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Apple Columnar Gene MdDMR6 Increases the Salt Stress Tolerance in Transgenic Tobacco Seedling and Apple Calli

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Abstract

Recent studies have shown that the MdDMR6 is a key gene for the control of columnar growing habit. However, there has been no research report on the function of the MdDMR6 gene. In the present study, the columnar apple shoot cultures exhibited better tolerance than that of the standard apple shoot cultures under the salt stress. The expression of MdDMR6 was remarkably induced by the salt stress. Subsequently, the MdDMR6 was transferred into tobacco and apple calli via the Agrobacterium-mediated approach. Functional analysis showed that the overexpressing transgenic tobacco and apple calli displayed salt tolerance and ABA-insensitive phenotype through physiological and biochemical analysis. The MdDMR6 overexpression activated the transcript levels of several genes involved in the ABA-dependent stress genes under the salt condition. These results suggest that the MdDMR6 would increase the plant tolerance to the salt stress via activating or interacting other protein to indirectly activate ABA-dependent pathways.

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References

  • Ahmed I, Yadav D, Shukla P, Kirti PB (2018) Heterologous expression of Brassica juncea annexin, AnnBj2 confers salt tolerance and ABA insensitivity in transgenic tobacco seedlings. Funct Integr Genomic 18:569–579

    Article  CAS  Google Scholar 

  • Alexandersson E, Danielson JAH, Rade J, Moparthi VK, Fontes M, Kjellbom P, Johanson U (2010) Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. Plant J 61:650–660

    Article  CAS  Google Scholar 

  • An JP, Yao JF, Wang XN, You CX, Wang XF, Hao YJ (2017a) MdHY5 positively regulates cold tolerance via CBF-dependent and CBF-independent pathways in apple. J Plant Physiol 218:275–281

    Article  CAS  Google Scholar 

  • An JP, Liu X, Song LQ, You CX, Wang XF, Hao YJ (2017b) Apple RING finger E3 ubiquitin MdMIEL1 negatively regulates salt and oxidative stress tolerance. J Plant Biol 60:137–145

    Article  CAS  Google Scholar 

  • Ashraf M, Harris P (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16

    Article  CAS  Google Scholar 

  • Bai T, Zhu Y, Fernandez-Fernandez F, Keulemans J, Brown S, Xu K (2012) Fine genetic mapping of the Co locus controlling columnar growth habit in apple. Mol Genet Genomics 287:437–450

    Article  CAS  Google Scholar 

  • Baldi P, Wolters PJ, Komjanc M, Viola R, Velasco R, Salvi S (2013) Genetic and physical characterization of the locus controlling columnar habit in apple (Malus×domestic Borkh.). Mol Breeding 31:429–440

    Article  CAS  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  CAS  Google Scholar 

  • Cai G, Wang L, Liu Y, Pan J, Li D (2014) A maize mitogen activated protein kinase kinase, ZmMKK1, positively regulated the salt and drought tolerance in transgenic Arabidopsis. J Plant Physiol 171:1003–1016

    Article  CAS  Google Scholar 

  • Du C, Zhao P, Zhang H, Li N, Zheng L, Wang Y (2017) The Reaumuria trigyna transcription factor RtWRKY1 confers tolerance to salt stress in transgenic Arabidopsis. J Plant Pysiol 215:48–58

    Article  CAS  Google Scholar 

  • Hiscox JT, Isratelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. J Botany 57:1332–1334

    CAS  Google Scholar 

  • Hollender CA, Dardick C (2014) Molecular basis of angiosperm tree architecture. New Phytol 6:541–556

    Google Scholar 

  • Jacob HB, Herter FG, Leite GB, Raseira MDCB (2010) Breeding experiments of apple varieties with columnar growth and low chilling requirements. Acta Hortic 872:159–164

    Article  Google Scholar 

  • Kelsey DF, Brown SK (1992) ‘McIntosh Wijcik’: a columnar mutation of ‘McIntosh’ apple proving useful in physiology and breeding research. J Am Pomol Soc 46:83–87

    Google Scholar 

  • Kim SA, Ahn SY, Yun HK (2016) Analysis of structure and expression of grapevine 2-osoglutarate genes in response to low temperature. Korean J Hortic Sci 2:46–54

    Google Scholar 

  • Lapins KO (1976) Inheritance of compact growth type in apple. J Am Soc Hortic Sci 101:133–135

    Google Scholar 

  • Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748

    Article  CAS  Google Scholar 

  • Li J, Li Y, Yin Z, Jiang J, Zhang M, Guo X, Ye Z, Zhao Y, Xiong H, Zhang Z, Shao Y, Jiang C, Zhang H, An G, Paek NC, Ali J, Li Z (2017) OsASE5 enhances drought tolerance through a stomatal closure pathway associated with ABA and H2O2 signaling in rice. J Plant Biol 15:183–196

    CAS  Google Scholar 

  • Moriya S, Iwanami H, Kotoda N, Takahashi S, Yamamoto T, Abe K (2009) Development of a marker-assisted selection system for columnar growth habit in apple breeding. J Jpn Soc Hortic Sci 78:279–287

    Article  CAS  Google Scholar 

  • Moriya S, Okada K, Haji T, Yamamoto T, Abe K (2012) Fine mapping of Co, a gene controlling columnar growth habit located on apple (Malus×domestic Borkh). Plant Breed 131:641–647

    Article  CAS  Google Scholar 

  • Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, Narusaka M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Interaction between two cis-acting elements, AREB and DREB, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148

    Article  CAS  Google Scholar 

  • Okada K, Wada M, Moriya S, Katayose Y, Fujisawa H, Wu J, Kanamori H, Kurita K, Sasaki H, Fujii H, Terakami S, Iwanami H, Yamamoto T, Abe K (2016) Expression of a putative dioxygenase gene adjacent to an insertion mutation is involved in the short internodes of columnar apples (Malus×domestic). J Plant Res 129:1109–1126

    Article  CAS  Google Scholar 

  • Otto D, Petersen R, Brauksiepe B, Braun P, Schmidt ER (2014) The columnar mutation (‘Co gene’) of apple (Malus×domestic) is associated with an integration of a Gypsy-like retrotransposon. Mol Breed 33:863–880

    Article  CAS  Google Scholar 

  • Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Li D (2012) ZmMPK17, a novel maize group D MAP kinase gene, is involved multiple stress response. Planta 235:661–676

    Article  CAS  Google Scholar 

  • Petersen R, Krost C (2013) Tracing a key player in the regulation of plant architecture: the columnar growth habit of apple trees (Malus×domestica). Planta 238:1–22

    Article  CAS  Google Scholar 

  • Petersen R, Djozgic H, Rieger B, Rapp S, Schmidt ER (2015) Columnar apple primary roots share some features of the columnar specific gene expression profile of aerial plant parts as evidenced by RNA-Seq analysis. BMC Plant Biol 15:34

    Article  Google Scholar 

  • Pose D, Castanedo I, Borsani O, Nieto B, Rosado A, Taconnat L, Ferrer A, Dolan L, Valpuesta V, Botella MA (2009) Identification of the Arabidopsis dry2/sqe1-5 mutant reveals a central role for sterols in drought tolerance and regulation of reactive oxygen species. Plant J 59:63–76

    Article  CAS  Google Scholar 

  • Qin F, Sakuma Y, Tran LSP, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y, Miyazono KI (2008) Arabidopsis DREB2A-interacting proteins function as Ring E3 liagases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693–1707

    Article  CAS  Google Scholar 

  • Sato H, Takasaki H, Takahashi F, Suzuki T, Iuchi S, Mitsuda N, Ohme-Takagi M, Ikeda M, Seo M, Yamaguchi-Shinozaki K, Shinozaki K (2018) Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stresss. Proc Natl Acad Sci USA 115:E11178–E11187

    Article  CAS  Google Scholar 

  • Verma V, Ravindran P, Kumar P (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86

    Article  Google Scholar 

  • Wang YC, Qu GZ, Li HY, Wu YJ, Wang C, Liu GF, Yang CP (2010) Enhanced salt tolerance of transgenic poplar plants expressing a manganese superoxide dismutase from Tamarix androssowii. Mol Biol Rep 37:1119–1124

    Article  CAS  Google Scholar 

  • Wolters PJ, Schouten HJ, Velasco R, Si-Ammour A, Baldi P (2013) Evidence for regulation of columnar habit in apple by a putative 2OG-Fe(II) oxygenase. New Phytol 200:993–999

    Article  CAS  Google Scholar 

  • Yang W, Liu XD, Chi XJ, Wu CA, Li YZ, Song LL, Liu XM, Wang YF, Wang FW, Zhang C, Liu Y, Zong JM, Li HY (2011) Dwarf apple MbDREB1 enhances plant tolerance to low temperature, drought, and salt stress via both ABA-dependent and ABA-independent pathways. Planta 233:219–229

    Article  CAS  Google Scholar 

  • Yoshida T, Fujita Y, Sayama H, Kyonoshin S, Maruyama K, Mizoi J, Shinozaki K, Shinozaki KY (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 61:672–685

    Article  CAS  Google Scholar 

  • Yoshida T, Mogami J, Yamguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Plant Biol 21:133–139

    CAS  Google Scholar 

  • Zhang YG, Dai HY (2011) Comparison of photosynthetic and morphological characteristics, and micro-structure of roots and shoots, between columnar apple and standard apple trees of hybrid seedlings. Phyton 80:119–125

    Article  Google Scholar 

  • Zhang YG, Zhu J, Dai HY (2012) Characterization of transcriptional differences between columnar and standard apple trees using RNA-seq. Plant Mol Biol Rep 30:957–965

    Article  CAS  Google Scholar 

  • Zhang W, Yang H, You Y, Xu K, Ran K, Fans, (2014) Cloning, characterization and functional analysis of the role MhNCED3, a gene encoding 9-cis-epoxycarotenoid dioxygenase in Malus hupensis Rehd., plays in plant tolerance to osmotic and Cd2+ stress. Plant Soil 381:143–160

    Article  CAS  Google Scholar 

  • Zhang WW, Yan HQ, You SZ, Ran K (2015) MhNCED3 in Malus hupehensis Rehd. Induces NO generation under osmotic stress by regulating ABA accumulation. Plant Physiol Biochem 96:254–260

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to all the laboratory members for continuous technical advices and helpful discussions. This work was supported by the National Natural Science Foundation of China (Grant no. 31372032), China Agriculture Research System Foundation (Grant no. CARS-27), PhD Foundation of Qingdao Agricultural University (Grant No. 1118031). The first two authors contributed equally to this work.

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Correspondence to Yugang Zhang.

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Supplementary file 1 (DOCX 79 kb)

344_2020_10082_MOESM2_ESM.jpg

Supplementary file 2 Fig. S1 qRT-PCR analysis of MdDMr6 gene in transgenic apple calli lines (A) and tobacco lines (B) (JPEG 871 kb)

344_2020_10082_MOESM3_ESM.tiff

Supplementary file 3 Fig. S2 Expression analysis of ABA biosynthesis in apple shoot cultures, transgenic apple calli lines (L11, L12, L13) and tobacco lines (L4, L5, L15) (TIFF 506 kb)

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Sun, X., Wen, C., Zhu, J. et al. Apple Columnar Gene MdDMR6 Increases the Salt Stress Tolerance in Transgenic Tobacco Seedling and Apple Calli. J Plant Growth Regul 40, 187–196 (2021). https://doi.org/10.1007/s00344-020-10082-8

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  • DOI: https://doi.org/10.1007/s00344-020-10082-8

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