, Volume 54, Issue 4, pp 620–629 | Cite as

Exogenous Ca2+ alleviates waterlogging-caused damages to pepper

  • B. Z. Yang
  • Z. B. Liu
  • S. D. Zhou
  • L. J. Ou
  • X. Z. Dai
  • Y. Q. Ma
  • Z. Q. Zhang
  • W. C. Chen
  • X. F. Li
  • C. L. Liang
  • S. Yang
  • X. X. Zou
Original papers


Ca2+ has been considered as a necessary ion for alleviation of stress-induced damages in plants. We investigated effects of exogenous Ca2+ on waterlogging-induced damage to pepper and its underlying mechanisms. Pepper seedlings under stress were treated by spraying of 10 mM CaCl2. Applying exogenous Ca2+ increased the biomass of pepper leaves and roots, improved photosynthetic characteristics, membrane permeability, root activity, osmotic substance contents, antioxidant enzyme and alcohol dehydrogenase activities, while it reduced lactate dehydrogenase activity. It maintained hydroxide radical contents and activities of malate dehydrogenase and succinate dehydrogenase relatively high. Our results suggested that applying exogenous Ca2+ could regulate osmotic substance contents, antioxidant system activity, root respiration, and metabolism, and subsequently alleviate waterlogging-induced damages to pepper plants.

Additional key words

calcium Capsicum annuum respiratory waterlogging 



alcohol dehydrogenase






Ca2+ treatment group








dry mass




transpiration rate


minimal fluorescence yield at the dark adapted-state


minimal fluorescence yield at the light-adapted state


maximal fluorescence yield at the dark-adapted state


maximal fluorescence yield at the light-adapted state


fresh mass


maximal quantum yield of PSII photochemistry


glutathione reductase


stomatal conductance


lactate dehydrogenase




malate dehydrogenase


net photosynthetic rate




photochemical quenching coefficient


reactive oxygen species


standard deviation


succinate dehydrogenase


superoxide dismutase


triphenyl tetrazolium chloride


trityl hydrazone


waterlogging group


water-use efficiency


effective quantum yield of PSII photochemistry


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Arnon D.I.: Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta vulgaris.–Plant Physiol. 24: 1–15, 1949.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Boaretto L.F., Carvalho G., Borgo L. et al.: Water stress reveals differential antioxidant responses of tolerant and non-tolerant sugarcane genotypes.–Plant Physiol. Bioch. 74: 165–175, 2014.CrossRefGoogle Scholar
  3. Broughton S., Zhou G.F., Teakle N. L. et al.: Waterlogging tolerance is associated with root porosity in barley (Hordeum vulgare L.).–Mol Breeding. 35: 1–15, 2015.CrossRefGoogle Scholar
  4. Chen L.M.: [Effects of calcium treatment on physiological properties of cotton seedings under drought stress.]–Chin. Bull. Bot. 15: 70–72, 1998. [In Chinese]Google Scholar
  5. Christou A., Manganaris G.A., Fotopoulos V.: Systemic mitigation of salt stress by hydrogen peroxide and sodium nitroprusside in strawberry plants via transcriptional regulation of enzymatic and non-enzymatic antioxidants.–Environ. Exp. Bot. 107: 46–54, 2014.CrossRefGoogle Scholar
  6. Deng L.S., Tu P.F., Gong L. et al.: [Effect of calcium treatment by means of drip fertigation on growth and absorption of mineral nutrients in banana.]–Acta Agric. Univ. Jiangxi. 34: 34–39, 2012. [In Chinese]Google Scholar
  7. Duan Y.X., Song S.Q., Fu J.R.: [Effects of calcium on delaying senescence of leaves in hybrid rice.]–Hybrid Rice 12: 23–25, 1997. [In Chinese]Google Scholar
  8. Egert M., Tevini M.: Influence of drought on some physiological parameters symptomatic for oxidative stress in leaves of chives (Allium schoenoprasum).–Environ. Exp. Bot. 48: 43–49, 2002.CrossRefGoogle Scholar
  9. Fan X.T., Ma D.W., Xiang S. et al.: Chang in antioxidant enzymes of Galinsoga parviflora Cav. Under environmental stresses.–Chin. J. Appl. Environ. Biol. 14: 616–619, 2008.Google Scholar
  10. França M.G.C., Thi A.T.P., Pimentel C. et al.: Differences in growth and water relations among Phaseolus vulgaris cultivars in response to induced drought stress.–Environ. Exp. Bot. 43: 227–237, 2000.CrossRefGoogle Scholar
  11. Fukao T., Kennedy R.A., Yamasue Y. et al.: Genetic and biochemical analysis of anaerobically-induced enzymes during seed germination of Echinochloa crus-galli varieties tolerant and intolerant of anoxia.–Exp. Bot. 54: 1421–1429, 2003.CrossRefGoogle Scholar
  12. Gao H.B., Chen G.L.: [The effect of calmodulin antagonist and calcium on chilling resistance of eggplant seedling.]–Acta Hortic. Sin. 29: 243–246, 2002. [In Chinese]Google Scholar
  13. Gao H.B., Liu Y.H., Guo S.R. et al.: [Effect of calcium on polyamine content and polyamines oxidase active in muskmelon seedlings under hypoxia stress.]–Acta Phytoecol. Sin. 29: 652–658, 2005a. [In Chinese]Google Scholar
  14. Gao H.B., Guo S.R., Liu Y.H. et al.: [Effect of Ca2+, La3+ and EGTA on reactive oxygen species metabolism in muskmelon seedlings under hypoxia stress.]–J. Nanjing Agric. Univ. 28: 17–21, 2005b. [In Chinese]Google Scholar
  15. Genty B, Briantais J.M, Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.–Biochim. Biophys. Acta. 900: 87–92, 1989.CrossRefGoogle Scholar
  16. Gong M., Li Z.G.: Calmodulin-binding proteins from Zea mays germs.–Phytochemistry 40: 1335–1339, 1995.CrossRefGoogle Scholar
  17. Gong M., Li Y.J., Chen S.Z.: Abascisic acid-induced thermotolerance in maize seedlings is mediated by calcium and associated with antioxidant systems.–J. Plant Physiol. 153: 488–496, 1998.CrossRefGoogle Scholar
  18. Guo S.R., Nada K., Katoh H. et al.: [Differences between tomato and cucumber in ethanol, lactate and malate metabolisms and cell sap pH of roots under hypoxia.]–Jpn. Soc. Hortic. Sci. 68: 152–159, 1999. [In Japanese]CrossRefGoogle Scholar
  19. Han Y.H.: [Effect of water stress on plasma membrane of soybean (Glycine max) seedling leaves.]–J. Guangxi Norm. Univ. 17: 85–87, 1999. [In Chinese]Google Scholar
  20. Hu X.H., Li J., Guo S.R., et al.: [Effects of Ca2+ on respiratory metabolism in roots of cucumber seedlings under root-zone hypoxia stress.]–Acta Hortic. Sin. 33: 1113–1116, 2006. [In Chinese]Google Scholar
  21. Hu X.H., Guo S.R., Li J. et al.: Effects of calmodulin antagonist on polyamine content and respiratory metabolism in cucumber seedling roots under hypoxia stress.–Chin. Appl. Environ. Bio. 13: 475–480, 2007.Google Scholar
  22. Ismond K.P., Dolferus R., de Pauw M. et al.: Enhanced low oxygen survival in Arabidopsis through increased metabolic flux in the fermentative pathway.–Plant Physiol. 132: 1292–1302, 2003.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Issarakraisila M., Ma Q., Turner D.W.: Photosynthetic and growth responses of juvenile Chinese kale (Brassica oleracea var. alboglabra) and Caisin (Brassica rapa subsp. Parachinensis) to waterlogging and waterlogging and water deficit.–Sci. Hortic.-Amsterdam 111: 107–113, 2007CrossRefGoogle Scholar
  24. Kuai J., Liu Z.W., Wang Y.H. et al.: Waterlogging during flowering and boll forming stages affects sucrose metabolism in the leaves subtending the cotton boll and its relationship with boll weight.–Plant Sci. 223: 79–98, 2014.CrossRefPubMedGoogle Scholar
  25. Le Provost G., Sulmon C., Frigerio J.M. et al.: Role of waterlogging-responsive genes in shaping interspecific differentiation between two sympatric oak species.–Tree Physiol. 32: 119–134, 2012.CrossRefPubMedGoogle Scholar
  26. Liang Z.J., Tao H.B., Wang P.: [Recovery effects of morphology and photosynthetic characteristics of maize (Zea mays L.) seedling after water-logging.]–Acta Ecol. Sin. 29: 3977–3986, 2009. [In Chinese]Google Scholar
  27. Li M., Yang D., Li W.: Leaf gas exchange characteristics and chlorophyll fluorescence of three wetland plants in response to long-term soil flooding.–Photosynthetica 45: 222–228, 2007.CrossRefGoogle Scholar
  28. Li T.L., Li M., Sun Z.P.: [Regulation effect of calcium and salicy acid on defense enzyme acticvities in tomato leaves under subhigh temperature stress.]–Chin. J. Appl. Ecol. 20: 586–590, 2009. [In Chinese]Google Scholar
  29. Li Z.Y., Gao D.S., Wang C. et al.: [Effects of calcium application on calcium content and quality of nectarine under protected culture.]–Plant Nutr. Fert. Sci. 16: 191–196, 2010. [In Chinese]Google Scholar
  30. Lima A.L.S., DaMatta F.M., Pinheiro H. A. et al.: Photochemical responses and oxidative stress in two clones of Coffea canephora under water deficit conditions.–Environ. Exp. Bot. 47: 239–247, 2002.CrossRefGoogle Scholar
  31. McCord J.M., Fridovich J.: Superoxide dismutase: An enzymic function for erythrocuprein (hemocuprein).–J. Biol. Chem. 224: 6049–6055, 1969.Google Scholar
  32. McCord J.M., Fridovich I.: The biology and pathology of oxygen radicals.–Ann. Intern. Med. 89: 122–127, 1978.CrossRefPubMedGoogle Scholar
  33. Neill S.J., Burnett E.C.: Regulation of gene expression during water deficit stress.–Plant Growth Regul. 29: 23–33, 1999.CrossRefGoogle Scholar
  34. Ou L.J., Dai X.Z., Zhang Z. Q. et al.: Responses of pepper to waterlogging stress.–Photosynthetica 49: 339–345, 2011.CrossRefGoogle Scholar
  35. Ou L.J., Chen B., Zou X.X.: [Effects of drought stress on photosynthesis and associated physiological characters of pepper.]–Acta Ecol. Sin. 32: 2612–2619, 2012. [In Chinese]CrossRefGoogle Scholar
  36. Pan D.M., Zheng G.H., Xie H.C. et al.: [Superoxide dismutase activity and lipid peroxidation in leaves of loquat under water stress.]–J. Fujian Agri. Coll. 22: 254–257, 1993. [In Chinese]Google Scholar
  37. Pei B., Zhang G.C., Zhang S.Y. et al.: Effects of soil drought stress on photosynthetic characteristics and antioxidant enzyme activities in Hippophae rhamnoides Linn. seedings.–Acta Ecol. Sin. 33: 1386–1396, 2013.CrossRefGoogle Scholar
  38. Peng Q., Liang Y.L., Chen C., et al.: [Effects of soil moisture on growth and pepper fruit quality in greenhouse during fruiting stage]–J. Northwest A&F Univ. (Nat. Sci. Ed.) 38: 154–160, 2010. [In Chinese]Google Scholar
  39. Perata P., Alpi A.: Plant response to anaerobiosis.–Plant Sci. 93: 1–17, 1993.CrossRefGoogle Scholar
  40. Pistelli L., Iacona C., Miano D. et al.: Novel Prunus rootstock somaclonal variants with divergent ability to tolerate waterlogging.–Tree Physiol. 32: 355–368, 2012.CrossRefPubMedGoogle Scholar
  41. Prasad S., Ram P.C., Uma S.: Effect of waterlogging duration on chlorophyll content, nitrate reductase activity, soluble sugars and grain yield of maize.–Annu. Rev. Plant Physiol. 18: 1–5, 2004.Google Scholar
  42. Ren B.Z., Zhu Y.L., Li X. et al.: [Effects of waterlogging on photosynthetic characteristics of summer maize under field conditions.]–Acta Agron. Sin. 41: 329–338, 2015. [In Chinese]CrossRefGoogle Scholar
  43. Subbaish C.C., Sachs M.M.: Molecular and cellular adaptation maize to flooding stress.–Ann. Bot.-London 91: 119–127, 2003.CrossRefGoogle Scholar
  44. Tanaka K.: Tolerance to herbicides and air pollutants.–In: Foyer C.H., Mullineaux P.M. (ed.): Causes of Photoxidative Stress and Amelioration of Defense Systems in Plants. Pp. 365–378. CRC Press, Boca Raton 1994.Google Scholar
  45. Wang C.Y., Lou X.R., Wang J.L.: [Influence of agricultural meteorological disters on output of crop in China.]–J. Nat. Disaster 16: 37–42, 2007. [In Chinese]Google Scholar
  46. Wang Q., Sjolund R., Shih L.M.C.: Involvement of calcium in the anoxia-signaling pathway of Arabidopsis thaliana. Acta Photophysiol. Sin. 28: 441–448, 2002.Google Scholar
  47. Wang L.J., Liu Y.L., Ma K.: [The role of calcium in promotion of proline accumulation induced by salt stress in fig (Ficus carica L.) cells.]–Acta Phytophysiol. Sin. 25: 38–42, 1999. [In Chinese]Google Scholar
  48. Wang M., Xu X.R., Liu C.L. et al.: [The effect of calcium on the fruit quality and physiological and biochemical characteristics of peach in greenhouse.]–Chin. Agric. Sci. Bull. 25: 219–222, 2009. [In Chinese]Google Scholar
  49. Wu L., Zhang Z.D., Li Y.D. et al.: [Physiological reaction of blueberry under flooding treatment.]–J. Jilin Agric. Univ. 22: 62–64, 2000. [In Chinese]Google Scholar
  50. Wu F., Zhang G., Dominy P.: Four barley genotypes respond differently to cadmium: lipid peroxidation and activities of antioxidant capacity.–Environ. Exp. Bot. 50: 67–78, 2003.CrossRefGoogle Scholar
  51. Xiong L.M., Schumaker K.S., Zhu J.K.: Cell signaling during cold, drought, and salt stress.–Plant Cell 14: S165–S183, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhang E.R., Ren Y.Y., Hu H.Q., et al.: [Effects of calcium on growth and respiratory metabolism of hot pepper seeding roots under flood stress.]–Acta Hortic. Sin. 36: 1749–1754, 2009. [In Chinese]Google Scholar
  53. Zhang Z.X., Sun J., Guo S.R. et al.: [Effects of supplemental calcium on the photosynthetic characteristics and fruit quality of watermelon under salt stress.]–Acta Hortic. Sin. 38: 1929–1938, 2011. [In Chinese]Google Scholar
  54. Zhou L.Y., Li X.D., Wang L.L. et al.: [Effects of different Ca applications on physiological characteristics, yield and quality in peanut.]–Acta Agron. Sin. 34: 879–885, 2008. [In Chinese]CrossRefGoogle Scholar
  55. Zhu Q., Pan Y.Z., Zhao L. et al.: [Effects of different N, P, K, Ca application values on cut flower quality of Lilium Casa Blanca.]–Soil Fertil. Sci. Chin. 49: 48–54, 2012. [In Chinese]Google Scholar
  56. Zhu X.J., Yang J.S., Liang Y.C. et al.: Effects of exogenous calcium on photosynthesis and its related physiological characteristics of rice seedlings under salt stress.–Sci. Agric. Sin. 37: 1497–1503, 2004.Google Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  • B. Z. Yang
    • 1
    • 2
  • Z. B. Liu
    • 1
    • 2
  • S. D. Zhou
    • 2
  • L. J. Ou
    • 2
  • X. Z. Dai
    • 2
  • Y. Q. Ma
    • 2
  • Z. Q. Zhang
    • 2
  • W. C. Chen
    • 2
  • X. F. Li
    • 2
  • C. L. Liang
    • 2
  • S. Yang
    • 2
  • X. X. Zou
    • 1
    • 2
  1. 1.Longping Branch of Central South UniversityChangshaChina
  2. 2.Vegetable Institution of Hunan Academy of Agricultural ScienceChangshaChina

Personalised recommendations