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Alternative polyadenylation coordinates embryonic development, sexual dimorphism and longitudinal growth in Xenopus tropicalis

  • Xiang Zhou
  • Yangzi Zhang
  • Jennifer J. Michal
  • Lujiang Qu
  • Shuwen Zhang
  • Mark R. Wildung
  • Weiwei Du
  • Derek J. Pouchnik
  • Hui Zhao
  • Yin Xia
  • Honghua Shi
  • Guoli Ji
  • Jon F. Davis
  • Gary D. Smith
  • Michael D. Griswold
  • Richard M. Harland
  • Zhihua JiangEmail author
Original Article

Abstract

RNA alternative polyadenylation contributes to the complexity of information transfer from genome to phenome, thus amplifying gene function. Here, we report the first X. tropicalis resource with 127,914 alternative polyadenylation (APA) sites derived from embryos and adults. Overall, APA networks play central roles in coordinating the maternal–zygotic transition (MZT) in embryos, sexual dimorphism in adults and longitudinal growth from embryos to adults. APA sites coordinate reprogramming in embryos before the MZT, but developmental events after the MZT due to zygotic genome activation. The APA transcriptomes of young adults are more variable than growing adults and male frog APA transcriptomes are more divergent than females. The APA profiles of young females were similar to embryos before the MZT. Enriched pathways in developing embryos were distinct across the MZT and noticeably segregated from adults. Briefly, our results suggest that the minimal functional units in genomes are alternative transcripts as opposed to genes.

Keywords

Whole transcriptome termini site sequencing (WTTS-seq) Gene biotypes APA site types Genomic neighborhoods RNA origin 

Notes

Acknowledgements

This work was supported by the Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health under Award Number R21HD076845 and the National Institute of Food and Agriculture, United States Department of Agriculture under Award number 2016-67015-24470 to ZJ. Development of bioinformatics pipelines for the data analysis at Xiamen University, China was supported by the National Science Foundation of China under Award number 61573296 to GJ.

Compliance with ethical standards

Conflict of interest

We have filed a provisional patent for our WTSS-seq method.

Supplementary material

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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Xiang Zhou
    • 1
    • 9
  • Yangzi Zhang
    • 1
  • Jennifer J. Michal
    • 1
  • Lujiang Qu
    • 1
    • 10
  • Shuwen Zhang
    • 1
  • Mark R. Wildung
    • 2
  • Weiwei Du
    • 2
  • Derek J. Pouchnik
    • 2
  • Hui Zhao
    • 3
  • Yin Xia
    • 3
  • Honghua Shi
    • 4
  • Guoli Ji
    • 5
  • Jon F. Davis
    • 6
  • Gary D. Smith
    • 7
  • Michael D. Griswold
    • 2
  • Richard M. Harland
    • 8
  • Zhihua Jiang
    • 1
    Email author
  1. 1.Department of Animal Sciences and Center for Reproductive BiologyWashington State UniversityPullmanUSA
  2. 2.Laboratory for Biotechnology and Bioanalysis, Center for Reproductive BiologyWashington State UniversityPullmanUSA
  3. 3.School of Biomedical Sciences, Faculty of MedicineThe Chinese University of Hong KongHong KongChina
  4. 4.State Key Laboratory of Estuarine and Coastal ResearchEast China Normal UniversityShanghaiChina
  5. 5.Department of AutomationXiamen UniversityXiamenChina
  6. 6.Department of Integrative Physiology and NeuroscienceWashington State UniversityPullmanUSA
  7. 7.Departments of OB/GYN, Physiology, and UrologyUniversity of MichiganAnn ArborUSA
  8. 8.Department of Molecular and Cell BiologyUniversity of California BerkeleyBerkeleyUSA
  9. 9.College of Animal Sciences and Veterinary MedicineHuazhong Agricultural UniversityWuhanChina
  10. 10.College of Animal Sciences and TechnologyChina Agricultural UniversityBeijingChina

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