A lineage-resolved cartography of microRNA promoter activity in C. elegans empowers multidimensional developmental analysis

Weina Xu, Jinyi Liu, Huan Qi, Ruolin Si, Zhiguang Zhao, Zhiju Tao, Yuchuan Bai, Shipeng Hu, Xiaohan Sun, Yulin Cong, Haoye Zhang, Duchangjiang Fan, Long Xiao, Yangyang Wang, Yongbin Li () and Zhuo Du ()
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Weina Xu: Chinese Academy of Sciences
Jinyi Liu: Chinese Academy of Sciences
Huan Qi: Chinese Academy of Sciences
Ruolin Si: Capital Normal University
Zhiguang Zhao: Chinese Academy of Sciences
Zhiju Tao: Capital Normal University
Yuchuan Bai: Capital Normal University
Shipeng Hu: Capital Normal University
Xiaohan Sun: Chinese Academy of Sciences
Yulin Cong: Chinese Academy of Sciences
Haoye Zhang: Chinese Academy of Sciences
Duchangjiang Fan: Chinese Academy of Sciences
Long Xiao: Chinese Academy of Sciences
Yangyang Wang: Chinese Academy of Sciences
Yongbin Li: Capital Normal University
Zhuo Du: Chinese Academy of Sciences

Nature Communications, 2024, vol. 15, issue 1, 1-23

Abstract: Abstract Elucidating the expression of microRNAs in developing single cells is critical for functional discovery. Here, we construct scCAMERA (single-cell cartography of microRNA expression based on reporter assay), utilizing promoter-driven fluorescent reporters in conjunction with imaging and lineage tracing. The cartography delineates the transcriptional activity of 54 conserved microRNAs in lineage-resolved single cells throughout C. elegans embryogenesis. The combinatorial expression of microRNAs partitions cells into fine clusters reflecting their function and anatomy. Notably, the expression of individual microRNAs exhibits high cell specificity and divergence among family members. Guided by cellular expression patterns, we identify developmental functions of specific microRNAs, including miR-1 in pharynx development and physiology, miR-232 in excretory canal morphogenesis by repressing NHR-25/NR5A, and a functional synergy between miR-232 and miR-234 in canal development, demonstrating the broad utility of scCAMERA. Furthermore, integrative analysis reveals that tissue-specific fate determinants activate microRNAs to repress protein production from leaky transcripts associated with alternative, especially neuronal, fates, thereby enhancing the fidelity of developmental fate differentiation. Collectively, our study offers rich opportunities for multidimensional expression-informed analysis of microRNA biology in metazoans.

Date: 2024
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DOI: 10.1038/s41467-024-47055-4

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