ceRNA crosstalk mediated by ncRNAs is a novel regulatory mechanism in fish sex determination and differentiation [RESEARCH]

Lili Tang1,2, Fei Huang3, Wuxin You4, Ansgar Poetsch5,6,7, Rafael Henrique Nóbrega8, Deborah Mary Power9, Tengfei Zhu1,2, Kaiqiang Liu1,2, Hong-Yan Wang1,2, Qian Wang1,2, Xiwen Xu1,2, Bo Feng1,2, Manfred Schartl10,11 and Changwei Shao1,2 1Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, Shandong, 266071, China; 2Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, Shandong, 266237, China; 3Genosys, Incorporated, Shenzhen, Guangdong, 518000, China; 4NCU-QMUL Joint Research Institute of Precision Medical Sciences, Queen Mary School, Nanchang University, Nanchang, 330036, China; 5College of Marine Life Science, Ocean University of China, Qingdao, Shandong, 266003, China; 6Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, Shandong, 266237, China; 7Department of Plant Biochemistry, Ruhr University Bochum, Bochum, North Rhine-Westphalia, 44801, Germany; 8Institute of Biosciences Department of Structural and Functional Biology Division Morphology Reproductive and Molecular Biology Group, São Paulo State University, Botucatu, São Paulo, 01049-010, Brazil; 9Comparative Endocrinology and Integrative Biology, Centre of Marine Sciences, Universidade do Algarve, Campus de Gambelas, Faro, Algarve, 8005-139, Portugal; 10Developmental Biochemistry, Biocenter, University of Würzburg, Würzburg, Bayern, 97074, Germany; 11The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, San Marcos, Texas 78666, USA Corresponding authors: phch1biozentrum.uni-wuerzburg.de, shaocwysfri.ac.cn Abstract

Competing endogenous RNAs (ceRNAs) are vital regulators of gene networks in mammals. The involvement of noncoding RNAs (ncRNAs) as ceRNA in genotypic sex determination (GSD) and environmental sex determination (ESD) in fish is unknown. The Chinese tongue sole, which has both GSD and ESD mechanisms, was used to map the dynamic expression pattern of ncRNAs and mRNA in gonads during sex determination and differentiation. Transcript expression patterns shift during the sex differentiation phase, and ceRNA modulation occurs through crosstalk of differentially expressed long ncRNAs (lncRNAs), circular RNAs (circRNAs), microRNAs (miRNAs), and sex-related genes in fish. Of note was the significant up-regulation of a circRNA from the sex-determining gene dmrt1 (circular RNA dmrt1) and a lncRNA, called AMSDT (which stands for associated with male sex differentiation of tongue sole) in Chinese tongue sole testis. These two ncRNAs both share the same miRNA response elements with gsdf, which has an up-regulated expression when they bind to miRNA cse-miR-196 and concurrent down-regulated female sex-related genes to facilitate testis differentiation. This is the first demonstration in fish that ceRNA crosstalk mediated by ncRNAs modulates sexual development and unveils a novel regulatory mechanism for sex determination and differentiation.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.275962.121.

Freely available online through the Genome Research Open Access option.

Received July 2, 2021. Accepted June 29, 2022.

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