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.
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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
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
Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570
Barry CS (2009) The stay-green revolution: recent progress in deciphering the mechanisms of chlorophyll degradation in higher plants. Plant Sci 176:325–333
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
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
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
Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16
Chowdhury SR, Choudhuri MA (1986) Effects of calciumions on responses of two jute species under water deficit stress. Physiol Plant 68:86–92
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
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
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
Gruber BD, Giehl RFH, Friedel S, Von WN (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163(1):161–179
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
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
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
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
Jones RG, Lunt OR (1967) The function of calcium in plant. Bot Rev 33:407–426
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
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
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
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
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
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
Lan T, Yang ZM (2015) The interaction of salicylic acid and Ca2+ alleviates aluminum toxicity in Glycine max. Doctoral Thesis of Jilin University, Jilin
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
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
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
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
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
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
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
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
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
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
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
Schwartz A, Lan N, Grantz DA (1988) Calcium effects on stomatal movement in Commelina communis L. Plant Physiol 37:583–587
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
Shinozaki K, Yamaguchi SK (1997) Gene expression and signal transduction in water stress response. Plant Physiol 115:327–334
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
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
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
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
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
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
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.
Yamauchi N, Minamide T (1985) Chlorophyll degradation by peroxidase in parsley leaves. J Jpn Soc Hort Sci 54:265–271
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
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
Yang TL, Cui GX, Luo ZQ, Xiao HS (2004) Research progress of calcium on stress resistance of plant. Crop Res 5:380–384
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
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
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.
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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
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DOI: https://doi.org/10.1007/s10725-017-0273-4