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Genome-wide analysis of the bZIP gene lineage in apple and functional analysis of MhABF in Malus halliana

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Abstract

Main Conclusion

51 MdbZIP genes were identified from the apple genome by bioinformatics methods. MhABF-OE improved tolerance to saline–alkali stress in Arabidopsis, indicating it is involved in positive regulation of saline–alkali stress response.

Abstract

Saline–alkali stress is a major abiotic stress limiting plant growth all over the world. Members of the bZIP family play an important role in regulating gene expression in response to many kinds of biotic and abiotic stress, including salt stress. According to the transcriptome data, 51 MdbZIP genes responding to saline–alkali stress were identified in apple genome, and their gene structures, conserved protein motifs, phylogenetic analysis, chromosome localization, and promoter cis-acting elements were analyzed. Based on transcriptome data analysis, a MdbZIP family gene (MD15G1081800), which was highly expressed under stress, was selected to isolate and named as MhABF. Expression profile analysis by quantitative real-time PCR confirmed that the expression of MhABF in the leaves of Malus halliana was 10.6-fold higher than that of the control (0 days) after 2 days of stress. Then an MhABF gene was isolated from apple rootstock M. halliana. CaMV35S promoter drived MhABF gene expression vector was constructed to infect Arabidopsis with Agrobacterium-mediated infection. And overexpression MhABF gene plants were obtained. Compared with wild type, transgenic plants grew better under saline–alkali stress and the MhABF-OE lines showed higher chlorophyll content, POD, SOD and CAT activity, which indicated that they had strong resistance to stress. These results indicate that MhABF plays an important role in plant resistance to saline–alkali stress, which lays a foundation for further study on the functions in apple.

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References

  • Bajji M, Kinet JM, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul 36:61–70

    Article  CAS  Google Scholar 

  • Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014) Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE 9:e96014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Biłas R, Szafran K, Hnatuszko-Konka K, Kononowicz AK (2016) Cis-regulatory elements used to control gene expression in plants. Plant Cell Tiss Org 127:269–287

    Article  CAS  Google Scholar 

  • Cai W, Yang Y, Wang W, Guo G, Liu W, Bi C (2018) Overexpression of a wheat (Triticum aestivum L.) bZIP transcription factor gene, TabZIP6, decreased the freezing tolerance of transgenic Arabidopsis seedlings by down-regulating the expression of CBFs. Plant Physiol Biochem 2018:100–111

    Article  CAS  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Zhao T, Wu YX, Wang H, Zhang ZZ, Zhang D, Wang SC, Wang YX (2020) Identification of AP2/ERF genes in apple (Malus × domestica) and demonstration that MdERF017 enhances iron deficiency tolerance. Plant Cell Tissue Organ Cult 143:465–482

    Article  CAS  Google Scholar 

  • Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SS, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15-45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31:713–727

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Yoshida T, Yamaguchi-Shinozaki K (2013) Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol Plant 147:15–27

    Article  CAS  PubMed  Google Scholar 

  • Guo AX, Hu Y, Shi MF, Wang H, Wu YX, Wang YX (2020) Effects of iron deficiency and exogenous sucrose on the intermediates of chlorophyll biosynthesis in Malus halliana. PLoS ONE 15:e0232694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haberle V, Stark A (2018) Eukaryotic core promoters and the functional basis of transcription initiation. Nature Rev Mol Cell Biol 19:10

    Article  CAS  Google Scholar 

  • Hauser F, Li Z, Waadt R, Schroeder JI (2017) SnapShot: abscisic acid signaling. Cell 171:1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Himmelbach A, Yang Y, Grill E (2003) Relay and control of abscisic acid signaling. Curr Opin Plant Biol 6:470–479

    Article  CAS  PubMed  Google Scholar 

  • Hu DG, Sun MH, Sun CH (2015) Conserved vacuolar H+-ATPase subunit B1 improves salt stress tolerance in apple calli and tomato plants. Sci Hortic 197:107–116

    Article  CAS  Google Scholar 

  • Hu Y, Zhu YF, Guo AX, Jia XM, Cheng L, Zhao T, Wang YX (2018) Transcriptome analysis in Malus halliana roots in response to iron deficiency reveals insight into sugar regulation. Mol Genet Genomics 293:1523–1534

    Article  CAS  PubMed  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Javaux M, Schroder T, Vanderborght J, Vereecken H (2008) Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J 7:1079–1088

    Article  Google Scholar 

  • Jia XM, Wang H, Svetla S, Zhu YF, Hu Y, Cheng L, Zhao T, Wang YX (2019) Comparative physiological responses and adaptive strategies of apple Malus halliana to salt, alkali and saline-alkali stress. Sci Hortic 245:54–62

    Article  CAS  Google Scholar 

  • Kaur G, Pati PK (2016) Analysis of cis-acting regulatory elements of respiratory burst oxidase homolog (Rboh) gene families in Arabidopsis and rice provides clues for their diverse functions. Comput Biol Chem 62:104–118

    Article  CAS  PubMed  Google Scholar 

  • Kim JB, Kang JY, Kim SY (2010) Over-expression of a transcription factor regulating ABA-responsive gene expression confers multiple stress tolerance. Plant Biotechnol J 2:459–466

    Article  CAS  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Botany 63:1593

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Fan S, Hu W, Liu G, Wei Y, He C, Shi H (2017) Two cassava basic leucine zipper (bZIP) transcription factors (MebZIP3 and MebZIP5) confer disease resistance against cassava bacterial blight. Front Plant Sci 8:2110

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu JY, Chen NN, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng ZM (2014) Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics 15:281

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Z, Coulter JA, Li YM, Zhang XJ, Meng JG, Zhang JL, Liu YH (2020) Genome-wide identification and analysis of the Q-type C2H2 gene family in potato (Solanum tuberosum L.). Int J Biol Macromol 2020:153

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Cuenca MR, Iglesias DJ, Forner-Giner MA, Primo-Millo E, Legaz F (2013) The effect of sodium bicarbonate on plant performance and iron acquisition system of FA-5 (Forner-Alcaide 5) citrus seedlings. Acta Physiol Plant 35:2833–2845

    Article  CAS  Google Scholar 

  • Millar AH, Carrie C, Pogson B, Whelan J (2009) Exploring the function-location nexus: using multiple lines of evidence in defining the subcellular location of plant proteins. Plant Cell 2009:21

    Google Scholar 

  • Miller G, Suzuki N, Ciftciyilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Env 33:453–467

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder JI (2015) Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol 28:154–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochem Biophys Acta 1819:97–103

    CAS  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu ZM, Li GT, Hu HY, Lv JJ, Zheng QW, Liu JQ, Wan DS (2021) A gene that underwent adaptive evolution, LAC2 (LACCASE), in Populus euphratica improves drought tolerance by improving water transport capacity. Horticult Res 2021:8

    Google Scholar 

  • Nobutaka M, Masaru OT (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1248

    Article  CAS  Google Scholar 

  • Perez-Rodriguez P, Riano-Pachon DM, Correa LG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827

    Article  CAS  PubMed  Google Scholar 

  • Pompelli MF, Barata-Luis R, Vitorino HS, Gongalves ER, Rolim EV, Santos MG, Almeida-Cortez JS, Ferreira VM, Lemos EE, Endres L (2000) Photosynthesis, photoprotection and antioxidant activity of purging nut under drought deficit and recovery. Biomass Bioenerg 34:1207–1215

    Article  CAS  Google Scholar 

  • Sakuraba Y, Kim YS, Han SH, Lee BD, Paek NC (2015) The Arabidopsis transcription factor NAC016 promotes drought stress responses by repressing AREB1 transcription through a trifurcate feed-forward regulatory loop involving NAP. Plant Cell 27:1771–1787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandra O, Monica YE, Analia E, Isabel V, Enrique G, Simon RL, Casaretto JA (2010) The transcription factor SIAREBI confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208

    Article  CAS  Google Scholar 

  • Sara EG, Jaina M, Alex B, Sean RE, Aurélien L, Simon C, Potter MQ (2019) The Pfam protein families database in 2019. Nucleic Acids Res 28:263–266

    Google Scholar 

  • Satoh R, Fujita Y, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K (2004) A novel subgroup of bZIP proteins functions as transcriptional activators in hypoosmolarity-responsive expression of the ProDH gene in Arabidopsis. Plant Cell Physiol 45:309–317

    Article  CAS  PubMed  Google Scholar 

  • Sharoni AM, Nuruzzaman M, Satoh K, Moumeni A, Kikuchi S (2012) Comparative transcriptome analysis of AP2/EREBP gene family under normal and hormone treatments, and under two drought stresses in NILs setup by Aday selection and IR64. MGG 287:1–19

    CAS  PubMed  Google Scholar 

  • Su XJ, Xia YY, Jiang WB, Shen GA, Pang YZ (2020) GbMYBR1 from Ginkgo biloba represses phenylpropanoid biosynthesis and trichome development in Arabidopsis. Planta 252:68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun MY, Zhou J, Tan QP, Fu XL, Chen XD, Li L, Gao DS (2016) Analysis of basic leucine zipper genes and their expression during bud dormancy in apple (Malus×domestica). Sci Agric Sin 49:1325–1345

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang LL, Cai H, Ji W, Luo X, Wang ZY, Wu J, Wang XD, Cui L, Wang Y, Zhu YM, Bai X (2013) Overexpression of GsZFP1 enhances salt and drought tolerance in transgenic alfalfa (Medicago sativa L.). Plant Physiol Biochem 71:22–30

    Article  CAS  PubMed  Google Scholar 

  • Tu M, Wang X, Huang L, Guo R, Zhang H, Cai J, Wang X (2016) Expression of a grape bZIP transcription factor, VqbZIP39, in transgenic Arabidopsis thaliana confers tolerance of multiple abiotic stresses. Plant Cell Tissue Organ Culture 125:537–551

    Article  CAS  Google Scholar 

  • Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchishinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Gao C, Liang Y, Wang C, Yang C, Liu G (2010) A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J Plant Physiol 167:222–230

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011) Genomewide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol 53:212–231

    Article  CAS  PubMed  Google Scholar 

  • Wang N, Zheng Y, Xin H, Fang L, Li S (2013) Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep 32:61–75

    Article  PubMed  CAS  Google Scholar 

  • Wang YX, Hu Y, Zhu YF, Abdul WB, Jia XM, Guo AX (2018) Transcriptional and physiological analyses of short-term Iron deficiency response in apple seedlings provide insight into the regulation involved in photosynthesis. BMC Genom 19:461

    Article  CAS  Google Scholar 

  • Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang LN, Zhang LC, Xia C, Zhao GY, Liu J, Jia JZ, Kong XY (2015) A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol Plant 153:538

    Article  CAS  PubMed  Google Scholar 

  • Zhao SJ, Xu CC, Zou Q, Meng QW (1994) Improvements of method for measurement of malondialdehyde in plant tissues. Plant Physiol Commun 30:207–210

    CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66:675–683

    Article  CAS  PubMed  Google Scholar 

  • Zuo Z, Chen Z, Zhu Y (2014) Effects of NaCl and Na2CO3 stresses on photosynthetic ability of Chlamydomonas reinhardtii. Biologia 69:1314–1322

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by Special Fund for Discipline Construction of Gansu Agricultural University (GSAU-XKJS-2018-221) and National Natural Science Foundation of China (Project Number 31960581).

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Wang, S., Zhang, R., Zhang, Z. et al. Genome-wide analysis of the bZIP gene lineage in apple and functional analysis of MhABF in Malus halliana. Planta 254, 78 (2021). https://doi.org/10.1007/s00425-021-03724-y

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