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Quercus dentata responds to Na2CO3 stress with salt crystal deposits: ultrastructure, and physiological–biochemical parameters of leaves

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Our study elucidated that Q. dentata responds to Na2CO3 stress by excreting salt on the blade, accumulating osmotic protectants, and changing the cell ultrastructure and physiological-biochemical parameters of leaves.

Abstract

Quercus dentata Thunb is an important constructive species in the forest communities of the mountainous areas of northern China with high ecological and landscape value. However, soil salinization prevents the use of Q. dentata in the North China Plain. Therefore, it is necessary to explore how Q. dentata responds to saline-alkaline stress. Here, Q. dentata seedlings were exposed to different concentrations of an alkaline salt (Na2CO3) to determine the effects on leaf mesophyll cell ultrastructure and physiological-biochemical parameters. We first discovered crystallized deposits on the pressure side of Q. dentata leaf blades after the 100 mM Na2CO3 treatment. Scanning electron microscopy and energy-dispersive X-ray analysis revealed that the main component of the crystal deposits was sodium ions. However, no salt glands or bladders were detected in Q. dentata leaves. Moreover, the ultrastructure of the mesophyll cells changed as stress duration increased, and the number and size of the chloroplasts were limited by partial disintegration. The results also show that Na2CO3-stressed Q. dentata plants displayed increased soluble sugar and proline contents. Additionally, the low-concentration Na2CO3 stress slightly enhanced the activity of antioxidant enzymes, such as catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD). In summary, the results show that the cell structure of Q. dentata leaves was damaged by Na2CO3 stress. However, accumulating osmoprotectants and the excretion of salt onto the leaf blades enhanced saline-alkaline stress tolerance.

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Data availability

Data in this study are available from the corresponding authors upon reasonable request.

References

  • Al-Harrasi A, Rehman NU, Khan AL, Al-Broumi M, Al-Amri I, Hussain J, Hussain H, Csuk R (2018) Chemical, molecular and structural studies of Boswellia species: β-Boswellic Aldehyde and 3-epi-11β-dihydroxy BA as precursors in biosynthesis of boswellic acids. PLoS ONE 13:e0198666

    PubMed  PubMed Central  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    CAS  Google Scholar 

  • Beyer WF Jr, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    CAS  PubMed  Google Scholar 

  • Bolwell GP, Bindschedler LV, Blee KA, Butt VS, Davies DR, Gardner SL, Gerrish C, Minibayeva F (2002) The apoplastic oxidative burst in response to biotic stress in plants: a three-component system. J Exp Bot 53:1367–1376

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Cao L, Weinan C, Zenghui H, Pingsheng L (2018) Effect of saline-alkaline stress on the growth and photosynthetic characteristics of Quercus dentata seedlings. J Beijing Agric Coll 33:86–90

    Google Scholar 

  • Chuamnakthong S, Nampei M, Ueda A (2019) Characterization of Na(+) exclusion mechanism in rice under saline-alkaline stress conditions. Plant Sci 287:110171

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Denk T, Grimm GW, Manos PS, Deng M, Hipp AL (2017) An updated infrageneric classification of the oaks: review of previous taxonomic schemes and synthesis of evolutionary patterns. In: Gil-Pelegrín E, Peguero-Pina JJ, Sancho-Knapik D (eds) Oaks physiological ecology exploring the functional diversity of genus quercus L. Cham: Springer International Publishing 13–38

    Google Scholar 

  • Fuglsang AT, Guo Y, Cuin TA, Qiu Q, Song C, Kristiansen KA, Bych K, Schulz A, Shabala S, Schumaker KS, Palmgren MG, Zhu JK (2007) Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14-3-3 protein. Plant Cell 19:1617–1634

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo R, Shi L, Ding X, Hu Y, Tian S, Yan D, Shao S, Gao Y, Liu R, Yang Y (2010) Effects of saline and alkaline stress on germination, seedling growth, and ion balance in wheat. Agron J 102:1252–1260

    CAS  Google Scholar 

  • Guo R, Shi L, Yan C, Zhong X, Gu F, Liu Q, Xia X, Li H (2017) Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol 17:41

    PubMed  PubMed Central  Google Scholar 

  • Hartung W, Leport L, Ratcliffe RG, Sauter A, Duda R, Turner NC (2002) Abscisic acid concentration, root pH and anatomy do not explain growth differences of chickpea (Cicer arietinum L.) and lupin (Lupinus angustifolius L.) on acid and alkaline soils. Plant Soil 240:191–199

    CAS  Google Scholar 

  • Hasanuzzaman M, Davies NW, Shabala L, Zhou M, Brodribb TJ, Shabala S (2017) Residual transpiration as a component of salinity stress tolerance mechanism: a case study for barley. BMC Plant Biol 17:107

    PubMed  PubMed Central  Google Scholar 

  • He J, Chen F, Chen S, Lv G, Deng Y, Fang W, Liu Z, Guan Z, He C (2011) Chrysanthemum leaf epidermal surface morphology and antioxidant and defense enzyme activity in response to aphid infestation. J Plant Physiol 168:687–693

    CAS  PubMed  Google Scholar 

  • Irigoyen JJ, Einerich DW, Sánchez-Díaz M (1992) Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativd) plants. Physiol Plant 84:55–60

    CAS  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594

    CAS  PubMed  Google Scholar 

  • Kim KW, Koo K, Kim PG (2011) Seawater spray injury to Quercus acutissima leaves: crystal deposition, stomatal clogging, and chloroplast degeneration. Microsc Res Tech 74:449–456

    CAS  PubMed  Google Scholar 

  • Kosma DK, Murmu J, Razeq FM, Santos P, Bourgault R, Molina I, Rowland O (2014) AtMYB41 activates ectopic suberin synthesis and assembly in multiple plant species and cell types. Plant J 80:216–229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kotula L, Clode PL, Jimenez JC, Colmer TD (2019) Salinity tolerance in chickpea is associated with the ability to ‘exclude’ Na from leaf mesophyll cells. J Exp Bot 70:4991–5002

    CAS  PubMed  PubMed Central  Google Scholar 

  • Labidi N, Ammari M, Mssedi D, Benzerti M, Snoussi S, Abdelly C (2010) Salt excretion in Suaeda fruticosa. Acta Biol Hung 61:299–312

    PubMed  Google Scholar 

  • Li Z, Zhang WH (2013) Growth and physiological response of Quercus variabilis seedlings under NaCl stress. Acta Botan Boreali-Occiden Sin 33:1630–1637

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • More P, Agarwal P, Joshi PS, Agarwal PK (2019) The JcWRKY tobacco transgenics showed improved photosynthetic efficiency and wax accumulation during salinity. Sci Rep 9:19617

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Munns R, James RA, Gilliham M, Flowers TJ, Colmer TD (2016) Tissue tolerance: an essential but elusive trait for salt-tolerant crops. Funct Plant Biol FPB 43:1103–1113

    CAS  PubMed  Google Scholar 

  • Natali L, Vangelisti A, Guidi L, Remorini D, Cotrozzi L, Lorenzini G, Nali C, Pellegrini E, Trivellini A, Vernieri P, Landi M, Cavallini A, Giordani T (2018) How Quercus ilex L. saplings face combined salt and ozone stress: a transcriptome analysis. BMC Genom 19:872

    CAS  Google Scholar 

  • Niu M, Xie J, Chen C, Cao H, Sun J, Kong Q, Shabala S, Shabala L, Huang Y, Bie Z (2018) An early ABA-induced stomatal closure, Na+ sequestration in leaf vein and K+ retention in mesophyll confer salt tissue tolerance in Cucurbita species. J Exp Bot 69:4945–4960

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pankova E, Vorobieva L, Balyuk S, Khasankhanova G, Konyushkova M, Yamnova I. (2018) Salt-affected soils of the Eurasian region: diagnostics, criteria and distribution. Handbook for saline soil management 3–15

  • Paz RC, Rocco RA, Reinoso H, Menéndez AB, Pieckenstain FL, Ruiz OA (2012) Comparative study of alkaline, saline, and mixed saline-alkaline stresses with regard to their effects on growth, nutrient accumulation, and root morphology of Lotus tenuis. J Plant Growth Regul 31:448–459

    CAS  Google Scholar 

  • Reinoso H, Sosa L, Ramírez L, Luna V (2004) Salt-induced changes in the vegetative anatomy of Prosopis strombulifera (Leguminosae). Can J Bot 82:618–628

    Google Scholar 

  • Santos J, Al-Azzawi M, Aronson J, Flowers TJ (2016) eHALOPH a database of salt-tolerant plants: helping put halophytes to work. Plant Cell Physiol 57:e10

    PubMed  Google Scholar 

  • Shen Q, Yu J, Fu L, Wu L, Dai F, Jiang L, Wu D, Zhang G (2018) Ionomic, metabolomic and proteomic analyses reveal molecular mechanisms of root adaption to salt stress in tibetan wild barley. Plant Physiol Biochem 123:319–330

    CAS  PubMed  Google Scholar 

  • Suo J, Zhang H, Zhao Q, Zhang N, Zhang Y, Li Y, Song B, Yu J, Cao J, Wang T, Luo J, Guo L, Ma J, Zhang X, She Y, Peng L, Ma W, Guo S, Miao Y, Chen S, Qin Z, Dai S (2020) Na(2)CO(3)-responsive photosynthetic and ROS scavenging mechanisms in chloroplasts of alkaligrass revealed by phosphoproteomics. Genom Proteom Bioinform 18:271–288

    Google Scholar 

  • van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433

    PubMed  Google Scholar 

  • Xu W, Jia L, Baluška F, Ding G, Shi W, Ye N, Zhang J (2012) PIN2 is required for the adaptation of Arabidopsis roots to alkaline stress by modulating proton secretion. J Exp Bot 63:6105–6114

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276

    CAS  Google Scholar 

  • Yang C, Shi D, Wang D (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regul 56:179–190

    CAS  Google Scholar 

  • Yang Y, Qin Y, Xie C, Zhao F, Zhao J, Liu D, Chen S, Fuglsang AT, Palmgren MG, Schumaker KS, Deng XW, Guo Y (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22:1313–1332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: How do plants secrete salt? Front Plant Sci 7:977

    PubMed  PubMed Central  Google Scholar 

  • Zhang CL, Hu X, Zhang YL, Liu Y, Wang GL, You CX, Li YY, Hao YJ (2020) An apple long-chain acyl-CoA synthetase 2 gene enhances plant resistance to abiotic stress by regulating the accumulation of cuticular wax. Tree Physiol 40:1450–1465

    CAS  PubMed  Google Scholar 

  • Zhao Q, Suo J, Chen S, Jin Y, Ma X, Yin Z, Zhang Y, Wang T, Luo J, Jin W, Zhang X, Zhou Z, Dai S (2016) Na2CO3-responsive mechanisms in halophyte Puccinellia tenuiflora roots revealed by physiological and proteomic analyses. Sci Rep 6:32717

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was supported by the Innovative Transdisciplinary Program of Ecological Restoration Engineering under Beijing Municipal Education Commission (IDHT20190509), Scientific Research Project of Beijing Educational Committee (SQKM20181002015), and the grant for Beijing Forestry University Outstanding Postgraduate Mentoring Team Building (YJSY-DSTD2022005). We thank Editorbar Language Editing for editing the English text of a draft of this manuscript.

Funding

Beijing Forestry University Outstanding Postgraduate Mentoring Team Building, YJSY-DSTD2022005, Cunfu Lu, Innovative Transdisciplinary Program of Ecological Restoration Engineering under Beijing Municipal Education Commission,IDHT20190509, Scientific Research Project of Beijing Educational Committee, SQKM20181002015.

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Authors and Affiliations

  1. College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China

    Wen-Bo Wang & Cunfu Lu

  2. Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, China

    Wen-Bo Wang, Lei Cao, Weinan Chen, Zenghui Hu & Pingsheng Leng

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  1. Wen-Bo Wang
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Contributions

PSL, CFL, and ZHH conceived and designed the study; WBW, LC, and WNC prepared the materials, conducted the experiments, WBW analyzed the data and prepared the results; WBW wrote the manuscript; PSL, ZHH, and CFL edited and improved the manuscript; all authors read and approved the final manuscript.

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Correspondence to Cunfu Lu, Zenghui Hu or Pingsheng Leng.

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Communicated by Jinxing Lin.

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Wang, WB., Cao, L., Chen, W. et al. Quercus dentata responds to Na2CO3 stress with salt crystal deposits: ultrastructure, and physiological–biochemical parameters of leaves. Trees 37, 1001–1011 (2023). https://doi.org/10.1007/s00468-023-02400-w

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