Skip to main content
SpringerLink
Log in

Endophytic fungus, Fusarium sp. reduces alternative splicing events in rice plants under salinity stress

  • Original Article
  • Published:
Plant Physiology Reports Aims and scope Submit manuscript

Abstract

Alternative splicing (AS) of transcripts is a well-recognized phenomenon in plants. Several studies have shown that the frequency of AS events are significantly enhanced in plants subjected to abiotic stresses, presumably as an adaptation to increase transcript diversity. In this study, we examine the effect of a salt tolerant endophytic fungus, Fusarium sp. on the AS events of IR-64 rice plants, under salinity stress. RNA seq data generated from rice plants, treated and not treated with Fusarium sp. respectively and subjected to 150 mM salinity stress was used to analyze the number and type of AS events and their chromosomal distribution using approriate bioinformatics pipeline. Besides, we also annotated the locus IDs of genes for gene enrichment and KEGG pathway analysis. Our results show an unequivocal decrease in the number of AS events under salinity stress as influenced by the endophyte. The average AS events per gene also decreased from 2.28 to 2.11 upon colonization by the endophyte. This is the first documented evidence of an endophyte-induced alteration in the frequency of alternative splicing event in plants subjected to salinity stress. The exact mechanisms through which the splicing activities are restrained, however need to be further investigated.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Afridi, M. S., Mahmood, T., Salam, A., Mukhtar, T., Mehmood, S., Ali, J., et al. (2019). Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiology and Biochemistry,139, 569–577.

    Article  CAS  Google Scholar 

  • Arshad, M., Gruber, M. Y., Wall, K., & Hannoufa, A. (2017). An insight into microRNA156 role in salinity stress responses of alfalfa. Frontiers in Plant Science,8, 356.

    Article  Google Scholar 

  • Ashwini, N., Sajeevan, R. S., Udayakumar, M., & Nataraja, K. N. (2018). Identification of splice variant of OsGBF1 in Oryza sativa ssp. indica genotypes under salinity stress. 3 Biotech,8(8), 345.

    Article  Google Scholar 

  • Azad, K., & Kaminskyj, S. (2016). A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis,68(1–3), 73–78.

    Article  CAS  Google Scholar 

  • Berget, S. M., Moore, C., & Sharp, P. A. (1977). Spliced segments at the 5′ terminus of adenovirus 2 late mRNA. Proceedings of the National Academy of Sciences,74(8), 3171–3175.

    Article  CAS  Google Scholar 

  • Chaudhary, S., Khokhar, W., Jabre, I., Reddy, A. S., Byrne, L. J., Wilson, C. M., et al. (2019). Alternative splicing and protein diversity: Plants versus animals. Frontiers in Plant Science,10, 708.

    Article  Google Scholar 

  • Ding, F., Cui, P., Wang, Z., Zhang, S., Ali, S., & Xiong, L. (2014). Genome-wide analysis of alternative splicing of pre-mRNA under salt stress in Arabidopsis. BMC Genomics,15(1), 431. https://doi.org/10.1186/1471-2164-15-431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doktor, T., Heintz, C., Andresen, B., & Mair, W. (2018). Alternative splicing analysis of RNA-seq data using SAJR. Protocol Exchange,. https://doi.org/10.1038/protex.2018.029.

    Article  Google Scholar 

  • Drechsel, G., Kahles, A., Kesarwani, A. K., Stauffer, E., Behr, J., Drewe, P., et al. (2013). Nonsense-mediated decay of alternative precursor mRNA splicing variants is a major determinant of the Arabidopsis steady state transcriptome. The Plant Cell,25(10), 3726–3742.

    Article  CAS  Google Scholar 

  • Du, Z., Zhou, X., Ling, Y., Zhang, Z., & Su, Z. (2010). agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Research,38(Suppl_2), W64–W70.

    Article  CAS  Google Scholar 

  • Duque, P. (2011). A role for SR proteins in plant stress responses. Plant Signaling and Behavior,6(1), 49–54.

    Article  CAS  Google Scholar 

  • Filichkin, S. A., Cumbie, J. S., Dharmawardhana, P., Jaiswal, P., Chang, J. H., Palusa, S. G., et al. (2015). Environmental stresses modulate abundance and timing of alternatively spliced circadian transcripts in Arabidopsis. Molecular Plant,8(2), 207–227.

    Article  CAS  Google Scholar 

  • Jan, F. G., Hamayun, M., Hussain, A., Jan, G., Iqbal, A., Khan, A., et al. (2019). An endophytic isolate of the fungus Yarrowia lipolytica produces metabolites that ameliorate the negative impact of salt stress on the physiology of maize. BMC Microbiology,19(1), 3.

    Article  Google Scholar 

  • Jiang, J., Liu, X., Liu, C., Liu, G., Li, S., & Wang, L. (2017). Integrating omics and alternative splicing reveals insights into grape response to high temperature. Plant Physiology,173(2), 1502–1518. https://doi.org/10.1104/pp.16.01305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalyna, M., Simpson, C. G., Syed, N. H., Lewandowska, D., Marquez, Y., Kusenda, B., et al. (2011). Alternative splicing and nonsense-mediated decay modulate expression of important regulatory genes in Arabidopsis. Nucleic Acids Research,40(6), 2454–2469.

    Article  Google Scholar 

  • Laloum, T., Martín, G., & Duque, P. (2018). Alternative splicing control of abiotic stress responses. Trends in Plant Science,23(2), 140–150.

    Article  CAS  Google Scholar 

  • Lanza, M., Haro, R., Conchillo, L. B., & Benito, B. (2019). The endophyte Serendipita indica reduces the sodium content of Arabidopsis plants exposed to salt stress: Fungal ENA ATPases are expressed and regulated at high pH and during plant co-cultivation in salinity. Environmental Microbiology. https://doi.org/10.1111/1462-2920.14619.

    Article  PubMed  Google Scholar 

  • Lewis, B. P., Green, R. E., & Brenner, S. E. (2003). Evidence for the widespread coupling of alternative splicing and nonsense-mediated mRNA decay in humans. Proceedings of the National Academy of Sciences,100(1), 189–192.

    Article  CAS  Google Scholar 

  • Li, Y., Breitling, R., Snoek, L. B., van der Velde, K. J., Swertz, M. A., Riksen, J., et al. (2010). Global genetic robustness of the alternative splicing machinery in Caenorhabditis elegans. Genetics, 186(1), 405–410.

    Article  CAS  Google Scholar 

  • Mazin, P., Xiong, J., Liu, X., Yan, Z., Zhang, X., Li, M., et al. (2013). Widespread splicing changes in human brain development and aging. Molecular Systems Biology,9(1), 633.

    Article  Google Scholar 

  • Ner-Gaon, H., Halachmi, R., Savaldi-Goldstein, S., Rubin, E., Ophir, R., & Fluhr, R. (2004). Intron retention is a major phenomenon in alternative splicing in Arabidopsis. The Plant Journal,39(6), 877–885.

    Article  CAS  Google Scholar 

  • Ottens, F., & Gehring, N. H. (2016). Physiological and pathophysiological role of nonsense-mediated mRNA decay. Pflügers Archiv-European Journal of Physiology,468(6), 1013–1028.

    Article  CAS  Google Scholar 

  • Pan, X., Qin, Y., & Yuan, Z. (2018). Potential of a halophyte-associated endophytic fungus for sustaining Chinese white poplar growth under salinity. Symbiosis,76(2), 109–116.

    Article  CAS  Google Scholar 

  • Reddy, A. S., Marquez, Y., Kalyna, M., & Barta, A. (2013). Complexity of the alternative splicing landscape in plants. The Plant Cell, 25(10), 3657–3683.

    Article  CAS  Google Scholar 

  • Rho, H., Hsieh, M., Kandel, S. L., Cantillo, J., Doty, S. L., & Kim, S.-H. (2018). Do endophytes promote growth of host plants under stress? A meta-analysis on plant stress mitigation by endophytes. Microbial Ecology,75(2), 407–418.

    Article  Google Scholar 

  • Rodriguez, R. J., Henson, J., Van Volkenburgh, E., Hoy, M., Wright, L., Beckwith, F., et al. (2008). Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal,2(4), 404.

    Article  Google Scholar 

  • Sablok, G., Gupta, P. K., Baek, J.-M., Vazquez, F., & Min, X. J. (2011). Genome-wide survey of alternative splicing in the grass Brachypodium distachyon: a emerging model biosystem for plant functional genomics. Biotechnology letters, 33(3), 629–636.

    Article  CAS  Google Scholar 

  • Sangamesh, M. B., Jambagi, S., Vasanthakumari, M. M., Shetty, N. J., Kolte, H., Ravikanth, G., et al. (2018). Thermotolerance of fungal endophytes isolated from plants adapted to the Thar Desert, India. Symbiosis,75(2), 135–147.

    Article  Google Scholar 

  • Supek, F., Bošnjak, M., Škunca, N., & Šmuc, T. (2011). REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE,6(7), e21800.

    Article  CAS  Google Scholar 

  • Syed, N. H., Kalyna, M., Marquez, Y., Barta, A., & Brown, J. W. (2012). Alternative splicing in plants—Coming of age. Trends in Plant Science,17(10), 616–623.

    Article  CAS  Google Scholar 

  • Yun, B.-W., Spoel, S. H., & Loake, G. J. (2012). Synthesis of and signalling by small, redox active molecules in the plant immune response. Biochimica et Biophysica Acta (BBA)-General Subjects,1820(6), 770–776.

    Article  CAS  Google Scholar 

  • Zhang, T., Huang, L., Wang, Y., Wang, W., Zhao, X., Zhang, S., et al. (2017). Differential transcriptome profiling of chilling stress response between shoots and rhizomes of Oryza longistaminata using RNA sequencing. PLoS ONE,12(11), e0188625. https://doi.org/10.1371/journal.pone.0188625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, G., Li, W., Zhang, F., & Guo, W. (2018). RNA-seq analysis reveals alternative splicing under salt stress in cotton, Gossypium davidsonii. BMC Genomics,19(1), 73.

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Rice Research Station, Vytilla, Kerala Agricultural University, Kerala, India for access to the Pokkali land race.

Funding

The work was supported by Grants from the Department of Biotechnology, New Delhi Project on “Chemical Ecology of the North East Region (NER) of India: A collaborative programme Linking NER and Bangalore Researchers” (DBT-NER/Agri/24/2013). RUS was supported by an ICAR Emeritus Scientist Grant.

Author information

Authors and Affiliations

  1. School of Ecology and Conservation, University of Agricultural Sciences, GKVK, Bangalore, 560065, India

    Megha H. Sampangi-Ramaiah & R. Uma Shaanker

  2. Division of Biotechnology, ICAR - Indian Institute of Horticultural Research, Hessaraghatta Lake Post, Bangalore, 560089, India

    Kundapura V. Ravishankar

  3. Department of Crop Physiology, University of Agricultural Sciences, GKVK, Bangalore, 560065, India

    Karaba N. Nataraja & R. Uma Shaanker

  4. Ashoka Trust for Research in Ecology and the Environment, Royal Enclave, Srirampura, Jakkur Post, Bangalore, 560064, India

    R. Uma Shaanker

Authors
  1. Megha H. Sampangi-Ramaiah
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kundapura V. Ravishankar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karaba N. Nataraja
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. R. Uma Shaanker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Megha H. Sampangi-Ramaiah.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sampangi-Ramaiah, M.H., Ravishankar, K.V., Nataraja, K.N. et al. Endophytic fungus, Fusarium sp. reduces alternative splicing events in rice plants under salinity stress. Plant Physiol. Rep. 24, 487–495 (2019). https://doi.org/10.1007/s40502-019-00487-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40502-019-00487-3

Keywords

Search

Navigation