Skip to main content
Log in

Exogenous application of Ca2+ mitigates simulated acid rain stress on soybean productivity and quality by maintaining nutrient absorption

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Acid rain is a global environmental problem that threatens agricultural production. Calcium (Ca), as a signal substance for physiological activities, has been known to regulate plant growth under abiotic stresses. To clarify whether calcium could be one of possible ways to alleviate the reduction caused by acid rain in agricultural production and investigate its regulating mechanism on adaptation of plants under acid rain stress, we studied the effect of exogenous Ca2+ (5 mM CaCl2) on growth of soybean at different growth stages (seedling, flowering-podding, and filling stages) as well as yield and grain quality of soybean under simulated acid rain (pH 4.5 or pH 3.0) stress. We found that the application of Ca2+ could regulate the activity of plasma membrane H+-ATPase, for mitigating the increase of ammonium and the decrease of nitrate and phosphorus in soybean roots, which mitigated the inhibition on growth and improved the yield and grain quality of soybean under simulated acid rain stress. In addition, the alleviating effect of exogenous Ca2+ on soybean was the most significant at seedling stage. The results indicate that the exogenous Ca2+ could enhance the adaptation of soybean and facilitate the recovery of soybean productivity and grain quality under simulated acid rain stress by maintaining the uptake of nitrate, ammonium, and phosphorus.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbasi T, Poornima P, Kannadasan T, Abbasi SA (2013) Acid rain: past, present, and future. Int J Environmental Engineering 5:229–272

    Article  Google Scholar 

  • Baginski ES, Foa PP, Zak B (1967) Determination of phosphate: study of labile organic phosphate interference. Clin Chim Acta 15:155–158

    Article  CAS  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529

    Article  CAS  Google Scholar 

  • Blanpain JP, Ronjat M, Supply P, Dufour JP, Goffeau A, Dupont Y (1992) The yeast plasma membrane H+-ATPase. An essential change of conformation triggered by H+. J Biol Chem 267:3735–3740

    CAS  Google Scholar 

  • Bradford M (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  Google Scholar 

  • Bradstreet RB (1965) Kjeldahl method for organic nitrogen. Anal Chem 26:169–234

    Google Scholar 

  • Carvalho RDSC, Bastos RG, Souza CF (2018) Influence of the use of wastewater on nutrient absorption and production of lettuce grown in a hydroponic system. Agric Water Manag 203:311–321

    Article  Google Scholar 

  • Castro LD, Priego-Capote F (2010) Soxhlet extraction: past and present panacea. J Chromatogr A 1217:2383–2389

    Article  CAS  Google Scholar 

  • Chen J, Li W, Gao F (2010) Biogeochemical effects of forest vegetation on acid precipitation-related water chemistry: a case study in Southwest China. J Environ Monit 12:1799

    Article  CAS  Google Scholar 

  • Chen GF, Huang YY, Xiong LM, Liu B, Liu YX (2013) Effect of calcium fertilizer on the fruit yield and quality of Chuntian tangerine. J South Agric 85:87–98

    Google Scholar 

  • Farooq M, Aziz T, Basra SMA, Wahid A, Khaliq A, Cheema MA (2010) Exploring the role of calcium to improve chilling tolerance in hybrid maize. J Agron Crop Sci 194:350–359

    Article  Google Scholar 

  • Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818

    Article  CAS  Google Scholar 

  • Grossman YL, Dejong TM (1994) PEACH: a simulation model of reproductive and vegetative growth in peach trees. Tree Physiol 14:329–345

    Article  CAS  Google Scholar 

  • Han X (2003) Effects of various soil moisture on the yield of soybean. Soybean Sci 22:269–272

    Google Scholar 

  • Haruta M, Tan LX, Bushey DB, Swanson SJ, Sussman MR (2017) Environmental and genetic factors regulating localization of the plant plasma membrane H+-ATPase. Plant Physiol 176:364–377

    Article  CAS  Google Scholar 

  • Hirschi KD (2004) The calcium conundrum. Both versatile nutrient and specific signal. Plant Physiol 136:2438–2442

    Article  CAS  Google Scholar 

  • Hlawiczka S, Korszun K (2012) The effect of particulate matter components on the acidity of rain in upper Silesia (Poland). Acta Hydrochim Hydrobiol 40:673–680

    CAS  Google Scholar 

  • Hlawiczka S, Dyduch B, Fudala J (2003) Long-term changes of particulate emission in the industrial region of upper Silesia (Poland) and their effect on the acidity of rainwater. Water Air Soil Pollut 142:151–163

    Article  CAS  Google Scholar 

  • Hong Wen XU, Song FB, Zhu XC, Tong SY (2009) Analysis on chlorophyll fluorescence of husk leaves of maize at different growing stages. Acta Agric Boreali Sinica 24:74–77

    Google Scholar 

  • Jia R, Lei MQ, Xu JN, Lu RQ, Huang X (2014) Research progress of Ca2+ channel and the effect of Ca2+ on plant resistance mechanism in plant cells. Plant Physiol J 50:1791–1800

    CAS  Google Scholar 

  • Jiang T, Zhan X, Xu Y, Zhou L, Zong L (2005) Roles of calcium in stress-tolerance of plants and its ecological significance. Chin J Appl Ecol 16:971–976

    CAS  Google Scholar 

  • Kłobus G, Buczek J (1995) The role of plasma membrane oxidoreductase activity in proton transport. J Plant Physiol 146:103–107

    Article  Google Scholar 

  • Larssen T, Lydersen E, Tang DG, He Y, Gao JX, Liu HY, Duan L, Seip HM, Vogt RD, Mulder J, Shao M, Wang YH, Shang H, Zhang XS, Solberg S, Aas W, Okland T, Eilertsen O, Angell V, Liu QR, Zhao DW, Xiang RJ, Xiao JS, Luo JH (2006) Acid rain in China. Environ Sci Technol 40:418–425

    Article  CAS  Google Scholar 

  • Larssen T, Lydersen E, Tang D, He Y, Gao J, Liu H, Duan L, Seip HM, Vogt RD, Mulder J (2007) Acid rain in China. Environ Sci Technol 40:418–425

    Article  Google Scholar 

  • Li C (2006) Study of the influence of shading stress to yield and yield characters of soybean. Soybean Sci 25:294–298

    CAS  Google Scholar 

  • Li YS, Ming D, Zhang QY, Wang GH, Hashemi M, Liu XB (2012) Greater differences exist in seed protein, oil, total soluble sugar and sucrose content of vegetable soybean genotypes [Glycine max (L.) Merrill] in Northeast China. Aust J Crop Sci 6:1681–1686

    CAS  Google Scholar 

  • Li SP, Bi YL, Chen PZ, Liu S, Zhang J, Zhou J, Gao F (2013) Influence of exogenous calcium on the growth of maize under arid-stress in mine area. J China Univ Min Technol 42:477–482

    Google Scholar 

  • Liang C, Zhang B (2018) Effect of exogenous calcium on growth, nutrients uptake and plasma membrane H+-ATPase and Ca2+-ATPase activities in soybean (Glycine max) seedlings under simulated acid rain stress. Ecotoxicol Environ Saf 165:261–269

    Article  CAS  Google Scholar 

  • Liu YL (2011) Effects of water stress on plasma membrane permeability and protective enzyme activities of red pine seedlings needles. Bull Bot Res 31:49–55

    CAS  Google Scholar 

  • Liu H, Ren X, Zhu J, Wu X, Liang C (2018) Effect of exogenous abscisic acid on morphology, growth and nutrient uptake of rice (Oryza sativa) roots under simulated acid rain stress. Planta 248:647–659

    Article  CAS  Google Scholar 

  • Lüthje S, Möller B, Perrineau FC, Wöltje K (2013) Plasma membrane electron pathways and oxidative stress. Antioxid Redox Signal 18:2163–2183

    Article  CAS  Google Scholar 

  • Marschnert H, Kirkby EA, Engels C (2015) Importance of cycling and recycling of mineral nutrients within plants for growth and development. Plant Biol 110:265–273

    Google Scholar 

  • Menz FC, Seip HM (2004) Acid rain in Europe and the United States: an update. Environ Sci Pol 7:253–265

    Article  CAS  Google Scholar 

  • Michelet B, Boutry M (1995) The plasma membrane H+-ATPase (a highly regulated enzyme with multiple physiological functions). Plant Physiol 108(1):1–6

    Article  CAS  Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71

    Article  CAS  Google Scholar 

  • Okumura M, Takahashi K, Inoue SI, Kinoshita T (2012) Evolutionary appearance of the plasma membrane H+-ATPase containing a penultimate threonine in the bryophyte. Plant Signal Behav 7:979–982

    Article  CAS  Google Scholar 

  • Ou LJ, Liu ZB, Zhang YP, Zou XX, Ou LJ, Liu ZB, Zhang YP, Zou XX (2017) Effects of exogenous Ca2+ on photosynthetic characteristics and fruit quality of pepper under waterlogging stress. Chil J Agric Res 77:126–133

    Article  Google Scholar 

  • Oufattole MM, Boutry M (2000) Identification and expression of three new Nicotiana plumbaginifolia genes which encode isoforms of a plasma-membrane H+-ATPase, and one of which is induced by mechanical stress. Planta 210:715–722

    Article  CAS  Google Scholar 

  • Porto BN, Alves JD, Magalhães PC, Castro EM, Campos NA, Souza KRD, Magalhães MM, Andrade CA, Santos MO (2013) Calcium-dependent tolerant response of cell wall in maize mesocotyl under flooding stress. J Agron Crop Sci 199:134–143

    Article  CAS  Google Scholar 

  • Raja R, Ravisankar N, Chaudhari SG, Ambast SK, Chand S, Din M, Meena B, Subramani T, Ahmed Z (2012) Effect of supplemental irrigation on yield and water productivity of dry season crops in Andaman and Nicobar Islands. Indian J Agric Sci 82:15–20

    Google Scholar 

  • Ramlall C, Varghese B, Ramdhani S, Pammenter NW, Bhatt A, Berjak P, Sershen (2015) Effects of simulated acid rain on germination, seedling growth and oxidative metabolism of recalcitrant-seeded Trichilia dregeana grown in its natural seed bank. Physiol Plant 153:149–160

    Article  CAS  Google Scholar 

  • Roseli ANM, Tsan FY (2018) Vegetative and reproductive growth behaviour of Xanthostemon chrysanthus (F. Muell.) Benth. – an ornamental tree in Malaysia. Sains Malaysiana 47:227–233

  • Scheiner D (1976) Determination of ammonia and Kjeldahl nitrogen by indophenol method. Water Res 10:31–36

    Article  CAS  Google Scholar 

  • Simeunovic A, Mair A, Wurzinger B, Teige M (2016) Know where your clients are: subcellular localization and targets of calcium-dependent protein kinases. J Exp Bot 67:3855–3872

    Article  CAS  Google Scholar 

  • Singh A, Sagar S, Biswas DK (2018) Calcium dependent protein kinase, a versatile player in plant stress management and development. Crit Rev Plant Sci 36:336–352

    Article  Google Scholar 

  • Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482

    Article  CAS  Google Scholar 

  • Sonoda Y, Hara T (1983) Comparison of micronutrient uptake among crop plants under saline soil conditions (part 2): effects of Ca salinity and pH of soil on growth and micronutrient uptake of crop plants. Res Bull Fac Agric Gifu Univ (Japan) 48:95–100

    Google Scholar 

  • Sumner JB (1944) A method for the colorimetric determination of phosphorus. Science 100:413–414

    Article  CAS  Google Scholar 

  • Sun Z, Wang L, Zhou Q, Huang X (2013) Effects and mechanisms of the combined pollution of lanthanum and acid rain on the root phenotype of soybean seedlings. Chemosphere 93:344

    Article  CAS  Google Scholar 

  • Sun Q, Jie H, Xiaojing WU, Jiang H, Qin Z (2016) Effect of different acidities of acid rain on nitrogen and sulfur metabolism and grain protein levels in wheat after anthesis. Acta Ecol Sin 36:190–199

    Article  Google Scholar 

  • Tang Y, Li-Jun LI, Liu P, Bai GJ (2018) Effects of irrigation and fertilization on nutrient absorption and yield of cucumber and soil quality in greenhouse. Soil Fertil Sci in China 1:77–82

    Google Scholar 

  • Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants : protective role of exogenous polyamines. Plant Sci 151:59–66

    Article  CAS  Google Scholar 

  • Wang Q, Xu C (2005) Affects of nitrogen and phosphorus on plant leaf photosynthesis and carbon partitioning. J Shandong For Sci Technol 160:59–62

    Google Scholar 

  • Wang H, Qiuzhu LI, Zhao H, Wei Y, Pan J (2007) Effect of drought treatment at different growth stages on activity of protective enzyme and yield in spring maize. J Northeast Agric Univ 38:13–17

    CAS  Google Scholar 

  • Wei G (2011) The role of Ca2+ in plant response to abiotic stress. Chem Life 31:107–111

    Google Scholar 

  • Wen K, Liang C, Wang L, Hu G, Zhou Q (2011) Combined effects of lanthanum ion and acid rain on growth, photosynthesis and chloroplast ultrastructure in soybean seedlings. Chemosphere 84:601–608

    Article  CAS  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  CAS  Google Scholar 

  • Wu X, Liang C (2017) Enhancing tolerance of rice (Oryza sativa) to simulated acid rain by exogenous abscisic acid. Environ Sci Pollut Res:1–11

  • Yin Y, Yang R, Han Y, Gu Z (2015) Comparative proteomic and physiological analyses reveal the protective effect of exogenous calcium on the germinating soybean response to salt stress. J Proteome 113:110–126

    Article  CAS  Google Scholar 

  • Yu H, Chen J, Wang X (2001) Effects of salt stress on the activity and the amount of tonoplast H+-ATPase from pea roots. Acta Bot Sin 43:586–591

    CAS  Google Scholar 

  • Zhang JL, Guo F, Meng JJ, Xiao-Xia YU, Yang S, Zhang SB, Geng Y, Xin-Guo LI, Wan SB, Center B (2015) Effects of calcium fertilizer on yield, quality and related enzyme activities of peanut in acidic soil. Chin J Plant Ecol 39:1101–1109

    Article  Google Scholar 

  • Zhang B, Bu J, Liang C (2016a) Root morphology and growth regulated by mineral nutrient absorption in rice roots exposed to simulated acid rain. Water Air Soil Pollut 227:457

    Article  CAS  Google Scholar 

  • Zhang QH, Xiao L, Yu-Huan SU, Liu BH (2016b) Research progress on the impacts of acid rain on wheat. J Hebei Agric Sci 20:97–99

    CAS  Google Scholar 

  • Zhang B, Bu J, Liang C (2017a) Regulation of nitrogen and phosphorus absorption by plasma membrane H+-ATPase in rice roots under simulated acid rain. Int J Environ Sci Technol 14:1–12

    Article  CAS  Google Scholar 

  • Zhang J, Wei J, Li D, Kong X, Rengel Z, Chen L, Yang Y, Cui X, Chen Q (2017b) The role of the plasma membrane H+-ATPase in plant responses to aluminum toxicity. Front Plant Sci 8:1757 jbc.RA117.000128

    Article  Google Scholar 

  • Zhang F, Hu H, Wang L, Zhou Q, Huang X (2018) Effects of rare earth and acid rain pollution on plant chloroplast ATP synthase and element contents at different growth stages. Chemosphere 194:441–449

    Article  CAS  Google Scholar 

  • Zhao W, Zhang J, Müller C, Cai Z (2018) Effects of pH and mineralisation on nitrification in a subtropical acid forest soil. Soil Res 56:275–283

    Article  CAS  Google Scholar 

Download references

Funding

The authors are grateful for the financial support provided by the National Natural Science Foundation of China (31000245, 31370517) and the Natural Science Foundation of Jiangsu Province (No. BK20161131).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chanjuan Liang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Responsible editor: Gangrong Shi

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Liang, C. Exogenous application of Ca2+ mitigates simulated acid rain stress on soybean productivity and quality by maintaining nutrient absorption. Environ Sci Pollut Res 26, 4975–4986 (2019). https://doi.org/10.1007/s11356-018-4034-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-4034-3

Keywords