Abstract
In modern sugarcane cultivars, around 70–80% of the genetic information originates from Saccharum officinarum, which contributed important sugar content traits. Although several studies have identified microRNAs in Saccharum hybrids, they have not yet been studied in S. officinarum. In this study, by deep sequencing and in silico approaches, 268 miRNA candidates were predicted in S. officinarum, and 52 were found to likely be real miRNAs based on our analysis with stringent criteria. Among these 52 miRNAs, 43 miRNAs from 26 miRNA families were found to have homologous miRNAs in public miRBase Release 21, and 9 miRNAs were identified to be novel in S. officinarum. Out of the 52 miRNAs, 6 were randomly chosen and verified by stem-loop RT-PCR. The 52 miRNAs were predicted to have 237 and 76 targets in sugarcane and sorghum, respectively, including auxin response factor, MADS-box transcription factor, zinc finger-like protein. MicroRNAs were found to be involved in critical sugarcane pathways, such as sucrose metabolism and cellulose metabolism. In addition, the first miRNA (sof-novel1) derived from the Saccharum chloroplast genome was identified. These results provide the foundation for future studies to distinguish the miRNAs from S. spontaneum and S. officinarum in Saccharum hybrid, and valuable information to further study the miRNA functions in Saccharum species.
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References
Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503
Bottino MC, Rosario S, Grativol C, Grativol C, Rojas CA, Farrineli L, Hemerly AS, Ferreira PC (2013) High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One 8:e59423
Bushati N, Cohen SM (2007) microRNA functions. Annu Rev Cell Dev Biol 23:175–205
Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377
Chen C, Ridzon DA, Broomer AJ, Zhou ZH, Lee DH, Nguyen JT, Barbisin M, Xu NL, Mahuvakar VR, Andersen MR, Lao KQ, Livak KJ, Guegler KJ (2005) Real-time quantification of microRNAs by stem–loop RT–PCR. Nucleic Acids Res 33:e179–e179
Chen Y, Zhang Q, Hu W, Zhang X, Wang L, Hua X, Yu Q, Ming R, Zhang J (2017) Evolution and expression of the fructokinase gene family in Saccharum. BMC Genomics 18 (1)
Chuck G, Whipple C, Jackson D, Hake S (2010) The maize SBP-box transcription factor encoded by tasselsheath4 regulates bract development and the establishment of meristem boundaries. Development 137:1243–1250
Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159
Daniels J, Roach BT (1987) Taxonomy and evolution. Sugarcane improvement through breeding. Elsevier, Amsterdam 7:7–84
D'hont A, Paulet F, Glaszmann JC (2002) Oligoclonal interspecific origin of ‘north Indian’and ‘Chinese’sugarcanes. Chromosom Res 10:253–262
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic acids research: gkq310
Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, Carrington JC (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22:1074–1089
Ferreira TH, Gentile A, Vilela RD, Costa GG, Dias LI, Endres L, Menossi M (2012) microRNAs associated with drought response in the bioenergy crop sugarcane (Saccharum spp.). PLoS one 7: e46703
Gentile FTH, Mattos RS, Dias LI, Hoshino AA, Carneiro MS, Souza GM, Calsa T Jr, Nogueira RM, Endres L, Menossi M (2013) Effects of drought on the microtranscriptome of field-grown sugarcane plants. Planta 237:783–798
Gentile A, Dias LI, Mattos RS, Ferreira TH, Menossi M (2015) MicroRNAs and drought responses in sugarcane. Front Plant Sci 6:58
Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, Bellini C (2009) Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. Plant Cell 21:3119–3132
Hwan Lee J, Joon Kim J, Ahn JH (2012) Role of SEPALLATA3 (SEP3) as a downstream gene of miR156-SPL3-FT circuitry in ambient temperature-responsive flowering. Plant Signal Behav 7:1151–1154
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799
Jones-Rhoades MW, Bartel DP (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Lao K, Xu NL, Yeung V, Chen C, Livak KJ, Straus NA (2006) Multiplexing RT-PCR for the detection of multiple miRNA species in small samples. Biochem Biophys Res Commun 343:85–89
Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056
Mecchia MA, Debernardi JM, Rodriguez RE, Schommer C, Palatnik JF (2013) MicroRNA miR396 and RDR6 synergistically regulate leaf development. Mech Dev 130:2–13
Mette MF, van der Winden J, Matzke M, Matzke AJ (2002) Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol 130:6–9
Meyers BC et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190
Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, Palatnik JF (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137:103–112
Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochimica et Biophysica Acta (BBA)-Gene regulatory mechanisms 1779: 743-748
Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019
Sunkar R, Zhu JK (2007) MicroRNAs and short-interfering RNAs in plants. J Integr Plant Biol 49:817–826
Sunkar R, Li YF, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203
Thiebaut F, Grativol C, Carnavale-Bottino M, Rojas CA, Tanurdzic M, Farinelli L, Martienssen RA, Hemerly AS, Ferreira PC (2012a) Computational identification and analysis of novel sugarcane microRNAs. BMC Genomics 13:1
Thiebaut F, Rojas CA, Almeida KL, Grativol C, Domiciano GC, Lamb CR, Engler Jde A, Hemerly AS, Ferreira PC (2012b) Regulation of miR319 during cold stress in sugarcane. Plant Cell Environ 35:502–512
Wang J, Roe B, Macmil S, Yu Q, Murray JE, Tang H, Chen C, Najar F, Wiley G, Bowers J, Van Sluys MA, Rokhsar DS, Hudson ME, Moose SP, Paterson AH, Ming R (2010) Microcollinearity between autopolyploid sugarcane and diploid sorghum genomes. BMC Genomics 11:1
Wang L, Gu X, Xu D, Wang W, Wang H, Zeng M, Chang Z, Huang H, Cui X (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Exp Bot 62:761–773
Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547
Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133:4211–4218
Yang X, Li L (2011) miRDeep-P: a computational tool for analyzing the microRNA transcriptome in plants. Bioinformatics 27:2614–2615
Yang C, Li D, Mao D, Liu X, Ji C, Li X, Zhao X, Cheng Z, Chen C, Zhu L (2013) Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativa L.) Plant Cell Environ 36:2207–2218
Zanca AS, Vicentini R, Ortiz-Morea FA, Del Bem LE, da Silva MJ, Vincentz M, Nogueira FT (2010) Identification and expression analysis of microRNAs and targets in the biofuel crop sugarcane. BMC Plant Biol 10:1
Zhang B, Pan X, Cobb GP, Anderson TA (2006) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16
Zhang J, Nagai C, Yu Q, Pan YB, Tomas AS, Schnell RJ, Comstock JC, Arumuganathan AK, Ming R (2012) Genome size variation in three Saccharum species. Euphytica 185:511–519
Zhang Q, Hu W, Zhu F, Wang L, Yu Q, Ming R, Zhang J (2016) Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum. BMC Genomics 17 (1)
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Acknowledgements
This project was supported by grants from the 863 program (2013AA100604), NSFC (31201260) and Fujian Provincial Department of Education (No. JA12082). We are grateful for the invaluable help and comments of Dr. Jianping Wang and Dr. Rui Xia.
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Jisen Zhang and Aijuan Xue conceived the study, designed the experiments and wrote the manuscript. Aijuan Xue, Fan Zhu, Zhen Li, Muche Cai, Qing Zhang, Xingtan Zhang, and Ray Ming performed the experiments and analyzed the data. All authors read and approved the final article.
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Communicated by: Blake Meyers
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Xue, A., Li, Z., Cai, M. et al. Identification and Characterization of microRNAs from Saccharum officinarum L by Deep Sequencing. Tropical Plant Biol. 10, 134–150 (2017). https://doi.org/10.1007/s12042-017-9190-y
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DOI: https://doi.org/10.1007/s12042-017-9190-y