Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)

Abstract Background Sturgeons (Acipenseriformes) are polyploid chondrostean fish that constitute an important model species for studying development and evolution in vertebrates. To better understand the mechanisms of reproduction regulation in sturgeon, this study combined PacBio isoform sequencing...

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Published in:Frontiers in Zoology
Main Authors: Xiujuan Zhang, Jiabin Zhou, Linmiao Li, Wenzhong Huang, Hafiz Ishfaq Ahmad, Huiming Li, Haiying Jiang, Jinping Chen
Format: Article
Language:English
Published: BMC 2020-04-01
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Online Access:http://link.springer.com/article/10.1186/s12983-020-00355-z
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author Xiujuan Zhang
Jiabin Zhou
Linmiao Li
Wenzhong Huang
Hafiz Ishfaq Ahmad
Huiming Li
Haiying Jiang
Jinping Chen
author_facet Xiujuan Zhang
Jiabin Zhou
Linmiao Li
Wenzhong Huang
Hafiz Ishfaq Ahmad
Huiming Li
Haiying Jiang
Jinping Chen
author_sort Xiujuan Zhang
collection DOAJ
container_title Frontiers in Zoology
description Abstract Background Sturgeons (Acipenseriformes) are polyploid chondrostean fish that constitute an important model species for studying development and evolution in vertebrates. To better understand the mechanisms of reproduction regulation in sturgeon, this study combined PacBio isoform sequencing (Iso-Seq) with Illumina short-read RNA-seq methods to discover full-length genes involved in early gametogenesis of the Amur sturgeon, Acipenser schrenckii. Results A total of 50.04 G subread bases were generated from two SMRT cells, and herein 164,618 nonredundant full-length transcripts (unigenes) were produced with an average length of 2782 bp from gonad tissues (three testes and four ovaries) from seven 3-year-old A. schrenckii individuals. The number of ovary-specific expressed unigenes was greater than those of testis (19,716 vs. 3028), and completely different KEGG pathways were significantly enriched between the ovary-biased and testis-biased DEUs. Importantly, 60 early gametogenesis-related genes (involving 755 unigenes) were successfully identified, and exactly 50% (30/60) genes of those showed significantly differential expression in testes and ovaries. Among these, the Amh and Gsdf with testis-biased expression, and the Foxl2 and Cyp19a with ovary-biased expression strongly suggested the important regulatory roles in spermatogenesis and oogenesis of A. schrenckii, respectively. We also found the four novel Sox9 transcript variants, which increase the numbers of regulatory genes and imply function complexity in early gametogenesis. Finally, a total of 236,672 AS events (involving 36,522 unigenes) were detected, and 10,556 putative long noncoding RNAs (lncRNAs) and 4339 predicted transcript factors (TFs) were also respectively identified, which were all significantly associated with the early gametogenesis of A. schrenckii. Conclusions Overall, our results provide new genetic resources of full-length transcription data and information as a genomic-level reference for sturgeon. Crucially, we explored the comprehensive genetic characteristics that differ between the testes and ovaries of A. schrenckii in the early gametogenesis stage, which could provide candidate genes and theoretical basis for further the mechanisms of reproduction regulation of sturgeon.
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spelling doaj-art-7d2b9704a68c48c19bbf1f0ae206d03c2025-08-19T20:57:54ZengBMCFrontiers in Zoology1742-99942020-04-0117112110.1186/s12983-020-00355-zFull-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)Xiujuan Zhang0Jiabin Zhou1Linmiao Li2Wenzhong Huang3Hafiz Ishfaq Ahmad4Huiming Li5Haiying Jiang6Jinping Chen7Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesGuangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Guangdong Institute of Applied Biological ResourcesAbstract Background Sturgeons (Acipenseriformes) are polyploid chondrostean fish that constitute an important model species for studying development and evolution in vertebrates. To better understand the mechanisms of reproduction regulation in sturgeon, this study combined PacBio isoform sequencing (Iso-Seq) with Illumina short-read RNA-seq methods to discover full-length genes involved in early gametogenesis of the Amur sturgeon, Acipenser schrenckii. Results A total of 50.04 G subread bases were generated from two SMRT cells, and herein 164,618 nonredundant full-length transcripts (unigenes) were produced with an average length of 2782 bp from gonad tissues (three testes and four ovaries) from seven 3-year-old A. schrenckii individuals. The number of ovary-specific expressed unigenes was greater than those of testis (19,716 vs. 3028), and completely different KEGG pathways were significantly enriched between the ovary-biased and testis-biased DEUs. Importantly, 60 early gametogenesis-related genes (involving 755 unigenes) were successfully identified, and exactly 50% (30/60) genes of those showed significantly differential expression in testes and ovaries. Among these, the Amh and Gsdf with testis-biased expression, and the Foxl2 and Cyp19a with ovary-biased expression strongly suggested the important regulatory roles in spermatogenesis and oogenesis of A. schrenckii, respectively. We also found the four novel Sox9 transcript variants, which increase the numbers of regulatory genes and imply function complexity in early gametogenesis. Finally, a total of 236,672 AS events (involving 36,522 unigenes) were detected, and 10,556 putative long noncoding RNAs (lncRNAs) and 4339 predicted transcript factors (TFs) were also respectively identified, which were all significantly associated with the early gametogenesis of A. schrenckii. Conclusions Overall, our results provide new genetic resources of full-length transcription data and information as a genomic-level reference for sturgeon. Crucially, we explored the comprehensive genetic characteristics that differ between the testes and ovaries of A. schrenckii in the early gametogenesis stage, which could provide candidate genes and theoretical basis for further the mechanisms of reproduction regulation of sturgeon.http://link.springer.com/article/10.1186/s12983-020-00355-zAmur sturgeon, Acipenser schrenckiiIsoform sequencingGonad transcriptomeEarly gametogenesis
spellingShingle Xiujuan Zhang
Jiabin Zhou
Linmiao Li
Wenzhong Huang
Hafiz Ishfaq Ahmad
Huiming Li
Haiying Jiang
Jinping Chen
Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
Amur sturgeon, Acipenser schrenckii
Isoform sequencing
Gonad transcriptome
Early gametogenesis
title Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
title_full Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
title_fullStr Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
title_full_unstemmed Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
title_short Full-length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of Amur sturgeon (Acipenser schrenckii)
title_sort full length transcriptome sequencing and comparative transcriptomic analysis to uncover genes involved in early gametogenesis in the gonads of amur sturgeon acipenser schrenckii
topic Amur sturgeon, Acipenser schrenckii
Isoform sequencing
Gonad transcriptome
Early gametogenesis
url http://link.springer.com/article/10.1186/s12983-020-00355-z
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