Skip to main content
Log in

Plant Intron-Splicing Efficiency Database (PISE): exploring splicing of ∼1,650,000 introns in Arabidopsis, maize, rice, and soybean from ∼57,000 public RNA-seq libraries

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Intron retention is the most common alternative splicing event in plants and plays a crucial role in the responses of plants to environmental signals. Despite a large number of RNA-seq libraries from different treatments and genetic mutants stored in public domains, a resource for querying the intron-splicing ratio of individual intron is still required. Here, we established the first-ever large-scale splicing efficiency database in any organism. Our database includes over 57,000 plant public RNA-seq libraries, comprising 25,283 from Arabidopsis, 17,789 from maize, 10,710 from rice, and 3,974 from soybean, and covers a total of 1.6 million introns in these four species. In addition, we manually curated and annotated all the mutant- and treatment-related libraries as well as their matched controls included in our library collection, and added graphics to display intron-splicing efficiency across various tissues, developmental stages, and stress-related conditions. The result is a large collection of 3,313 treatment conditions and 3,594 genetic mutants for discovering differentially regulated splicing efficiency. Our online database can be accessed at https://plantintron.com/.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Chamala, S., Feng, G., Chavarro, C., and Barbazuk, W.B. (2015). Genome-wide identification of evolutionarily conserved alternative splicing events in flowering plants. Front Bioeng Biotechnol 3, 33.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaudhary, S., Khokhar, W., Jabre, I., Reddy, A.S.N., Byrne, L.J., Wilson, C.M., and Syed, N.H. (2019). Alternative splicing and protein diversity: plants versus animals. Front Plant Sci 10, 708.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng, C., Wang, Z., Yuan, B., and Li, X. (2017). RBM25 mediates abiotic responses in plants. Front Plant Sci 8.

  • Deng, X., Lu, T., Wang, L., Gu, L., Sun, J., Kong, X., Liu, C., and Cao, X. (2016). Recruitment of the NineTeen complex to the activated spliceosome requires AtPRMT5. Proc Natl Acad Sci USA 113, 5447–5452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, C., He, F., Berkowitz, O., Liu, J., Cao, P., Tang, M., Shi, H., Wang, W., Li, Q., Shen, Z., et al. (2018). Alternative splicing plays a critical role in maintaining mineral nutrient homeostasis in rice (Oryza sativa). Plant Cell 30, 2267–2285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filichkin, S.A., Hamilton, M., Dharmawardhana, P.D., Singh, S.K., Sullivan, C., Ben-Hur, A., Reddy, A.S.N., and Jaiswal, P. (2018). Abiotic stresses modulate landscape of poplar transcriptome via alternative splicing, differential intron retention, and isoform ratio switching. Front Plant Sci 9, 5.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jacob, A.G., and Smith, C.W.J. (2017). Intron retention as a component of regulated gene expression programs. Hum Genet 136, 1043–1057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, J., Long, Y., Zhang, H., Li, Z., Liu, Z., Zhao, Y., Lu, D., Jin, X., Deng, X., Xia, R., et al. (2020). Post-transcriptional splicing of nascent RNA contributes to widespread intron retention in plants. Nat Plants 6, 780–788.

    Article  CAS  PubMed  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., and Muñoz, M.J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat Rev Mol Cell Biol 14, 153–165.

    Article  CAS  PubMed  Google Scholar 

  • Laloum, T., Martín, G., and Duque, P. (2018). Alternative splicing control of abiotic stress responses. Trends Plant Sci 23, 140–150.

    Article  CAS  PubMed  Google Scholar 

  • Lee, S.K., Eom, J.S., Hwang, S.K., Shin, D., An, G., Okita, T.W., and Jeon, J.S. (2016). Plastidic phosphoglucomutase and ADP-glucose pyrophosphorylase mutants impair starch synthesis in rice pollen grains and cause male sterility. J Exp Bot 67, 5557–5569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15, 550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Marquez, Y., Brown, J.W.S., Simpson, C., Barta, A., and Kalyna, M. (2012). Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22, 1184–1195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martín, G., Márquez, Y., Mantica, F., Duque, P., and Irimia, M. (2021). Alternative splicing landscapes in Arabidopsis thaliana across tissues and stress conditions highlight major functional differences with animals. Genome Biol 22, 35.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mei, W., Boatwright, L., Feng, G., Schnable, J.C., and Barbazuk, W.B. (2017a). Evolutionarily conserved alternative splicing across monocots. Genetics 207, 465–480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mei, W., Liu, S., Schnable, J.C., Yeh, C.T., Springer, N.M., Schnable, P.S., and Barbazuk, W.B. (2017b). A comprehensive analysis of alternative splicing in paleopolyploid maize. Front Plant Sci 8, 694.

    Article  PubMed  PubMed Central  Google Scholar 

  • Middleton, R., Gao, D., Thomas, A., Singh, B., Au, A., Wong, J.J.L., Bomane, A., Cosson, B., Eyras, E., Rasko, J.E.J., et al. (2017). IRFinder: assessing the impact of intron retention on mammalian gene expression. Genome Biol 18, 51.

    Article  PubMed  PubMed Central  Google Scholar 

  • Reddy, A.S.N., Marquez, Y., Kalyna, M., and Barta, A. (2013). Complexity of the alternative splicing landscape in plants. Plant Cell 25, 3657–3683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson, J.T., Thorvaldsdóttir, H., Wenger, A.M., Zehir, A., and Mesirov, J.P. (2017). Variant review with the integrative genomics viewer. Cancer Res 77, e31–e34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, Q.A., Catlin, N.S., Brad Barbazuk, W., and Li, S. (2019). Computational analysis of alternative splicing in plant genomes. Gene 685, 186–195.

    Article  CAS  PubMed  Google Scholar 

  • Staiger, D., and Brown, J.W.S. (2013). Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 25, 3640–3656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Syed, N.H., Kalyna, M., Marquez, Y., Barta, A., and Brown, J.W.S. (2012). Alternative splicing in plants—coming of age. Trends Plant Sci 17, 616–623.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szcześniak, M.W., Kabza, M., Pokrzywa, R., Gudyś, A., and Makalowska, I. (2013). Erisdb: a database of plant splice sites and splicing signals. Plant Cell Physiol 54, e10.

    Article  PubMed  Google Scholar 

  • Tu, Y.T., Chen, C.Y., Huang, Y.S., Chang, C.H., Yen, M.R., Hsieh, J.W.A., Chen, P.Y., and Wu, K. (2022). HISTONE DEACETYLASE 15 and MOS4-associated complex subunits 3A/3B coregulate intron retention of ABA-responsive genes. Plant Physiol 190, 882–897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vicente, J., Mendiondo, G.M., Pauwels, J., Pastor, V., Izquierdo, Y., Naumann, C., Movahedi, M., Rooney, D., Gibbs, D.J., Smart, K., et al. (2019). Distinct branches of the N-end rule pathway modulate the plant immune response. New Phytol 221, 988–1000.

    Article  CAS  PubMed  Google Scholar 

  • Wang, B.B., and Brendel, V. (2006). Genomewide comparative analysis of alternative splicing in plants. Proc Natl Acad Sci USA 103, 7175–7180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, X., Hu, L., Wang, X., Li, N., Xu, C., Gong, L., and Liu, B. (2016). DNA methylation affects gene alternative splicing in plants: an example from rice. Mol Plant 9, 305–307.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z., Ji, H., Yuan, B., Wang, S., Su, C., Yao, B., Zhao, H., and Li, X. (2015). ABA signalling is fine-tuned by antagonistic HAB1 variants. Nat Commun 6, 8138.

    Article  PubMed  Google Scholar 

  • Wei, G., Liu, K., Shen, T., Shi, J., Liu, B., Han, M., Peng, M., Fu, H., Song, Y., Zhu, J., et al. (2018). Position-specific intron retention is mediated by the histone methyltransferase SDG725. BMC Biol 16, 44.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu, Y., Zhang, H., Long, Y., Shu, Y., and Zhai, J. (2022). Plant Public RNA-seq Database: a comprehensive online database for expression analysis of ∼45000 plant public RNA-Seq libraries. Plant Biotechnol J 20, 806–808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhan, X., Qian, B., Cao, F., Wu, W., Yang, L., Guan, Q., Gu, X., Wang, P., Okusolubo, T.A., Dunn, S.L., et al. (2015). An Arabidopsis PWI and RRM motif-containing protein is critical for pre-mRNA splicing and aba responses. Nat Commun 6, 8139.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H., Zhang, F., Yu, Y., Feng, L., Jia, J., Liu, B., Li, B., Guo, H., and Zhai, J. (2020). A comprehensive online database for exploring ∼20,000 public Arabidopsis RNA-Seq libraries. Mol Plant 13, 1231–1233.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, R., Calixto, C.P.G., Marquez, Y., Venhuizen, P., Tzioutziou, N.A., Guo, W., Spensley, M., Entizne, J.C., Lewandowska, D., Ten Have, S., et al. (2017). A high quality Arabidopsis transcriptome for accurate transcript-level analysis of alternative splicing. Nucl Acids Res 45, 5061–5073.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Z., Zhang, S., Zhang, Y., Wang, X., Li, D., Li, Q., Yue, M., Li, Q., Zhang, Y., Xu, Y., et al. (2011). Arabidopsis floral initiator SKB1 confers high salt tolerance by regulating transcription and pre-mRNA splicing through altering histone H4R3 and small nuclear ribonucleoprotein LSM4 methylation. Plant Cell 23, 396–411.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the research groups that contributed RNA-seq data to the community, and we regret not being able to cite all the related papers in the main text owing to space constraints. References for all libraries used are listed in PISE ‘All Libraries’. Computation was supported by Center for Computational Science and Engineering at Southern University of Science and Technology. The group of J.Z. was supported by the National Key R&D Program of China (2019YFA0903903), the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (2016ZT06S172), the Shenzhen Sci-Tech Fund (KYTDPT20181011104005), the Key Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes (2019KSYS006), and the Stable Support Plan Program of Shenzhen Natural Science Fund (20200925153345004). J.J. was supported by the National Natural Science Foundation of China (32100444) and the Shenzhen Fundamental Research Program (JCYJ20210324105202007).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jixian Zhai.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, H., Jia, J. & Zhai, J. Plant Intron-Splicing Efficiency Database (PISE): exploring splicing of ∼1,650,000 introns in Arabidopsis, maize, rice, and soybean from ∼57,000 public RNA-seq libraries. Sci. China Life Sci. 66, 602–611 (2023). https://doi.org/10.1007/s11427-022-2193-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-022-2193-3

Navigation