Abstract
MicroRNAs (miRNAs) play key roles in plant responses to various metal stresses. To investigate the miRNA-mediated plant response to heavy metals, cotton (Gossypium hirsutum L.), the most important fiber crop in the world, was exposed to different concentrations (0, 25, 50, 100, and 200 µM) of lead (Pb) and then the toxicological effects were investigated. The expression patterns of 16 stress-responsive miRNAs and 10 target genes were monitored in cotton leaves and roots by quantitative real-time PCR (qRT-PCR); of these selected genes, several miRNAs and their target genes are involved in root development. The results show a reciprocal regulation of cotton response to lead stress by miRNAs. The characterization of the miRNAs and the associated target genes in response to lead exposure would help in defining the potential roles of miRNAs in plant adaptation to heavy metal stress and further understanding miRNA regulation in response to abiotic stress.
Similar content being viewed by others
References
Ali I, Amin I, Briddon RW, Mansoor S (2013) Artificial microRNA-mediated resistance against the monopartite begomovirus cotton leaf curl Burewala virus. Virol J 10:231. doi:10.1186/1743-422X-10-231
Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141(3):988–999. doi:10.1104/pp. 106.079707
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297
Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233. doi:10.1016/j.cell.2009.01.002
Bharwana SA, Ali S, Farooq MA, Ali B, Iqbal N, Abbas F, Ahmad MS (2014) Hydrogen sulfide ameliorates lead-induced morphological, photosynthetic, oxidative damages and biochemical changes in cotton. Environ Sci Pollut Res Int 21(1):717–731. doi:10.1007/s11356-013-1920-6
Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190. doi:10.1126/science.1159151
Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLoS One 7(5):e34783. doi:10.1371/journal.pone.0034783
Butcher, DJ (2009) Phytoremediation of lead in soil: recent applications and future prospects. Appl Spectrosc Rev 44(2):123–139
Chen L, Wang T, Zhao M, Tian Q, Zhang WH (2012) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235(2):375–386. doi:10.1007/s00425-011-1514-9
Daud MK, Ali S, Variath MT, Zhu SJ (2013) Differential physiological, ultramorphological and metabolic responses of cotton cultivars under cadmium stress. Chemosphere 93(10):2593–2602
Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62(10):3563–3573. doi:10.1093/jxb/err046
Eldem V, Okay S, Unver T (2013) Plant microRNAs: new players in functional genomics. Turk J Agric For 37(1):1–21. doi:10.3906/tar-1206-50
Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249. doi:10.1016/j.ecoenv.2013.07.006
Frazier TP, Burklew CE, Zhang B (2014) Titanium dioxide nanoparticles affect the growth and microRNA expression of tobacco (Nicotiana tabacum). Funct Integr Genom 14(1):75–83. doi:10.1007/s10142-013-0341-4
Gielen H, Remans T, Vangronsveld J, Cuypers A (2012) MicroRNAs in metal stress: specific roles or secondary responses? Int J Mol Sci 13(12):15826–15847. doi:10.3390/ijms131215826
Grejtovský A, Mo K, Nováková L (2008) Lead uptake by Matricaria chamomilla L. Plant Soil Environ 54(2):47–54
Gupta DK, Nicoloso FT, Schetinger MR, Rossato LV, Huang HG, Srivastava S, Yang XE (2011) Lead induced responses of Pfaffia glomerata, an economically important Brazilian medicinal plant, under in vitro culture conditions. Bull Environ Contam Toxicol 86(3):272–277. doi:10.1007/s00128-011-0226-y
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(1–2):1–18. doi:10.1007/s11103-013-0120-6
Hossain Z, Komatsu S (2012) Contribution of proteomic studies towards understanding plant heavy metal stress response. Front Plant Sci 3:310. doi:10.3389/fpls.2012.00310
Huang SQ, Xiang AL, Che LL, Chen S, Li H, Song JB, Yang ZM (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8(8):887–899. doi:10.1111/j.1467-7652.2010.00517.x
Jeong D-H, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. J Plant Biol 56(4):187–197. doi:10.1007/s12374-013-0213-4
Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6):787–799. doi:10.1016/j.molcel.2004.05.027
Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Integr Genom 10(4):493–507. doi:10.1007/s10142-010-0181-4
Kidner CA, Martienssen RA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428(6978):81–84. doi:10.1038/nature02366
Levine E, McHale P, Levine H (2007) Small regulatory RNAs may sharpen spatial expression patterns. PLoS Comput Biol 11(3)
Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci CMLS 69(19):3187–3206. doi:10.1007/s00018-012-1089-z
Liu Q, Zhang H (2012) Molecular identification and analysis of arsenite stress-responsive miRNAs in rice. J Agric Food Chem 60(26):6524–6536. doi:10.1021/jf300724t
Liu D, Jiang W, Liu C, Xin C, Hou W (2000) Uptake and accumulation of lead by roots, hypocotyls and shoots of Indian mustard [Brassica juncea (L.)]. Bioresour Technol 71 273 ± 277
Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297(5589):2053–2056. doi:10.1126/science.1076311
Lopez-Gomollon S, Mohorianu I, Szittya G, Moulton V, Dalmay T (2012) Diverse correlation patterns between microRNAs and their targets during tomato fruit development indicates different modes of microRNA actions. Planta 236(6):1875–1887. doi:10.1007/s00425-012-1734-7
Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38(Suppl):S31–S36. doi:10.1038/ng1791
Mendoza-Soto AB, Sanchez F, Hernandez G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:105. doi:10.3389/fpls.2012.00105
Needleman H (2004) Lead poisoning. Annu Rev Med 55:209–222. doi:10.1146/annurev.med.55.091902.103653
Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510. doi:10.1146/annurev.arplant.043008.092111
Schutzendubel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53(372):1351–1365
Srivastava S, Srivastava AK, Suprasanna P, D’Souza SF (2013) Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. J Exp Bot 64(1):303–315. doi:10.1093/jxb/ers333
Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18(8):2051–2065. doi:10.1105/tpc.106.041673
Sunkar R, Chinnusamy V, Zhu J, Zhu JK (2007) Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends Plant Sci 12(7):301–309. doi:10.1016/j.tplants.2007.05.001
Valdes-Lopez O, Yang SS, Aparicio-Fabre R, Graham PH, Reyes JL, Vance CP, Hernandez G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187(3):805–818. doi:10.1111/j.1469-8137.2010.03320.x
Wang M, Wang Q, Zhang B (2013) Response of miRNAs and their targets to salt and drought stresses in cotton (Gossypium hirsutum L.). Gene 530(1):26–32. doi:10.1016/j.gene.2013.08.009
Wierzbicka M, Potocka A (2002) Lead tolerance in plants growing on dry and moist soils. Acta Biol Cracov Ser Bot 44:21–28
Xie FL, Huang SQ, Guo K, Xiang AL, Zhu YY, Nie L, Yang ZM (2007) Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett 581(7):1464–1474. doi:10.1016/j.febslet.2007.02.074
Xie F, Stewart CN, Taki FA, He Q, Liu H, Zhang B (2014) High-throughput deep sequencing shows that microRNAs play important roles in switchgrass responses to drought and salinity stress. Plant Biotechnol J 12:354–366. doi:10.1111/pbi.12142
Yang ZM, Chen J (2013) A potential role of microRNAs in plant response to metal toxicity. Metallomics Integr Biometal Sci 5(9):1184–1190. doi:10.1039/c3mt00022b
Yang X, Wang L, Yuan D, Lindsey K, Zhang X (2013) Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. J Exp Bot 64(6):1521–1536. doi:10.1093/jxb/ert013
Yao Y, Ni Z, Peng H, Sun F, Xin M, Sunkar R, Zhu J-K, Sun Q (2010) Non-coding small RNAs responsive to abiotic stress in wheat (Triticum aestivum L.). Funct Integr Genom 10(2):187–190. doi:10.1007/s10142-010-0163-6
Yin Z, Li Y, Han X, Shen F (2012a) Genome-wide profiling of miRNAs and other small non-coding RNAs in the Verticillium dahliae-inoculated cotton roots. PLoS One 7(4):e35765. doi:10.1371/journal.pone.0035765
Yin Z, Li Y, Yu J, Liu Y, Li C, Han X, Shen F (2012b) Difference in miRNA expression profiles between two cotton cultivars with distinct salt sensitivity. Mol Biol Rep 39(4):4961–4970. doi:10.1007/s11033-011-1292-2
Zahur M, Maqbool A, Ifran M, Barozai MY, Rashid B, Riazuddin S, Husnain T (2009) Isolation and functional analysis of cotton universal stress protein promoter in response to phytohormones and abiotic stresses. Mol Biol 43(4):628–635
Zhang B, Pan X (2009) Expression of microRNAs in cotton. Mol Biotechnol 42(3):269–274. doi:10.1007/s12033-009-9163-y
Zhang BH, Pan XP, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46(2):243–259. doi:10.1111/j.1365-313X.2006.02697.X
Zhang B, Wang Q, Wang K, Pan X, Liu F, Guo T, Cobb GP, Anderson TA (2007a) Identification of cotton microRNAs and their targets. Gene 397(1–2):26–37. doi:10.1016/j.gene.2007.03.020
Zhang BH, Wang QL, Pan XP (2007b) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210(2):279–289. doi:10.1002/jcp.20869
Zhou ZS, Huang SQ, Guo K, Mehta SK, Zhang PC, Yang ZM (2007) Metabolic adaptations to mercury-induced oxidative stress in roots of Medicago sativa L. J Inorg Biochem 101(1):1–9. doi:10.1016/j.jinorgbio.2006.05.011
Zhou ZS, Huang SQ, Yang ZM (2008) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374(3):538–542. doi:10.1016/j.bbrc.2008.07.083
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(12):4597–4613. doi:10.1093/jxb/ers136
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table S1
(XLS 30 kb)
Supplementary Table S2
(XLS 28 kb)
Rights and permissions
About this article
Cite this article
He, Q., Zhu, S. & Zhang, B. MicroRNA–target gene responses to lead-induced stress in cotton (Gossypium hirsutum L.). Funct Integr Genomics 14, 507–515 (2014). https://doi.org/10.1007/s10142-014-0378-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-014-0378-z