Abstract
microRNAs (miRNA) families play a critical role in plant growth, development, and responses to abiotic stress. In this study, we characterized Up-miR-843 and its targets genes in Ulva prolifera responses to nitrogen depravation and heat stress. The data demonstrated that 184 target genes of Up-miR-843 could be successfully validated. N deficiency not heat stress stimulus induced increase in abundance of the Up-miR-843 while exhibited reverse expression of target genes, including cyclin A3 and cyclin L, which were strictly required for cell cycle progression. In addition, U. prolifera with highly expression of Up-miR-843 showed improved biomass, and photosynthesis compared with that under normal growth conditions. Thus, the N deprivation and heat responsive miRNAs might be a possible member mediating the expression of these target genes, which further regulated the growth of U. prolifera.
Similar content being viewed by others
References
Anion D I. 1949. Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24(1): 1–15, doi: https://doi.org/10.1104/pp.24.1.1
Bi Y M, Wang R L, Zhu T, et al. 2007. Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics, 8: 281, doi: https://doi.org/10.1186/1471-2164-8-281
Breuer G, Lamers P P, Martens D E, et al. 2012. The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresource Technology, 124: 217–226, doi: https://doi.org/10.1016/j.biortech.2012.08.003
Chiou T J, Aung K, Lin S I, et al. 2006. Regulation of phosphate homeostasis by microRNA in Arabidopsis. The Plant Cell, 18(2): 412–421, doi: https://doi.org/10.1105/tpc.105.038943
Conley D J, Paerl H W, Howarth R W, et al. 2009. Controlling eutrophication: nitrogen and phosphorus. Science, 323(5917): 1014–1015, doi: https://doi.org/10.1126/science.1167755
Coutinho R, Zingmark R. 1993. Interactions of light and nitrogen on photosynthesis and growth of the marine macroalga Ulva curvata (Kützing) De Toni. Journal of Experimental Marine Biology and Ecology, 167(1): 11–19, doi: https://doi.org/10.1016/0022-0981(93)90180-V
Ferreira P, Hemerly A, De Almeida Engler J, et al. 1994. Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. Proceedings of the National Academy of Sciences of the United States of America, 91(24): 11313–11317, doi: https://doi.org/10.1073/pnas.91.24.11313
Forment J, Naranjo M Á, Roldán M, et al. 2002. Expression of Arabidopsis SR-like splicing proteins confers salt tolerance to yeast and transgenic plants. The Plant Journal, 30(5): 511–519, doi: https://doi.org/10.1046/j.1365-313X.2002.01311.x
Gao Si, Guo Chengjin, Zhang Yongsheng, et al. 2016. Wheat microRNA member TaMIR444a is nitrogen deprivation-responsive and involves plant adaptation to the nitrogen-starvation stress. Plant Molecular Biology Reporter, 34(5): 931–946, doi: https://doi.org/10.1007/s11105-016-0973-3
Giacomelli J I, Weigel D, Chan R L, et al. 2012. Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytologist, 195(4): 766–773, doi: https://doi.org/10.1111/j.1469-8137.2012.04259.x
Hackenberg M, Gustafson P, Langridge P, et al. 2015. Differential expression of microRNAs and other small RNAs in barley between water and drought conditions. Plant Biotechnology Journal, 13(1): 2–13, doi: https://doi.org/10.1111/pbi.12220
Hasanuzzaman M, Nahar K, Alam M M, et al. 2013. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. International Journal of Molecular Sciences, 14(5): 9643–9684, doi: https://doi.org/10.3390/ijms14059643
He Yuan, Ma Yafeng, Du Yu, et al. 2018. Differential gene expression for carotenoid biosynthesis in a green alga Ulva prolifera based on transcriptome analysis. BMC Genomics, 19: 916, doi: https://doi.org/10.1186/s12864-018-5337-y
Hsieh L C, Lin S I, Shih A C C, et al. 2009. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology, 151(4): 2120–2132, doi: https://doi.org/10.1104/pp.109.147280
Huang Aiyou, Wang Guangce, He Linwen, et al. 2011. Characterization of small RNAs from Ulva prolifera by high-throughput sequencing and bioinformatics analysis. Chinese Science Bulletin, 56(27): 2916–2921, doi: https://doi.org/10.1007/s11434-011-4678-6
Jones-Rhoades M W, Bartel D P, Bartel B. 2006. MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology, 57: 19–53, doi: https://doi.org/10.1146/annurev.arplant.57.032905.105218
Kouchi H, Sekine M, Hata S. 1995. Distinct classes of mitotic cyclins are differentially expressed in the soybean shoot apex during the cell cycle. The Plant Cell, 7(8): 1143–1155
Kruszka K, Pacak A, Swida-Barteczka A, et al. 2014. Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. Journal of Experimental Botany, 65(20): 6123–6135, doi: https://doi.org/10.1093/jxb/eru353
Lartigue J, Neill A, Hayden B L, et al. 2003. The impact of salinity fluctuations on net oxygen production and inorganic nitrogen uptake by Ulva lactuca (Chlorophyceae). Aquatic Botany, 75(4): 339–350, doi: https://doi.org/10.1016/S0304-3770(02)00193-6
Li J, Wu L Q, Zheng W Y, et al. 2015. Genome-wide identification of microRNAs responsive to high temperature in rice (Oryza sativa) by high-throughput deep sequencing. Journal of Agronomy and Crop Science, 201(5): 379–388, doi: https://doi.org/10.1111/jac.12114
Liang Gang, Yang Fengxi, Yu Diqiu. 2010. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. The Plant Journal, 62(6): 1046–1057
Liao Jieren, Wu Xiayuan, Xing Zhiqiang, et al. 2017. γ-Aminobutyric Acid (GABA) accumulation in tea (Camellia sinensis L.) through the GABA shunt and polyamine degradation pathways under anoxia. Journal of Agricultural and Food Chemistry, 65(14): 3013–3018, doi: https://doi.org/10.1021/acs.jafc.7b00304
Lin Hanzhi, Jiang Peng, Zhang Jiaxu, et al. 2011. Genetic and marine cyclonic eddy analyses on the largest macroalgal bloom in the world. Environmental Science & Technology, 45(11): 5996–6002
Lu Yibin, Yang Lintong, Qi Yiping, et al. 2014. Identification of boron-deficiency-responsive microRNAs in Citrus sinensis roots by Illumina sequencing. BMC Plant Biology, 14: 123, doi: https://doi.org/10.1186/1471-2229-14-123
May P, Liao W, Wu Yijin, et al. 2013. The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nature Communications, 4: 2145, doi: https://doi.org/10.1038/ncomms3145
McGlathery K J. 2001. Macroalgal blooms contribute to the decline of seagrass in nutrient-enriched coastal waters. Journal of Phycology, 37(4): 453–456, doi: https://doi.org/10.1046/j.1529-8817.2001.037004453.x
Meskiene I, Bögre L, Dahl M, et al. 1995. cycMs3, a novel B-type alfalfa cyclin gene, is induced in the G0-to-G1 transition of the cell cycle. The Plant Cell, 7(6): 759–771
Mironov V, De Veylder L, Van Montagu M, et al. 1999. Cyclin-dependent kinases and cell division in plants—the nexus. The Plant Cell, 11(4): 509–521
Niu Jun, Wang Jia, An Jiyong, et al. 2016. Integrated mRNA and miRNA transcriptome reveal a cross-talk between developing response and hormone signaling for the seed kernels of Siberian apricot. Scientific Reports, 6: 35675, doi: https://doi.org/10.1038/srep35675
Pérez-Mayorga D M, Ladah L B, Zertuche-González J A, et al. 2011. Nitrogen uptake and growth by the opportunistic macroalga Ulva lactuca (Linnaeus) during the internal tide. Journal of Experimental Marine Biology and Ecology, 406(1–2): 108–115
Patel D, Franklin K A. 2009. Temperature-regulation of plant architecture. Plant Signaling & Behavior, 4(7): 577–579
Paul S, Datta S K, Datta K. 2015. miRNA regulation of nutrient homeostasis in plants. Frontiers in Plant Science, 6: 232
Reichheld J P, Chaubet N, Shen Wenhui, et al. 1996. Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proceedings of the National Academy of Sciences of the United States of America, 93(24): 13819–13824, doi: https://doi.org/10.1073/pnas.93.24.13819
Stumpf R P, Gelfenbaum G, Pennock J R. 1993. Wind and tidal forcing of a buoyant plume, Mobile Bay, Alabama. Continental Shelf Research, 13(11): 1281–1301, doi: https://doi.org/10.1016/0278-4343(93)90053-Z
Suzuki N, Rivero R M, Shulaev V, et al. 2014. Abiotic and biotic stress combinations. New Phytologist, 203(1): 32–43, doi: https://doi.org/10.1111/nph.12797
Taylor R, Fletcher R L, Raven J A. 2001. Preliminary studies on the growth of selected’ Green tide’ algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Botanica Marina, 44(4): 327–336
Vidal E A, Araus V, Lu Cheng, et al. 2010. Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America, 107(9): 4477–4482, doi: https://doi.org/10.1073/pnas.0909571107
Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4): 669–687, doi: https://doi.org/10.1016/j.cell.2009.01.046
Wang Zongling, Xiao Jie, Fan Shiliang, et al. 2015. Who made the world’s largest green tide in China?—an integrated study on the initiation and early development of the green tide in Yellow Sea Limnology and Oceanography, 60(4): 1105–1117, doi: https://doi.org/10.1002/lno.10083
Xu Zhenhua, Zhong Sihui, Li Xinhai, et al. 2011. Genome-wide identification of microRNAs in response to low nitrate availability in maize leaves and roots. PLoS One, 6(11): e28009, doi: https://doi.org/10.1371/journal.pone.0028009
Zhang Baohong. 2015. MicroRNA: a new target for improving plant tolerance to abiotic stress. Journal of Experimental Botany, 66(7): 1749–1761, doi: https://doi.org/10.1093/jxb/erv013
Zhao Meng, Ding Hong, Zhu Jiankang, et al. 2011. Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytologist, 190(4): 906–915, doi: https://doi.org/10.1111/J.1469-8137.2011.03647.x
Author information
Authors and Affiliations
Corresponding author
Additional information
Foundation item
The National Key R&D Program of China under contract No. 2016YFC1402102; the project funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).
Rights and permissions
About this article
Cite this article
Yang, J., Yu, D. & Shen, S. Expression analyses of miRNA Up-MIR-843 and its target genes in Ulva prolifera. Acta Oceanol. Sin. 39, 27–34 (2020). https://doi.org/10.1007/s13131-020-1657-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13131-020-1657-2