Abstract
MicroRNAs (miRNAs) play key roles in regulating zinc (Zn) toxicity tolerance in plants. Solanum nigrum is a typical Zn/Cd-accumulating plant that has a high Zn/Cd tolerance. Despite their importance, no miRNAs have been identified from S. nigrum thus far. In this study, small RNA sequencing was used to identify Zn-responsive miRNAs in S. nigrum roots. We identified 176 differentially expressed miRNAs in S. nigrum roots in response to Zn toxicity. We also found that all these differentially expressed Zn-miRNAs simultaneously respond to the exogenous NO donor sodium nitroprusside (SNP), indicating that NO is involved in Zn-mediated miRNA expression in S. nigrum. These differentially expressed miRNAs are involved in regulating the following processes in S. nigrum roots: phenylpropanoid catabolic and metabolic processes; lignin catabolic and metabolic processes; and programmed cell death in response to ROS. These results suggest that these miRNAs play key roles in the Zn toxicity tolerance of S. nigrum.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221
Correa-Aragunde NM, Graziano ML, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905
Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573
Gupta OP, Sharma P, Gupta RK, Sharma I (2014) MicroRNA mediated regulation of metal toxicity in plants: present status and future perspectives. Plant Mol Biol 84:1–18
Hoagland DR, Arnon DI (1950) The water-culture for growing plants without soil. California Agricultural Experiment Station Circular 347, Berkeley
Jin Q, Xue Z, Dong C et al (2015) Identification and characterization of MICRORNAS from tree peony (Paeonia ostii) and their response to copper stress. PLoS One 10:e0117584
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53
Kramer U, Talkea IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272
Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25
Li YL, Zhang Y, Shi DQ, Liu XJ, Ge Q, Xu LH, Pan XL, Li W, Qin J, Zhu YY, Xu J (2013) Spatial-temporal analysis of zinc homeostasis reveals the response mechanisms to zinc deficiency in Sorghum bicolor. New Phytol 200:1102–1115
Michael PI, Krishnaswamy M (2011) The effect of zinc stress combined with high irradiance stress on membrane damage and antioxidative response in bean seedlings. Environ Exp Bot 74:171–177
Mittra B, Ghosh P, Henry SL, Mishra J, Das TK, Ghosh S, Mohanty P (2004) Novel mode of resistance to Fusarium infection by a mild dose pre-exposure of cadmium in wheat. Plant Physiol Biochem 42:781–787
Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:277–284
Sharma PN, Kumar P, Tewari RK (2004) Early signs of oxidative stress in wheat plants subjected to zinc deficiency. J Plant Nutr 27:449–461
Shi DQ, Zhang Y, Li YL, Xu J (2013) Identification of zinc deficiency-responsive microRNAs in Brassica juncea roots by small RNA sequencing. J Integr Agric 12:2036–2044
Song CN, Wang C, Zhang CQ, Nicholas KK, Yu HP, Ma ZQ, Fang JG (2010) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genom 11:431
Su J, Liu X, Sun H et al (2015) Identification of differentially expressed microRNAs in placentas of cloned and normally produced calves by Solexa sequencing. Anim Reprod Sci 155:64–74
Sun J, Wang S, Li C et al (2014) Novel expression profiles of microRNAs suggest that specific miRNAs regulate gene expression for the sexual maturation of female Schistosoma japonicum after pairing. Parasites Vectors 7:1
Wang C, Zhang SH, Wang PF, Hou J, Zhang WJ, Li W, Lin ZP (2009) The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. Chemosphere 75:1468–1476
Wang R, Xu L, Zhu X et al (2015) Transcriptome-wide characterization of novel and heat-stress-responsive microRNAs in radish (Raphanus sativus L.) using next-generation sequencing. Plant Mol Biol Rep 33:867–880
Xu J, Yin HX, Li X (2009) Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep 28:325–333
Xu J, Yin H, Li Y, Liu X (2010) Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol 154:1319–1334
Xu J, Wang WY, Sun JH, Zhang Y, Ge Q, Du LG, Yin HX, Liu XJ (2011) Involvement of auxin and nitric oxide in plant Cd-stress responses. Plant Soil 346:107–119
Yao YY, Guo GG, Ni ZF, Sunkar R, Du JK, Zhu JK, Sun QX (2007) Cloning and characterization of microRNAs from wheat (Triticum aestivum L.). Genome Biol 8:R96
Zhao CZ, Xia H, Frazier T, Yao YY, Bi YP, Li AQ, Li MJ, Li CS, Zhang BH, Wang XJ (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3
Zhou ZS, Song JB, Yang ZM (2012) Genome-wide identification of Brassica napus microRNAs and their targets in response to cadmium. J Exp Bot 63:4597–4613
Zhu L, Chen T, Sui M et al (2016) Comparative profiling of differentially expressed microRNAs between the follicular and luteal phases ovaries of goats. SpringerPlus 5:1233
Acknowledgements
This work was supported by the China National Natural Sciences Foundation (31170228, 31272239), the National Key Research and Development Program of China (2016YFC0501901), Yunnan Province Foundation for academic leader (2014HB043), and Hebei Province National Natural Sciences Foundation for Distinguished Young Scientists (C2013503042). The authors gratefully acknowledge the Central Laboratory of the Xishuangbanna Tropical Botanical Garden for providing research facilities.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Schleiff.
Z. Xie, P. Zhang, and Jingjing Zhao contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xie, Z., Zhang, P., Zhao, J. et al. Identification of microRNAs from Zn-treated Solanum nigrum roots by small RNA sequencing. Acta Physiol Plant 39, 32 (2017). https://doi.org/10.1007/s11738-016-2337-x
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-016-2337-x