Skip to main content
SpringerLink
Log in

Effects of alkali stress on dry matter accumulation, root morphology, ion balance, free polyamines, and organic acids of sugar beet

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Sugar beet is strongly resistant to salt-alkalinity. Understanding the physiological alkali stress resistance mechanism of sugar beet is important for fully utilizing saline–alkaline soil. Sugar beet seedlings from cultivars KWS0143 (alkali-tolerant) and Beta464 (alkali-sensitive) were treated with five concentrations of mixed alkaline solutions (NaHCO3: Na2CO3, 2:1), namely, 0 (control), 25, 50, 75, and 100 mM (mole concentration was calculated in Na+). A sharper decrease in dry weight per plant (87.1%) and total root length (91.7%) of Beta464 were observed compared to the 61.5% and 85.0% decrease in those of KWS0143 under 100 mM alkali treatment. With increasing alkaline stress, Na+ accumulation hindered K+ and Ca2+ absorption by roots. Free polyamines contents and phosphoenolpyruvate carboxylase (PEPC) activity in roots of both cultivars were all significantly enhanced by 50 and 75 mM alkali treatments. KWS0143 exhibited higher dissociated putrescine (Put), spermine (Spm), as well as spermidine (Spd) levels within the roots compared to Beta464 under alkali conditions. Root free Spd contents of KWS0143 and Beta464 increased by 154.2 and 64.5% treated with 50 mM alkali in comparison with the control. After treated with the dose of 25 mM, root succinic acid (SA) contents of KWS0143 and Beta464 increased by 90.4 and 14.3%, respectively, compared to the plants subjected to the control. Our results imply that polyamines and PEPC contribute to the tolerance of sugar beet to alkali stress. Those results could be useful for enriching the theory of plant stress response.

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

Similar content being viewed by others

References

  • Alzahrani SM, Alaraidh IA, Migdadi H, Alghamdi S, Altaf Khan M, Ahmad P (2019) Physiological, biochemical, and antioxidant properties of two genotypes of Vicia faba grown under salinity stress. Pak J Bot. https://doi.org/10.30848/pjb2019-3(3)

    Article  Google Scholar 

  • An LZ et al (2004) Effect of enhanced UV-B radiation on polyamine content and membrane permeability in cucumber leaves Russian. J Plant Physiol 51:658–662. https://doi.org/10.1023/b:rupp.0000040753.29607.58

    Article  CAS  Google Scholar 

  • An YM, Song LL, Liu YR, Shu YJ, Guo CH (2016) De Novo Transcriptional Analysis of Alfalfa in Response to Saline-Alkaline Stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00931

    Article  PubMed  PubMed Central  Google Scholar 

  • Aziz A, Larher F (1995) Changes in polyamine titers associated with the proline response and osmotic adjustment of rape leaf discs submitted to osmotic stresses. Plant Sci 112:175–186

    Article  CAS  Google Scholar 

  • Azooz MM, Metwally A, Abou-Elhamd MF (2015) Jasmonate-induced tolerance of Hassawi okra seedlings to salinity in brackish water. Acta Physiol Plant 37:1–13

    Article  CAS  Google Scholar 

  • Bai L, Wang C, Zang S, Zhang Y, Hao Q, Wu Y (2016) Remote sensing of soil alkalinity and salinity in the Wuyu’er-Shuangyang river Basin. Northeast China Remote Sens 8:163

    Article  Google Scholar 

  • Baron K, Stasolla C (2008) The role of polyamines during in vivo and in vitro development. In Vitro Cell Dev Biol Plant 44:384–395

    Article  CAS  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bueno M, Cordovilla M-P (2019) Polyamines in halophytes. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00439

    Article  PubMed  PubMed Central  Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen SS, Xing JJ, Lan HY (2012) Comparative effects of neutral salt and alkaline salt stress on seed germination, early seedling growth and physiological response of a halophyte species Chenopodium glaucum. Afr J Biotechnol 11(40):9572–9581

    CAS  Google Scholar 

  • Chen W et al (2009) Comparative effects of salt and alkali stresses on organic acid accumulation and ionic balance of seabuckthorn (Hippophae rhamnoides L.). Ind Crops Prod 30:351–358. https://doi.org/10.1016/j.indcrop.2009.06.007

    Article  CAS  Google Scholar 

  • Chen YT, Cai-Feng LI, Zhao LY, Peng Y, Wang YY, Teng XY (2010) Screening of Salinity Tolerance And Response Of Seedling To Salt Stress In Sugar Beet (Beta vulgaris L.). Plant Physiol Commun 46:1121–1128

    Google Scholar 

  • Eshghiizadeh HR, Kafi M, Nezami A, Khoshgoftarmanesh A (2012) Studies on the role of root morphology attribution in salt tolerance of blue-panicgrass (Panicum antidotale Retz) using artificial neural networks (ANN). Res Crops 13:534–544

    Google Scholar 

  • Fu HJ, Yu HY, Li TX, Wu Y (2019) Effect of cadmium stress on inorganic and organic components in xylem sap of high cadmium accumulating rice line (Oryza sativa L.). Ecotox Environ Safe 168:330–337

    Article  CAS  Google Scholar 

  • Guo J, Li CF, Chen M, Xu Y, Ma FM (2015) Effects of Na2CO3 stress on the growth and antioxidant enzymes of beta vulgaris seedlings. Plant Physiol J 51:840–846

    CAS  Google Scholar 

  • Guo J, Li CF, Liu L, Sang LM, Wang YB (2016) Variation of rhizosphere environmental factors of sugarbeet seedlings under Na2CO3 stress and their correlation. Chin J Appl Ecol 27:904–910

    CAS  Google Scholar 

  • Guo R et al (2017) Ionomic and metabolic responses to neutral salt or alkaline salt stresses in maize (Zea mays L.) seedlings. BMC Plant Biol 17:41. https://doi.org/10.1186/s12870-017-0994-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hazman M, Hause B, Eiche E, Riemann M, Nick P (2016) Different forms of osmotic stress evoke qualitatively different responses in rice. J Plant Physiol 202:45–56

    Article  CAS  PubMed  Google Scholar 

  • Hossain MS, ElSayed AI, Moore M, Dietz KJ (2017) Redox and reactive oxygen species network in acclimation for salinity tolerance in sugar beet. J Exp Bot 68:1283–1298. https://doi.org/10.1093/jxb/erx019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jesus J, Castro F, Niemelä A, Borges MT, Danko AS (2015) Evaluation of the impact of different soil salinization processes on organic and mineral soils water. Air Soil Pollut 226:1–12

    Article  CAS  Google Scholar 

  • Jiang C-C, Fang Z-Z, Zhou D-R, Pan S-L, Ye X-F (2019) Changes in secondary metabolites, organic acids and soluble sugars during the development of plum fruit cv. ‘Furongli’ (Prunus salicina Lindl). J Sci Food Agric 99:1010–1019. https://doi.org/10.1002/jsfa.9265

    Article  CAS  PubMed  Google Scholar 

  • Latef AAA, Tran LSP (2016) Impacts of priming with silicon on the growth and tolerance of maize plants to alkaline stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00243

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H et al (2015) Salt stress response of membrane proteome of sugar beet monosomic addition line M14. J Proteomics 127:18–33. https://doi.org/10.1016/j.jprot.2015.03.025

    Article  CAS  PubMed  Google Scholar 

  • Li L et al (2018) Exogenously applied spermidine alleviates photosynthetic inhibition under drought stress in maize (Zea mays L.) seedlings associated with changes in endogenous polyamines and phytohormones. Plant Physiol Biochem 129:35–55. https://doi.org/10.1016/j.plaphy.2018.05.017

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Huang L, Zhang H, Wang M, Liang Z (2017) Assessment of ammonia volatilization losses and ntrogen utilization during the rice growing season in alkaline salt-affected soils. Sustainability 9:132. https://doi.org/10.3390/su9010132

    Article  CAS  Google Scholar 

  • Li Z, Yu J, Peng Y, Huang B (2016) Metabolic pathways regulated by abscisic acid, salicylic acid, and γ-aminobutyric acid in association with improved drought tolerance in creeping bentgrass (Agrostis stolonifera ). Physiol Plant. https://doi.org/10.1111/ppl.12483

    Article  PubMed  Google Scholar 

  • Liu D et al (2014) Effect of Zn toxicity on root morphology, ultrastructure, and the ability to accumulate Zn in Moso bamboo (Phyllostachys pubescens). Environ Sci Pollut Res Int 21:13615–13624. https://doi.org/10.1007/s11356-014-3271-3

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Shi D-C (2010) Photosynthesis, chlorophyll fluorescence, inorganic ion and organic acid accumulations of sunflower in responses to salt and salt-alkaline mixed stress. Photosynthetica 48:127–134. https://doi.org/10.1007/s11099-010-0017-4

    Article  CAS  Google Scholar 

  • Liu JH, Nakajima I, Moriguchi T (2011) Effects of salt and osmotic stresses on free polyamine content and expression of polyamine biosynthetic genes in Vitis vinifera. Biol Plant 55:340–344

    Article  CAS  Google Scholar 

  • Ma B et al (2015) Comparative assessment of sugar and malic acid composition in cultivated and wild apples. Food Chem 172:86–91. https://doi.org/10.1016/j.foodchem.2014.09.032

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Wang XP, Zhang SF, Shi DC, Sheng LX (2016) Effects of salt and alkali stress on growth, accumulation of oxalic acid, and activity of oxalic acid-metabolizing enzymes in Kochia sieversiana. Biol Plant 60:774–782. https://doi.org/10.1007/s10535-016-0650-2

    Article  CAS  Google Scholar 

  • Magaña C et al (2011) Direct prediction of bioethanol yield in sugar beet pulp using near infrared spectroscopy. Biores Technol 102:9542

    Article  Google Scholar 

  • Moschou P, Paschalidis K, Roubelakis-Angelakis K (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3:1061–1066. https://doi.org/10.4161/psb.3.12.7172

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1007/s00344-011-9254-4

    Article  CAS  Google Scholar 

  • Politycka B, Kubiś J (2000) Changes in free polyamine level and di- and polyamine oxidase activity in cucumber roots under allelochemical stress conditions. Acta Physiol Plant 22:11–16

    Article  CAS  Google Scholar 

  • Radi AA, Abdelwahab DA, Hamada AM (2012) Evaluation of some bean lines tolerance to alkaline soil. J Biol Earth Sci 2

  • Radić S, Prolić M, Pavlica M, Pevalek-Kozlina B (2005) Cytogenetic effects of osmotic stress on the root meristem cells of Centaurea ragusina L. Environ Exp Bot 54:213–218

    Article  Google Scholar 

  • Shafi M, Guoping Z, Bakht J, AmanKhan M, Islam UE, Khan MD, Raziuddin GZ (2010) Effect of cadmium and salinity stresses on root morphology of wheat. Pak J Bot 42:2747–2754

    CAS  Google Scholar 

  • Smith TA, Barker JH (1985) The DI- and polyamine oxidases of plants. Adv Exp Med Biol 13:319–322

    CAS  Google Scholar 

  • Tang W, Newton RJ (2005) Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine. Plant Growth Regul 46:31–43

    Article  CAS  Google Scholar 

  • Vastarelli P, Moschella A, Pacifico D, Mandolino G (2013) Water Stress in Beta vulgaris: Osmotic Adjustment Response and Gene Expression Analysis in ssp. Vulgaris and maritime. Am J Plant Sci 04:11–16

    Article  Google Scholar 

  • Witzel K et al (2018) Plasma membrane proteome analysis identifies a role of barley membrane steroid binding protein in root architecture response to salinity Plant. Cell Environ 41:1311–1330. https://doi.org/10.1111/pce.13154

    Article  CAS  Google Scholar 

  • Xu Z-M et al (2018) Low root/shoot (R/S) biomass ratio can be an indicator of low cadmium accumulation in the shoot of Chinese flowering cabbage (Brassica campestris L. ssp. chinensis var. utilis Tsen et Lee) cultivars. Environ Sci Pollut Res 25:36328–36340. https://doi.org/10.1007/s11356-018-3566-x

    Article  CAS  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

    Article  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 Regulat 56:179–190. https://doi.org/10.1007/s10725-008-9299-y

    Article  CAS  Google Scholar 

  • Yang JY, Zheng W, Tian Y, Wu Y, Zhou DW (2011) Effects of various mixed salt-alkaline stresses on growth, photosynthesis, and photosynthetic pigment concentrations of Medicago ruthenica seedlings. Photosynthetica 49:275–284. https://doi.org/10.1007/s11099-011-0037-8

    Article  CAS  Google Scholar 

  • Yang L, Ma C, Wang L, Chen S, Li H (2012) Salt stress induced proteome and transcriptome changes in sugar beet monosomic addition line M14. J Plant Physiol 169:839–850. https://doi.org/10.1016/j.jplph.2012.01.023

    Article  CAS  PubMed  Google Scholar 

  • Zhang JL, Shi H (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115:1–22

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Fernie AR (2018) On the role of the tricarboxylic acid cycle in plant productivity. J Integr Plant Biol 60:1199–1216. https://doi.org/10.1111/jipb.12690

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Shi G, Yuan Q (2008) Polyamines content and physiological and biochemical responses to ladder concentration of nickel stress in Hydrocharis dubia (Bl.) Backer leaves. Biometals 21:665

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y et al (2019) Application of exogenous glutathione confers salinity stress tolerance in tomato seedlings by modulating ions homeostasis and polyamine metabolism. Sci Hortic 250:45–58. https://doi.org/10.1016/j.scienta.2019.02.026

    Article  CAS  Google Scholar 

  • Zou C, Sang L, Gai Z, Wang Y, Li C (2018) Morphological and physiological responses of sugar beet to alkaline stress. Sugar Tech 20:202–211. https://doi.org/10.1007/s12355-017-0547-1

    Article  CAS  Google Scholar 

  • Zou CL et al (2019) Photosynthetic capacity, osmotic adjustment and antioxidant system in sugar beet (Beta vulgaris L.) in response to alkaline stress. Photosynthetica 57:350–360

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Natural Science Foundation of China (31671622) and Modern Agricultural Industrial Technology System of China (CARS-170201).

Author information

Author notes

  1. Chun-Lei Zou and Yu-Bo Wang have equally contributed to the current manuscript.

Authors and Affiliations

  1. College of Agronomy, Northeast Agricultural University, Harbin, 150030, China

    Chun-Lei Zou, Yu-Bo Wang, Bin Wang, Dan Liu, Lei Liu & Cai-Feng Li

Authors
  1. Chun-Lei Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yu-Bo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cai-Feng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cai-Feng Li.

Additional information

Communicated by M. J. Reigosa.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zou, CL., Wang, YB., Wang, B. et al. Effects of alkali stress on dry matter accumulation, root morphology, ion balance, free polyamines, and organic acids of sugar beet. Acta Physiol Plant 43, 13 (2021). https://doi.org/10.1007/s11738-020-03194-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-020-03194-x

Keywords

Search

Navigation