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Overexpression of a Malus xiaojinensis WRKY transcription factor gene (MxWRKY55) increased iron and high salinity stress tolerance in Arabidopsis thaliana

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Abstract

Apple, as one of the most important economic forest tree species, is widely grown in the world. Abiotic stresses, such as high salinity and iron deficiency, affect apple growth and development. WRKY transcription factors (TFs) are widely involved in the responses of plants to adverse stresses. In the present study, a new WRKY gene was isolated from Malus xiaojinensis and designated as MxWRKY55. Subcellular localization showed that MxWRKY55 was localized to the nucleus. The expression level of MxWRKY55 was highly affected by salt, low-Fe, and high-Fe stresses in M. xiaojinensis seedlings. When MxWRKY55 was introduced into Arabidopsis thaliana, it greatly enhanced the salt and Fe tolerance. When dealt with high- and low-Fe stresses, the overexpression of MxWRKY55 in transgenic A. thaliana resulted in higher levels of root length and fresh weight as well as contents of chlorophyll and Fe than wild type (WT). Increased expression of MxWRKY55 in transformed A. thaliana also contributed to higher contents of chlorophyll and proline and higher activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), while malondialdehyde (MDA) content was lower, especially in response to salt stress. Therefore, these results show that MxWRKY55 plays a positive role in the process of plant resistance to salt, low-Fe, and high-Fe stresses.

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References

  • Abadía J, López-Millán AF, Rombolà A, Abadía A (2002) Organic acids and Fe deficiency: a review. Plant Soil 241:75–86

    Article  Google Scholar 

  • An G, Watson BD, Chang CC (1986) Transformation of tobacco, tomato, potato, and Arabidopsis thaliana using a binary Ti vector system. Plant Physiol 81:301–305

    Article  CAS  Google Scholar 

  • Cai R, Zhao Y, Wang Y, Lin Y, Peng X, Li Q, Chang Y, Jiang H, Xiang Y, Cheng B (2014) Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice. Plant Cell Tissue Organ Cult 119:565–577

    Article  CAS  Google Scholar 

  • Chanwala J, Satpati S, Dixit A, Parida A, Giri MK, Dey N (2020) Genome-wide identification and expression analysis of WRKY transcription factors in pearl millet (Pennisetum glaucum) under dehydration and salinity stress. BMC Genomics 1:231

    Article  CAS  Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    Article  CAS  Google Scholar 

  • Ding W, Fang W, Shi S, Zhao Y, Li X, Xiao K (2016) Wheat WRKY type transcription factor gene TaWRKY1 is essential in mediating drought tolerance associated with an ABA-dependent pathway. Plant Mol Biol Report 34:1111–1126

    Article  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Schmelzer E, Hahlbrock K, Somssich IE (1999) Early nuclear events in plant defense signalling: rapid gene activation by WRKY transcription factors. EMBO J 18:4689–4699

    Article  CAS  Google Scholar 

  • Gong XQ, Liu JH (2013) Genetic transformation and genes for resistance to abiotic and biotic stresses in citrus and its related genera. Plant Cell Tissue Organ Cult 113:137–147

    Article  CAS  Google Scholar 

  • Hao NB, Du WG, Ge QY, Zhang GR, Li WH, Man WQ, Peng DC, Bai KZ, Kuang TY (2002) Progress in the breeding of soybean for high photosynthetic efficiency. Acta Bot Sin 44:253–258

    CAS  Google Scholar 

  • Han D, Du M, Zhou Z, Wang S, Li T, Han J, Xu T, Yang G (2020a) Overexpression of a Malus baccata NAC transcription factor gene MbNAC25 increases cold and salinity tolerance in Arabidopsis. Int J Mol Sci 21:1198

    Article  CAS  Google Scholar 

  • Han D, Han J, Yang G, Wang S, Xu T, Li W (2020b) An ERF transcription factor gene from Malus baccata (L.) Borkh, MbERF11, affects cold and salt stress tolerance in Arabidopsis. Forests 11:514

    Article  Google Scholar 

  • Han D, Hou Y, Wang Y, Ni B, Li Z, Yang G (2019) Overexpression of a Malus baccata WRKY transcription factor gene (MbWRKY5) increases drought and salt tolerance in transgenic tobacco. Can J Plant Sci 99:173–183

    Article  CAS  Google Scholar 

  • Han D, Shi Y, Yu Z, Liu W, Lv B, Wang B, Yang G (2015) Isolation and functional analysis of MdCS1: a gene encoding a citrate synthase in Malus domestica (L.) Borkh. Plant Growth Regul 75:209–218

    Article  CAS  Google Scholar 

  • Han D, Wang Y, Zhang Z, Pu Q, Ding H, Han J, Fan T, Bai X, Yang G (2017) Isolation and functional analysis of MxCS3: a gene encoding a citrate synthase in Malus xiaojinensis, with functions in tolerance to iron stress and abnormal flower in transgenic Arabidopsis thaliana. Plant Growth Regul 82:479–489

    Article  CAS  Google Scholar 

  • Han D, Zhang Z, Ding H, Chai L, Liu W, Li H, Yang G (2018a) Isolation and characterization of MbWRKY2 gene involved in enhanced drought tolerance in transgenic tobacco. J Plant Interact 13:163–172

    Article  CAS  Google Scholar 

  • Han D, Zhang Z, Ding H, Wang Y, Liu W, Li H, Yang G (2018b) Molecular cloning and functional analysis of MbWRKY3 involved in improved drought tolerance in transformed tobacco. J Plant Interact 13:329–337

    Article  CAS  Google Scholar 

  • Han D, Zhang Z, Ni B, Ding H, Liu W, Li W, Chai L, Yang G (2018c) Isolation and functional analysis of MxNAS3 involved in enhanced iron stress tolerance and abnormal flower in transgenic Arabidopsis. J Plant Interact 13:433–441

    Article  CAS  Google Scholar 

  • Han Z, Shen T, Korcak RF, Baligar VC (1998) Iron absorption by iron-efficient and inefficient species of apples. J Plant Nutr 21:181–190

    Article  CAS  Google Scholar 

  • Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPFI, that recognizes SP8 sequence in the 5′ upstream regions of genes coding for sporamin and beta-amylase from sweetpotato. Mol Gen Genet 244:563–571

    Article  CAS  Google Scholar 

  • Jaffar MA, Song A, Faheem M, Chen S, Jiang J, Liu C, Fan Q, Chen F (2016) Involvement of CmWRKY10 in drought tolerance of chrysanthemum through the ABA-signaling pathway. Int J Mol Sci 17:693

    Article  CAS  Google Scholar 

  • Jia H, Wang C, Wang F, Liu S, Li G, Guo X (2015) GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana benthamiana. PLoS One 10:e0120646

    Article  CAS  Google Scholar 

  • Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  CAS  Google Scholar 

  • Lee H, Cha J, Choi C, Choi N, Ji H, Park S, Lee S, Hwang D (2018) Rice WRKY11 plays a role in pathogen defense and drought tolerance. Rice 11:5

    Article  Google Scholar 

  • Li G, Wang Z, Yokosho K, Ding B, Fan W, Gong Q, Li G, Wu Y, Yang J, Ma J, Zheng S (2018) Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice. New Phytol 219:149–162

    Article  CAS  Google Scholar 

  • Li QL, Xu KD, Pan YZ, Jiang BB, Liu GL, Jia Y, Zhang HQ (2014) Functional analysis of a novel chrysanthemum WRKY transcription factor gene involved in salt tolerance. Plant Mol Biol Report 32:282–289

    Article  CAS  Google Scholar 

  • Liu W, Wu T, Li Q, Zhang X, Xu X, Li T, Han Z, Wang Y (2018) An ethylene response factor (MxERF4) functions as a repressor of Fe acquisition in Malus xiaojinensis. Sci Rep 8:1068

    Article  CAS  Google Scholar 

  • López-Millán AF, Fermín M, Gogorcena Y, Abadía A, Abadía J (2009) Metabolic responses in iron deficient tomato plants. J Plant Physiol 166:375–384

    Article  CAS  Google Scholar 

  • Luan Q, Chen C, Liu M, Li Q, Wang L, Ren Z (2019) CsWRKY50 mediates defense responses to Pseudoperonospora cubensis infection in Cucumis sativus. Plant Sci 279:59–69

    Article  CAS  Google Scholar 

  • Ma Q, Xia Z, Cai Z, Li L, Cheng Y, Liu J, Nian H (2019) GmWRKY16 enhances drought and salt tolerance through an ABA-mediated pathway in Arabidopsis thaliana. Front Plant Sci 9:1979

    Article  Google Scholar 

  • Marschner H, Romheld V (1994) Strategies of plants for acquisition of iron. Plant Soil 165:261–274

    Article  CAS  Google Scholar 

  • Matysik J, Alia A, Bhalu B, Mohanty P (2002) Molecular mechanism of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Pan Y, Wu LJ, Yu ZL (2006) Effect of salt and drought stress on antioxidant enzymes activities and SOD isoenzymes of liquorice (Glycyrrhiza uralensis Fisch). Plant Growth Regul 49:157–165

    Article  CAS  Google Scholar 

  • Parvaiz A, Satyawati S (2008) Salt stress and phyto-biochemical responses of plants. Plant Soil Environ 54:89–99

    Article  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  Google Scholar 

  • Qin L, Rao Y, Li L, Huang J, Xu W, Li X (2013) Cotton GalT1 encoding a putative glycosyltransferase is involved in regulation of cell wall pectin biosynthesis during plant development. PLoS One 8:e59115

    Article  CAS  Google Scholar 

  • Qin Y, Tian Y, Liu X (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochem Biophys Res Commun 464:428–433

    Article  CAS  Google Scholar 

  • Ranieri A, Petacco F, Castagna A, Soldatini GF (2000) Redox state and peroxidase system in sunflower plants exposed to ozone. Plant Sci 159:159–167

    Article  CAS  Google Scholar 

  • Ricachenevsky FK, Sperotto RA, Menguer PK, Fett JP (2010) Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence. Mol Biol Rep 37:3735–3745

    Article  CAS  Google Scholar 

  • Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700

    Article  CAS  Google Scholar 

  • Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  Google Scholar 

  • Tang N, Zhang H, Li XH, Xiao JH, Xiong LZ (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  CAS  Google Scholar 

  • Toka I, Planchais S, Cabassa C, Justin AM, Vos DD, Richard L, Savouré A, Carol P (2010) Mutations in the hyperosmotic stress-responsive mitochondrial basic amino acid carrier 2 enhance proline accumulation in Arabidopsis. Plant Physiol 152:1851–1862

    Article  CAS  Google Scholar 

  • Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, Yao N, Feng Y, Chai R, Yang G, He G (2013) A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS One 8:e65120

    Article  CAS  Google Scholar 

  • Wang X, Yan Y, Li Y, Chu X, Wu C, Guo X (2014) GhWRKY40, a multiple stress-responsive cotton WRKY gene, plays an important role in the wounding response and enhances susceptibility to Ralstonia solanacearum infection in transgenic Nicotiana benthamiana. PLoS One 9:e93577

    Article  CAS  Google Scholar 

  • Wu K, Guo Z, Wang H, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26

    Article  CAS  Google Scholar 

  • Xiu H, Nuruzzaman M, Guo X, Cao H, Huang J, Chen X, Wu K, Zhang R, Huang Y, Luo J, Luo Z (2016) Molecular cloning and expression analysis of eight PgWRKY genes in Panax ginseng responsive to salt and hormones. Int J Mol Sci 17:319

    Article  CAS  Google Scholar 

  • Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585

    Article  CAS  Google Scholar 

  • Yan JY, Li CX, Sun L, Ren JY, Li GX, Ding ZJ, Zheng SJ (2016) A WRKY transcription factor regulates Fe translocation under Fe deficiency. Plant Physiol 171:2017–2027

    Article  Google Scholar 

  • Yang G, Li J, Liu W, Yu Z, Shi Y, Lv B, Wang B, Han D (2015) Molecular cloning and characterization of MxNAS2, a gene encoding nicotianamine synthase in Malus xiaojinensis, with functions in tolerance to iron stress and misshapen flower in transgenic tobacco. Sci Hortic 183:77–86

    Article  CAS  Google Scholar 

  • Zhang L, Xi D, Luo L, Meng F, Li Y, Wu C, Guo X (2011) Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress. FEBS J 278:1367–1378

    Article  CAS  Google Scholar 

  • Zhou S, Zheng W, Liu B, Zheng J, Dong F, Liu Z, Wen Z, Yang F, Wang H, Xu Z, Zhao H, Liu Y (2019) Characterizing the role of TaWRKY13 in salt tolerance. Int J Mol Sci 20:5712

    Article  CAS  Google Scholar 

  • Zhu D, Hou L, Xiao P, Guo Y, Deyholos MK, Liu X (2019) VvWRKY30, a grape WRKY transcription factor, plays a positive regulatory role under salinity stress. Plant Sci 28:132–142

    Article  CAS  Google Scholar 

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Funding

This project was supported by the National Natural Science Foundation of China (31301757), the Natural Science Fund Joint Guidance Project of Heilongjiang Province (LH2019C031; LH2020C009), the Young Talent Project of Northeast Agricultural University (19QC06), and the Postdoctoral Scientific Research Development Fund of Heilongjiang Province, China (LBH-Q16020).

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Authors and Affiliations

  1. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Northeast Region), Ministry of Agriculture and Rural Affairs, College of Horticulture & Landscape Architecture, Northeast Agricultural University, Harbin, 150030, China

    Deguo Han, Zhengyi Zhou, Man Du, Tiemei Li, Xuemei Wu, Jing Yu, Peng Zhang & Guohui Yang

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  1. Deguo Han
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  2. Zhengyi Zhou
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  3. Man Du
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  4. Tiemei Li
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  7. Peng Zhang
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Correspondence to Tiemei Li or Guohui Yang.

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Editor: Yong Eui Choi

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Han, D., Zhou, Z., Du, M. et al. Overexpression of a Malus xiaojinensis WRKY transcription factor gene (MxWRKY55) increased iron and high salinity stress tolerance in Arabidopsis thaliana. In Vitro Cell.Dev.Biol.-Plant 56, 600–609 (2020). https://doi.org/10.1007/s11627-020-10129-1

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