miRNAs, such as ath-miR5021, han-miR3630-3p, and ppe-miR858, which may play important roles in regulating triterpenoid saponin biosynthesis. In addition, 58 miRNAs might participate in saponin biosynthesis pathways by predicting the targets of those miRNAs to 53 saponin biosynthesis structural genes. And 75 miRNAs were identified to potentially play vital role in saponin accumulation by targeting transcript factor genes, bHLH, bZIP, ERF, MYB, and WRKY, respectively, which are candidate regulatory genes in the pathway of saponin biosynthesis. The results of weighted gene coexpression network analysis (WGCNA) suggested that two saponin-specific miRNA modules and 10 hub miRNAs may participate in saponin biosynthesis. Furthermore, multiple miRNA–mRNA regulatory networks potentially involved in saponin biosynthesis were generated, e.g., ath-miR5021–SmIDI2/SmGPS5/SmbAS1/SmCYP71D-3/SmUGT74G-2, han-miR3630-3p–SmCYP71A-14/SmbHLH54/SmMYB135/SmWRKY32, and ppe-miR858–SmMYB5/SmMYB32. qRT-PCR analysis validated the expression patterns of nine miRNAs and 12 corresponding target genes. This study represents the first comprehensive analysis of miRNAs in soapberry and lays the foundation for further understanding of miRNA-based regulation in triterpenoid saponin biosynthesis.

Published in Frontiers in Plant Science

ISSN: 1664-462X (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Agriculture: Plant culture
Website: https://www.frontiersin.org/journals/plant-science

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