Skip to main content
Log in

Calcium chloride improves photosynthesis and water status in the C4 succulent xerophyte Haloxylon ammodendron under water deficit

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Our results showed that in addition to sodium (Na+), succulent xerophyte Haloxylon ammodendron was more inclined to absorb and accumulate large amount of calcium (Ca2+) than potassium (K+) as an important osmotica for osmotic adjustment (OA) under arid environments. To further reveal the possible physiological mechanisms of Ca2+ accumulation involved in drought resistance of H. ammodendron, 8-week-old plants were treated with a series concentration of external Ca2+ (calcium chloride, 1 × 10−4 to 8 × 10−4 g CaCl2 g−1 dry soil) by potted sandy soil culture experiments in field. Plants were also subjected to water deficit (30% of field water capacity) in the presence or absence of Ca2+ (4 × 10−4 g CaCl2 g−1dry soil) by potted sand culture experiments in greenhouse. The results showed that 4 × 10−4 g CaCl2 g−1 soil resulted in optimal plant growth and effectively mitigated harmful impacts of water deficit on the growth of H. ammodendron, by inducing a significant drop in PB water potential and, concomitantly, increasing PB turgor pressure and chlorophyll concentration resulting in an enhancement of overall plant photosynthetic activity. Furthermore, 4 × 10−4 g CaCl2 g−1 soil had no effects on the photosystem II photochemistry, but mitigated the inhibitory effect of water deficit on the activity of photosystem II in H. ammodendron. The contribution of Ca2+ to the total osmotic potential varied from 6.2% in the control to 11.4% in plants subjected to water deficit and, surprisingly, to 21.6% in plants grown in the presence of 4 × 10−4 g CaCl2 g−1 soil under water deficit; however, the contribution of K+ significantly decreased from 12.1 to 7.0%. These findings suggest that, under arid environments, H. ammodendron is able to accumulate high concentration of Ca2+ in its PB and use it directly for OA, which was coupled with an improvement in PB hydration and photosynthetic activity.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abdel BR (1998) Calcium channels and membrane disorders induced by drought stress in Vicia faba plants supplemented with calcium. Acta Physiol Plant 20(2):149–153

    Article  Google Scholar 

  • An B, Chen Y, Li B, Qin G, Tian S (2014) Ca2+-CaM regulating viability of Candida guilliermondii under oxidative stress by acting on detergent resistant membrane proteins. J. Proteom 109: 38–49

    Article  CAS  Google Scholar 

  • Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570

    Article  CAS  Google Scholar 

  • Barry CS (2009) The stay-green revolution: recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants. Plant Sci 176:325–333

    Article  CAS  Google Scholar 

  • Ben Hassine A, Bouzid S, Lutts S (2010) Does habitat of Atriplex halimus L. affect plant strategy for osmotic adjustment? Acta Physiol Plant 32(2):325–331

    Article  Google Scholar 

  • Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2010) Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci 2(12):85

    Google Scholar 

  • Cai JY, Ma Q, Zhou XR, Zhang JL, Wang SM (2011) Physiological role of Na+ in adaptation of Zygophyllum xanthoxylum to osmotic stress. Acta Pratuacul Sci 20(1):89–95

    Google Scholar 

  • Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16

    Article  CAS  Google Scholar 

  • Chowdhury SR, Choudhuri MA (1986) Effects of calciumions on responses of two jute species under water deficit stress. Physiol Plant 68:86–92

    Article  CAS  Google Scholar 

  • Debez A, Saadaoui D, Balasubramanian R, Zeineb O, Hans-Werner K, Bernhard H, Chedly A (2006) Leaf H+-ATPase activity and photosynthetic capacity of Cakile maritima under increasing salinity. Environ Exp Bot 57(3):285–295

    Article  CAS  Google Scholar 

  • Filella I, Liusia J, Piol J (1989) Leaf gas exchange and the fluorescence of Phillg ralatifolia. Pistacia lentiscus and Quercusilex samplings in severe drought and high temperature conditions. Environ Exp Bot 39:213–219

    Article  Google Scholar 

  • Franks PJ, Buckley TN, Shope JC, Mott KA (2001) Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe. Plant Physiol 125:1577–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruber BD, Giehl RFH, Friedel S, Von WN (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163(1):161–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerrier G (1996) Fluxes of Na+, K+ and Cl, and osmotic adjustment in Lycopersicon pimpinellifolium and L. esculentum during short- and long-term exposures to NaCl. Physiol Plant 97:583–591

    Article  CAS  Google Scholar 

  • Hao YY, Yue LJ, Kang JJ, Wang SM (2012) Research progress on” desert ginseng”-Cistanche deserticola and Cynomorium Songaria. Acta Pratac Sin 21(2):286–293

    Google Scholar 

  • Janz D, Polle A (2012) Harnessing salt for woody biomass production. Tree Physiol 32(1):1–3

  • Jiang BY, Li JH, Fang LY, Wang CZ (2008) Effect of calcium treatments on the drought resistance of Medicago sativa. Chin J Grassl 30(1):117–120

    Google Scholar 

  • Jiang SS, Zhang D, Kong XP, Zhou Y, Li DQ (2013) Research progress of structural characteristics and functions of Calcium-dependent protein kinases in plants. Biotechnol Bull 6:12–19

    Google Scholar 

  • Jones RG, Lunt OR (1967) The function of calcium in plant. Bot Rev 33:407–426

    Article  CAS  Google Scholar 

  • Kang JJ, Duan JJ, Wang SM, Zhao M, Li GY, Yang ZH (2013) Na compound fertilizer promotes growth and enhances drought resistance of the succulent xerophyte Haloxylon ammodendron. Soil Sci Plant Nutr 59(2):289–299

    Article  CAS  Google Scholar 

  • Kang JJ, Zhao WZ, Su PX, Zho M, Yang ZH (2014) NaCl and H2SiO3 coexistence stimulates growth and improves drought resistance in the succulent xerophyte Haloxylon ammodendron. Soil Sci Plant Nutr 60(5):659–669

    Article  CAS  Google Scholar 

  • Kang JJ, Zhao WZ, Zhao M, Zheng Y, Yang F (2015) NaCl and Na2SiO3 coexistence strengthens growth of the succulent xerophyte Nitraria tangutorum under drought. Plant Growth Regul 77(2):223–232

    Article  CAS  Google Scholar 

  • Kang JJ, Zhao WZ, Zhu X (2016a) Silicon improves photosynthesis and strengthens enzyme activities in the C3 succulent xerophyte Zygophyllum xanthoxylum. J Plant Physiol 199:76–86

    Article  CAS  PubMed  Google Scholar 

  • Kang JJ, Yue LJ, Wang SM, Zhao WZ, Bao AK (2016b). Na compound fertilizer promotes growth and improves drought resistance of the succulent xerophyte Nitraria tangutorum (Bobr) after breaking seed dormancy. Soil Sci Plant Nutr 62(5–6):489–499

    Article  CAS  Google Scholar 

  • Knight MR, Anthory KC, Steven MS (1991) Transgenic plant aequorin reports the effects of touch and cold-shock and elicitors on cytoplasmic calcium. Nature 352(6335):524–526

    Article  CAS  PubMed  Google Scholar 

  • Lan T, Yang ZM (2015) The interaction of salicylic acid and Ca2+ alleviates aluminum toxicity in Glycine max. Doctoral Thesis of Jilin University, Jilin

    Google Scholar 

  • Li H, Lian HF, Liu SQ, Yu XH, Sun YL, Guo HP (2015) Effects of exogenous calcium on the growth and physiological traits of garlic seedlings under cadmium stress. J Animal Plant Sci 24(6):1193–1198

    Google Scholar 

  • Liu FL, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environ Exp Bot 54:33–40

    Article  CAS  Google Scholar 

  • Lu CM, Qiu NW, Wang BS, Zhang JH (2003) Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. J Exp Bot 54:851–860

    Article  CAS  PubMed  Google Scholar 

  • Lu SY, Li YC, Guo ZF, Li BS, Li MQ (1999) Enhancement of drought resistance of rice seedlings by calcium. Chinese J Rice Sci 13(3):161–164

    Google Scholar 

  • Luo WC, Zeng FJ, Liu B, Zhang LG, Liu Z, Song C, Peng SL, Peng HQ (2013) Photosynthetic and physiological characteristic of introduced plants at the desert-oasis ecotone. Acta Pratacul Sin 22(2):273–280

    Google Scholar 

  • Ma CC, Gao YB, Guo HY, Wang JL (2003) Interspecific transition among Caragana microphylla, C. davazamcii and C. korshinskii along geographic gradient. I. Characteristics of photosynthesis and water metabolism. Acta Bot Sin 45(10):1228–1237

    Google Scholar 

  • Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32(1):4–13

    Article  CAS  PubMed  Google Scholar 

  • Ma Q, Li YX, Yuan HJ, Hu J, Wei L, Bao AK, Zhang JL, Wang SM (2014) ZxSOS1 is essential for long-distance transport and spatial distribution of Na+ and K+ in the xerophyte Zygophyllum xanthoxylum. Plant Soil 374:661–676

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriendemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Qiu N, Lu Q, Lu CM (2003) Photosynthesis, photosystem II efficiency and the xanthophyll cycle in the salt-adapted halophyte Atriplex centralasiatica. New Phytol 159:479–486

    Article  CAS  Google Scholar 

  • Ray S, Agarwal P, Arora R, Kapoor S, Tyagi AK (2007) Expression analysis of calcium-dependent protein kinase gene family during reproductive development and abiotic stress conditions in Rice (Oryza sativa L. ssp. indica). Mol Genet Genomics 278(5):493–505

    Article  CAS  PubMed  Google Scholar 

  • Schwartz A, Lan N, Grantz DA (1988) Calcium effects on stomatal movement in Commelina communis L. Plant Physiol 37:583–587

    Article  Google Scholar 

  • Shabala S, Baekgaard L, Shabala L, Fuglsang A, Babourina O, Palmgren MG, Cuin TA, Rengel Z, Nemchinov LG (2011) Plasma membrane Ca2+ transporters mediate virus-induced acquired resistance to oxidative stress. Plant Cell Environ 34:406–417

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi SK (1997) Gene expression and signal transduction in water stress response. Plant Physiol 115:327–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slama I, Ghnaya T, Messedi D, Hessini K, Labidi N, Grignon C, Savoure A (2007) Effect of sodium chloride on the response of the halophyte species Sesuvium portulacastrum grow in mannitol-induced water stress. J Plant Res 120(2):291–299

    Article  CAS  PubMed  Google Scholar 

  • Tao DY, Wang XD, Xue Q (2006) The mensuration of eight kinds mineral matters contents of partial plants in Tarim Basin. Chin Agricul Sci Bull 4(4):127–130

    Google Scholar 

  • The Ministry of Agriculture of China (1995) The determination of soil total amount of calcium, magnesium and sodium (NY/T 296–1995)

  • Ueda A, Kanechi M, Uno Y, Inagaki N (2003) Photosynthetic limitations of a halophyte sea aster (Aster tripolium L.) under water stress and NaCl stress. J Plant Res 116(1):65–70

    CAS  PubMed  Google Scholar 

  • Wang SM, Wan CG, Wang YR, Chen H, Zhou ZY, Fu H, Sosebeeb RE (2004) The characteristics of Na+, K+ and free prolinedistribution in several drought-resistant plants of the Alxa Desert, China. J Arid Environ 56:525–539

    Article  Google Scholar 

  • Wang SM, Zhou XR, Yue LJ (2007) Na Compound Fertilizer and its application and method of application, China. Patent No. 2007100188400

  • Wu DK, Wu BH (1997) Effects of calcium on physiological and biochemical characteristics of bare barley leaves under drought stress. Tritical Crops 17(2):42–44

    Google Scholar 

  • Wu GQ, Xi JJ, Wang Q, Bao AK, Ma Q, Zhang JL, Wang SM (2011) The ZxNHX gene encoding tonoplast Na+/H+ antiporter from the xerophyte Zygophyllum xanthoxylum plays important roles in response to salt and drought. J Plant Physiol 168:758–767

    Article  CAS  PubMed  Google Scholar 

  • Xu M, You J, Hou N, Zhang H, Chen G, Yang Z (2010) Mitochondrial enzymes and citrate transporter contribute to the aluminium-induced citrate secretion from soybean (Glycine max) roots. Funct Plant Biol 37:285–295.

    Article  CAS  Google Scholar 

  • Yamauchi N, Minamide T (1985) Chlorophyll degradation by peroxidase in parsley leaves. J Jpn Soc Hort Sci 54:265–271

    Article  CAS  Google Scholar 

  • Yamauchi N, Watada AE (1994) Effectiveness of various phenolic compounds in degradation of chlorophyll by in vitro peroxidase-hydrogen peroxide system. J Jpn Soc Hort Sci 63:439–444

    Article  CAS  Google Scholar 

  • Yang Z, Zhang YY (2015) Study on the effect of Calcium to Ginseng. Master’s thesis of Chinese Academy of Agricultural Sciences

  • Yang GP, Gao XY, Jing JH (1995) Calcium can improve photosynthesis of soybean leaves under water stress. Acta Agron Sin 21(6):711–716

    Google Scholar 

  • Yang TL, Cui GX, Luo ZQ, Xiao HS (2004) Research progress of calcium on stress resistance of plant. Crop Res 5:380–384

    Google Scholar 

  • Yue LJ, Li SX, Ma Q, Zhou XR, Wu GQ, Bao AK, Zhang JL, Wang SM (2012) NaCl stimulates growth and alleviates water stress in the xerophyte Zygophyllum xanthoxylum. J Arid Environ 87:153–160

    Article  Google Scholar 

  • Yun F, Liu GS (2014) Regulation effects and mechanism of exogenous calcium salts on the flue-curred tobacco under adverse conditions of different light intensity and temperature levels. Doctoral Thesis of Henan Agricultural University

  • Zhang Y, Fang L, Li TF, Yao ZB, Feng YX, Wu YC (2002) Effect of Ca2+ on activities of some enzymes in tobacco seedling under cold stress. Chin Bull Bot 19(3):342–347

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Key Project of Chinese National Programs (973 Program) for Fundamental Research and Development (Grant No. 2013CB429903) and the Chinese National Natural Science Foundation (Grant No. Y511601001, 31360086). The authors are very grateful to the anonymous reviewers as well as editors for their critical review and comments which helped to improve and clarify the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenzhi Zhao.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 32 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kang, J., Zhao, W., Zheng, Y. et al. Calcium chloride improves photosynthesis and water status in the C4 succulent xerophyte Haloxylon ammodendron under water deficit. Plant Growth Regul 82, 467–478 (2017). https://doi.org/10.1007/s10725-017-0273-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0273-4

Keywords

Navigation