Skip to main content
SpringerLink
Log in

Chloride homeostasis via enhanced salt ion secretion selectivity contributes to salt tolerance of recretohalophytic mangrove Avicennia marina

  • Research Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and Aims

Avicennia marina, a pioneer recretohalophyte mangrove species living in intertidal wetlands, has high salinity tolerance. To understand the mechanism of salt adaptability, the seedlings of A. marina were treated with different salinities. We hypothesized that A. marina would demonstrate adaptive mechanisms at both physiological and molecular levels to tolerate tidal salinity through ion selectivity and chloride homeostasis.

Methods

In this study, the combination of growth, chlorophyll fluorescence analysis, electron microscopy, electrophysiological and molecular approaches were employed to investigate the mechanism of salt adaptability of A. marina seedlings.

Results

400 mM NaCl promoted chloroplast development, and chlorophyll fluorescence Fv/Fm, Fv/Fo, and qP decreased with increasing NaCl concentration, while ETR remained stable. NaCl contributed to increased Na+ and Cl− content in roots, leaves and exudates of salt glands, while relative high Cl− was stored in the roots and more Na+ in the leaves. Flux measurements of Na+, Cl−, K+, H+, and NO3− in the leaf salt glands and the root tips treated with 0 and 400 mM NaCl indicated the presence of an ion selectivity that was suppressed by specific Na+/H+ antiporter inhibitor amiloride, PM H+-ATPase inhibitor vanadate, and Na+:K+:2Cl− cotransporter inhibitor bumetanide. Further analysis showed that the expressions of chloride transport-related homolog genes CLCc, CLCf, and CCC1 were significantly up-regulated, whereas CLCd was down-regulated under salt treatment.

Conclusions

In conclusion, the chloride homeostasis regulated by salt ion secretion selectivity and transport-associated genes in leaf and root serves a crucial role in the salt tolerance of A. marina.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Aharonovitz O, Kapus A, Szászi K, Coady-Osberg N, Jancelewicz T, Orlowski J, Grinstein S (2001) Modulation of Na+/H+ exchange activity by Cl−. Am J Physiol Cell Physiol 281:C133–C141

    Article  CAS  PubMed  Google Scholar 

  • Al-Yassin A (2004) Influence of salinity on citrus: A review paper. J Central Eur Agric 5:263–272

    Google Scholar 

  • Apse MP, Blumwald E (2007) Na+ transport in plants. FEBS Lett 581:2247–2254

    Article  CAS  PubMed  Google Scholar 

  • Ball MC, Critchley C (1982) Photosynthetic responses to irradiance by the grey mangrove, Avicennia marina, grown under different light regimes. Plant Physiol 70:1101–1106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barhoumi Z, Atia A, Hussain AA, Maatallah M, Alalmaie A, Alaskri KI, Assiri AM (2023) Effects of salinity and iron deficiency on growth and physiological attributes of Avicennia marina (Forssk.) Vierh. Arch Agron Soil Sci 69:2753–2766

    Article  CAS  Google Scholar 

  • Belkhodja R, Morales F, Abadia A, Gomez-Aparisi J, Abadia J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiol 104:667–673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry WL (1970) Characteristics of salts secreted by Tamarix aphylla. Am J Bot 57:1226–1230

    Article  CAS  Google Scholar 

  • Beyenbach KW, Wieczorek H (2006) The V-type H+ ATPase: Molecular structure and function, physiological roles and regulation. J Exp Biol 209:577–589

    Article  CAS  PubMed  Google Scholar 

  • Biber PD (2006) Measuring the effects of salinity stress in the red mangrove, Rhizophora mangle L. Afr J Agric Res 1:1–4

    Google Scholar 

  • Botella M, Martinez V, Pardines J, Cerda A (1997) Salinity induced potassium deficiency in maize plants. J Plant Physiol 150:200–205

    Article  CAS  Google Scholar 

  • Byrt CS, Platten JD, Spielmeyer W, James RA, Lagudah ES, Dennis ES, Tester M, Munns R (2007) HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143:1918–1928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cattle M (1935) The estimation of small amounts of chloride in plant tissues. New Phytol 34:151–154

    Article  CAS  Google Scholar 

  • Chen J, Shen ZJ, Lu WZ, Liu X, Wu FH, Gao GF, Liu YL, Wu CS, Yan CL, Fan HQ, Zheng H-L (2017) Leaf miner-induced morphological, physiological and molecular changes in mangrove plant Avicennia marina (Forsk.) Vierh. Tree Physiol 37:82–97

    CAS  PubMed  Google Scholar 

  • Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H-L (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H+-ATPase and Na+/H+ antiporter under high salinity. Tree Physiol 30:1570–1585

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Xiong DY, Wang WH, Hu WJ, Simon M, Xiao Q, Liu TW, Liu X, Zheng H-L (2013) Nitric oxide mediates root K+/Na+ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+ antiporter under high salinity. PLoS ONE 8:e71543

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi BJ, Guo ZJ, Wei MY, Song SW, Zhong YH, Liu JW, Zhang YC, Li J, Xu CQ, Zhu XY, Zheng H-L (2023) Structural, developmental and functional analyses of leaf salt glands of mangrove recretohalophyte Aegiceras corniculatum. Tree Physiology 43. https://doi.org/10.1093/treephys/tpad123.

  • Christian R (2005) Interactive effects of salinity and irradiance on photoprotection in acclimated seedlings of two sympatric mangroves. Trees 19:596–606

    Article  CAS  Google Scholar 

  • Colmenero-Flores JM, Martínez G, Gamba G, Vázquez N, Iglesias DJ, Brumós J, Talón M (2007) Identification and functional characterization of cation–chloride cotransporters in plants. Plant J 50:278–292

    Article  CAS  PubMed  Google Scholar 

  • Dai J, Duan L, Dong H (2015) Comparative effect of nitrogen forms on nitrogen uptake and cotton growth under salinity stress. J Plant Nutr 38:1530–1543

    Article  CAS  Google Scholar 

  • Darvishzadeh R, Alavi SR, Sarafi A (2011) Genetic variability for chlorine concentration in oriental tobacco genotypes. Arch Agron Soil Sci 57:167–177

    Article  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flowers T, Troke P, Yeo A (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28:89–121

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  PubMed  Google Scholar 

  • Gaymard F, Pilot G, Lacombe B, Bouchez D, Sentenac H (1998) Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94:647–655

    Article  CAS  PubMed  Google Scholar 

  • Gimeno V, Syvertsen JP, Nieves M, Simón I, Martínez V, García-Sánchez F (2009) Additional nitrogen fertilization affects salt tolerance of lemon trees on different rootstocks. Sci Horticult 121:305

    Article  Google Scholar 

  • Gorham J (1995) Mechanism of salt tolerance of halophytes. In: Choukr-Allah R, Malcolm CV, Hamdy A (eds) Halophytes and Biosaline Agriculture. Marcel Dekker, New York, pp 207–223

    Google Scholar 

  • Grieve CM, Grattan SR, Maas EV (2012) Plant salt tolerance. ASCE Manual Reports Eng Pract 71:405–459

    Google Scholar 

  • Grigore M-N, Toma C (2021) Morphological and anatomical adaptations of halophytes: A review. In: Grigore MN (ed) Handbook of Halophytes: From Molecules to Ecosystems towards Biosaline Agriculture. Springer, Berlin, pp 1079–1221

    Chapter  Google Scholar 

  • Guo W, Zuo Z, Cheng X, Sun J, Li H, Li L, Qiu JL (2014) The chloride channel family gene CLCd negatively regulates pathogen-associated molecular pattern (PAMP)-triggered immunity in Arabidopsis. J Exp Bot 65:1205–1215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Z, Wei MY, Zhong YH, Wu X, Chi BJ, Li J, Li H, Zhang LD, Wang XX, Zhu XY, Zheng H-L (2023) Leaf sodium homeostasis controlled by salt gland is associated with salt tolerance in mangrove plant Avicennia marina. Tree Physiol 43:817–831

    Article  CAS  PubMed  Google Scholar 

  • Hafeez MB, Raza A, Zahra N, Shaukat K, Akram MZ, Iqbal S, Basra SMA (2021) Gene regulation in halophytes in conferring salt tolerance. Handbook of Bioremediation. Academic Press, Cambridge, pp 341–370

    Chapter  Google Scholar 

  • Heibert T, Steinkamp T, Hinnah S, Schwarz M, Flueggel UI, Weber A, Wagner R (1995) Ion channels in the chloroplast envelope membrane. Biochemistry 34:15906–15917

    Article  CAS  Google Scholar 

  • Henderson SW, Wege S, Qiu J, Blackmore DH, Walker AR, Tyerman SD, Walker RR, Gilliham M (2015) Grapevine and Arabidopsis cation-chloride cotransporters localize to the Golgi and trans-Golgi network and indirectly influence long-distance ion transport and plant salt tolerance. Plant Physiol 169:2215–2229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horie T, Hauser F, Schroeder JI (2009) HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends Plant Sci 14:668

    Article  Google Scholar 

  • Horie T, Schroeder JI (2004) Sodium transporters in plants: Diverse genes and physiological functions. Plant Physiol 136:2457–2462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua BG, Mercier RW, Leng Q, Berkowitz GA (2003) Plants do it differently: A new basis for potassium/sodium selectivity in the pore of an ion channel. Plant Physiol 132:1353–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jossier M, Kroniewicz L, Dalmas F, Le Thiec D, Ephritikhine G, Thomine S, Barbier-Brygoo H, Vavasseur A, Filleur S, Leonhardt N (2010) The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant J 64:563–576

    Article  CAS  PubMed  Google Scholar 

  • Kong L, Sun M, Wang F, Liu J, Feng B, Si J, Zhang B, Li S, Li H (2014) Effects of high NH4+ on K+ uptake, culm mechanical strength and grain filling in wheat. Front Plant Sci 5:703

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong X, Luo Z, Dong H, Eneji AE, Li W (2012) Effects of non-uniform root zone salinity on water use, Na+ recirculation, and Na+ and H+ flux in cotton. J Exp Bot 63:2105–2116

    Article  CAS  PubMed  Google Scholar 

  • Kuo J (2014) Processing plant tissues for ultrastructural study. In: Kuo J (ed) Methods in Molecular Biology. Humana Press, Totowa, pp 39–55

    Google Scholar 

  • Li G, Cai W, Wu Y, Liu D, Zhang Z, Huang J (1987) The relationship between structural status and photochemical activity of chloroplasts. Acta Phytophysiol Sin 3:295–301

    Google Scholar 

  • Li N, Chen S, Zhou X, Li C, Shao J, Wang R, Fritz E, Hüttermann A, Polle A (2008) Effect of NaCl on photosynthesis, salt accumulation and ion compartmentation in two mangrove species, Kandelia candel and Bruguiera gymnorhiza. Aquat Bot 88:303–310

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu CX, Yuan F, Guo JR, Han GL, Wang CF, Chen M, Wang BS (2021) Current understanding of role of vesicular transport in salt secretion by salt glands in recretohalophytes. Int J Mol Sci 22:2203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubitz W, Chrysina M, Cox N (2019) Water oxidation in photosystem II. Photosynth Res 142:105–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lyu H, He Z, Wu CI, Shi S (2018) Convergent adaptive evolution in marginal environments: Unloading transposable elements as a common strategy among mangrove genomes. New Phytol 217:428–438

    Article  CAS  PubMed  Google Scholar 

  • Maser P, Gierth M, Schroeder JI (2002) Molecular mechanisms of potassium and sodium uptake in plants. Plant Soil 247:43–54

    Article  Google Scholar 

  • Mason MJ, Smith JD, Garcia-Soto JJ, Grinstein S (1989) Internal pH-sensitive site couples Cl-(-)HCO3- exchange to Na+-H+ antiport in lymphocytes. Am J Physiol Cell Physiol 256:C428–C433

    Article  CAS  Google Scholar 

  • Michelet B, Boutry M (1995) The Plasma Membrane H+-ATPase (a highly regulated enzyme with multiple physiological functions). Plant Physiol 108:1–6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Naidoo G (2006) Factors contributing to dwarfing in the mangrove Avicennia marina. Ann Bot 97:1095–1101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Natarajan P, Murugesan AK, Govindan G, Gopalakrishnan A, Kumar R, Duraisamy P, Balaji R, Tanuja SPS, Parida AK, Parani M (2021) A reference-grade genome identifies salt-tolerance genes from the salt-secreting mangrove species Avicennia marina. Commun Biol 4:851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen HT, Meir P, Sack L, Evans JR, Oliveira RS, Ball MC (2017) Leaf water storage increases with salinity and aridity in the mangrove Avicennia marina: Integration of leaf structure, osmotic adjustment and access to multiple water sources. Plant Cell Environ 40:1576–1591

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB, Sanada Y, Mohanty P (2004) Effects of salinity on biochemical components of the mangrove, Aegiceras corniculatum. Aquat Bot 80:77–87

    Article  CAS  Google Scholar 

  • Parida AK, Jha B (2010) Salt tolerance mechanisms in mangroves: A review. Trees 24:199–217

    Article  Google Scholar 

  • Parker JC (1983) Passive calcium movements in dog red blood cells: anion effects. Am J Physiol Cell Physiol 244:C318–C323

    Article  CAS  Google Scholar 

  • Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R (2009) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proc Nat Acad Sci U S A 106:5019–5024

    Article  ADS  CAS  Google Scholar 

  • Rodríguez-Navarro A, Rubio F (2006) High-affinity potassium and sodium transport systems in plants. J Exp Bot 57:1149–1160

    Article  PubMed  Google Scholar 

  • Rozema J, Flowers T (2008) Crops for a salinized world. Science 322:1478–1480

    Article  CAS  PubMed  Google Scholar 

  • Rozema J, Gude H, Pollak G (1981) An ecophysiological study of the salt secretion of four halophytes. New Phytol 89:201–217

    Article  CAS  Google Scholar 

  • Schönknecht G, Hedrich R, Junge W, Raschke K (1988) A voltage-dependent chloride channel in the photosynthetic membrane of a higher plant. Nature 336:589–592

    Article  ADS  Google Scholar 

  • Shahid MA, Sarkhosh A, Khan N, Balal RM, Ali S, Rossi L, Gómez C, Mattson N, Nasim W, Garcia-Sanchez F (2020) Insights into the physiological and biochemical impacts of salt stress on plant growth and development. Agronomy 10:938

    Article  CAS  Google Scholar 

  • Shi H, Lee B-h, Wu S-J, Zhu J-K (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21:81–85

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Chen M, Feng G, Jia Y, Wang B, Zhang F (2009) Effect of salinity on growth, ion accumulation and the roles of ions in osmotic adjustment of two populations of Suaeda salsa. Plant Soil 314:133–141

    Article  CAS  Google Scholar 

  • Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z (2008) NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol 149:1141–1153

    Article  PubMed  Google Scholar 

  • Terry N (1977) Photosynthesis, growth, and the role of chloride. Plant Physiol 60:69–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomson WW (1975) The Structure and Function of Salt Glands. In: Polijakoff-Mayber A, Gale J (eds) Plants in Saline Environments. Springer, Berlin, pp 118–146

    Chapter  Google Scholar 

  • Volkov V, Amtmann A (2006) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, has specific root ion-channel features supporting K+/Na+ homeostasis under salinity stress. Plant Cell Environ 27:1–14

    Article  Google Scholar 

  • Waisel Y, Eshel A, Agami M (1986) Salt balance of leaves of the mangrove Avicennia marina. Physiol Plant 67:67–72

    Article  CAS  Google Scholar 

  • Wei MY, Li H, Zhang LD, Guo ZJ, Liu JY, Ding QS, Zhong YH, Li J, Ma DN, Zheng HL (2022) Exogenous hydrogen sulfide mediates Na+ and K+ fluxes of salt gland in salt-secreting mangrove plant Avicennia marina. Tree Physiol 42:1812–1826

    Article  CAS  PubMed  Google Scholar 

  • Wei Q, Liu Y, Zhou G, Li Q, Yang C, Peng SA (2013) Overexpression of CsCLCc, a chloride channel gene from Poncirus trifoliata, enhances salt tolerance in Arabidopsis. Plant Mol Biol Report 31:1548–1557

    Article  CAS  Google Scholar 

  • Werner A, Stelzer R (1990) Physiological responses of the mangrove Rhizophora mangle grown in the absence and presence of NaCl. Plant Cell Environ 13:243–255

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2001) Chloride in soils and its uptake and movement within the plant: A review. Ann Bot 88:967–988

    Article  CAS  Google Scholar 

  • Yan S, McLamore ES, Dong S, Gao H, Taguchi M, Wang N, Zhang T, Su X, Shen Y (2015) The role of plasma membrane H+-ATP ase in jasmonate-induced ion fluxes and stomatal closure in Arabidopsis thaliana. Plant J 83:638–649

    Article  CAS  PubMed  Google Scholar 

  • Yuan F, Wang B (2020) Adaptation of recretohalophytes to salinity. In: Grigore MN (ed) Handbook of Halophytes, From Molecules to Ecosystems towards Biosaline Agriculture. Springer, Cham, pp 1–21

    Google Scholar 

  • Zhang C, Meng S, Li Y, Zhao Z (2014) Net NH4+ and NO3− fluxes, and expression of NH4+ and NO3− transporter genes in roots of Populus simonii after acclimation to moderate salinity. Trees 28:1813–1821

    Article  CAS  Google Scholar 

  • Zhang J, Jiang C, Ping J (2008) Research advances about the effect of salt stress on photosynthesis of plant. J Agric Sci 29:74–80

    CAS  Google Scholar 

  • Zhang JL, Flowers TJ, Wang SM (2010) Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326:45–60

    Article  CAS  Google Scholar 

  • Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zhu XG (1999) Advances in the research on the effects of NaCl on photosynthesis. Chin Bull Botany 16:332

    ADS  Google Scholar 

  • Zhu Z, Zhang R, Liu T, Zheng H-L (2011) Solute accumulation and osmotic adjustment characteristics of the mangrove Avicennia marina under NaCl-induced salinity stress. Bot Mar 54:335–341

    Article  CAS  Google Scholar 

  • Zifarelli G, Pusch M (2010) CLC transport proteins in plants. FEBS Lett 584:2122–2127

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was financially supported by the Natural Science Foundation of China (NSFC) (32171740, 31870581, 31570586) and the National Key Research and Development Program of China (2017YFC0506102).

Author information

Author notes

  1. Qian-Su Ding and Chao-Qun Xu contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of the Ministry of Education for Coastal and Wetland Ecosystems, College of the Environment and Ecology, Xiamen University, Xiamen, Fujian, 361002, China

    Qian-Su Ding, Chao-Qun Xu, Dong-Na Ma, Ming-Yue Wei, Chang-Hao Gao, Shan Zhang, Huan Li, Xue-Yi Zhu & Hai-Lei Zheng

  2. Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN, 55108, USA

    Qian-Su Ding

  3. National Engineering Research Center for Cereal Fermentation and Food Biomanufacturing, State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu, 214122, China

    Dong-Na Ma

  4. School of Ecology, Resources and Environment, Dezhou University, Dezhou, Shandong, 253000, China

    Ming-Yue Wei

  5. College of Food and Bio-Engineering, Bengbu University, Bengbu, Anhui, 233030, China

    Huan Li

Authors
  1. Qian-Su Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao-Qun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dong-Na Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ming-Yue Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chang-Hao Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Huan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xue-Yi Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hai-Lei Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.-Q.S., Z.-X.Y. and Z.-H.L. designed the experiments. D.-Q.S., X.-C.Q., D,-N.M. and W.-M.Y. performed the experiments and analyzed the data. D.-Q.S. wrote the paper. G.-C.H., X.-C.Q., Z.S., and L.H. gave the suggestions. D.-Q.S. and Z.-H.L. revised this paper. All authors have read and approved the manuscript.

Corresponding author

Correspondence to Hai-Lei Zheng.

Ethics declarations

Conflict of Interest

The authors declare no conflicts of interest.

Additional information

Responsible Editor: Vadim Volkov.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 13 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ding, QS., Xu, CQ., Ma, DN. et al. Chloride homeostasis via enhanced salt ion secretion selectivity contributes to salt tolerance of recretohalophytic mangrove Avicennia marina. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06619-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11104-024-06619-5

Keywords

Search

Navigation