Skip to main content
SpringerLink
Log in

The effects of grafting on glycolysis and the tricarboxylic acid cycle in Ca(NO3)2-stressed cucumber seedlings with pumpkin as rootstock

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

Abstract

In this research, we investigated the effects of grafting on intermediate metabolites and key enzymes of glycolysis and the tricarboxylic acid (TCA) cycle in self-grafted and salt-tolerant pumpkin rootstock-grafted cucumber seedlings supplied with nutrient solution and subjected to 80 mM Ca(NO3)2 stress for 6 days. Ca(NO3)2 stress induced accumulation of 3-phosphoglycerate (3-PGA) and phosphoenolpyruvate (PEP) in the leaves of self-grafted cucumber seedlings and enhanced the activities of phosphoenolpyruvate carboxylase (PEPC) and enolase (ENO). Succinic acid and malic acid contents and isocitrate dehydrogenase, succinate dehydrogenase (SDH), and malate dehydrogenase (MDH) activities in self-grafted seedlings were significantly decreased by Ca(NO3)2 stress. In addition, activities of PEPC, ENO, SDH, and MDH and contents of glycolysis intermediate metabolites (citric, succinic, and malic acids) were significantly higher in leaves of rootstock-grafted seedlings compared with those in self-grafted seedlings under saline conditions. Furthermore, leaf adenosine triphosphate (ATP) content of rootstock-grafted seedlings was relatively higher than that in self-grafted plants under salt stress, with an opposite effect observed on adenosine diphosphate content. These results indicate that rootstock grafting alleviates Ca(NO3)2 stress-induced inhibition of the glycolytic pathway and the TCA cycle in cucumber seedling leaves, which may aid the respiratory metabolism of cucumber seedlings and help maintain a high ATP synthesis level, thereby increasing the biomass of cucumber seedlings and enhancing their salt tolerance.

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

Similar content being viewed by others

Abbreviations

ADP:

Adenosine diphosphate

ATP:

Adenosine triphosphate

ENO:

Enolase

HPLC:

High-performance liquid chromatographic

IDH:

Isocitrate dehydrogenase

MDH:

Malate dehydrogenase

PEP:

Phosphoenolpyruvate

PEPC:

Phosphoenolpyruvate carboxylase

SDH:

Succinate dehydrogenase

TCA:

Tricarboxylic acid cycle

3-PGA:

3-phosphoglycerate

References

  • Amthor J (1991) Respiration in a future, higher-CO2 world. Plant Cell Environ 14:13–20

    Article  CAS  Google Scholar 

  • Ap Rees T, Bryce J, Wilson P, Green J (1983) Role and location of NAD malic enzyme in thermogenic tissues of Araceae. Arch Biochem Biophys 227:511–521

    Article  CAS  PubMed  Google Scholar 

  • Asins M, Bolarín M, Pérez-Alfocea F, Estañ M, Martínez-Andújar C, Albacete A, Villalta I, Bernet G, Dodd IC, Carbonell E (2010) Genetic analysis of physiological components of salt tolerance conferred by Solanum rootstocks. What is the rootstock doing for the scion? Theor Appl Genet 121:105–115

    Article  CAS  PubMed  Google Scholar 

  • Bansal P, Sharma P, Goyal V (2002) Impact of lead and cadmium on enzyme of citric acid cycle in germinating pea seeds. Biol Plant 45:125–127

    Article  CAS  Google Scholar 

  • Bergmeyer HU, Gawehn K (1970) Methoden der enzymatischen Analyse, vol 432. Verlag Chemie, Weinheim

  • Bloom A, Epstein E (1984) Varietal differences in salt-induced respiration in barley. Plant Sci Lett 35:1–3

    Article  CAS  Google Scholar 

  • Bouthour D, Hajjaji-Nasraoui A, Saafi L, Gouia H, Chaffei-Haouari C (2012) Effects of NaCl on growth and activity of enzymes involved in carbon metabolism in leaves of tobacco (Nicotiana rustica). Afr J Biotechnol 11:12619–12629

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Centeno DC, Oliver SN, Nunes-Nesi A, Geigenberger P, Machado DN, Loureiro ME, Silva MA, Fernie AR (2008) Metabolic regulation of pathways of carbohydrate oxidation in potato (Solanum tuberosum) tubers. Physiol Plant 133:744–754

    Article  CAS  PubMed  Google Scholar 

  • Davis AR, Perkins-Veazie P, Sakata Y, López-Galarza S, Morato JV, Lee SG, Huh YC, Sun Z, Miguel A, King S, Cohen R, Lee JM (2008) Cucurbit grafting. Crit Rev Plant Sci 27:50–74

    Article  Google Scholar 

  • Day D, Bertagnolli B, Hanson J (1978) The effect of calcium on the respiratory responses of corn mitochondria. Biochimica et Biophysica Acta (BBA)-Bioenergetics 502:289–297

  • Estañ M, Villalta I, Bolarín M, Carbonell E, Asins M (2009) Identification of fruit yield loci controlling the salt tolerance conferred by solanum rootstocks. Theor Appl Genet 118:305–312

    Article  PubMed  Google Scholar 

  • Fernie AR, Martinoia E (2009) Malate. Jack of all trades or master of a few? Phytochemistry 70:828–832

    Article  CAS  PubMed  Google Scholar 

  • Fernie AR, Carrari F, Sweetlove LJ (2004) Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr Opin Plant Biol 7:254–261

    Article  CAS  PubMed  Google Scholar 

  • Forsthoefel NR, Cushman MAF, Cushman JC (1995) Posttranscriptional and posttranslational control of enolase expression in the facultative Crassulacean acid metabolism plant Mesembryanthemum crystallinum L. Plant Physiol 108:1185–1195

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hrubec TC, Robinson JM, Donaldson RP (1985) Effects of CO2 enrichment and carbohydrate content on the dark respiration of soybeans. Plant Physiol 79:684–689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huerta-Ocampo JA, Barrera-Pacheco A, Mendoza-Hernández CS, Espitia-Rangel E, Mock H-P, Barba de la Rosa AP (2014) Salt stress-induced alterations in the root proteome of Amaranthus cruentus L. J Proteome Res 13:3607–3627

    Article  CAS  PubMed  Google Scholar 

  • Idso SB, Kimball BA (1992) Effects of atmospheric CO2 enrichment on photosynthesis, respiration, and growth of sour orange trees. Plant Physiol 99:341–343

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jacoby RP, Taylor NL, Millar AH (2011) The role of mitochondrial respiration in salinity tolerance. Trends Plant Sci 16:614–623

    Article  CAS  PubMed  Google Scholar 

  • Lambers H, Chapin SF III, Pons TL (1998) Plant physiological ecology. Springer, New York

    Book  Google Scholar 

  • Lee J-M (1994) Cultivation of grafted vegetables I. Current status, grafting methods, and benefits. HortScience 29:235–239

    Google Scholar 

  • Liu H, Jiang Y, Luo Y, Jiang W (2006) A simple and rapid determination of ATP, ADP and AMP concentrations in pericarp tissue of litchi fruit by high performance liquid chromatography. Food Technol Biotechnol 44:531–534

    CAS  Google Scholar 

  • Liu Z, Bie Z, Huang Y, Zhen A, Lei B, Zhang H (2012) Grafting onto Cucurbita moschata rootstock alleviates salt stress in cucumber plants by delaying photoinhibition. Photosynthetica 50:152–160

    Article  CAS  Google Scholar 

  • López M, Herrera-Cervera JA, Iribarne C, Tejera NA, Lluch C (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J Plant Physiol 165:641–650

    Article  PubMed  Google Scholar 

  • Miller G, Suzuki N, CIFTCI-YILMAZ S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

  • Nunes-Nesi A, Araújo WL, Obata T, Fernie AR (2013) Regulation of the mitochondrial tricarboxylic acid cycle. Curr Opin Plant Biol 16:335–343

    Article  CAS  PubMed  Google Scholar 

  • Osorio S, Vallarino JG, Szecowka M, Ufaz S, Tzin V, Angelovici R, Galili G, Fernie AR (2013) Alteration of the interconversion of pyruvate and malate in the plastid or cytosol of ripening tomato fruit invokes diverse consequences on sugar but similar effects on cellular organic acid, metabolism, and transitory starch accumulation. Plant Physiol 161:628–643

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pellet DM, Grunes DL, Kochian LV (1995) Organic acid exudation as an aluminum-tolerance mechanism in maize (Zea mays L.). Planta 196:788–795

    Article  CAS  Google Scholar 

  • Prabhakar V, Löttgert T, Gigolashvili T, Bell K, Flügge U-I, Häusler RE (2009) Molecular and functional characterization of the plastid-localized Phosphoenolpyruvate enolase (ENO1) from Arabidopsis thaliana. FEBS Lett 583:983–991

    Article  CAS  PubMed  Google Scholar 

  • Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rouphael Y, Schwarz D, Krumbein A, Colla G (2010) Impact of grafting on product quality of fruit vegetables. Sci Hortic 127:172–179

    Article  Google Scholar 

  • Santa-Cruz A, Martínez-Rodríguez M, Bolarín M, Cuartero J (2000) Response of plant yield and leaf ion contents to salinity in grafted tomato plants. In: V international symposium on protected cultivation in mild winter climates: current trends for suistainable technologies, vol 559, pp 413–417

  • Slama I, Ghnaya T, Savouré A, Abdelly C (2008) Combined effects of long-term salinity and soil drying on growth, water relations, nutrient status and proline accumulation of Sesuvium portulacastrum. CR Biol 331:442–451

    Article  CAS  Google Scholar 

  • Stitt M, Quick WP (1989) Photosynthetic carbon partitioning: its regulation and possibilities for manipulation. Physiol Plant 77:633–641

    Article  CAS  Google Scholar 

  • Taylor NL, Tan Y-F, Jacoby RP, Millar AH (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J Proteom 72:367–378

    Article  CAS  Google Scholar 

  • Tong Y, Chen D (1991) Study on the cause and control of secondary saline soils in greenhouses. Acta Hortic Sin 18:159–162

    Google Scholar 

  • Turner JF, Tomlinson JD, Caldwell RA (1980) Effect of salts on the activity of carrot phosphofructokinase. Plant Physiol 66:973–977

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Van Der Straeten D, Rodrigues-Pousada RA, Goodman HM, Van Montagu M (1991) Plant enolase: gene structure, expression, and evolution. Plant Cell Online 3:719–735

    Article  Google Scholar 

  • Vidal J, Chollet R (1997) Regulatory phosphorylation of C 4 PEP carboxylase. Trends Plant Sci 2:230–237

    Article  Google Scholar 

  • Wang L-P, Guo S-R, Sun J, Tian J, Yang Y-J, He L-Z (2012) Analysis of photosynthetic characteristics and key enzyme genes expression of carbon assimilation in cucumber by grafting onto salt-tolerant rootstock under iso-osmotic Ca (NO3)2 or NaCl stress. J Nanjing Agric Univ 35:31–36 (in Chinese)

    Google Scholar 

  • Widodo W, Patterson J, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60:4089–4103

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Winicov I (1998) New molecular approaches to improving salt tolerance in crop plants. Ann Bot 82:703–710

    Article  CAS  Google Scholar 

  • Xing W-W, Lin L, Pan G, Li H, Shao Q-S, Shu S, Sun J, Guo S-R (2015) Effects of grafting with pumpkin rootstock on carbohydrate metabolism in cucumber seedlings under Ca (NO3)2 stress. Plant Physiol Biochem 87:124–132

    Article  CAS  PubMed  Google Scholar 

  • Yang N-C, Ho W-M, Chen Y-H, Hu M-L (2002) A convenient one-step extraction of cellular ATP using boiling water for the luciferin–luciferase assay of ATP. Anal Biochem 306:323–327

    Article  CAS  PubMed  Google Scholar 

  • Yang Y-J, Wang L-P, Tian J, Li J, Sun J, He L-Z, Guo S-R, Tezuka T (2012) Proteomic study participating the enhancement of growth and salt tolerance of bottle gourd rootstock-grafted watermelon seedlings. Plant Physiol Biochem 58:54–65

    Article  CAS  PubMed  Google Scholar 

  • Yeo A (1983) Salinity resistance: physiologies and prices. Physiol Plant 58:214–222

    Article  CAS  Google Scholar 

  • Yuan L-Y, Du J, Yuan Y-H, Shu S, Sun J, Guo S-R (2013) Effects of 24-epibrassinolide on ascorbate–glutathione cycle and polyamine levels in cucumber roots under Ca (NO3)2 stress. Acta Physiologiae Plantarum 35:253–262

    Article  CAS  Google Scholar 

  • Zhou J, Tian X, Qiao L (2012) Qin P (2012) Respiratory enzyme activity and regulation of respiration pathway in seashore mallow (‘Kosteletzkya virginica’) seedlings under waterlogging conditions [online]. Aust J Crop Sci 6(4):756–762

    CAS  Google Scholar 

  • Zijlstra S, Groot SPC, Jansen J (1994) Genotypic variation of rootstocks for growth and production in cucumber: possibilities for improving the root system by plant breeding. Sci Hortic 56:185–196

    Article  Google Scholar 

  • Zuther E, Koehl K, Kopka J (2007) Comparative metabolome analysis of the salt response in breeding cultivars of rice. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Berlin, pp 285–315

Download references

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31401919, No. 31471869 and No. 31272209), the Central Research Institutes of Basic Research Fund (6J0745), the China Earmarked Fund for Modern Agro-industry Technology Research System (CARS-25-C-03), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and sponsored by the Research Fund for the Doctoral Program of Higher Education (20130097120015).

Author information

Author notes

    Authors and Affiliations

    1. Key Laboratory of Southern Vegetables Genetic Improvement of Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing, 210095, China

      Lin Li, Wen-wen Xing, Qiao-sai Shao, Sheng Shu, Jin Sun & Shi-rong Guo

    2. Facility Horticulture Institute, Nanjing Agricultural University, Suqian, 223800, Jiangsu, China

      Jin Sun & Shi-rong Guo

    Authors
    1. Lin Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Wen-wen Xing
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Qiao-sai Shao
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Sheng Shu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Jin Sun
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Shi-rong Guo
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Shi-rong Guo.

    Additional information

    Communicated by W. Wang.

    L. Li and W. Xing are contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Li, L., Xing, Ww., Shao, Qs. et al. The effects of grafting on glycolysis and the tricarboxylic acid cycle in Ca(NO3)2-stressed cucumber seedlings with pumpkin as rootstock. Acta Physiol Plant 37, 259 (2015). https://doi.org/10.1007/s11738-015-1978-5

    Download citation

    • Received:

    • Revised:

    • Accepted:

    • Published:

    • DOI: https://doi.org/10.1007/s11738-015-1978-5

    Keywords

    Search

    Navigation