biologia plantarum

International journal on Plant Life established by Bohumil Nìmec in 1959

Biologia plantarum 64:104-109, 2020 | DOI: 10.32615/bp.2019.121

High-throughput sequencing reveals the change of microRNA expression caused by allopolyploidization in Cucumis

X. YU1,2, Z. ZHU1,2, T. ZHANG3, J. LI1,2, C. CHENG1,2, Q. LOU1,2, C.-O. OTTOSEN4, J. CHEN1,2,*
1 Nanjing Agricultural University, Nanjing,210095 P.R. China
2 National Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing, 210095 P.R. China
3 Shanghai Qingpu Vegetable Technology Promotion Station, Shanghai, 201799 P.R. China
4 Department of Food Science, Aarhus University, Aarhus, 8200 Denmark

Allopolyploidy is long recognized as an essential driving force in plant evolution. Recent studies have demonstrated that small RNAs, including microRNAs (miRNAs), play important roles in the process of allopolyploidy. However, the question that how the distinct parent-of-origin miRNAs are maintained in allopolyploids and how these small RNAs affect gene expression and phenotype remain to be answered. Therefore, we investigated the miRNA expression profiles of a synthesized allotetraploid, Cucumis ×hytivus and its parents. The different developmental stages of leaves of C.×hytivus showing contrasting leaf colour were compared as well. Following high-throughput sequencing, 546 conserved d 287 novel miRNAs were identified. The expressions of nine miRNAs obtained by real-time quantitative PCR were consistent with the sequencing results. We detected that 15 miRNAs were divergently expressed between the parent species, and 23 miRNAs were differentially expressed in C. ×hytivus compared to either of its parents or both, which suggests the significant effect of allopolyploidization on miRNAs accumulation. Additionally, 26 conserved and 13 novel miRNAs differed in expression between the young and mature leaves of C. ×hytivus, indicating an essential role of miRNA-mediated regulation of leaf development following allopolyploidization. This study enriches the context of allopolyploidy effect on miRNAs and lays a foundation for the elucidation of the miRNA-mediated regulatory mechanism in phenotypic variation in allopolyploids.

Keywords: cucumber, gene expression, leaf development, next-generation sequencing.

Received: March 21, 2019; Accepted: September 2, 2019; Published online: February 10, 2020  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
YU, X., ZHU, Z., ZHANG, T., LI, J., CHENG, C., LOU, Q., OTTOSEN, C.-O., & CHEN, J. (2020). High-throughput sequencing reveals the change of microRNA expression caused by allopolyploidization in Cucumis. Biologia plantarum, 64, Article 104-109. https://doi.org/10.32615/bp.2019.121
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download fileYu6208 Suppl.pdf

    File size: 1.56 MB

    References

    1. Bartel, D.P.: MicroRNAs: genomics, biogenesis, mechanism, and function. - Cell 116: 281-297, 2004. Go to original source...
    2. Cao, X., Wu, Z., Jiang, F., Zhou, R., Yang, Z.: Identification of chilling stress-responsive tomato microRNAs and their target genes by high-throughput sequencing and degradome analysis. - BMC Genomics 15: 1130, 2014. Go to original source...
    3. Cer, R.Z., Herrera-Galeano, J.E., Anderson, J.J., Bishop-Lilly, K.A., Mokashi, V.P.: miRNA temporal analyzer (mirnaTA): a bioinformatics tool for identifying differentially expressed microRNAs in temporal studies using normal quantile transformation. - Gigascience 3: 20, 2014. Go to original source...
    4. Chen, J., Kirkbride, J.H.: A new synthetic species of Cucumis (Cucurbitaceae) from interspecific hybridization and chromosome doubling. - Brittonia 52: 315-319, 2000. Go to original source...
    5. Chen, J., Staub, J., Adelberg, J., Lewis, S., Kunkle, B.: Synthesis and preliminary characterization of a new species (amphidiploid) in Cucumis. - Euphytica 123: 315-322, 2002. Go to original source...
    6. Chen. J., Staub, J., Qian, C., Jiang, J., Luo, X., Zhuang, F.: Reproduction and cytogenetic characterization of interspecific hybrids derived from Cucumis hystrix Chakr. × Cucumis sativus L. - Theor. appl. Genet. 106: 688-695, 2003. Go to original source...
    7. Chen, L., Chen, J.: Changes of cytosine methylation induced by wide hybridization and allopolyploidy in Cucumis. - Genome 51: 789-799, 2008. Go to original source...
    8. Chen, L., Lou, Q., Zhuang, Y., Chen, J., Zhang, X., Wolukau, J.N.: Cytological diploidization and rapid genome changes of the newly synthesized allotetraploids Cucumis × hytivus. - Planta 225: 603-614, 2007. Go to original source...
    9. Ghani, M.A., Li, J., Rao, L., Raza, M.A., Cao, L., Yu, N., Zou, X., Chen, L.: The role of small RNAs in wide hybridisation and allopolyploidisation between Brassica rapa and Brassica nigra. - BMC Plant Biol. 14: 272, 2014. Go to original source...
    10. Guan, X., Song, Q., Chen, Z.J.: Polyploidy and small RNA regulation of cotton fiber development. -Trends Plant Sci. 19: 516-528, 2014. Go to original source...
    11. Ha, M., Lu, J., Tian, L., Ramachandran, V., Kasschau, K.D., Chapman, E.J., Carrington, J.C., Chen, X., Wang, X.J., Chen, Z.J.: Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. - Proc. nat. Acad. Sci. USA 106: 17835-17840, 2009. Go to original source...
    12. Ha, M., Pang, M., Agarwal, V., Chen, Z.J.: Interspecies regulation of microRNAs and their targets. - Biochim. biophys. Acta 1779: 735-742, 2008. Go to original source...
    13. Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, P.E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, P.S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J., De Pamphilis, C.W.: Ancestral polyploidy in seed plants and angiosperms. - Nature 473: 97-100, 2011. Go to original source...
    14. Kenan-Eichler, M., Leshkowitz, D., Tal, L., Noor, E., Melamed-Bessudo, C., Feldman, M., Levy, A.A.: Wheat hybridization and polyploidization results in deregulation of small RNAs. - Genetics 188: 263-272, 2011. Go to original source...
    15. Li, A., Liu, D., Wu, J., Zhao, X., Hao, M., Geng, S., Yan, J., Jiang, X., Zhang, L., Wu, J., Yin, L., Zhang, R., Wu, L., Zheng, Y., Mao, L.: mRNA and small RNA transcriptomes reveal insights into dynamic homoeolog regulation of allopolyploid heterosis in nascent hexaploid wheat. - Plant Cell 26: 1878-1900, 2014. Go to original source...
    16. Manzaneda, A.J., Rey, P.J., Bastida, J.M., Weiss-Lehman, C., Raskin, E., Mitchell-Olds, T.: Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae). - New Phytol. 193: 797-805, 2012. Go to original source...
    17. Ma, Z., Hu, X., Cai, W., Huang, W., Zhou, X., Luo, Q., Yang, H., Wang, J., Huang, J.: Arabidopsis miR171-targeted scarecrow-like proteins bind to GT cis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions. - PLoS Genet. 10: e1004519, 2014. Go to original source...
    18. Mao, W., Li, Z., Xia, X., Li, Y., Yu, J.: A combined approach of high-throughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber. - PloS ONE 7: e33040, 2012. Go to original source...
    19. Morin, R.D., Aksay, G., Dolgosheina, E., Ebhardt, H.A., Magrini, V., Mardis, E.R., Sahinalp, S.C., Unrau, P.J.: Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa - Genome Res. 18: 571-584, 2008. Go to original source...
    20. Ng, D.W., Lu, J., Chen, Z.J.: Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. - Curr. Opin. Plant. Biol. 15: 154-161, 2012. Go to original source...
    21. Palatnik, J.F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J.C., Weigel, D.: Control of leaf morphogenesis by microRNAs. - Nature 425: 257-263, 2003. Go to original source...
    22. Pulido, A., Laufs, P.: Coordination of developmental processes by small RNAs during leaf development. - J. exp. Bot. 61: 1277-1291, 2010. Go to original source...
    23. Shen, Y., Zhao, Q., Zou, J., Wang, W., Gao, Y., Meng, J., Wang, J.: Characterization and expression patterns of small RNAs in synthesized Brassica hexaploids. - Plant mol. Biol. 85: 287-299, 2014. Go to original source...
    24. Wang, J., Tian, L., Lee, H.S., Wei, N.E., Jiang, H., Watson, B., Madlung, A., Osborn, T.C., Doerge, R.W., Comai, L., Chen, Z.J.: Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. - Genetics 172: 507-517, 2006. Go to original source...
    25. Wang, H., Qi, X., Gao, R., Wang, J., Dong, B., Jiang, J., Chen, S., Guan, Z., Fang, W., Liao, Y., Chen, F.: Microsatellite polymorphism among Chrysanthemum sp. polyploids: the influence of whole genome duplication. - Sci. Rep. 4: 6730, 2014. Go to original source...
    26. Wang, Q., Zhang, B.: MicroRNAs in cotton: an open world needs more exploration. - Planta 241: 1303-1312, 2015. Go to original source...
    27. Xie, K., Shen, J., Hou, X., Yao, J., Li, X., Xiao, J., Xiong, L.: Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. - Plant Physiol. 158: 1382-1394, 2012. Go to original source...
    28. Xu, Y., Xu, H., Wu, X., Fang, X., Wang, J.: Genetic changes following hybridization and genome doubling in synthetic Brassica napus. - Biochem. Genet. 50: 616-624, 2012. Go to original source...
    29. Yang, X., Wang, L., Yuan, D., Lindsey, K., Zhang, X.: Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. - J. exp. Bot. 64: 1521-1536, 2013. Go to original source...
    30. Yu, X., Wang, X., Hyldgaard, B., Zhu, Z., Zhou, R., Kjaer, K.H., Ouzounis, T., Lou, Q., Li, J., Cai, Q., Rosenqvist, E., Ottosen, C.O., Chen, J.: Allopolyploidization in Cucumis contributes to delayed leaf maturation with repression of redundant homoeologous genes. - Plant J. 94: 393-404, 2018. Go to original source...
    31. Zhang, B., Pan, X., Cannon, C.H., Cobb, G.P.: Anderson TA Conservation and divergence of plant microRNA genes. - Plant J. 46: 243-259, 2006. Go to original source...

    Return to the content