Abstract
Heavy metals (HMs) are among the most common environmental problems on a global scale and adversely affect plant growth and productivity. Several plants, including licorice, can carry out the phytoremediation process of HMs using a variety of protein families, including the Metal Tolerance Protein or MTP family. In the present study, 13 genes were recognized as MTP family members which had cation efflux domain. All of these proteins had transmembrane domains which were localized in a vacuole and divided phylogenetically into three sub-families (Zn-MTP, Mn-MTP, and Fe/Zn-MTP) and seven groups. GuMTPs exhibited similar gene structures inside the same sub-family, which was very evident for the Zn-MTP sub-family. The recognized simple sequence repeat (SSR) marker could be helpful in the marker selection associated programs. Analysis of gene-targeted miRNA and gene expression in different tissues and stress conditions found that the evaluated genes have a crucial role in plant development and respond to various stimuli. The expression of GuMTP9.2 and GuMTP8.1 increased under salinity stress due to their similar activation process thus it’s possible to up-regulation in response to HMs. Three-dimensional structures of this family identify the ligand-protein interactions through docking, which indicates this protein’s potential in the diffusion of HMs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- CDF:
-
Cation Diffusion Facilitator
- CBI:
-
Codon Bias Index
- ENC:
-
Effective Number of Codon
- GC3:
-
GC content at the third site position
- HMs:
-
Heavy Metals
- JA :
-
Jasmonic Acid
- KDD:
-
Knowledge Discovery from Data
- MTP:
-
Metal Tolerance Protein
- MeJA:
-
Methyl Jasmonate
- OS :
-
OxidativeStress
- ROS:
-
Reactive Oxygen Species
- RSCU:
-
Relative Synonymous Codon Usage
- SChi2:
-
Scaled Chi-square
- SSR:
-
Simple Sequence Repeat
References
Ahmad P (2016) Water stress and crop plants: a sustainable approach. Wiley, Hoboken. https://doi.org/10.1002/9781119054450
Armanini D, Nacamulli D, Francini-Pesenti F, Battagin G, Ragazzi E, Fiore C (2005) Glycyrrhetinic acid, the active principle of licorice, can reduce the thickness of subcutaneous thigh fat through topical application. Steroids 70(8):538–542. https://doi.org/10.1016/j.steroids.2005.01.007
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37 (suppl_2):W202-W208. https://doi.org/10.1093/nar/gkp335
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281–297. https://doi.org/10.1016/s0092-8674(04)00045-5
Bhaduri AM, Fulekar M (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Biotechnol 11(1):55–69. https://doi.org/10.1007/s11157-011-9251-x
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. https://doi.org/10.1371/journal.pone.0034783
Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301(5631):336–338. https://doi.org/10.1126/science.1085242
Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Sci 45(2):437–448. https://doi.org/10.2135/cropsci2005.0437
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7(7):309–315. https://doi.org/10.1016/S1360-1385(02)02295-1
De Mandal S, Mazumder TH, Panda AK, Kumar NS, Jin F (2020) Analysis of synonymous codon usage patterns of HPRT1 gene across twelve mammalian species. Genomics 112(1):304–311. https://doi.org/10.1016/j.ygeno.2019.02.010
Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V (2014)Stress-induced electrolyte leakage: the role of K+-permeable channels and involvement in programmed cell death and metabolic adjustment. J Exp Bot 65(5):1259–1270. https://doi.org/10.1093/jxb/eru004
Draghici S, Khatri P, Tarca AL, Amin K, Done A, Voichita C, Georgescu C, Romero R (2007) A systems biology approach for pathway level analysis. Genome Res 17(10):1537–1545. https://doi.org/10.1101/gr.6202607
Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) AgriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70. https://doi.org/10.1093/nar/gkx382
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.2307/2408678
Fu XZ, Tong YH, Zhou X, Ling LL, Chun CP, Cao L, Zeng M, Peng LZ (2017)Genome-wide identification of sweet orange (Citrus sinensis) metal tolerance proteins and analysis of their expression patterns under zinc, manganese, copper, and cadmium toxicity. Gene 629:1–8. https://doi.org/10.1016/j.gene.2017.07.072
Gao Y, Yang F, Liu J, Xie W, Zhang L, Chen Z, Peng Z, Ou Y, Yao Y (2020)Genome-wide identification of metal tolerance protein genes in Populus trichocarpa and their roles in response to various heavy metal stresses. Int J Mol Sci 21(5):1680. https://doi.org/10.3390/ijms21051680
Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: The proteomics protocols handbook. Springer, Berlin, pp 571–607. https://doi.org/10.1385/1-59259-584-7:531
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. https://doi.org/10.3390/ijms131215826
Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008)Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35(2):105–118. https://doi.org/10.1016/S1673-8527(08)60016-8
Guo J, Wu J, Ji Q, Wang C, Luo L, Yuan Y, Wang Y, Wang J (2008)Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genomics 35(2):105–118. https://doi.org/10.1016/S1673-8527(08)60016-8
Gupta N, Ram H, Kumar B (2016) Mechanism of Zinc absorption in plants: Uptake, transport, translocation and accumulation. Rev Environ Sci Biotechnol 15:89–109. https://doi.org/10.1007/s11157-016-9390-1
Gustin JL, Zanis MJ, Salt DE (2011) Structure and evolution of the plant cation diffusion facilitator family of ion transporters. BMC Evol Biol 11(1):76. https://doi.org/10.1186/1471-2148-11-76
Haasl RJ, Payseur BA (2012) Microsatellites as targets of natural selection. Mol Biol Evol 30(2):285–298. https://doi.org/10.1093/molbev/mss247
Hajiahmadi Z, Abedi A, Wei H, Sun W, Ruan H, Zhuge Q, Movahedi A (2020) Identification, evolution, expression, and docking studies of fatty acid desaturase genes in wheat (Triticum aestivum L.). BMC Genom 21(1):1–20. https://doi.org/10.1186/s12864-020-07199-1
Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53(366):1–11. https://doi.org/10.1093/jexbot/53.366.1
Hasan M, Cheng Y, Kanwar MK, Chu XY, Ahammed GJ, Qi ZY (2017) Responses of plant proteins to heavy metal stress. a review. Front Plant Sci 5(8):1492. https://doi.org/10.3389/fpls.2017.01492
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. J Bioinform 31(8):1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. https://doi.org/10.1146/annurev.arplant.57.032905.105218
Kabata-Pendias A, Pendias H (2001) Trace elements in soils and plants, 3rd edn. CRC Press, Boca Raton. https://doi.org/10.1201/9781420039900
Kobae Y, Uemura T, Sato MH, Ohnishi M, Mimura T, Nakagawa T, Maeshima M (2004) Zinc transporter of Arabidopsis thaliana AtMTP1 is localized to vacuolar membranes and implicated in zinc homeostasis. Plant Cell Physiol 45(12):1749–1758. https://doi.org/10.1093/pcp/pci015
Kolaj-Robin O, Russell D, Hayes KA, Pembroke JT, Soulimane T (2015) Cation diffusion facilitator family: structure and function. FEBS Lett 589(12):1283–1295. https://doi.org/10.1016/j.febslet.2015.04.007
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305(3):567–580. https://doi.org/10.1006/jmbi.2000.4315
Lee TH, Tang H, Wang X, Paterson AH (2012) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41(D1):D1152–D1158. https://doi.org/10.1093/nar/gks1104
Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40(D1):D302-D305. https://doi.org/10.1093/nar/gkr931
Li Q, Cai S, Mo C, Chu B, Peng L, Yang F (2010) Toxic effects of heavy metals and their accumulation in vegetables grown in saline soil. Ecotoxicol Environ Saf 73(1):84–88. https://doi.org/10.1016/j.ecoenv.2009.09.002
Lima J, Arenhart R, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Biol 10(4):2817–2832. https://doi.org/10.4238/2011
Liu Y (2020) A code within the genetic code: codon usage regulates co-translational protein folding. Cell Commun Signal 18(1):1–9. https://doi.org/10.1186/s12964-020-00642-6
Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat Struct Mol Biol 16(10):1063. https://doi.org/10.1038/nsmb.1662
Lv S, Nie X, Wang L, Du X, Biradar SS, Jia X, Weining S (2012) Identification and characterization of microRNAs from barley (Hordeum vulgare L.) by high-throughput sequencing. Int J Mol Sci 13(3):2973–2984. https://doi.org/10.3390/ijms13032973
Migocka M, Papierniak A, Kosieradzka A, Posyniak E, Maciaszczyk-Dziubinska E, Biskup R, Garbiec A, Marchewka T (2015) Cucumber metal tolerance protein CsMTP 9 is a plasma membrane H+2+2+. Plant J 84(6):1045–1058. https://doi.org/10.1111/tpj.13056
Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genom 8(1):107. https://doi.org/10.1186/1471-2164-8-107
Nagajyoti PC, Lee KD, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8(3):199–216. https://doi.org/10.1007/s10311-010-0297-8
Qin Z, Wang Y, Wang Q, Li A, Hou F, Zhang L (2015) Evolution analysis of simple sequence repeats in plant genome. PLoS ONE 10(12):e0144108. https://doi.org/10.1371/journal.pone.0144108
Ricachenevsky FK, Menguer PK, Sperotto RA, Williams LE, Fett JP (2013) Roles of plant metal tolerance proteins (MTP) in metal storage and potential use in biofortification strategies. Front Plant Sci 4:144. https://doi.org/10.3389/fpls.2013.00144
Rizwan M, Meunier JD, Miche H, Keller C (2012) Effect of silicon on reducing cadmium toxicity in durum wheat (Triticum turgidum L. cv. Claudio W.) grown in a soil with aged contamination. J Hazard Mater 209:326–334. https://doi.org/10.1016/j.jhazmat.2012.01.033
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. J Bioinform 19(18):2496–2497. https://doi.org/10.1093/bioinformatics/btg359
Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J (2006) [9] TM4 microarray software suite. Methods Enzymol 411:134–193. https://doi.org/10.1016/S0076-6879(06)11009-5
Shirazi Z, Piri K, Asl AM, Hasanloo T (2012) Glycyrrhizin and isoliquiritigenin production by hairy root culture of Glycyrrhiza glabra J Med Plant Res 6(31):4640–4646. https://doi.org/10.5897/JMPR11.1651
Shirazi Z, Abedi A, Kordrostami M, Burritt DJ, Hossain MA (2019)Genome-wide identification and characterization of the metal tolerance protein (MTP) family in grape (Vitis vinifera L.). 3 Biotech 9(5):199. https://doi.org/10.1007/s13205-019-1728-2
Shiu SH, Bleecker AB (2003) Expansion of the receptor-likekinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132(2):530–543. https://doi.org/10.1104/pp.103.021964
Siddiqi KS, Husen A (2019) Plant response to jasmonates: current developments and their role in changing environment. Doc Bull Natl Res Cent 43(1):1–11. https://doi.org/10.1186/s42269-019-0195-6
Singh RK, Anandhan S, Singh S, Patade VY, Ahmed Z, Pande V (2011)Metallothionein-like gene from Cicer microphyllumis regulated by multiple abiotic stresses. Protoplasma 248 (4):839-847. https://doi.org/10.1007/s00709-010-0249-y
Sunkar R, Kapoor A, Zhu K (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. https://doi.org/10.1105/tpc.106.041673
Takeda R, Sato Y, Yoshimura R, Komemushi S, Sawabe A (2010) Accumulation of heavy metals by cucumber and Brassica juncea under different cultivation conditions. In: Proceedings of the Annual International Conference on Soils, Sediments, Water and Energy, (1)19
Thompson JD (1994) Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. https://doi.org/10.1093/nar/22.22.4673
Valdés-López O, Yang SS, Aparicio‐Fabre R, Graham PH, Reyes JL, Vance CP, Hernández G (2010) MicroRNA expression profile in common bean (Phaseolus vulgaris) under nutrient deficiency stresses and manganese toxicity. New Phytol 187(3):805–818. https://doi.org/10.1111/j.1469-8137.2010.03320.x
Vatansever R, Filiz E, Eroglu S (2017)Genome-wide exploration of metal tolerance protein (MTP) genes in common wheat (Triticum aestivum): insights into metal homeostasis and biofortification. Biometals 30(2):217–235. https://doi.org/10.1007/s10534-017-9997-x
Wu X, Wang JT, Jain L, Zaki MJ, Shasha D, Toivonen H (2005) Data mining in bioinformatics. Springer Science and Business Media, Berlin, p 337
You FM, Huo N, Gu YQ, Luo M-c, Ma Y, Hane D, Lazo GR, Dvorak J, Anderson OD (2008) BatchPrimer3: a high throughput web application for PCR and sequencing primer design. BMC Bioinformatics 9(1):253. https://doi.org/10.1186/1471-2105-9-253
Zhang Y, Gao M, Singer SD, Fei Z, Wang H, Wang X (2012)Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE 7(9):444–465. https://doi.org/10.1371/journal.pone.0044465
Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J, Kalyanaraman B (2005) Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. PNAS USA 5(15):102–727. https://doi.org/10.1073/pnas.0501719102
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. https://doi.org/10.1016/j.bbrc.2008.07.083
Zhou ZS, Zeng HQ, Liu ZP, Yang ZM (2012)Genome-wide identification of Medicago truncatula microRNAs and their targets reveals their differential regulation by heavy metal. Plant Cell Environ 35(1):86–99. https://doi.org/10.1111/j.1365-3040.2011.02418.x
Zwolak A, Sarzyńska 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(7):164. https://doi.org/10.1007/s11270-019-4221-y
Author information
Authors and Affiliations
Contributions
Z.SH conceived, designed, and performed the methodology. M.N.CH analyzes the SRA data, Z.SH and S.S write the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Shirazi, Z., Samavat, S., Nezamivand Chegini, M. et al. Identification and characterization of Metal Tolerance Protein (MTP) family in Glycyrrhiza uralensis. Biologia 76, 3221–3233 (2021). https://doi.org/10.1007/s11756-021-00880-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00880-0