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

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

doi:10.3389/fpls.2022.1037784

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

Front Plant Sci. 2023 Jan 9:13:1037784. doi: 10.3389/fpls.2022.1037784. eCollection 2022.

Authors

Yuanyuan Xu^{1

2

3}, Jiming Liu^{1

2

3}, Xiangqin Ji⁴, Guochun Zhao^{1

2

3}, Tianyun Zhao^{1

2

3}, Xin Wang^{1

2

3}, Lixian Wang^{1

2

3}, Shilun Gao^{1

2

3}, Yingying Hao^{1

2

3}, Yuhan Gao^{1

2

3}, Yuan Gao⁵, Xuehuang Weng⁶, Liming Jia^{1

2

3}, Zhong Chen^{1

2

3

7}

Affiliations

¹ Key Laboratory of Silviculture and Conservation of the Ministry of Education, College of Forestry, Beijing Forestry University, Beijing, China.
² National Energy R&D Center for Non-food Biomass, Beijing Forestry University, Beijing, China.
³ National Innovation Alliance of Sapindus Industry, Beijing Forestry University, Beijing, China.
⁴ Bioinformatics Analysis Department, Hangzhou KaiTai Biotechnology Co., Ltd, Hangzhou, Zhejiang, China.
⁵ Planning and Design Institute of Forest Products Industry, National Forestry and Grassland Administration, Beijing, China.
⁶ Research and Development Department, Yuanhua Forestry Biological Technology Co., Ltd., Sanming, Fujian, China.
⁷ Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.

Abstract

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.

Keywords: Sapindus mukorossi; biosynthesis; coexpression network; miRNA; triterpenoid saponin.

Grants and funding

This work was supported by the National Natural Science Foundation of China (No. 32071793) and the Special Foundation for National Science and Technology Basic Research Program of China (No. 2019FY100803).