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Heterologous expression of a Fraxinus velutina SnRK2 gene in Arabidopsis increases salt tolerance by modifying root development and ion homeostasis

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Abstract

Key message

FvSnRK2182 is involved in regulating the growth and stress response.

Abstract

SnRK2 family members are positive regulators of downstream signals in the abscisic acid (ABA) signaling pathway, playing key roles in the plant responses to abiotic stresses. Fraxinus velutina Torr. is a candidate phytoremediator of saline–alkali areas, and is a valuable research subject because of its adaptability in saline soil. We identified a SnRK2 gene in F. velutina (named FvSnRK2182), which was significantly upregulated under salt stress. A bioinformatics analysis showed that FvSnRK2182 has a Ser/Thr kinase domain typical of the SnRK2 subfamily. Compared with wild-type (WT) Arabidopsis, its heterologous expression in Arabidopsis resulted in higher auxin content during seed germination and seedling growth, leading to longer primary roots and more lateral roots. The transgenic lines were better able to tolerate treatments with NaCl (100 mM) and/or ABA (0.2 and 0.5 µM), producing a greater biomass than the WT plants. Under NaCl treatment, the shoots of the transgenic lines had lower Na+ contents and higher K+ contents than the WT plants, and the genes encoding the ion transport–related proteins SOS1, HKT1, NHX1, and AKT1 were significantly upregulated. In addition, the expression of the genes functioning downstream of SnRK2 in the ABA signaling pathway (Rboh, AREB4, ABF2, and ABF3) were significantly upregulated in transgenic lines under NaCl stress. These results showed that expressing FvSnRK2182 in Arabidopsis significantly increased their resistance to ABA and salt stress by regulating root development and maintaining ion homeostasis, which suggests that FvSnRK2182 may be involved in regulating the growth and stress response of F. velutina.

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References

  • Abdeen A, Schnell J, Miki B (2010) Transcriptome analysis reveals absence of unintended effects in drought-tolerant transgenic plants overexpressing the transcription factor ABF3. BMC Genomics 11:69

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ali A, Raddatz N, Pardo JM, Yun DJ (2021) HKT sodium and potassium transporters in Arabidopsis thaliana and related halophyte species. Physiol Plant 171(4):546–558

    Article  CAS  PubMed  Google Scholar 

  • Belda-Palazón B, Adamo M, Valerio C, Ferreira LJ, Confraria A, Reis-Barata D, Rodrigues A, Meyer C, Rodriguez PL, Baena-González E (2020) A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat Plants 6(11):1345–1353

    Article  PubMed  CAS  Google Scholar 

  • Cao BH, Wu LY (2008) Studies on soil enzyme activity and soil nutrient content of mixed stands with Robinia pseudoacacia and Fraxinus velutina in coastal saline soil. J Soil Water Conserv 01:128–133 ((in Chinese))

    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(3):1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17(12):3470–3488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Nakashima K, Yoshida T, Katagiri T, Kidokoro S, Kanamori N, Umezawa T, Fujita M, Maruyama K, Ishiyama K, Kobayashi M, Nakasone S, Yamada K, Ito T, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50(12):2123–2132

    Article  CAS  PubMed  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geiger D, Scherzer S, Mumm P, Marten I, Ache P, Matschi S, Liese A, Wellmann C, Al-Rasheid KA, Grill E, Romeis T, Hedrich R (2010) Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107(17):8023–8028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gong Z, Xiong L, Shi H, Yang S, Herrera-Estrella LR, Xu G, Chao DY, Li J, Wang PY, Qin F, Li J, Ding Y, Shi Y, Wang Y, Yang Y, Guo Y, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674

    Article  PubMed  Google Scholar 

  • Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14(12):3177–3189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kawa D, Meyer AJ, Dekker HL, Abd-El-Haliem AM, Gevaert K, Van De Slijke E, Maszkowska J, Bucholc M, Dobrowolska G, De Jaeger G, Schuurink RC, Haring MA, Testerink C (2020) SnRK2 protein kinases and mRNA decapping machinery control root development and response to salt. Plant Physiol 182(1):361–377

    Article  CAS  PubMed  Google Scholar 

  • Kim S, Choi HI, Ryu HJ, Park JH, Kim MD, Kim SY (2004) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136(3):3639–3648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(6):939–949

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19(3):1065–1080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulik A, Wawer I, Krzywińska E, Bucholc M, Dobrowolska G (2011) SnRK2 protein kinases-key regulators of plant response to abiotic stresses. OMICS 15(12):859–872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Zhao C, Zhang M, Yuan F, Chen M (2019) Exogenous melatonin improves seed germination in Limonium bicolor under salt stress. Plant Signal Behav 14(11):1659705

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu Z, Ge X, Yang Z, Zhang C, Zhao G, Chen E, Liu J, Zhang X, Li F (2017) Genome-wide identification and characterization of SnRK2 gene family in cotton (Gossypium hirsutum L.). BMC Genet 18(1):54

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu CX, Zhao C, Liu J, Li KL, Wang BS, Chen M (2021) Increased salinity and groundwater levels lead to degradation of the Robinia pseudoacacia forest in the Yellow River Delta. J For Res 1–13. https://doi.org/10.1007/s11676-021-01422-9

  • Maathuis FJ, Ichida AM, Sanders D, Schroeder JI (1997) Roles of higher plant K+ channels. Plant Physiol 114(4):1141–1149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchant A, Kargul J, May ST, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18(8):2066–2073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mazur R, Maszkowska J, Anielska-Mazur A, Garstka M, Polkowska-Kowalczyk L, Czajkowska A, Zmienko A, Dobrowolska G, Kulik A (2021) The SnRK2.10 kinase mitigates the adverse effects of salinity by protecting photosynthetic machinery. Plant Physiol 187(4):2785–2802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLoughlin F, Galvan-Ampudia CS, Julkowska MM, Caarls L, van der Does D, Laurière C, Munnik T, Haring MA, Testerink C (2012) The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J 72(3):436–449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieva C, Busk PK, Domínguez-Puigjaner E, Lumbreras V, Testillano PS, Risueño MC, Pagès M (2005) Isolation and functional characterisation of two new bZIP maize regulators of the ABA responsive gene rab28. Plant Mol Biol 58(6):899–914

    Article  CAS  PubMed  Google Scholar 

  • Pang CH, Xia Y, Li SY, Zhou J, Wang ZM (2015) The Salt-tolerant Gene FvSnRK2.1 of Fraxinus velutina Torr and its application, CN105177030A [P] (in Chinese)

  • Shabala S, Pottosin I (2014) Regulation of potassium transport in plants under hostile conditions: implications for abiotic and biotic stress tolerance. Physiol Plant 151(3):257–279

    Article  CAS  PubMed  Google Scholar 

  • Song X, Yu X, Hori C, Demura T, Ohtani M, Zhuge Q (2016) Heterologous overexpression of poplar SnRK2 genes enhanced salt stress tolerance in Arabidopsis thaliana. Front Plant Sci 7:612

    PubMed  PubMed Central  Google Scholar 

  • Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MH, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88

    Article  CAS  PubMed  Google Scholar 

  • Sumimoto H (2008) Structure, regulation and evolution of Nox-family NADPH oxidases that produce reactive oxygen species. FEBS J 275(13):3249–3277

    Article  CAS  PubMed  Google Scholar 

  • Trull MC, Guiltinan MJ, Lynch JP, Deikman J (2008) The responses of wild-type and ABA mutant Arabidopsis thaliana plants to phosphorus starvation. Plant Cell Environ 20(1):85–92

    Article  Google Scholar 

  • Wang P, Guo Q, Wang Q, Zhou XR, Wang SM (2015) PtAKT1 maintains selective absorption capacity for K+ over Na+ in halophyte Puccinellia tenuiflora under salt stress. Acta Physiol Plant 37(5):100

    Article  CAS  Google Scholar 

  • Won C, Shen X, Mashiguchi K, Zheng Z, Dai X, Cheng Y, Kasahara H, Kamiya Y, Chory J, Zhao Y (2011) Conversion of tryptophan to indole-3-acetic acid by TRYPTOPHAN AMINOTRANSFERASES OF ARABIDOPSIS and YUCCAs in Arabidopsis. Proc Natl Acad Sci USA 108(45):18518–18523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan L, Liu C, Wang Y, Wang K, Ren F, Yao J, Wu D (2019) De novo transcriptome analysis of Fraxinus velutina Torr. in response to NaCl stress. Tree Genet Genomes 15(4):1–7

    Article  Google Scholar 

  • Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217(2):523–539

    Article  CAS  PubMed  Google Scholar 

  • Ying S, Zhang DF, Li HY, Liu YH, Shi YS, Song YC, Wang TY, Li Y (2011) Cloning and characterization of a maize SnRK2 protein kinase gene confers enhanced salt tolerance in transgenic Arabidopsis. Plant Cell Rep 30(9):1683–1699

    Article  CAS  PubMed  Google Scholar 

  • Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43(12):1473–1483

    Article  CAS  PubMed  Google Scholar 

  • Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K (2006) The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J Biol Chem 281(8):5310–5318

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61(4):672–685

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Fujita Y, Maruyama K, Mogami J, Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signaling in response to osmotic stress. Plant Cell Environ 38(1):35–49

    Article  CAS  PubMed  Google Scholar 

  • Yu L (1996) Studies on the cultivation of Fraxinus velutina in saline soils of coastal region. J Liaoning for Sci Technol 4:13–16 ((in Chinese))

    Google Scholar 

  • Zhang H, Mao X, Wang C, Jing R (2010) Overexpression of a common wheat gene TaSnRK2.8 enhances tolerance to drought, salt and low temperature in Arabidopsis. PLoS ONE 5(12):e16041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the NSFC (National Natural Science Research Foundation of China, project nos. 32170281; 31600488), Shandong Provincial “Bohai Granary” Science and Technology Demonstration Project (2019BHLC004), Shandong Province Natural Science Foundation (ZR2019MC065), Agricultural Variety Improvement Project of Shandong Province (2019LZGC009).

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Author notes

  1. Mingjing Zhang and Li Liu have contributed equally to this work.

Authors and Affiliations

  1. Shandong Provincial Key Laboratory of Plant Stress Research, College of Life Science, Shandong Normal University, Jinan, 250014, China

    Mingjing Zhang, Li Liu, Chunxiao Chen, Yang Zhao & Min Chen

  2. Shandong Provincial Key Laboratory of Forest Tree Genetic Improvement, Shandong Academy of Forestry, Jinan, 250014, China

    Caihong Pang

  3. Dongying Institute, Shandong Normal University, No. 2 Kangyang Road, Dongying, 257000, China

    Min Chen

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  1. Mingjing Zhang
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  2. Li Liu
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  3. Chunxiao Chen
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  4. Yang Zhao
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  5. Caihong Pang
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Contributions

MC and CP: designed the research, MZ, LL and CC: performed the experiments. MZ: wrote the paper with contributions from the other authors. MZ and YZ: analyzed the data. MC: revised the paper. All authors read and approved the final manuscript.

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Correspondence to Caihong Pang or Min Chen.

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Communicated by Chun-Hai Dong.

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Zhang, M., Liu, L., Chen, C. et al. Heterologous expression of a Fraxinus velutina SnRK2 gene in Arabidopsis increases salt tolerance by modifying root development and ion homeostasis. Plant Cell Rep 41, 1895–1906 (2022). https://doi.org/10.1007/s00299-022-02899-2

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