The upstream regulatory mechanism of BplMYB46 and the function of upstream regulatory factors that mediate resistance to stress in Betula platyphylla

Previously, we have shown that the transcription factor BplMYB46 in Betula platyphylla can enhance tolerance to salt and osmotic stress and promote secondary cell wall deposition, and we characterized its downstream regulatory mechanism. However, its upstream regulatory mechanism remains unclear. Here, the promoter activity and upstream regulatory factors of BplMYB46 were studied. Analyses of β-glucuronidase (GUS) staining and activity indicated that BplMYB46 promoter was specific temporal and spatial expression, and its expression can be induced by salt and osmotic stress. We identified three upstream regulatory factors of BplMYB46: BpDof1, BpWRKY3, and BpbZIP3. Yeast-one hybrid assays, GUS activity, chromatin immunoprecipitation, and quantitative real-time polymerase chain reaction revealed that BpDof1, BpWRKY3, and BpbZIP3 can directly regulate the expression of BplMYB46 by specifically binding to Dof, W-box, and ABRE elements in the BplMYB46 promoter, respectively. BpDof1, BpWRKY3, and BpbZIP3 were all localized to the nucleus, and their expressions can be induced by stress. Overexpression of BpDof1, BpWRKY3, and BpbZIP3 conferred the resistance of transgenic birch plants to salt and osmotic stress. Our findings provide new insights into the upstream regulatory mechanism of BplMYB46 and reveal new upstream regulatory genes that mediate resistance to adverse environments. The genes identified in our study provide novel targets for the breeding of forest tree species.

[1]  B. Bello,et al.  A Novel mechanisms of the signaling cascade associated with the SAPK10-bZIP20-NHX1 synergistic interaction to enhance tolerance of plant to abiotic stress in rice (Oryza sativa L.). , 2022, Plant science : an international journal of experimental plant biology.

[2]  Yuan-Yuan Li,et al.  The Transcription Factor MdMYB2 Influences Cold Tolerance and Anthocyanin Accumulation by Activating SUMO E3 Ligase MdSIZ1 in Apple. , 2022, Plant physiology.

[3]  Deguo Han,et al.  Molecular Cloning and Characterization of MbMYB108, a Malus baccata MYB Transcription Factor Gene, with Functions in Tolerance to Cold and Drought Stress in Transgenic Arabidopsis thaliana , 2022, International journal of molecular sciences.

[4]  Shengli Wei,et al.  Overexpression of PnMYB2 from Panax notoginseng induces cellulose and lignin biosynthesis during cell wall formation , 2022, Planta.

[5]  Ludan Li,et al.  TcMYB29a, an ABA-Responsive R2R3-MYB Transcriptional Factor, Upregulates Taxol Biosynthesis in Taxus chinensis , 2022, Frontiers in Plant Science.

[6]  OUP accepted manuscript , 2022, The Plant Cell.

[7]  Jinhui Chen,et al.  Genome-wide characterization of bZIP transcription factors and their expression patterns in response to drought and salinity stress in Jatropha curcas. , 2021, International journal of biological macromolecules.

[8]  Jiyu Zhang,et al.  Genome-Wide Analysis and Expression Profiles of the Dof Family in Cleistogenes songorica under Temperature, Salt and ABA Treatment , 2021, Plants.

[9]  G. Cannarozzi,et al.  Complex evolution of novel red floral color in Petunia , 2021, The Plant cell.

[10]  S. Chen,et al.  A transcriptional regulatory module controls lipid accumulation in soybean. , 2021, The New phytologist.

[11]  Gaojie Li,et al.  Genome-wide identification and comparative analysis of the WRKY gene family in aquatic plants and their response to abiotic stresses in giant duckweed (Spirodela polyrhiza). , 2021, Genomics.

[12]  Xueying Zhang,et al.  Involvement of the R2R3-MYB transcription factor MYB21 and its homologs in regulating flavonol accumulation in Arabidopsis stamen , 2021, Journal of experimental botany.

[13]  Xiaorui Guo,et al.  MYB Transcription Factors and Its Regulation in Secondary Cell Wall Formation and Lignin Biosynthesis during Xylem Development , 2021, International journal of molecular sciences.

[14]  Yu-Cheng Wang,et al.  ThNAC12 from Tamarix hispida directly regulates ThPIP2;5 to enhance salt tolerance by modulating reactive oxygen species. , 2021, Plant physiology and biochemistry : PPB.

[15]  A. Hashem,et al.  Plant Defense Responses to Biotic Stress and Its Interplay With Fluctuating Dark/Light Conditions , 2021, Frontiers in Plant Science.

[16]  Huizi Liu,et al.  The BpMYB4 Transcription Factor From Betula platyphylla Contributes Toward Abiotic Stress Resistance and Secondary Cell Wall Biosynthesis , 2021, Frontiers in Plant Science.

[17]  Q. Qian,et al.  MORE FLORET1 Encodes a MYB Transcription Factor That Regulates Spikelet Development in Rice1 , 2020, Plant Physiology.

[18]  Xiaofeng Liu,et al.  Correction to: The MYB transcription factor CiMYB42 regulates limonoids biosynthesis in citrus , 2020, BMC Plant Biology.

[19]  Yucheng Wang,et al.  Building a Robust Chromatin Immunoprecipitation Method with Substantially Improved Efficiency1 , 2020, Plant Physiology.

[20]  A. Shakoor,et al.  Biochemically Triggered Heat and Drought Stress Tolerance in Rice by Proline Application , 2020, Journal of Plant Growth Regulation.

[21]  Xiaofeng Liu,et al.  The MYB transcription factor CiMYB42 regulates limonoids biosynthesis in citrus , 2020, BMC Plant Biology.

[22]  Sujit Roy,et al.  Investigation of the effect of UV-B light on Arabidopsis MYB4 (AtMYB4) transcription factor stability and detection of a putative MYB4-binding motif in the promoter proximal region of AtMYB4 , 2019, PloS one.

[23]  Lijun Wang,et al.  R2R3-MYB transcription factor MYB6 promotes anthocyanin and proanthocyanidin biosynthesis but inhibits secondary cell wall formation in Populus tomentosa. , 2019, The Plant journal : for cell and molecular biology.

[24]  Jian-Ping An,et al.  An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1‐mediated degradation , 2019, Plant biotechnology journal.

[25]  A. Allan,et al.  PbrMYB169 positively regulates lignification of stone cells in pear fruit , 2019, Journal of experimental botany.

[26]  Yuan Meng,et al.  CaMADS, a MADS-box transcription factor from pepper, plays an important role in the response to cold, salt, and osmotic stress. , 2019, Plant science : an international journal of experimental plant biology.

[27]  Chuanping Yang,et al.  BpNAC012 Positively Regulates Abiotic Stress Responses and Secondary Wall Biosynthesis1[OPEN] , 2018, Plant Physiology.

[28]  Chunrui Zhang,et al.  Identification of novel cis-elements bound by BplMYB46 involved in abiotic stress responses and secondary wall deposition. , 2018, Journal of integrative plant biology.

[29]  Yong Guo,et al.  Arabidopsis thaliana Trihelix Transcription Factor AST1 Mediates Salt and Osmotic Stress Tolerance by Binding to a Novel AGAG-Box and Some GT Motifs , 2018, Plant & cell physiology.

[30]  S. Satyawati,et al.  Salt stress and phyto-biochemical responses of plants - a review , 2018 .

[31]  Qi Wu,et al.  Constitutive expression of OsDof4, encoding a C2-C2 zinc finger transcription factor, confesses its distinct flowering effects under long- and short-day photoperiods in rice (Oryza sativa L.) , 2017, BMC Plant Biology.

[32]  Yucheng Wang,et al.  ThDof1.4 and ThZFP1 constitute a transcriptional regulatory cascade involved in salt or osmotic stress in Tamarix hispida , 2017, Plant Molecular Biology.

[33]  Chunrui Zhang,et al.  Expression of the MYB transcription factor gene BplMYB46 affects abiotic stress tolerance and secondary cell wall deposition in Betula platyphylla , 2016, Plant Biotechnology Journal.

[34]  J. Franco-Zorrilla,et al.  Identification of plant transcription factor target sequences. , 2017, Biochimica et biophysica acta. Gene regulatory mechanisms.

[35]  Xiaoming Zhang,et al.  The R2R3 MYB transcription factor PavMYB10.1 involves in anthocyanin biosynthesis and determines fruit skin colour in sweet cherry (Prunus avium L.) , 2016, Plant biotechnology journal.

[36]  Chunrui Zhang,et al.  ThWRKY4 from Tamarix hispida Can Form Homodimers and Heterodimers and Is Involved in Abiotic Stress Responses , 2015, International journal of molecular sciences.

[37]  Yucheng Wang,et al.  Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. , 2015, The New phytologist.

[38]  Daoyuan Zhang,et al.  A novel ethylene-responsive factor from Tamarix hispida, ThERF1, is a GCC-box- and DRE-motif binding protein that negatively modulates abiotic stress tolerance in Arabidopsis. , 2014, Physiologia plantarum.

[39]  Yucheng Wang,et al.  A Transient Transformation System for the Functional Characterization of Genes Involved in Stress Response , 2014, Plant Molecular Biology Reporter.

[40]  Christopher A. Penfold,et al.  A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves , 2013, The Plant journal : for cell and molecular biology.

[41]  G. Dan,et al.  Effect of Drought Stress and Re-watering on Active Oxygen Scavenging System of Fructus Evodiae Cutting Seedling , 2013 .

[42]  Yucheng Wang,et al.  A Versatile Agrobacterium-Mediated Transient Gene Expression System for Herbaceous Plants and Trees , 2012, Biochemical Genetics.

[43]  Yunliu Fan,et al.  Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species , 2011, Plant Molecular Biology.

[44]  Q. Shen,et al.  WRKY transcription factors. , 2010, Trends in plant science.

[45]  Wen-Wu Guo,et al.  An efficient protocol for genomic DNA extraction fromCitrus species , 2003, Plant Molecular Biology Reporter.

[46]  Suk-Yoon. Kwon,et al.  Enhanced drought tolerance of transgenic rice plants expressing a pea manganese superoxide dismutase. , 2005, Journal of plant physiology.

[47]  Moonil Kim,et al.  Activation of the Programmed Cell Death Pathway by Inhibition of Proteasome Function in Plants* , 2003, Journal of Biological Chemistry.

[48]  S. Yanagisawa The Dof family of plant transcription factors. , 2002, Trends in plant science.

[49]  G. Horgan,et al.  Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR , 2002 .

[50]  D. Hagenbeek,et al.  Functional Interactions of Lanthanum and Phospholipase D with the Abscisic Acid Signaling Effectors VP1 and ABI1-1 in Rice Protoplasts* , 2001, The Journal of Biological Chemistry.