Abstract
miRNAs are important regulators of plant gene expression. There are few studies on the regulation of miRNAs in Lonicera edulis. We used high-throughput sequencing technology to analyse miRNAs in L. edulis, aiming to identify miRNAs and elucidate their function in L. edulis. In the present study, we employed the high-throughput sequencing technology to profile miRNAs in L. edulis. A total of 51,819,072 small RNA tags with sizes ranging from 18 to 30 nt were obtained, indicating that L. edulis have a large and diverse small RNA population. Bioinformatic analysis identified 507 mature miRNAs, and 16 predicted novel miRNAs that are likely to be unique to L. edulis. Three miRNAs related to anthocyanin biosynthesis were locked by gene ontology (GO) analysis and target gene analysis. The selected three miRNAs are relatively high in the expression of L. edulis. Some of the previous studies have studied these types of miRNAs involved in the anthocyanin metabolism pathway in fruits. Among them, expression profiles of three conserved miRNAs were validated by stem loop qRT-PCR. Further, the potential target genes of conserved and novel miRNAs were predicted and subjected to GO annotation. Enrichment analysis of the GO-represented biological processes and molecular functions revealed that these target genes were potentially involved in a wide range of metabolic pathways and developmental processes. In particular, different families of miRNAs can directly or indirectly regulate anthocyanin biosynthesis. In recent years, the research on miRNAs has become more and more clear, but the research on miRNAs involved in the regulation of anthocyanin synthesis of L. edulis is still lagging. This study provides a useful resource for further elucidation of the functional roles of miRNAs during fruit development and ripening.
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An X. H., Tian Y., Chen K. Q., Wang X. F. and Hao Y. J. 2012 The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. J. Plant Physiol. 169, 710–717.
Che R., Tong H., Shi B., Liu Y., Fang S., Liu D. et al. 2015 Control of grain size and rice yield by GL2-mediated brassino steroid responses. Nat. Plants 2, 15195.
Chiu L. W., Zhou X., Burke S., Wu X., Prior R. L. and Li L. 2010 The purple cauliflower arises from activation of a MYB transcription factor. Plant Physiol. 154, 1470–1480.
Christopher D. 2013 Trans-acting small interfering RNA4: key to nutraceutical synthesis in grape development? Trends Plant Sci. 18, 601–610.
Dong Q., Fei Y., Rui M., Xiaobing J., Huijuan Y., Ziyi G. et al. 2016 Identification of microRNAs and their targets associated with fruit-bagging and subsequent sunlight re-exposure in the ‘Granny Smith’ apple exocarp using high-throughput sequencing. Front Plant Sci. 7, 27.
Duan P., Ni S., Wang J., Zhang B., Xu R., Wang Y. et al. 2015 Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat. Plants 2, 15203.
Gandía-Herrero F and García-Carmona F. 2013 Biosynthesis of betalains: yellow and violet plant pigments. Trends Plant Sci. 18, 334–343.
Gao F., Wang K., Liu Y., Chen Y., Chen P., Shi Z. et al. 2015 Blocking miR396 increases rice yield by shaping inflorescence architecture. Nat. Plants 2, 15196.
Gao X, Cui Q, Cao Q. Z, Liu Q, He H. B, Zhang D. M et al. 2017 Transcriptome-wide analysis of Botrytis elliptica responsive microRNAs and their targets in Lilium Regale Wilson by high-throughput sequencing and degradome analysis. Front. Plant Sci. 8, 753.
Gonzalez A., Zhao M., Leavitt J. M. and Lloyd A. M. 2008 Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814–827.
Gou J. Y., Felippes F. F., Liu C. J., Weigel D. and Wang J. W. 2011 Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23, 1512–1522.
Guan X., Pang M., Nah G., Shi X., Ye W., Stelly D. M. et al. 2014 miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050.
Jia X., Shen J., Liu H., Li F., Ding N., Gao C. et al. 2015 Small tandem target mimic-mediated blockage of microRNA858 induces anthocyanin accumulation in tomato. Planta 242, 283–293.
Kong J. M., Chia L. S., Goh N. K., Chia T. F. and Brouillard R. 2003 Analysis and biological activities of anthocyanins. Phytochemistry (Amsterdam) 64, 923–933.
Kuijt S. J. H., Greco R., Agalou A., Shao J., “t Hoen C. C. J., Overnas E. et al. 2014 Interaction between the growth-regulating factor and knotted1-like homeobox families of transcription factors [W]. Plant Physiol. 164, 1952–1966.
Li J. C., Li T. Z., Wang Z. G. and Li B. J. 2010 Cloning and expression of UFGT gene in skin of Max Red Bartlett. Acta Botanica Boreali-Occidentalia Sinica 30, 30–34.
Li Z., Yu J. J., Peng Y. and Huang B. R. 2016 Metabolic pathways regulated by abscisic acid, salicylic acid, and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (agrostis stolonifera). Physiol. Plantarum 159, 42.
Liang G., Yang F. and Yu D. 2010 Microrna395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J. 62, 1046–1057.
Liu H., Guo S., Xu Y., Li C., Zhang Z., Zhang D. et al. 2014 OsmiR396d-regulated OsGRFs function in floral organogenesis in rice through binding to their targets OsJMJ706 and OsCR4. Plant Physiol. 165, 160–174.
Liu P., Huo J. W., Wang Y., Qin D. and Zhao L. J. 2016 De novo transcriptome sequencing of blue honeysuckle fruit (Lonicera caerulea L.) and analysis of major genes involved in anthocyanin biosynthesis. Acta Physiol. Plant. 38, 180.
Luo A. D., Liu L., Tang Z. S., Bai X. Q., Cao S. Y. and Chu C. C. 2005 Down-regulation of OsGRF1 gene in rice rhd1 mutant results in reduced heading date. J. Integr. Plant Biol. 47, 8.
Rock C. D. 2013 Trans-acting small interfering rna4: key to nutraceutical synthesis in grape development? Trends Plant Sci. 18, 601–610.
Sun Y., Qiu Y., Duan M., Wang J., Zhang X., Wang H. et al. 2016 Identification of anthocyanin biosynthesis related microRNAs in a distinctive chinese radish (Raphanus sativus L.) by high-throughput sequencing. Mol. Genet. Genomics 292, 1–15.
Tang Y., Liu H., Guo S., Wang B., Li Z., Chong K. et al. 2018 OsmiR396d affects gibberellin and brassino steroid signaling to regulate plant architecture in rice. Plant Physiol. 176, 946.
Wang C. J., Wang J. M., Lin W. L., Chu C. Y., Chou F. P. and Tseng T. H. 2000 Protective effect of hibiscus anthocyanins against tert-butyl hydroperoxide-induced hepatic toxicity in rats. Food Chem. Toxicol. 38, 411–416.
Wang J. W., Wang L. J., Mao Y. B., Cai W. J., Xue H. W. and Chen X. Y. 2005 Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell. 17, 2204–2216.
Wang M. Q., Xie Z. P., Sun X., Li X. P., Zhu X. D., Wang C. et al. 2017 Function analysis of miR159 and its target gene VvGAMYB in grape flower development. Acta Horticult. Sinica. https://doi.org/10.16420/j.issn.0513-353x.2016-0816.
Xia R., Zhu H., An Y. Q., Beers E. P. and Liu Z. 2012 Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol. 13, Article R47.
Xie K., Shen J., Hou X., Yao J., Li X., Xiao J. et al. 2012 Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiol. 158, 1382–1394.
Yao F., Zhu H., Yi C., Qu H. and Jiang Y. 2015 MicroRNAs and targets in senescent litchi fruit during ambient storage and post-cold storage shelf life. BMC Plant Biol. 15, 181.
Yoshimoto M., Okuno S., Yoshinaga M., Yamakawa O. and Yamada J. 1999 Antimutagenicity of sweetpotato (Ipomoea batatas) roots. Biosci. Biotech. Bioch. 63, 537–541.
Yuan Y., Wang Z., Jiang C., Wang X. and Huang L. 2014 Exploiting genes and functional diversity of chlorogenic acid and luteolin biosyntheses in Lonicera japonica and their substitutes. Gene 534, 408–416.
Yue J. Y., Lu X. H., Zhang H., Ge J., Gao X. L. and Liu Y. S. 2017 Identification of conserved and novel microRNAs in blueberry. Front. Plant Sci. 8, 1155.
Zhang Y. T., Hu W. J., Peng X. R., Sun B., Wang X. R. and Tang H. R. 2018 Characterization of anthocyanin and proanthocyanidin biosynthesis in two strawberry genotypes during fruit development in response to different light qualities. J. Photoch. Photobio. B. 186, 225–231.
Zhao H. N. 2018 Identification and regulation functions of miRNAs involved in anthocyanin synthesis in mulberry. Shandong Agricultural University, Shandong.
Zhao X. Y., Pang M. L., Zhao Q., Ren Y. R., Hao Y. J. and You C. X. 2015 Cloning and expression analysis of tomato LeLAC (mir397) gene. Acta Horticul. Sinica 42, 1285–1298.
Acknowledgements
This research was funded by National Natural Science Foundation Project and Heilongjiang Provincial Financial Forestry Science and Technology Promotion Fund, grant number 31571731 and 2015ST-11. Thanks to Prof. Li Binsheng of Heilongjiang Forest Botanical Garden for providing the resource, experimental sample planting, cultivation, management, picking; and thanks to the sequencing support of Huada Gene.
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Corresponding editor: Manoj Prasad
JC, experimental guidance and analysis; BL, provided the resource, experimental sample planting, cultivation, management, picking; JL and XL, analysed the data; CW, collect samples; DC & CD, revised the manuscript.
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Cui, J., Gao, Z., Li, B. et al. Identification of anthocyanin biosynthesis related microRNAs and total microRNAs in Lonicera edulis by high-throughput sequencing. J Genet 99, 31 (2020). https://doi.org/10.1007/s12041-020-01194-x
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DOI: https://doi.org/10.1007/s12041-020-01194-x