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A novel AP2/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis

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Here we first found that GsERF71, an ERF factor from wild soybean could increase plant alkaline stress tolerance by up-regulating H+-ATPase and by modifing the accumulation of Auxin.

Abstract

Alkaline soils are widely distributed all over the world and greatly limit plant growth and development. In our previous transcriptome analyses, we have identified several ERF (ethylene-responsive factor) genes that responded strongly to bicarbonate stress in the roots of wild soybean G07256 (Glycine soja). In this study, we cloned and functionally characterized one of the genes, GsERF71. When expressed in epidermal cells of onion, GsERF71 localized to the nucleus. It can activate the reporters in yeast cells, and the C-terminus of 170 amino acids is essential for its transactivation activity. Yeast one-hybrid and EMSA assays indicated that GsERF71 specifically binds to the cis-acting elements of the GCC-box, suggesting that GsERF71 may participate in the regulation of transcription of the relevant biotic and abiotic stress-related genes. Furthermore, transgenic Arabidopsis plants overexpressing GsERF71 showed significantly higher tolerance to bicarbonate stress generated by NaHCO3 or KHCO3 than the wild type (WT) plants, i.e., the transgenic plants had greener leaves, longer roots, higher total chlorophyll contents and lower MDA contents. qRT-PCR and rhizosphere acidification assays indicated that the expression level and activity of H+-ATPase (AHA2) were enhanced in the transgenic plants under alkaline stress. Further analysis indicated that the expression of auxin biosynthetic genes and IAA contents were altered to a lower extent in the roots of transgenic plants than WT plants under alkaline stress in a short-term. Together, our data suggest that GsERF71 enhances the tolerance to alkaline stress by up-regulating the expression levels of H+-ATPase and by modifying auxin accumulation in transgenic plants.

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Abbreviations

WT:

Wild type

OX:

Overexpression

TF:

Transcription factor

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31670272 to XD, 31171578 to YZ, 31501331 to DZ), Heilongjiang Provincial Higher School Science and Technology Innovation Team Building Program (2011TD005), and the NEAU starting grant to XD.

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Authors and Affiliations

  1. Key Laboratory of Agricultural Biological Functional Genes, Northeast Agricultural University, Harbin, 150030, China

    Yang Yu, Xiangbo Duan, Xiaodong Ding, Chao Chen, Lei Cao, Xuewei Song, Pinghui Zhu, Qiang Li, Zaib_un Nisa, Jiyang Yu, Jianying Du, Yu Song, Huiqing Li & Yanming Zhu

  2. College of Life Science, Qingdao Agricultural University, Qingdao, 266109, China

    Dan Zhu

  3. School of Life Science and Biotechnology, Heilongjiang Bayi Agricultural University, Daqing, 163319, China

    Kuide Yin

  4. Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, 413, Sweden

    Beidong Liu

Authors
  1. Yang Yu
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  2. Xiangbo Duan
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  3. Xiaodong Ding
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  4. Chao Chen
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  5. Dan Zhu
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  6. Kuide Yin
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  7. Lei Cao
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  8. Xuewei Song
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  9. Pinghui Zhu
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  10. Qiang Li
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  11. Zaib_un Nisa
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  12. Jiyang Yu
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  13. Jianying Du
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  14. Yu Song
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  15. Huiqing Li
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  16. Beidong Liu
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  17. Yanming Zhu
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Contributions

Yang Yu and Yanming Zhu conceived the project; Yang Yu, Xiangbo Duan, Chao Chen, Lei Cao, Xuewei Song, Zaib_un Nisa, Jiyang Yu and Qiang Li performed the experiments; Pinghui Zhu, Dan Zhu, Jianying Du, Yu Song and Huiqing Li analyzed the data; Yang Yu wrote the manuscript; Beidong Liu, Kuide Yin and Xiaodong Ding revised the manuscript.

Corresponding author

Correspondence to Yanming Zhu.

Electronic supplementary material

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11103_2017_623_MOESM1_ESM.tif

Supplemental Figure 1 The transcript levels of GsERF71 in the WT and OX lines. The transcription expression level of GsERF71were analyzed by semi-quantitative RT-PCR, the Actin2 gene was used as an internal standard. Supplementary material 1 (TIF 400 KB)

11103_2017_623_MOESM2_ESM.tif

Supplemental Figure 2 Overexpression of GsERF71 in Arabidopsis enhanced KHCO3 tolerance. a The phenotype of WT and GsERF71 transgenic seedlings grown on 1/2 MS medium with 0 or 6mM KHCO3. b Quantitative evaluation of leaf opening and greening rates. Experiments were performed at least three times. The bars represent standard errors. The mean values (±SE) were based on three replicates (each with 90 seeds for each line). *P< 0.05, **P< 0.01 by Student’s t test. c-d Phenotypes and measurements of primary root length of WT and OX seedlings under normal and KHCO3 stress. All mean values (±SE) were based on three independent experiments (30 seedlings per experiment). *P< 0.05, **P< 0.01 by Student’s t test. Supplementary material 2 (TIF 8931 KB)

11103_2017_623_MOESM3_ESM.tif

Supplemental Figure 3 GsERF71 did not affect plant tolerance of high pH (KOH) stress. a The growth of WT and OX seedlings on 1/2 MS medium with pH 7.5 or 8.2. Photographs were taken 7 days after germination. b Quantitative evaluation of leaf opening and greening rates. Experiments were performed at least three times (each with 90 seeds for each line). c-d Phenotypes and measurements of primary root lengths of WT and OX seedlings under normal and high pH stress. Seven-day-old seedlings grown on 1/2 MS were transferred to new solid agar plates with pH 5.8, 7.5 and 8.2, respectively. Photographs were taken after 7d growth on the media. All values are means (±SE) from three independent experiments (30 seedlings per experiment). *P < 0.05, **P < 0.01 by Student’s t test. Supplementary material 3 (TIF 1811 KB)

11103_2017_623_MOESM4_ESM.tif

Supplemental Figure 4 Expression patterns of auxin synthesis- or transport-related genes in the roots of WT and GsERF71 transgenic Arabidopsis under alkaline stress. 7-d-old WT and GsERF71 transgenic seedlings treated with 6mM NaHCO3 for up to 5 days. The mean values were based on three biological replicates for each. *P< 0.05, **P< 0.01 by two-way ANOVA with Bonferroni posttests compared with the WT at each time point. Supplementary material 4 (TIF 34011 KB)

Supplementary material 5 (DOCX 20 KB)

Supplementary material 6 (DOCX 20 KB)

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Yu, Y., Duan, X., Ding, X. et al. A novel AP2/ERF family transcription factor from Glycine soja, GsERF71, is a DNA binding protein that positively regulates alkaline stress tolerance in Arabidopsis . Plant Mol Biol 94, 509–530 (2017). https://doi.org/10.1007/s11103-017-0623-7

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  • DOI: https://doi.org/10.1007/s11103-017-0623-7

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