Abstract
Small RNAs influence the gene expression at the post-transcriptional level by guiding messenger RNA (mRNA) cleavage, translational repression, and chromatin modifications. In addition to model plants, the microRNAs (miRNAs) have been identified in different crop species. In this work, we developed a specific pipeline to search for coffee miRNA homologs on expressed sequence tags (ESTs) and genome survey sequences (GSS) databases. As a result, 36 microRNAs were identified and a total of 616 and 362 potential targets for Coffea arabica and Coffea canephora, respectively. The evolutionary analyses of these molecules were performed by comparing the primary and secondary structures of precursors and mature miRNAs with their orthologs. Moreover, using a stem-loop RT-PCR assay, we evaluated the accumulation of mature miRNAs in genomes with different ploidy levels, detecting an increase in the miRNAs accumulation according to the ploidy raising. Finally, a 5′ RACE (Rapid Amplification of cDNA Ends) assay was performed to verify the regulation of auxin responsive factor 8 (ARF8) by MIR167 in coffee plants. The great variety of target genes indicates the functional plasticity of these molecules and reinforces the importance of understanding the RNAi-dependent regulatory mechanisms. Our results expand the study of miRNAs and their target genes in this crop, providing new challenges to understand the biology of these species.
Similar content being viewed by others
References
Akter, A., Islam, M. M., Mondal, S. I., Mahmud, Z., Jewel, N. A., Ferdous, S., Amin, M. R., & Rahman, M. M. (2014). Computational identification of miRNA and targets from expressed sequence tags of coffee (C. arabica). Saudi Journal of Biological Sciences, 21, 3–12.
Axtell, M. J. (2013). Classification and comparison of small RNAs from plants. Annual Review of Plant Biology, 64, 137–159.
Barakat, A., Wall, K., Leebens-Mack, J., Wang, Y. J., Carlson, J. E., & dePamphilis, C. W. (2007). Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant Journal, 51, 991–1003.
Bonnet, E., Wuyts, J., Rouze, P. & Van de Peer, Y. (2004) Detection of 91 potential in plant conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes. Proceedings of the National Academy of Sciences of the United States of America, 101, 11511–11516.
Chapman, E. J., & Carrington, J. C. (2007). Specialization and evolution of endogenous small RNA pathways. Nature Reviews Genetics, 8, 884–896.
Chen, Z. J. (2007). Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology, 58, 377–406.
Dai, X., & Zhao, P. X. (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 39, W155–W159.
Dai, X. B., & Zhao, P. X. (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 39, W155–W159.
Davis, A. P., Govaerts, R., Bridson, D. M., & Stoffelen, P. (2006). An annotated taxonomic conspectus of the genus Coffea (Rubiaceae). Botanical Journal of the Linnean Society, 152, 465–512.
de Souza Gomes, M., Muniyappa, M. K., Carvalho, S. G., Guerra-Sa, R., & Spillane, C. (2011). Genome-wide identification of novel microRNAs and their target genes in the human parasite Schistosoma mansoni. Genomics, 98, 96–111.
Denoeud, F., Carretero-Paulet, L., Dereeper, A., Droc, G., Guyot, R., Pietrella, M., Zheng, C., Alberti, A., Anthony, F., Aprea, G., Aury, J.-M., Bento, P., Bernard, M., Bocs, S., Campa, C., Cenci, A., Combes, M.-C., Crouzillat, D., Da Silva, C., Daddiego, L., De Bellis, F., Dussert, S., Garsmeur, O., Gayraud, T., Guignon, V., Jahn, K., Jamilloux, V., Joët, T., Labadie, K., Lan, T., Leclercq, J., Lepelley, M., Leroy, T., Li, L.-T., Librado, P., Lopez, L., Muñoz, A., Noel, B., Pallavicini, A., Perrotta, G., Poncet, V., Pot, D., Priyono, Rigoreau, M., Rouard, M., Rozas, J., Tranchant-Dubreuil, C., VanBuren, R., Zhang, Q., Andrade, A. C., Argout, X., Bertrand, B., de Kochko, A., Graziosi, G., Henry, R. J., Jayarama, Ming, R., Nagai, C., Rounsley, S., Sankoff, D., Giuliano, G., Albert, V. A., Wincker, P. & Lashermes, P. (2014) The coffee genome provides insight into the convergent evolution of caffeine biosynthesis. Science, 345, 1181–1184.
Ding, Y., Tao, Y. & Cheng, Z. (2013) Emerging roles of microRNA in the mediaton of drought stress response in plants. Journal of Experimental Botany.
Dong, Z., Han, M.-H. & Fedoroff, N. (2008) The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proceedings of the National Academy of Sciences of the United States of America, 105, 9970–9975.
Ebhardt, H. A., Fedynak, A., & Fahlman, R. P. (2010). Naturally occurring variations in sequence length creates microRNA isoforms that differ in argonaute effector complex specificity. Silence pp., 1-6.
Gardner, P. P., Daub, J., Tate, J. G., Nawrocki, E. P., Kolbe, D. L., Lindgreen, S., Wilkinson, A. C., Finn, R. D., Griffiths-Jones, S., Eddy, S. R., & Bateman, A. (2009). Rfam: updates to the RNA families database. Nucleic Acids Research, 37, D136–D140.
Gentile, A., Dias, L. I., Mattos, R. S., Ferreira, T. H. & Menossi, M. (2015) MicroRNAs and drought responses in sugarcane.
Ha, M., Lu, J., Tian, L., Ramachandran, V., Kasschau, K. D., Chapman, E. J., Carrington, J. C., Chen, X. M., Wang, X. J. & Chen, Z. J. (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proceedings of the National Academy of Sciences of the United States of America, 106, 17835–17840.
Ha, M., Pang, M. X., Agarwal, V., & Chen, Z. J. (2008). Interspecies regulation of microRNAs and their targets. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms, 1779, 735–742.
He, G. M., Zhu, X. P., Elling, A. A., Chen, L. B., Wang, X. F., Guo, L., Liang, M. Z., He, H., Zhang, H. Y., Chen, F. F., Qi, Y. J., Chen, R. S., & Deng, X. W. (2010). Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 22, 17–33.
Hegarty, M. J., Barker, G. L., Wilson, I. D., Abbott, R. J., Edwards, K. J., & Hiscock, S. J. (2006). Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Current Biology, 16, 1652–1659.
Hofacker, I. L. (2009) RNA secondary structure analysis using the Vienna RNA package. Curr Protoc Bioinformatics, Chapter 12, Unit12 12.
Huang, Y., Zou, Q., Sun, X., & Zhao, L. (2014). Computational identification of microRNAs and their targets in perennial Ryegrass (Lolium perenne). Applied Biochemistry and Biotechnology, 173, 1011–1022.
Jones-Rhoades, M. W., & Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell, 14, 787–799.
Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J., Tyagi, A., & Kapoor, S. (2008). Genome-wide identification, organization and phylogenetic analysis of dicer-like, argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics, 9, 451.
Kenan-Eichler, M., Leshkowitz, D., Tal, L., Noor, E., Melamed-Bessudo, C., Feldman, M., & Levy, A. A. (2011). Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics, 188, 263–U259.
Lai, E. C., Tomancak, P., Williams, R. W., & Rubin, G. M. (2003). Computational identification of drosophila microRNA genes. Genome Biology, 4.
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. & Higgins, D. G. (2007) Clustal W & Clustal X version 2.0. Bioinformatics (Oxford, England), 23, 2947–2948.
Livak, K. J. & Schmittgen, T. D. (2001) Analysis of relative gene expression data using realtime quantitative PCR and the 2(−Delta Delta CT) Method. Methods, pp. 402–408. San Diego.
Loss-Morais, G., Ferreira, D. C. R., Margis, R., Alves-Ferreira, M., & Corrêa, R. L. (2014). Identification of novel and conserved microRNAs in C. canephora and C. arabica. Genetics and Molecular Biology, 37, 671–682.
Mallory, A. C., & Vaucheret, H. (2009). ARGONAUTE 1 homeostasis invokes the coordinate action of the microRNA and siRNA pathways. EMBO Reports, 10, 521–526.
Melo, E. F., Fernandes-Brum, C. N., Pereira, F. J., Castro, E. M. d. & Chalfun-Júnior, A. (2014) Anatomic and physiological modifications in seedlings of C. arabica cultivar Siriema under drought conditions. Ciência e Agrotecnologia, 38, 25–33.
Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., Wu, L., Li, S., Zhou, H., Long, C., Chen, S., Hannon, G. J., & Qi, Y. (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5 ‘terminal nucleotide. Cell, 133, 116–127.
Molnar, A., Melnyk, C., & Baulcombe, D. C. (2011). Silencing signals in plants: a long journey for small RNAs. Genome Biology, 12.
Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., Chapman, E. J., Fahlgren, N., Allen, E., & Carrington, J. C. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 transacting siRNA formation. Cell pp., 128-141.
Ng, D. W. K., Lu, J., & Chen, Z. J. (2012). Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. Current Opinion in Plant Biology, 15, 154–161.
Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H. & Poethig, R. S. (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 102, 3691–3696.
Pattanayak, D., Solanke, A. U., & Kumar, P. A. (2013). Plant RNA interference pathways: diversity in function, similarity in action. Plant Molecular Biology Reporter, 31, 493–506.
Qin, Z., Li, C., Mao, L., & Wu, L. (2014). Novel insights from non-conserved microRNAs in plants. Frontiers in Plant Science, 5, 586.
Rajagopalan, R., Vaucheret, H., Trejo, J., & Bartel, D. P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes & Development, 20, 3407–3425.
Rebijith, K. B., Asokan, R., Ranjitha, H. H., Krishna, V., & Nirmalbabu, K. (2013). In silico mining of novel microRNAs from coffee (C. arabica) using expressed sequence tags. Journal of Horticultural Science and Biotechnology, 88, 325–337.
Spanudakis, E., & Jackson, S. (2014). The role of microRNAs in the control of flowering time. Journal of Experimental Botany, 65, 365–380.
Sunkar, R., & Jagadeeswaran, G. (2008). In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biology, 8.
Thakur, V., Wanchana, S., Xu, M., Bruskiewich, R., Quick, W., Mosig, A., & Zhu, X.-G. (2011). Characterization of statistical features for plant microRNA prediction. BMC Genomics, 12, 108.
Tirosh, I., Reikhav, S., Levy, A. A., & Barkai, N. (2009). A yeast hybrid provides insight into the evolution of gene expression regulation. Science, 324, 659–662.
Varkonyi-Gasic, E., Wu, R. M., Wood, M., Walton, E. F., & Hellens, R. P. (2007). Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods, 3.
Vaucheret, H. (2006). Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes & Development, 20, 759–771.
Vaucheret, H. (2009). AGO1 homeostasis involves differential production of 21-nt and 22-nt miR168 species by MIR168a and MIR168b. PloS One, 4.
Veitia, R. A., Bottani, S., & Birchler, J. A. (2008). Cellular reactions to gene dosage imbalance: genomic, transcriptomic and proteomic effects. Trends in Genetics, 24, 390–397.
Voinnet, O. (2009). Origin, biogenesis, and activity of plant MicroRNAs. Cell, 136, 669–687.
Wahid, F., Shehzad, A., Khan, T., & Kim, Y. Y. (2010). MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, 1803, 1231–1243.
Wu, G. (2013). Plant microRNAs and development. Journal of Genetics and Genomics, 40, 217–230.
Xie, F. L., Huang, S. Q., Guo, K., Xiang, A. L., Zhu, Y. Y., Nie, L., & Yang, Z. M. (2007). Computational identification of novel microRNAs and targets in Brassica napus. FEBS Letters, 581, 1464–1474.
Yan-du, L., Qin-hua, G., Xiao-yuan, C. & Song, Q. (2008) Identification and characterization of microRNAs and their targets in grapevine (Vitis vinifera). Agricultural Sciences in China, pp. 929–943. Amsterdam.
Yu, B., Yang Z Fau - Li, J., Li J Fau - Minakhina, S., Minakhina S Fau - Yang, M., Yang M Fau - Padgett, R. W., Padgett Rw Fau - Steward, R., Steward R Fau - Chen, X. & Chen, X. Methylation as a crucial step in plant microRNA biogenesis.
Zhang, B., Pan, X., Cannon, C. H., Cobb, G. P., & Anderson, T. A. (2006). Conservation and divergence of plant microRNA genes. The Plant Journal, 46, 243–259.
Zhang, B. H., Pan, X. P., Cox, S. B., Cobb, G. P., & Anderson, T. A. (2006). Evidence that miRNAs are different from other RNAs. Cellular and Molecular Life Sciences, 63, 246–254.
Zhang, B. H., Pan, X. P., Wang, Q. L., Cobb, G. P., & Anderson, T. A. (2005). Identification and characterization of new plant microRNAs using EST analysis. Cell Research, 15, 336–360.
Zhang, B. H., Pan, X. P., Wang, Q. L., Cobb, G. P., & Anderson, T. A. (2006). Computational identification of microRNAs and their targets. Computational Biology and Chemistry, 30, 395–407.
Zhang, B. H., Wang, Q. L., Wang, K. B., Pan, X. P., Liu, F., Guo, T. L., Cobb, G. P., & Anderson, T. A. (2007). Identification of cotton microRNAs and their targets. Gene, 397, 26–37.
Zhang, T., Wang J Fau - Zhou, C. & Zhou, C. (2015) The role of miR156 in developmental transitions in Nicotiana tabacum.
Zhang, T. Q., Lian, H., Tang, H., Dolezal, K., Zhou, C. M., Yu, S., Chen, J. H., Chen, Q., Liu, H., Ljung, K. & Wang, J. W. A.-O. h. o. o. (2015) An intrinsic microRNA timer regulates progressive decline in shoot regenerative capacity in plants.
Zhao, M. A.-O. h. o. o., Meyers, B. C. A.-O. h. o. o., Cai, C., Xu, W. A.-O. h. o. o. & Ma, J. A.-O. h. o. o. X. (2015) Evolutionary patterns and coevolutionary consequences of miRNA genes and microRNA targets triggered by multiple mechanisms of genomic duplications in soybean. LID - tpc.15.00048 [pii].
Zhou, X. F., Ruan, J. H., Wang, G. D., & Zhang, W. X. (2007). Characterization and identification of microRNA core promoters in four model species. PLoS Computational Biology, 3, 412–423.
Acknowledgments
The authors thank the Laboratory of Plant Molecular Physiology (LFMP) of the Federal University of Lavras (UFLA), the National Council for Scientific and Technological Development (CNPq) for the fellowships granted, the Minas Gerais Research Foundation (FAPEMIG), and National Institute for Science and Technology for Coffee (INCT-Café) for funding this work and the Coordination of Improvement of Higher Education (CAPES) for grants.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary 1
(GIF 25.1 kb)
Rights and permissions
About this article
Cite this article
Chaves, S.S., Fernandes-Brum, C.N., Silva, G.F.F. et al. New Insights on Coffea miRNAs: Features and Evolutionary Conservation. Appl Biochem Biotechnol 177, 879–908 (2015). https://doi.org/10.1007/s12010-015-1785-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-015-1785-x