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Exogenous 6-BA enhances salt tolerance of Limonium bicolor by increasing the number of salt glands

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Abstract

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Exogenous 6-BA can increase endogenous hormone content, improve photosynthesis, decrease Na+ by increasing leaf salt gland density and salt secretion ability, and reduce ROS content so that it can promote L. bicolor growth.

Abstract

6-benzyl adenine (6-BA) is an artificial cytokinin and has been widely applied to improving plant adaptation to stress. However, it is rarely reported that 6-BA alleviates salt damage of halophytes. In this paper, we treated Limonium bicolor seedlings, a recretohalophyte with high medicinal and ornamental values, with 300 mM NaCl and different concentrations of 6-BA (0.5, 1.0, and 1.5 mg/L) and measured plant growth, physiological index, the density of salt gland, and the salt secretion ability of leaves. The results showed that exogenous applications 1.0 mg/L 6-BA significantly improved plant growth and photosynthesis, increased cytokinin and auxins contents, K+ and organic soluble matter contents, the activities of SOD, CAT, APX, and POD, and decreased Na+, H2O2, and O2 contents compared to that treated with 300 mM NaCl. Further research showed that exogenous 6-BA significantly increased the density of salt gland and the salt secretion ability of leaves by upregulating the expression of the salt gland developmental genes, therefore, can secrete more excess Na+, and thus reduces the Na+ concentration in leaves, which can alleviate Na+ damage to the species. In all, exogenous 1.0 mg/L 6-BA can increase endogenous hormone, improve photosynthesis, decrease Na+ by increasing secretion ability, and reduce ROS content of L. bicolor so that it can improve the growth. These results above systematically prove the new role of 6-BA in salt tolerance of L. bicolor.

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References

  • Chen M, Yang Z, Liu J, Zhu TT, Wei XC, Fan H, Wang BS (2018) Adaptation mechanism of salt excluders under saline conditions and its applications. Int J Mol Sci 19(11):3668

    Article  PubMed  PubMed Central  Google Scholar 

  • Choi SJ, Kim SB, Lee HY, Na DH, Yoon YS, Lee SS, Kim JH, Lee KC, Lee HS (2001) Column-switching high-performance liquid chromatographic determination of clarithromycin in human plasma with electrochemical detection. Talanta 54:377–382

    Article  CAS  PubMed  Google Scholar 

  • Dat JDH, Foyer CH, Scott IM (1992) Effects of salicylic acid on oxidative stress and thermo tolerance in tobacco. J Plant Physiol 156:659–665

    Article  Google Scholar 

  • Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol 43:599–626

    Article  CAS  Google Scholar 

  • Ding F, Chen M, Sui N, Wang BS (2010) Ca2+ significantly enhanced development and salt–secretion rate of salt glands of Limonium bicolor under NaCl treatment. S Afr J Bot 76:95–101

    Article  CAS  Google Scholar 

  • Galuszka P, Frébortová J, Luhová L, Bilyeu KD, English JT, Frébort I (2005) Tissue localization of cytokinin dehydrogenase in maize possible involvement of quinone species generated from plant phenolics by other enzymatic systems in the catalytic reaction. Plant Cell Physiol 46(5):716–728

    Article  CAS  PubMed  Google Scholar 

  • Gan Y, Kumimoto R, Liu C, Ratcliffe O, Yu H, Broun P (2006) Glabrous inflorescence stems modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18:1383–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao YR, Zhao BQ, Jiao XM, Chen M, Wang BS, Yuan F (2021) Coupled development of salt glands, stomata, and pavement cells in Limonium bicolor. Front Plant Sci 12:745422

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo JR, Li YD, Han G, Song J, Wang BS (2018) NaCl markedly improved the reproductive capacity of the euhalophyte Suaeda salsa. Funct Plant Biol 45:350–361

    Article  CAS  PubMed  Google Scholar 

  • Han N, Lan W, He X, Shao Q, Wang BS (2011) Expression of a Suaeda salsa, Vacuolar H+/Ca2+, Transporter Gene in Arabidopsis, Contributes to Physiological Changes in Salinity. Plant Mol Biol Rep 30:470–477

    Article  Google Scholar 

  • Han GL, Wang MJ, Yuan F, Sui N, Song J, Wang BS (2014) The CCCH zinc finger protein gene AtZFP1, improves salt resistance in Arabidopsis thaliana. Plant Mol Biol 86:237–253

    Article  CAS  PubMed  Google Scholar 

  • Han GL, Qiao ZQ, Li YX, Yang ZR, Zhang ZW, Zhang YY, Guo JJ, Liu LL, Wang CF, Wang BS (2022) LbMYB48 positively regulates salt gland development of Limonium bicolor and salt tolerance of plants. Front Plant Sci 13:1039984

    Article  PubMed  PubMed Central  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salt. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Ren B, Dong S, Liu P, Zhao B, Zhang J (2020) Comparative proteomic analysis reveals that exogenous 6-benzyladenine (6-BA) improves the defense system activity of waterlogged summer maize. BMC Plant Biol 20(1):44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hyoung S, Cho SH, Chung JH, So WM, Cui MH, Shin JS (2020) Cytokinin oxidase PpCKX1 plays regulatory roles in development and enhances dehydration and salt tolerance in Physcomitrella patens. Plant Cell Rep 39(3):419–430

    Article  CAS  PubMed  Google Scholar 

  • Jiao XM, Zhao BQ, Wang BS, Yuan F (2022) An uncharacterized gene Lb1G04794 from Limonium bicolor promotes salt tolerance and trichome development in Arabidopsis. Front Plant Sci 13:1079534

    Article  PubMed  PubMed Central  Google Scholar 

  • Leng BY, Yuan F, Dong XX, Wang BS (2018) Salt gland distribution in Limonium bicolor at the individual level. IOP Conference Series: earth and environmental science 012202

  • Li X, Liu Y, Chen M, Song YP, Song J, Wang BS, Feng G (2012) Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations. Plant Biosyst 146:142–149

    Article  Google Scholar 

  • Li JP, Yuan F, Liu YL, Zhang MJ, Liu Y, Zhao Y, Wang BS, Chen M (2020) Exogenous melatonin enhances salt secretion from salt glands by upregulating the expression of ion transporter and vesicle transport genes in Limonium bicolor. BMC Plant Biol 20(1):493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li JP, Liu Y, Zhang MJ, Xu HL, Ning K, Wang BS, Chen M (2022) Melatonin increases growth and salt tolerance of Limonium bicolor by improving photosynthetic and antioxidant capacity. BMC Plant Biol 22(1):16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin J, Li JP, Yuan F, Yang Z, Wang BS, Chen M (2018) Transcriptome profiling of genes involved in photosynthesis in Elaeagnus angustifolia L. under salt stress. Photosynthetica 56:998–1009

    Article  CAS  Google Scholar 

  • Lu CX, Feng ZT, Yuan F, Han GL, Guo JR, Chen M, Wang BS (2020) The SNARE protein LbSYP61 participates in salt secretion in Limonium bicolor. Environ Exp Bot 176:104076

    Article  CAS  Google Scholar 

  • Ma H, Tian C, Feng G, Yuan J (2011) Ability of multicellular salt glands in Tamarix species to secrete Na+ and K+ selectively. Sci China Life Sci 54(3):282–289

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Physiol 35:15–44

    Article  CAS  Google Scholar 

  • Ren BZ, Zhu YL, Zhang JW, Dong ST, Liu P, Zhao B (2016) Effects of spraying exogenous hormone 6-benzyladenine (6-BA) after waterlogging on grain yield and growth of summer maize. Field Crops Res 188:96–104

    Article  Google Scholar 

  • Rezaei Ghaleh Z, Sarmast MK, Atashi S (2020) 6-Benzylaminopurine (6-BA) ameliorates drought stress response in tall fescue via the influencing of biochemicals and strigolactone-signaling genes. Plant Physiol Biochem 155:877–887

    Article  CAS  PubMed  Google Scholar 

  • Shabala S (2013) Learning from halophytes: physiological basis and strategies to improve abiotic stress tolerance in crops. Ann Bot 12:1209–1221

    Article  Google Scholar 

  • Shelden MC, Dias DA, Jayasinghe NS, Bacic A, Roessner U (2016) Root spatial metabolite profiling of two genotypes of barley (Hordeum vulgare L.) reveals differences in response to short-term salt stress. J Exp Bot 67:3731–3745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheng M, Tang M, Chen H (2008) Influence of arbuscular mycorrhizae on photosynthesis and water status of maize plants under salt stress. Mycorrhiza 18(6–7):287–296

    Article  CAS  PubMed  Google Scholar 

  • Shi HP, Qi Y, Zhang Y, Liang S (2006) Induction of cucumber hairy roots and effect of cytokinin 6-BA on its growth and morphology. J Biotechnol 22(3):514–520

    CAS  Google Scholar 

  • Song J, Wang BS (2014) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Luo JP, Wei ZJ, Zhang JC (2009) Molecular cloning and expression analysis of a cytokinin oxidase(DhCKX) gene in Dendrobium huoshanense. Mol Biol Rep 36:1331–1338

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Liu D, Wei M, Man J (2020) Spraying 6-BA could alleviate the harmful impacts of waterlogging on dry matter accumulation and grain yield of wheat. PeerJ 8:e8193

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang K, Shen Y, Wang H, He S, Kim WS, Shang W, Wang Z, Shi L (2022a) Effects of exogenous salicylic acid (SA), 6-benzylaminopurine (6-BA), or abscisic acid (ABA) on the physiology of Rosa hybrida ‘Carolla’ under high-temperature stress. Hortic 8(9):851

    Article  Google Scholar 

  • Wang X, Wang BS, Yuan F (2022b) Lb1G04202, an uncharacterized protein from recretohalophyte Limonium bicolor, is important in salt tolerance. Int J Mol Sci 23(10):5401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X, He J, Chen J, Yang S, Zha D (2014) Alleviation of exogenous 6-benzyladenine on two genotypes of eggplant (Solanum melongena Mill.) growth under salt stress. Protoplasma 251:169–176

    Article  CAS  PubMed  Google Scholar 

  • Wu X, He J, Ding H, Zhu Z, Chen J, Xu S, Zha D (2015) Modulation of zinc-induced oxidative damage in Solanum melongena by 6-benzylaminopurine involves ascorbate–glutathione cycle metabolism. Environ Exp Bot 116:1–11

    Article  CAS  Google Scholar 

  • Yan A, Wu M, Zhao Y, Zhang A, Liu B, Schiefelbein J, Gan Y (2014) Involvement of C2H2 zinc finger proteins in the regulation of epidermal cell fate determination in Arabidopsis. J Integr Plant Biol 56(12):1112–1117

    Article  CAS  PubMed  Google Scholar 

  • Yasmeen A, Basra SMA, Farooq M, Rehman H, Hussain N (2013) Exogenous application of moringa leaf extract modulates the antioxidant enzyme system to improve wheat performance under saline conditions. Plant Growth Regul 69:225–233

    Article  CAS  Google Scholar 

  • Yuan F, Lyu MJA, Leng BY, Zheng GY, Feng ZT, Li PH, Zhu XG, Wang BS (2015) Comparative transcriptome analysis of developmental stages of the Limonium bicolor leaf generates insights into salt gland differentiation. Plant Cell Environ 38:1637–1657

    Article  CAS  PubMed  Google Scholar 

  • Yuan F, Leng BY, Wang BS (2016a) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt. Front Plant Sci 7:977

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan F, Lyu MJA, Leng BY, Zhu XG, Wang BS (2016b) The transcriptome of NaCl-treated Limonium bicolor leaves reveals the genes controlling salt secretion of salt gland. Plant Mol Biol 91(3):241–256

    Article  CAS  PubMed  Google Scholar 

  • Yuan F, Liang X, Li Y, Yin SS, Wang BS (2018) Methyl jasmonate improves tolerance to high salt stress in the recretohalophyte Limonium bicolor. Funct Plant Biol 46:82–92

    Article  PubMed  Google Scholar 

  • Yuan F, Leng BY, Zhang HK, Wang X, Han GL, Wang BS (2019) A WD40-repeat protein from the recretohalophyte Limonium bicolor enhances trichome formation and salt tolerance in Arabidopsis. Front Plant Sci 10:1456

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan F, Wang X, Zhao BQ, Xu XJ, Shi M, Leng BY, Dong XX, Lu CX, Feng ZT, Guo JR, Han GL, Zhang HK, Huang JW, Chen M, Wang BS (2022) The genome of the recretohalophyte Limonium bicolor provides insights into salt gland development and salinity adaptation during terrestrial evolution. Mol Plant 15(6):1024–1044

    Article  CAS  PubMed  Google Scholar 

  • Zeng QW, Qin S, Song SQ, Zhang M, Xiao YH, Luo M, Hou L, Pei Y (2012) Molecular cloning and characterization of a cytokinin dehydrogenase gene from upland cotton (Gossypium hirsutum L.). Plant Mol Biol Rep 30(1):1–9

    Article  CAS  Google Scholar 

  • Zhang MJ, Chen Z, Yuan F, Wang BS, Chen M (2022a) Integrative transcriptome and proteome analyses provide deep insights into the molecular mechanism of salt tolerance in Limonium bicolor. Plant Mol Biol 108(1–2):127–143

    Article  CAS  PubMed  Google Scholar 

  • Zhang WJ, Wang BB, Zhang AM, Zhou QR, Li Y, Li LY, Ma SY, Fan YH, Huang ZL (2022b) Exogenous 6-benzylaminopurine enhances waterlogging and shading tolerance after anthesis by improving grain starch accumulation and grain filling. Front Plant Sci 13:1003920

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao BQ, Zhou YL, Jiao XM, Wang X, Wang BS, Yuan F (2022) Bracelet salt glands of the recretohalophyte Limonium bicolor: distribution, morphology, and induction. J Integr Plant Biol 65(4):950–966

    Article  Google Scholar 

  • Zhou ZJ, An LJ, Sun LL, Zhu SJ, Xi WY, Broun P, Yu H, Gan Y (2011) Zinc finger protein5 is required for the control of trichome initiation by acting upstream of zinc finger protein8 in Arabidopsis. Plant Physiol 157(2):673–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou ZJ, An LJ, Sun LL, Gan YB (2012) ZFP5 encodes a functionally equivalent GIS protein to control trichome initiation. Plant Signal Behav 7(1):28–30

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou ZJ, Sun LL, Zhao YQ, An LJ, Yan A, Meng XF, Gan YB (2013) Zinc Finger Protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytol 198(3):699–708

    Article  CAS  PubMed  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 H, Leng BY, Gao YR, Wang BS, Yuan F (2023) The MYB transcription factor LbCPC of Limonium bicolor negatively regulates salt gland development and salt tolerance. Environ Exp Bot 209:105310

    Article  CAS  Google Scholar 

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Funding

This work was supported by the NSFC (National Natural Science Research Foundation of China, Project No. 32170281) and the Agricultural Variety Improvement Project of Shandong Province (2022LZGC018).

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MC and HF designed the research, JL and FM performed the experiments. JL and FM wrote the paper with contributions from the other authors. AJ, XH, and QL analyzed the data. MC revised the paper. All authors read and approved the final manuscript.

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Correspondence to Hai Fan or Min Chen.

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Communicated by Chun-Hai Dong.

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Liu, J., Meng, F., Jiang, A. et al. Exogenous 6-BA enhances salt tolerance of Limonium bicolor by increasing the number of salt glands. Plant Cell Rep 43, 12 (2024). https://doi.org/10.1007/s00299-023-03104-8

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