Genome-wide identification and expression analysis of ZIP transporter gene family in Brassica napus

doi:10.19802/j.issn.1007-9084.2021071

Abstract

Abstract:

ZIP transporter gene family, which is mainly involved in absorption and transport of metal cations,and plays an important role in plant, development and response to heavy metal stress. In this study, 51 members of the ZIP gene family in Brassica napus were identified by bioinformatics method,. Tandem duplication were found in A and C subgenomes as compared with three basic species of Brassica. Using Brassica napus CV ZS11 as a reference genome, the ZIP gene family was mapped onto 17 chromosomes, and 10 motif were predicted, all of which contained ZIP domain. Moreover, the cis-regulatory elements locating at 3 kb upstream of promoter region were predicted. Based on phylogenetic tree analysis, the ZIP gene family of Brassica napus was divided into three major groups,and was conserved among the three basic species of Brassica. In addition, ZIP gene family showed tissue-specificand BnaIRT3 genes were ac⁃tively expressed in different tissues and different developmental stages. We also found that BnaIRT1.A01a was expressed in both leaves and roots of rape treated with different concentrations of cadmium, which might play an important role in response of rape to cadmium stress. These results might provide references for the subsequent biological functions of the ZIP gene family.

Key words: , Brassica napus；ZIP gene family；cadmium；genome-wide analysis

CLC Number:

中图分类号：S565.4

HE Dan, YANG Tai-hua, LI Ting, WU Jin-feng, PENG Jia-shi, LIU Li-li, ZHANG Da-wei, YAN Ming-li, LI Zai-yun. Genome-wide identification and expression analysis of ZIP transporter gene family in Brassica napus[J]. CHINESE JOURNAL OF OIL CROP SCIENCES, 2021, 43(3): 392-.

References

[1] Huang Y, Chen Q, Deng M, et al. Heavy metal pollution and health risk assessment of agricultural soils in a typical peri-urban area in southeast China[J]. Environ Manage, 2018, 207: 159-168. DOI: 10.1016/j.jenvman.2017.10.072

[2] Ikenaka Y, Nakayama S M. M., Muzandu K, et al. Heavy metal contamination of soil and sediment in Zambia[J]. African Journal of Environmental Science and Technology, 2010, 4(11):729-739. DOI: 10.5897/AJEST10.179

[3] Li F T, Qi J M, Zhang G Y, et al. Effect of Cadmium Stress on the Growth, Antioxidative Enzymes and Lipid Peroxidation in Two Kenaf (Hibiscus cannabinus L.) Plant Seedlings[J]. Journal of Integrative Agriculture, 2013, 12(4):610-620. DOI: 10.1016/s2095-3119(13)60279-8

[4] Vestena S, Cambraia J, Ribeiro C, et al. Cadmium-induced Oxidative Stress and Antioxidative Enzyme Response in Water Hyacinth and Salvinia[J]. Brazilian Society of Plant Physiology, 2011, 23(2):131-139. DOI: 10.1590/S1677-04202011000200005

[5] Hasan S.A, Fariduddin Q, Ali B, S, et al. Cadmium: Toxicity and tolerance in plants[J]. Journal of Environmental Biology, 2009, 30(2):165-174.

[6] Clemens S, Aarts M G, Thomine S, et al. Plant science: the key to preventing slow cadmium poisoning[J]. Trends Plant Sci, 2013, 18(2):92-99. DOI: 10.1016/j.tplants.2012.08.003

[7] Waalkes M P. Cadmium carcinogenesis in review[J]. Journal of Inorganic Biochemistry, 2000, 79: 241-244. DOI: 10.1016/S0162-0134(00)00009-X

[8] Chen H, Teng Y, Lu S, et al. Contamination features and health risk of soil heavy metals in China[J]. Sci Total Environ, 2015, 512-513, 143-153. DOI: 10.1016/j.scitotenv.2015.01.025

[9] Järup L. Hazards of heavy metal contamination[J]. British Medical Bulletin, 2003, 68: 167–182. DOI: 10.1093/bmb/ldg032

[10] Kushwahaa A, Rania R, Kumar S, et al. Heavy metal detoxification and tolerance mechanisms in plants: Implications for phytoremediation[J]. Environmental Reviews, 2016, 24(1): 39–51. DOI:10.1139/er-2015-0010

[11] Memon A R, Schroder P. Implications of metal accumulation mechanisms to phytoremediation[J]. Environ Sci Pollut Res Int, 2009, 16(2): 162-175. DOI:10.1007/s11356-008-0079-z

[12] Hall J L, Williams L E. Transition metal transporters in plants[J]. J Exp Bot, 2003, 54(393): 2601-2613. DOI:10.1093/jxb/erg303

[13] Milner M J, Seamon J, Craft E, et al. Transport properties of members of the ZIP family in plants and their role in Zn and Mn homeostasis[J]. Journal of Experimental Botany, 2013, 64(1):369-381. DOI: 10.1093/jxb/ers315

[14] Fan W, Liu C, Cao B, et al. A meta-analysis of transcriptomic profiles reveals molecular pathways response to cadmium stress of Gramineae[J]. Ecotoxicol Environ Saf, 2021, 209: 111816. DOI: 10.1016/j.ecoenv.2020.111816

[15] Zheng X, Chen L, Li X. Arabidopsis and rice showed a distinct pattern in ZIPs genes expression profile in response to Cd stress[J]. Bot Stud, 2018, 59(1): 22. DOI: 10.1186/s40529-018-0238-6

[16] Weber M, Harada E, Vess C, et al. Comparative microarray analysis of Arabidopsis thaliana and Arabidopsis halleri roots identifies nicotianamine synthase, a ZIP transporter and other genes as potential metal hyperaccumulation factors[J]. Plant J, 2004, 37(2): 269-281. DOI: 10.1046/j.1365-313x.2003.01960.x

[17] Chen W R, Feng Y, Chao Y E, et al. Genomic analysis and expression pattern of OsZIP1, OsZIP3, and OsZIP4 in two rice (Oryza sativa L.) genotypes with different zinc efficiency[J]. Russian Journal of Plant Physiology, 2008, 55(3): 400-409. DOI: 10.1134/s1021443708030175

[18] Tiong J, McDonald G K, Genc Y, et al. HvZIP7 mediates zinc accumulation in barley (Hordeum vulgare) at moderately high zinc supply[J]. New Phytol, 2014, 201(1): 131-143. DOI:10.1111/nph.12468

[19] Pedas P, Husted S. Zinc transport mediated by barley ZIP proteins are induced by low pH[J]. Plant Signaling & Behavior, 2009, 4:9: 842-845. DOI: 10.4161/ psb.4.9.9375

[20] Evens N P, Buchner P, Williams L E, et al. The role of ZIP transporters and group F bZIP transcription factors in the Zn-deficiency response of wheat (Triticum aestivum)[J]. Plant J, 2017, 92(2): 291-304. DOI: 10.1111/tpj.13655

[21] Li S Z, Zhou X J, Huang Y Q, et al. Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize[J]. BMC Plant Biology, 2013, 13:114. DOI: 10.1186/1471-2229-13-114

[22] Astudillo C, Fernandez A C, Blair M W, et al. The Phaseolus vulgaris ZIP gene family: identification, characterization, mapping, and gene expression[J]. Front Plant Sci, 2013, 4: 286. DOI: 10.3389/fpls.2013.00286

[23] Huang S, Sasaki A, Yamaji N, et al. The ZIP Transporter Family Member OsZIP9 Contributes To Root Zinc Uptake in Rice under Zinc-Limited Conditions[J]. Plant Physiol, 2020, 183(3): 1224-1234. DOI: 10.1104/pp.20.00125

[24] Gasco G, Alvarez M L, Paz-Ferreiro J, et al. Combining phytoextraction by Brassica napus and biochar amendment for the remediation of a mining soil in Riotinto (Spain)[J]. Chemosphere, 2019, 231, 562-570. DOI: 10.1016/j.chemosphere.2019.05.168

[25] Zhang F, Xiao X, Wu X. Physiological and molecular mechanism of cadmium (Cd) tolerance at initial growth stage in rapeseed (Brassica napus L.)[J]. Ecotoxicol Environ Saf, 2020, 197, 110613. DOI: 10.1016/j.ecoenv.2020.110613

[26] Zeng X, Zou D, Wang A, et al. Remediation of cadmium-contaminated soils using Brassica napus: Effect of nitrogen fertilizers[J]. Journal of Environmental Management, 2020, 255: 109885. DOI: 10.1016/j.jenvman.2019.109885

[27] Zhang X D, Meng J G, Zhao K X, et al. Annotation and characterization of Cd-responsive metal transporter genes in rapeseed (Brassica napus)[J]. Biometals, 2018, 31(1): 107-121. DOI: 10.1007/s10534-017-0072-4

[28] Chen L, Wan H, Qian J, et al. Genome-Wide Association Study of Cadmium Accumulation at the Seedling Stage in Rapeseed (Brassica napus L.)[J]. Front Plant Sci, 2018, 9: 375. DOI: 10.3389/fpls.2018.00375

[29] Meng J G, Zhang X D, Tan S K, et al. Genome-wide identification of Cd-responsive NRAMP transporter genes and analyzing expression of NRAMP 1 mediated by miR167 in Brassica napus[J]. Biometals, 2017, 30(6): 917-931. DOI: 10.1007/s10534-017-0057-3

[30] Wang S, Sun J, Li S, et al. Physiological, genomic and transcriptomic comparison of two Brassica napus cultivars with contrasting cadmium tolerance[J]. Plant and Soil, 2019, 441(1-2): 71-87. DOI: 10.1007/s11104-019-04083-0

[31] Li N, Xiao H, Sun J, et al. Genome-wide analysis and expression profiling of the HMA gene family in Brassica napus under cd stress[J]. Plant and Soil, 2018, 426(1-2): 365-381. DOI: 10.1007/s11104-018-3637-2

[32] Zhang X D, Zhao K X, Yang Z M. Identification of genomic ATP binding cassette (ABC) transporter genes and Cd-responsive ABCs in Brassica napus[J]. Gene, 2018, 664, 139-151. DOI: 10.1016/j.gene.2018.04.060

[33] Kaul S, Koo H L, Jenkins J, et al. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana[J]. nature, 2000, 408(6814): 796-815. DOI: 10.1038/35048692

[34] Wang X, Wang H, Wang J, et al. The genome of the mesopolyploid crop species Brassica rapa[J]. Nature genetics, 2011, 43(10): 1035-1039. DOI: 10.1038/ng.919

[35] Perumal S, Koh C S, Jin L, et al. A high-contiguity Brassica nigra genome localizes active centromeres and defines the ancestral Brassica genome[J]. Nature plants, 2020, 6(8): 929-941. DOI: 10.1038/s41477-020-0735-y

[36] Belser C, Istace B, Denis E, et al. Chromosome-scale assemblies of plant genomes using nanopore long reads and optical maps[J]. Nature plants, 2018, 4(11): 879-887. DOI: 10.1038/s41477-018-0289-4

[37] Chalhoub B, Denoeud F, Liu S, et al. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome[J]. science, 2014, 345(6199): 950-953. DOI: 10.1126/science.1253435

[38] Song J M, Guan Z, Hu J, et al. Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus[J]. Nature Plants, 2020, 6(1): 34-45. DOI: 10.1038/s41477-019-0577-7

[39] Song J M, Liu D X, Xie W Z, et al. BnPIR: Brassica napus Pan‐genome Information Resource for 1,689 accessions[J]. Plant Biotechnology Journal, 2020, pp. 1–3. DOI: 10.1111/PBI.13491

[40] Hu B, Jin J, Guo A Y, et al. GSDS 2.0: an upgraded gene feature visualization server[J]. Bioinformatics, 2015, 31(8): 1296-1297. DOI: 10.1093/bioinformatics/btu817

[41] Bailey T L, Boden M, Buske F A, et al. MEME SUITE: tools for motif discovery and searching[J]. Nucleic acids research, 2009, 37(suppl_2): W202-W208.3. DOI: 10.1093/nar/gkp335

[42] Lescot M, Déhais P, Thijs G, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences[J]. Nucleic acids research, 2002, 30(1): 325-327. DOI: 10.1093/nar/30.1.325

[43] Lu S, Wang J, Chitsaz F, et al. CDD/SPARCLE: the conserved domain database in 2020[J]. Nucleic acids research, 2020, 48(D1): D265-D268. DOI: 10.1093/nar/gkz991

[44] Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A.;Protein Identification and Analysis Tools on the ExPASy Server;(In) John M. Walker (ed): The Proteomics Protocols Handbook, Humana Press (2005).pp. 571-607. DOI: 10.1385/1-59259-890-0:571

[45] Waterhouse A, Bertoni M, Bienert S, et al. SWISS-MODEL: homology modelling of protein structures and complexes[J]. Nucleic acids research, 2018, 46(W1): W296-W303. DOI: 10.1093/nar/gky427

[46] Chou K C, Shen H B. Cell-PLoc: a package of Web servers for predicting subcellular localization of proteins in various organisms[J]. Nature protocols, 2008, 3(2): 153. DOI: 10.1038/nprot.2007.494

[47] Chen C, Chen H, Zhang Y, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data[J]. Molecular plant, 2020, 13(8): 1194-1202. DOI: 10.1016/j.molp.2020.06.009

[48] Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets[J]. Molecular biology and evolution, 2016, 33(7): 1870-1874. DOI: 10.1093/molbev/msw054

[49] Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method[J]. Proceedings of the National Academy of Sciences, 2004, 101(30): 11030-11035. DOI: 10.1073/pnas.0404206101

[50] Wang Y, Tang H, DeBarry J D, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity[J]. Nucleic acids research, 2012, 40(7): e49-e49. DOI: 10.1093/nar/gkr1293

[51] Havlickova L, He Z, Wang L, et al. Validation of an updated Associative Transcriptomics platform for the polyploid crop species Brassica napus by dissection of the genetic architecture of erucic acid and tocopherol isoform variation in seeds[J]. The Plant Journal, 2018, 93(1): 181-192. DOI: 10.1111/tpj.13767

[52] Bolger A M, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data[J]. Bioinformatics, 2014, 30(15): 2114-2120. DOI: 10.1093/bioinformatics/btu170

[53] Kim D, Paggi J M , Park C , et al. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype[J]. Nature Biotechnology, 2019, 37(8):1. DOI: 10.1038/s41587-019-0201-4

[54] Liao Y, Smyth G K, Shi W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote[J]. Nucleic acids research, 2013, 41(10): e108-e108. DOI: 10.1093/nar/gkt214

[55] Di F, Jian H, Wang T, et al. Genome-Wide Analysis of the PYL Gene Family and Identification of PYL Genes That Respond to Abiotic Stress in Brassica napus[J]. Genes, 2018, 9(3): 156. DOI: 10.3390/genes9030156

[56] Liang Y, Xiong Z, Zheng J, et al. Genome-wide identification, structural analysis and new insights into late embryogenesis abundant (LEA) gene family formation pattern in Brassica napus[J]. Sci Rep, 2016, 6: 24265. DOI: 10.1038/srep24265

[57] 宋敏, 张瑶, 王丽莹, 等. 甘蓝型油菜ZF-HD基因家族的鉴定与系统进化分析[J]. 植物学报, 2019, 54(6): 699–710. DOI: 10.11983/CBB19055

[58] 贾永鹏，李开祥，昝领兄, 等. 甘蓝型油菜全基因组 DELLA 蛋白基因家族的鉴定和表达分析[J].中国油料作物学报, 2019, 41( 3) : 360-368. DOI: 10. 7505/j. issn. 1007-9084. 2019. 03. 007

[59] Lin Y F, Aarts M G M. The molecular mechanism of zinc and cadmium stress response in plants[J]. Cellular and Molecular Life Sciences, 2012, 69(19): 3187–3206. DOI: 10.1007/s00018-012-1089-z

[60] Krishna A T P, Maharajan T, Roch G V, et al. Structure, Function, Regulation and Phylogenetic Relationship of ZIP Family Transporters of Plants[J]. Front Plant Sci, 2020, 11: 662. DOI: 10.3389/fpls.2020.00662