Abstract
Heavy metals (HMs), in particular the toxic/carcinogenic non-essential ones including cadmium (Cd), arsenic (As), aluminum (Al), mercury (Hg), and lead (Pb) are known to exert severe impacts on plant growth and yields. HM contamination and/or toxicity is seen a major threat for global food production, quality, and security. Plants use intricate molecular mechanisms for responding and adapting to HM stress, both at transcriptional and post-transcriptional levels, and microRNA (miRNA) have emerged as key post-transcriptional regulators. These tiny (19–25 nucleotide) non-coding RNA species found abundantly in plants are pivotal in tight regulation of gene expression via miRNA-directed mRNA cleavage, translational repression, chromatin remodeling, or through epigenetic modification. MiRNAs are reported to be involved in regulation of HM uptake and transport, besides their chelation and homeostasis, as well as in HM-induced oxidative stress and antioxidative defense. There are also reports of involvement of miRNAs in metallic cross- and co-tolerance. Technological advents in small RNA sequencing coupled with computational tools and databases have resulted into the identification, characterization, and validation of several HM-responsive miRNAs along with their respective target genes. Through his review, we present and discuss current understandings on miRNAs, their biosynthesis, and functions in plants, emphasizing on HM stress responses and adaptations. The main aim of this review is to discuss the possible exploration of plant miRNAs as potential targets for engineering plants (via loss-/gain-of-function approaches) to confer HM tolerance. Successful case studies, current challenges, and future directions are also discussed.
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References
Abedi T, Mojiri A (2020) Cadmium uptake by wheat (Triticum aestivum L.): an overview. Plants 9(4):500. https://doi.org/10.3390/plants9040500
Adamiec E, Jarosz-Krzemińska E, Wieszała R (2016) Heavy metals from non-exhaust vehicle emissions in urban and motorway road dusts. Environ Monit Assess 188(6):369. https://doi.org/10.1007/s10661-016-5377-1
Alias NF, Khan MF, Sairi NA et al (2020) Characteristics, emission sources, and risk factors of heavy metals in PM 25 from Southern Malaysia. ACS Earth Space Chem. 8:1309–1323. https://doi.org/10.1021/acsearthspacechem.0c00103
Anwar S, Khan S, Ashraf MY et al (2017) Impact of chelator-induced phytoextraction of cadmium on yield and ionic uptake of maize. Int J Phytoremed 19:505–513. https://doi.org/10.1080/15226514.2016.1254153
Arif N, Yadav V, Singh S et al (2016) Influence of high and low levels of plant-beneficial heavy metal ions on plant growth and development. Front Environ Sci 4:69. https://doi.org/10.3389/fenvs.2016.00069
ATSDR (2012) Agency for Toxic Substances and Disease Registry. Toxicological profile for cadmium. Available at: https://www.atsdr.cdc.gov/toxprofiles/tp5.pdf accessed on June 03, 2021
ATSDR (2020) Agency for Toxic Substances and Disease Registry. Toxicological profile for lead. Available at: https://www.atsdr.cdc.gov/toxprofiles/tp13.pdf, accessed on June, 03, 2021
Axelsen KB, Palmgren MG (2001) Inventory of the superfamily of P-Type Ion Pumps in Arabidopsis. Plant Physiol 126:696–706. https://doi.org/10.1104/pp.126.2.696
Bai B, Bian H, Zeng Z et al (2017) miR393-mediated auxin signaling regulation is involved in root elongation inhibition in response to toxic aluminum stress in barley. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcw211
Bakhat HF, Zia Z, Fahad S et al (2017) Arsenic uptake, accumulation and toxicity in rice plants: possible remedies for its detoxification: a review. Environ Sci Pollut Res 24:9142–9158. https://doi.org/10.1007/s11356-017-8462-2
Barrera-Figueroa BE, Gao L, Wu Z et al (2012) High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biol 12:132. https://doi.org/10.1186/1471-2229-12-132
Bartel DP (2004) MicroRNAs Cell 116:281–297. https://doi.org/10.1016/S0092-8674(04)00045-5
Beckers F, Rinklebe J (2017) Cycling of mercury in the environment: Sources, fate, and human health implications: A review. Crit Rev Environ Sci Technol 47:693–794. https://doi.org/10.1080/10643389.2017.1326277
Bienert GP, Thorsen M, Schüssler MD et al (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH)3 and Sb(OH)3 across membranes. BMC Biol 6:26. https://doi.org/10.1186/1741-7007-6-26
Bologna NG, Voinnet O (2014) The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu Rev Plant Biol 65:473–503. https://doi.org/10.1146/annurev-arplant-050213-035728
Bortey-Sam N, Nakayama S, Akoto O et al (2015) Accumulation of heavy metals and metalloid in foodstuffs from agricultural soils around tarkwa area in Ghana, and associated human health risks. Int J Environ Res Public Health 12:8811–8827. https://doi.org/10.3390/ijerph120808811
Bouazizi H, Jouili H, Geitmann A, El Ferjani E (2010) Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol Environ Saf 73:1304–1308. https://doi.org/10.1016/j.ecoenv.2010.05.014
Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genom 15:523–531. https://doi.org/10.1007/s10142-015-0451-2
Çelik Ö, Ayan A, Meriç S, Atak Ç (2020) Heavy Metal Stress-Responsive Phyto-miRNAs. In: Faisal M., Saquib Q., Alatar A.A. A-KAA (ed) Cellular and Molecular Phytotoxicity of Heavy Metals. Nanotechnology in the Life Sciences. Springer Cham pp 137–155. https://doi.org/10.1007/978-3-030-45975-8_9
Chaves SS, Fernandes-Brum CN, Silva GFF et al (2015) New insights on coffea miRNAs: features and evolutionary conservation. Appl Biochem Biotechnol 177:879–908. https://doi.org/10.1007/s12010-015-1785-x
Chen L, Wang T, Zhao M et al (2012) Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235:375–386. https://doi.org/10.1007/s00425-011-1514-9
Chen Q, Lu X, Guo X et al (2018) Differential responses to Cd stress induced by exogenous application of Cu, Zn or Ca in the medicinal plant Catharanthus roseus. Ecotoxicol Environ Saf 157:266–275. https://doi.org/10.1016/j.ecoenv.2018.03.055
Chinnusamy V, Zhu J, Zhou T, Small Z-K, Rnas, (2007) Big Role In Abiotic Stress Tolerance Of Plants. Advances in molecular breeding toward drought and salt tolerant crops. Springer, Netherlands, Dordrecht, pp 223–260
Chowra U, Yanase E, Koyama H, Panda SK (2017) Aluminium-induced excessive ROS causes cellular damage and metabolic shifts in black gram Vigna mungo (L.) Hepper. Protoplasma 254:293–302. https://doi.org/10.1007/s00709-016-0943-5
Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiol 116:1063–1072. https://doi.org/10.1104/pp.116.3.1063
D’Ario M, Griffiths-Jones S, Kim M (2017) Small RNAs: big impact on plant development. Trends Plant Sci 22:1056–1068. https://doi.org/10.1016/j.tplants.2017.09.009
DalCorso G, Manara A, Furini A (2013) An overview of heavy metal challenge in plants: from roots to shoots. Metallomics 5:1117–1132. https://doi.org/10.1039/c3mt00038a
Ding Y, Ding L, Xia Y et al (2020) Emerging RZOLES of microRNAs in plant heavy metal tolerance and homeostasis. J Agric Food Chem 68:1958–1965. https://doi.org/10.1021/acs.jafc.9b07468
Ding Y, Gong S, Wang Y et al (2018) MicroRNA166 modulates cadmium tolerance and accumulation in rice. Plant Physiol 177:1691–1703. https://doi.org/10.1104/pp.18.00485
Ding Y, Wang Y, Jiang Z et al (2017) MicroRNA268 overexpression affects rice seedling growth under cadmium stress. J Agric Food Chem 65:5860–5867. https://doi.org/10.1021/acs.jafc.7b01164
Ding Y, Ye Y, Jiang Z et al (2016) MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front Plant Sci 7:1–10. https://doi.org/10.3389/fpls.2016.00235
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. https://doi.org/10.1093/jxb/err046
DiTusa SF, Fontenot EB, Wallace RW et al (2016) A member of the Phosphate transporter 1 (Pht1) family from the arsenic-hyperaccumulating fern Pteris vittata is a high-affinity arsenate transporter. New Phytol 209:762–772. https://doi.org/10.1111/nph.13472
Drott A (2009) Chemical speciation and transformation of mercury in contaminated sediments (pp. 51–57). Umea, Sweden: Swedish University of Agricultural Sciences. https://pub.epsilon.slu.se/1990/1/Drott_A_090429.pdf
Dubey S, Shri M, Gupta A et al (2018) Toxicity and detoxification of heavy metals during plant growth and metabolism. Environ Chem Lett 16:1169–1192. https://doi.org/10.1007/s10311-018-0741-8
Duan L, Yu J, Xu L et al (2019) Functional characterization of a type 4 metallothionein gene (CsMT4) in cucumber. Hortic Plant J 5:120–128. https://doi.org/10.1016/j.hpj.2019.04.002
Edelstein M, Ben-Hur M (2018) Heavy metals and metalloids: Sources, risks and strategies to reduce their accumulation in horticultural crops. Sci Hortic 234:431–444. https://doi.org/10.1016/j.scienta.2017.12.039
Fang Y, Spector DL (2007) Identification of nuclear dicing bodies containing proteins for microrna biogenesis in living Arabidopsis plants. Curr Biol 17:818–823. https://doi.org/10.1016/j.cub.2007.04.005
Feng SJ, Zhang XD, Liu XS et al (2016) Characterization of long non-coding RNAs involved in cadmium toxic response in Brassica napus. RSC Adv 6:82157–82173. https://doi.org/10.1039/C6RA05459E
Filiz E, Saracoglu IA, Ozyigit II, Yalcin B (2019) Comparative analyses of phytochelatin synthase (PCS) genes in higher plants. Biotechnol Biotechnol Equip 33:178–194. https://doi.org/10.1080/13102818.2018.1559096
Franić M, Galić V (2019) As, Cd, Cr, Cu, Hg: Physiological Implications and Toxicity in Plants. Plant Metallomics and Functional Omics. Springer International Publishing, Cham, pp 209–251
Gao J, Liang Y, Li J et al (2021) Identification of a bacterial-type ATP-binding cassette transporter implicated in aluminum tolerance in sweet sorghum (Sorghum bicolor L. Plant Signal Behav. https://doi.org/10.1080/15592324.2021.1916211
Gao J, Luo M, Peng H et al (2019) Characterization of cadmium-responsive MicroRNAs and their target genes in maize (Zea mays) roots. BMC Mol Biol 20:1–9. https://doi.org/10.1186/s12867-019-0131-1
Gautam M, Pandey D, Agrawal SB, Agrawal M (2016) Metals from Mining and Metallurgical Industries and Their Toxicological Impacts on Plants In: Singh A., Prasad S. (eds) Plant Responses to Xenobiotics Springer Singapore Singapore, pp 231–272
Ghori N-H, Ghori T, Hayat MQ et al (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16:1807–1828. https://doi.org/10.1007/s13762-019-02215-8
Gielen H, Remans T, Vangronsveld J, Cuypers A (2012) MicroRNAs in metal stress: specific roles or secondary responses? Int J Mol Sci 13:15826–15847. https://doi.org/10.3390/ijms131215826
Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2007) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158. https://doi.org/10.1093/nar/gkm952
Grobelak A, Kowalska A (2020) Heavy metal mobility in soil under futuristic climatic conditions In: Prasad MNV, Pietrzykowski M (eds), Climate change and soil interactions Elsevier https://doi.org/10.1016/B978-0-12-818032-7.00016-3
Hall JL, Williams LE (2003) Transition metal transporters in plants. J Exp Bot 54:2601–2613. https://doi.org/10.1093/jxb/erg303
Hasan MK, Cheng Y, Kanwar MK et al (2017) Responses of plant proteins to heavy metal stress—A review. Front Plant Sci 8:1492. https://doi.org/10.3389/fpls.2017.01492
Hauqe S, Ferdous A, Sarker S, Md. Islam T, Hossain K, (2016) Identification and expression profiling of microRNAs and their corresponding targets related to phytoremediation of heavy metals in jute (Corchorus olitorius var. O-9897). Biores Commun 2:152–157
He Q, Zhu S, Zhang B (2014) MicroRNA-target gene responses to lead-induced stress in cotton (Gossypium hirsutum L.). Funct Integr Genomics 14:507–515. https://doi.org/10.1007/s10142-014-0378-z
He X, Zheng W, Cao F, Wu F (2016a) Identification and comparative analysis of the microRNA transcriptome in roots of two contrasting tobacco genotypes in response to cadmium stress. Sci Rep 6:32805. https://doi.org/10.1038/srep32805
He Z, Yan H, Chen Y et al (2016b) An aquaporin PvTIP4;1 from Pteris vittata may mediate arsenite uptake. New Phytol 209:746–761. https://doi.org/10.1111/nph.13637
Hernández LE, Sobrino-Plata J, Montero-Palmero MB et al (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911. https://doi.org/10.1093/jxb/erv063
Hong Y-S, Kim Y-M, Lee K-E (2012) Methylmercury Exposure and Health Effects. J Prev Med Public Heal 45:353–363. https://doi.org/10.3961/jpmph.2012.45.6.353
Huang CY, Shirley N, Genc Y et al (2011) Phosphate utilization efficiency correlates with expression of low-affinity phosphate transporters and noncoding RNA, IPS1 in Barley. Plant Physiol 156:1217–1229. https://doi.org/10.1104/pp.111.178459
Huang SQ, Xiang AL, Che LL et al (2010) A set of miRNAs from Brassica napus in response to sulphate deficiency and cadmium stress. Plant Biotechnol J 8:887–899. https://doi.org/10.1111/j.1467-7652.2010.00517.x
Huang Y, Hu Y, Liu Y (2009) Heavy metal accumulation in iron plaque and growth of rice plants upon exposure to single and combined contamination by copper, cadmium and lead. Acta Ecol Sin 29:320–326. https://doi.org/10.1016/j.chnaes.2009.09.011
Huen A, Bally J, Smith P (2018) Identification and characterisation of microRNAs and their target genes in phosphate-starved Nicotiana benthamiana by small RNA deep sequencing and 5’RACE analysis. BMC Genomics 19:940. https://doi.org/10.1186/s12864-018-5258-9
Hussain S, Rengel Z, Qaswar M et al (2019) Arsenic and heavy metal (Cadmium, Lead, Mercury and Nickel) contamination in plant-based foods. J Plant Human Health 2:447–490
Isayenkov SV, Maathuis FJM (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7;1 is a pathway for arsenite uptake. FEBS Lett 582:1625–1628. https://doi.org/10.1016/j.febslet.2008.04.022
Jaishankar M, Tseten T, Anbalagan N et al (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72. https://doi.org/10.2478/intox-2014-0009
Jalmi SK, Bhagat PK, Verma D et al (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00012
Jamla M, Khare T, Joshi S, Patil S, Suprasanna P, Kumar V (2021) Omics approaches for understanding heavy metal responses and tolerance in plants. Curr Plant Biol 27:100213. https://doi.org/10.1016/j.cpb.2021.100213
Jian H, Yang B, Zhang A et al (2018) Genome-Wide Identification of MicroRNAs in response to cadmium stress in oilseed Rape (Brassica napus L.) using high-throughput sequencing. Int J Mol Sci 19:1431. https://doi.org/10.3390/ijms19051431
Joshi R, Dkhar J, Singla-Pareek SL, Pareek A (2019) Molecular Mechanism and Signaling Response of Heavy Metal Stress Tolerance in Plants. In: Srivastava S, Srivastava A, Suprasanna P (eds) Plant-Metal Interactions. Springer, Cham, pp 29–47
Katsuhara M, Sasano S, Horie T et al (2014) Functional and molecular characteristics of rice and barley NIP aquaporins transporting water, hydrogen peroxide and arsenite. Plant Biotechnol 31:213–219. https://doi.org/10.5511/plantbiotechnology.14.0421a
Khalid N, Aqeel M, Noman A (2019) System Biology of Metal Tolerance in Plants: An Integrated View of Genomics, Transcriptomics, Metabolomics, and Phenomics. In: Sablok G (ed) Plant Metallomics and Functional Omics. Springer International Publishing, Cham, pp 107–144
Khanam R, Kumar A, Nayak AK et al (2020) Metal(loid)s (As, Hg, Se, Pb and Cd) in paddy soil: Bioavailability and potential risk to human health. Sci Total Environ 699:134330. https://doi.org/10.1016/j.scitotenv.2019.134330
Khare T, Shriram V, Kumar V (2018) RNAi Technology: The Role in Development of Abiotic Stress-Tolerant Crops. In: Biochemical, Physiological and Molecular Avenues for Combating Abiotic Stress Tolerance in Plants. Elsevier, pp 117–133
Khraiwesh B, Zhu J-K, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta - Gene Regul Mech 1819:137–148. https://doi.org/10.1016/j.bbagrm.2011.05.001
Kim D-Y, Bovet L, Kushnir S et al (2006) AtATM3 Is Involved in Heavy Metal Resistance in Arabidopsis. Plant Physiol 140:922–932. https://doi.org/10.1104/pp.105.074146
Kim TH, Park JH, Kim MC, Cho SH (2008) Cutin monomer induces expression of the rice OsLTP5 lipid transfer protein gene. J Plant Physiol 165:345–349. https://doi.org/10.1016/j.jplph.2007.06.004
Kohli SK, Khanna K, Bhardwaj R et al (2019) Assessment of Subcellular ROS and NO Metabolism in Higher Plants: Multifunctional Signaling Molecules. Antioxidants 8:641. https://doi.org/10.3390/antiox8120641
Krämer U, Talke IN, Hanikenne M (2007) Transition metal transport. FEBS Lett 581:2263–2272. https://doi.org/10.1016/j.febslet.2007.04.010
Kumar A, Prasad MNV (2018) Plant-lead interactions: Transport, toxicity, tolerance, and detoxification mechanisms. Ecotoxicol Environ Saf 166:401–418. https://doi.org/10.1016/j.ecoenv.2018.09.113
Kumar V, Khare T, Shriram V, Wani SH (2018) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 37:61–75. https://doi.org/10.1007/s00299-017-2210-4
Kumarathilaka P, Seneweera S, Meharg A, Bundschuh J (2018) Arsenic accumulation in rice (Oryza sativa L.) is influenced by environment and genetic factors. Sci Total Environ 642:485–496. https://doi.org/10.1016/j.scitotenv.2018.06.030
Kumarathilaka P, Seneweera S, Ok YS et al (2019) Arsenic in cooked rice foods: Assessing health risks and mitigation options. Environ Int 127:584–591. https://doi.org/10.1016/j.envint.2019.04.004
Kumari S, Amit JR et al (2020) Recent developments in environmental mercury bioremediation and its toxicity: A review. Environ Nanotechnol Monit Manag 13:100283. https://doi.org/10.1016/j.enmm.2020.100283
Lee M, Lee K, Lee J et al (2005) AtPDR12 contributes to lead resistance in Arabidopsis. Plant Physiol 138:827–836. https://doi.org/10.1104/pp.104.058107
Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854. https://doi.org/10.1016/0092-8674(93)90529-Y
Li Z, Mei X, Li T et al (2021) Effects of calcium application on activities of membrane transporters in Panax notoginseng under cadmium stress. Chemosphere 262:127905. https://doi.org/10.1016/j.chemosphere.2020.127905
Lima JC, Arenhart RA, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817–2832. https://doi.org/10.4238/2011.November.10.4
Lin L, Li J, Yang X et al (2020) Simultaneous immobilization of arsenic and cadmium in paddy soil by Fe-Mn binary oxide. Elem Sci Anthr 8:094. https://doi.org/10.1525/elementa.2020.094
Liu Q, Hu H, Zhu L et al (2015) Involvement of miR528 in the regulation of arsenite tolerance in rice (Oryza sativa L.). J Agric Food Chem 63:8849–8861. https://doi.org/10.1021/acs.jafc.5b04191
Liu Q, Zhang H (2012) Molecular identification and analysis of arsenite stress-responsive miRNAs in rice. J Agri Food Chem 60(26):6524–6536. https://doi.org/10.1021/jf300724t
Ma JF, Shen RF, Shao JF (2021) Transport of cadmium from soil to grain in cereal crops: A review. Pedosphere 31:3–10. https://doi.org/10.1016/S1002-0160(20)60015-7
Ma X, An F, Wang L et al (2020) Genome-wide identification of aluminum-activated malate transporter (ALMT) gene family in rubber trees (Hevea brasiliensis) highlights their involvement in aluminum detoxification. Forests 11:142. https://doi.org/10.3390/f11020142
Mahapatra K, Banerjee S, Roy S (2020) The Hows and Whys of Heavy Metal-Mediated Phytotoxicity: An Insight. In: Faisal M, Quaiser A, Abdulrahman A, Al-Khedhairy AA (eds) Cellular and Molecular Phytotoxicity of Heavy Metals. Cham Springer, pp 19–41
Martín-Rodríguez AJ, Ariani A, Leija A et al (2021) Phaseolus vulgaris MIR1511 genotypic variations differentially regulate plant tolerance to aluminum toxicity. Plant J 105:1521–1533. https://doi.org/10.1111/tpj.15129
Mendoza-Soto AB, Sánchez F, Hernández G (2012) MicroRNAs as regulators in plant metal toxicity response. Front Plant Sci 3:1–7. https://doi.org/10.3389/fpls.2012.00105
Mitani-Ueno N, Yamaji N, Ma JF (2016) High Silicon Accumulation in the shoot is required for down-regulating the expression of SI transporter genes in rice. Plant Cell Physiol 57:2510–2518. https://doi.org/10.1093/pcp/pcw163
Moon J, Belloeil C, Ianna M, Shin R (2019) Arabidopsis CNGC family members contribute to heavy metal ion uptake in plants. Int J Mol Sci 20:413. https://doi.org/10.3390/ijms20020413
Moon S, Jung KH (2014) Genome-wide expression analysis of rice ABC transporter family across spatio-temporal samples and in response to abiotic stresses. J Plant Physiol 171(14):1276–1288. https://doi.org/10.1016/j.jplph.2014.05.006
Mosa KA, Kumar K, Chhikara S et al (2012) Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21:1265–1277. https://doi.org/10.1007/s11248-012-9600-8
Murasugi A, Wada C, Hayashi Y (1981) Cadmium-Binding Peptide Induced in Fission Yeast, Schizosaccharomyces pombe. J Biochem 90:1561–1565. https://doi.org/10.1093/oxfordjournals.jbchem.a133627
Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8
Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750. https://doi.org/10.1007/s002530051457
Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24:10068–10082. https://doi.org/10.1007/s11356-017-8593-5
Noman A, Fahad S, Aqeel M et al (2017) miRNAs: Major modulators for crop growth and development under abiotic stresses. Biotechnol Lett 39:685–700. https://doi.org/10.1007/s10529-017-2302-9
Noman A, Sanaullah T, Khalid N, Islam W, Khan S, Kashif M, Aqeel IM (2019) Crosstalk between plant miRNA and heavy metal toxicity. In: Sablok G (ed) Plant metallomics and functional omics. Springer, Cham, pp 145–168. https://doi.org/10.1007/978-3-030-19103-0_7
Nozawa M, Miura S, Nei M (2012) Origins and evolution of MicroRNA genes in plant species. Genome Biol Evol 4:230–239. https://doi.org/10.1093/gbe/evs002
Ovečka M, Takáč T (2014) Managing heavy metal toxicity stress in plants: Biological and biotechnological tools. Biotechnol Adv 32:73–86. https://doi.org/10.1016/j.biotechadv.2013.11.011
Ozaki H, Watanabe I, Kuno K (2004) Investigation of the heavy metal sources in relation to automobiles. Water Air Soil Pollut 157:209–223. https://doi.org/10.1023/B:WATE.0000038897.63818.f7
Parihar P, Singh S, Singh R, et al (2019) An Integrated Transcriptomic, Proteomic, and Metabolomic Approach to Unravel the Molecular Mechanisms of Metal Stress Tolerance in Plants In: Srivastava S, Srivastava A, Suprasanna P (eds) Plant-Metal Interactions Springer, Cham. https://doi.org/10.1007/978-3-030-20732-8_1
Park MY, Wu G, Gonzalez-Sulser A et al (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci 102:3691–3696. https://doi.org/10.1073/pnas.0405570102
Patel P, Yadav K, Ganapathi TR, Penna S (2019) Plant miRNAome: Cross Talk in Abiotic Stressful Times. In: Rajpal V, Sehgal D, Kumar A, Raina S (eds) Genetic Enhancement of Crops for Tolerance to Abiotic Stress: Mechanisms and Approaches, Sustainable Development and Biodiversity. Springer, Cham. https://doi.org/10.1007/978-3-319-91956-0_2
Pedas P, Ytting CK, Fuglsang AT et al (2008) Manganese efficiency in Barley: identification and characterization of the metal ion transporter HvIRT1. Plant Physiol 148:455–466. https://doi.org/10.1104/pp.108.118851
Pilon M (2017) The copper microRNAs. New Phytol 213:1030–1035. https://doi.org/10.1111/nph.14244
Pourrut B, Shahid M, Dumat C et al (2011) Lead uptake, toxicity, and detoxification in plants. Rev Env Contam Toxicol 213:113–136. https://doi.org/10.1007/978-1-4419-9860-6_4
Rahman Z, Singh VP (2019) The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environ Monit Assess 191:419. https://doi.org/10.1007/s10661-019-7528-7
Rai KK, Pandey N, Meena RP, Rai SP (2021) Biotechnological strategies for enhancing heavy metal tolerance in neglected and underutilized legume crops: A comprehensive review. Ecotoxicol Environ Saf 208:111750. https://doi.org/10.1016/j.ecoenv.2020.111750
Regier N, Larras F, Bravo AG et al (2013) Mercury bioaccumulation in the aquatic plant Elodea nuttallii in the field and in microcosm: Accumulation in shoots from the water might involve copper transporters. Chemosphere 90:595–602. https://doi.org/10.1016/j.chemosphere.2012.08.043
Reinhart BJ (2002) MicroRNAs in plants. Genes Dev 16:1616–1626. https://doi.org/10.1101/gad.1004402
Rao KP, Vani G, Kumar K et al (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82. https://doi.org/10.1016/j.abb.2010.11.006
Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant MicroRNAs. Plant Cell 25:2383–2399. https://doi.org/10.1105/tpc.113.113159
Rout GR, Panigrahi J (2015) Analysis of signaling pathways during heavy metal toxicity a functional genomics perspective. Pandey G (ed) Elucidation of Abiotic Stress Signaling in Plants. Springer New York New York NY, Doi: https://doi.org/10.1007/978-1-4939-2540-7_11
Roychoudhury A., Chakraborty S (2020) Cellular and Molecular Phytotoxicity of Lead and Mercury. In: Faisal M., Saquib Q, Alatar AA, AlKhedhairy AA (eds) Cellular and Molecular Phytotoxicity of Heavy Metals Nanotechnology in the Life Sciences. Springer International Publishing Cham. pp 373–387 https://doi.org/10.1007/978-3-030-45975-8_18
Sandeep G, Vijayalatha KR, Anitha T (2019) Heavy metals and its impact in vegetable crops. Int J Chem Stud 7:1612–1621
Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice. Plant Cell 24:2155–2167. https://doi.org/10.1105/tpc.112.096925
Saxena P, Misra N (2010) Remediation of Heavy Metal Contaminated Tropical Land. In: Sherameti I, Varma A (eds) Soil Heavy Metals Soil Biology, vol 19. Springer, Berlin Heidelberg https://doi.org/10.1007/978-3-642-02436-8_19
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726. https://doi.org/10.1093/jxb/erj073
Shaw BP, Sahu SK, Mishra RK (2004) Heavy Metal Induced Oxidative Damage in Terrestrial Plants. In: Prasad MNV (ed) Heavy Metal Stress in Plants. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 84–126
Shriram V, Kumar V, Devarumath RM et al (2016) MicroRNAs As Potential Targets for Abiotic Stress Tolerance in Plants. Front Plant Sci 7:817. https://doi.org/10.3389/fpls.2016.00817
Shukla L, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta - Gene Regul Mech 1779:743–748. https://doi.org/10.1016/j.bbagrm.2008.04.004
Shukla T, Kumar S, Khare R et al (2015) Natural variations in expression of regulatory and detoxification related genes under limiting phosphate and arsenate stress in Arabidopsis thaliana. Front Plant Sci 6:898. https://doi.org/10.3389/fpls.2015.00898
Singh S, Parihar P, Singh R et al (2016) Heavy Metal Tolerance in Plants: Role of Transcriptomics, Proteomics, Metabolomics, and Ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143
Smeets K, Opdenakker K, Remans, et al (2013) The role of the kinase OXI1 in cadmium-and copper-induced molecular responses in Arabidopsis thaliana. Plant Cell Environ 36:1228–1238. https://doi.org/10.1111/pce.12056
Sone Y, Uraguchi S, Takanezawa Y et al (2017) A Novel Role of MerC in Methylmercury Transport and Phytoremediation of Methylmercury Contamination. Biol Pharm Bull 40:1125–1128. https://doi.org/10.1248/bpb.b17-00213
Sontheimer EJ (2005) Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol 6:127–138. https://doi.org/10.1038/nrm1568
Srivastava S, Srivastava AK, Suprasanna P, D’Souza SF (2013) Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea. J Exp Bot 64:303–315. https://doi.org/10.1093/jxb/ers333
Suprasanna P (2020) Plant abiotic stress tolerance: Insights into resilience build-up. J Biosci 45:120. https://doi.org/10.1007/s12038-020-00088-5
Stepien A, Knop K, Dolata J et al (2017) Posttranscriptional coordination of splicing and miRNA biogenesis in plants. Wiley Interdiscip Rev RNA 8:e1403. https://doi.org/10.1002/wrna.1403
Sun L, Ma Y, Wang H et al (2018) Overexpression of PtABCC1 contributes to mercury tolerance and accumulation in Arabidopsis and poplar. Biochem Biophys Res Commun 497:997–1002. https://doi.org/10.1016/j.bbrc.2018.02.133
Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17:196–203. https://doi.org/10.1016/j.tplants.2012.01.010
Sytar O, Ghosh S, Malinska H, Zivcak M, Brestic M (2020) Physiological and molecular mechanisms of metal accumulation in hyperaccumulator plants. Physiol Plant. https://doi.org/10.1111/ppl.13285
Thakur S, Singh L, Wahid ZA et al (2016) Plant-driven removal of heavy metals from soil: uptake, translocation, tolerance mechanism, challenges, and future perspectives. Environ Monit Assess 188:206. https://doi.org/10.1007/s10661-016-5211-9
UNEP (2010) Final review of scientific information on cadmium. Available at: https://www.unep.org/resources/report/final-review-scientific-information-cadmium, accessed on 11 June, 2021
Valdés-López O, Yang SS, Aparicio-Fabre R et al (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187:805–818. https://doi.org/10.1111/j.1469-8137.2010.03320.x
Verma PK, Verma S, Tripathi RD, Chakrabarty D (2020) A rice glutaredoxin regulate the expression of aquaporin genes and modulate root responses to provide arsenic tolerance. Ecotoxicol Environ Saf 195:110471. https://doi.org/10.1016/j.ecoenv.2020.110471
Voinnet O (2009) Origin, Biogenesis, and Activity of Plant MicroRNAs. Cell 136:669–687. https://doi.org/10.1016/j.cell.2009.01.046
Wang H, Shan X, Wen B et al (2007) Effect of indole-3-acetic acid on lead accumulation in maize (Zea mays L.) seedlings and the relevant antioxidant response. Environ Exp Bot 61:246–253. https://doi.org/10.1016/j.envexpbot.2007.06.004
Wang J, Mei J, Ren G (2019) Plant microRNAs: biogenesis, homeostasis, and degradation. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00360
Wang Y, Li R, Li D et al (2017) NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. Proc Natl Acad Sci U S A 114:5047–5052. https://doi.org/10.1073/pnas.1618557114
Wang Y, Zhao Z, Deng M, Liu R, Niu S, Fan G (2015) Identification and functional analysis of microRNAs and their targets in Platanus acerifolia under lead (Pb) stress. Int J Mol Sci 16(4):7098–7111. https://doi.org/10.3390/ijms16047098
Wani SH, Kumar V, Khare T et al (2020) miRNA applications for engineering abiotic stress tolerance in plants. Biologia 75:1063–1081. https://doi.org/10.2478/s11756-019-00397-7
Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855–862. https://doi.org/10.1016/0092-8674(93)90530-4
Wojas S, Ruszczyńska A, Bulska E et al (2007) Ca2+-dependent plant response to Pb2+ is regulated by LCT1. Environ Pollut 147:584–592. https://doi.org/10.1016/j.envpol.2006.10.012
Wu X, Hu J, Wu F et al (2021) Application of TiO2 nanoparticles to reduce bioaccumulation of arsenic in rice seedlings (Oryza sativa L): A mechanistic study. J Hazard Mater 405:124047. https://doi.org/10.1016/j.jhazmat.2020.124047
Xia J, Yamaji N, Kasai T, Ma JF (2010) Plasma membrane-localized transporter for aluminum in rice. Proc Natl Acad Sci USA 107:18381–18385. https://doi.org/10.1073/pnas.1004949107
Xia K, Zeng X, Jiao Z, Li M, Xu W, Nong Q, Mo H, Cheng T, Zhang M (2018) Formation of protein disulfide bonds catalyzed by OsPDIL1;1 is mediated by microRNA5144-3p in rice. Plant Cell Physiol 59(2):331–342. https://doi.org/10.1093/pcp/pcx189
Xie FL, Huang SQ, Guo K et al (2007) Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett 581:1464–1474. https://doi.org/10.1016/j.febslet.2007.02.074
Xie L, Hao P, Cheng Y et al (2018) Effect of combined application of lead, cadmium, chromium and copper on grain, leaf and stem heavy metal contents at different growth stages in rice. Ecotoxicol Environ Saf 162:71–76. https://doi.org/10.1016/j.ecoenv.2018.06.072
Xie Q, Yu Q, Jobe TO et al (2021) An amiRNA screen uncovers redundant CBF and ERF34/35 transcription factors that differentially regulate arsenite and cadmium responses. Plant Cell Environ 44:1692–1706. https://doi.org/10.1111/pce.14023
Xie Z, Allen E, Fahlgren N et al (2005) Expression of Arabidopsis MIRNA Genes. Plant Physiol 138:2145–2154. https://doi.org/10.1104/pp.105.062943
Xu J, Hou Q-M, Khare T et al (2019a) Exploring miRNAs for developing climate-resilient crops: A perspective review. Sci Total Environ 653:91–104. https://doi.org/10.1016/j.scitotenv.2018.10.340
Xu J, Hou Q-M, Khare T, Verma SK, Kumar V (2019b) Exploring miRNAs for developing climate-resilient crops: A perspective review. Sci Total Environ 653:91–104. https://doi.org/10.1016/j.scitotenv.2018.10.340
Xu L, Wang Y, Zhai L et al (2013) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64:4271–4287. https://doi.org/10.1093/jxb/ert240
Xu S, Sun B, Wang R et al (2017) Overexpression of a bacterial mercury transporter MerT in Arabidopsis enhances mercury tolerance. Biochem Biophys Res Commun 490:528–534. https://doi.org/10.1016/j.bbrc.2017.06.073
Yamaguchi N, Mori S, Baba K et al (2011) Cadmium distribution in the root tissues of solanaceous plants with contrasting root-to-shoot Cd translocation efficiencies. Environ Exp Bot 71:198–206. https://doi.org/10.1016/j.envexpbot.2010.12.002
Yamasaki H, Hayashi M, Fukazawa M et al (2009) SQUAMOSA promoter binding protein–like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361. https://doi.org/10.1105/tpc.108.060137
Yang Z, Chen J (2013) A potential role of microRNAs in plant response to metal toxicity. Metallomics 5:1184–1190. https://doi.org/10.1039/c3mt00022b
Zeng H, Xu L, Singh A et al (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci 6:600. https://doi.org/10.3389/fpls.2015.00600
Zhang B, Wang Q (2015) MicroRNA-based biotechnology for plant improvement. J Cell Physiol 230:1–15. https://doi.org/10.1002/jcp.24685
Zhang L, Ding H, Jiang H et al (2020a) Regulation of cadmium tolerance and accumulation by miR156 in Arabidopsis. Chemosphere 242:125168. https://doi.org/10.1016/j.chemosphere.2019.125168
Zhang LW, Song JB, Shu XX et al (2013) miR395 is involved in detoxification of cadmium in Brassica napus. J Hazard Mater 250–251:204–211. https://doi.org/10.1016/j.jhazmat.2013.01.053
Zhang X, Weir B, Wei B, Deng Z et al (2020b) Genome-wide identification and transcriptional analyses of MATE transporter genes in root tips of wild Cicer spp under aluminium stress. bioRxiv. https://doi.org/10.1101/2020.04.27.063065
Zhao M, Ding H, Zhu J et al (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915. https://doi.org/10.1111/j.1469-8137.2011.03647.x
Zhou M, Zheng S, Liu R et al (2019) The genome-wide impact of cadmium on microRNA and mRNA expression in contrasting Cd responsive wheat genotypes. BMC Genomics 20:1–19. https://doi.org/10.1186/s12864-019-5939-z
Zhou X, Joshi S, Khare T et al (2021a) Nitric oxide, crosstalk with stress regulators and plant abiotic stress tolerance. Plant Cell Rep. https://doi.org/10.1007/s00299-021-02705-5
Zhou X, Joshi S, Patil S, et al. (2021b) Reactive Oxygen, Nitrogen, Carbonyl and Sulfur Species and Their Roles in Plant Abiotic Stress Responses and Tolerance. J Plant Growth Regul doi: https://doi.org/10.1007/s00344-020-10294-y
Zhou X, Khare T, Kumar V (2020) Recent trends and advances in identification and functional characterization of plant miRNAs. Acta Physiol Plant 42:25. https://doi.org/10.1007/s11738-020-3013-8
Zhou ZS, Huang SQ, Yang ZM (2008) Bioinformatic identification and expression analysis of new microRNAs from Medicago truncatula. Biochem Biophys Res Commun 374:538–542. https://doi.org/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 63:4597–4613. https://doi.org/10.1093/jxb/ers136
Zhu F-Y, Li L, Lam PY et al (2013) Sorghum extracellular leucine-rich repeat protein SbLRR2 mediates lead tolerance in transgenic Arabidopsis. Plant Cell Physiol 54:1549–1559. https://doi.org/10.1093/pcp/pct101
Zwolak A, Sarzynska M, Szpyrka E, Stawarczyk K (2019) Sources of soil pollution by heavy metals and their accumulation in vegetables: a review. Water Air Soil Pollut 230:164. https://doi.org/10.1007/s11270-019-4221-y
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The authors acknowledge the use of facilities created at Modern College, Ganeshkhind, Pune through FIST Program (SR/FST/COLLEGE-/19/568) of the Department of Science and Technology (DST), Government of India, the DBT-Star College Scheme (BT/HRD/11/030/2012) and the DBT-BUILDER program of the Department of Biotechnology (DBT), Government of India.
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Jamla, M., Patil, S., Joshi, S. et al. MicroRNAs and Their Exploration for Developing Heavy Metal-tolerant Plants. J Plant Growth Regul 41, 2579–2595 (2022). https://doi.org/10.1007/s00344-021-10476-2
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DOI: https://doi.org/10.1007/s00344-021-10476-2