Abstract
Key message
Elevated root zone pH and NaCl caused a similar physiological response in all species tested. This may be a result of a deliberate stunting of growth.
Abstract
Surface mining for bitumen in the Athabasca oil sands region of Northern Alberta involves the removal of all vegetation and soil from native boreal forest lands. Revegetation is challenging because reclamation sites have soils with elevated pH and NaCl levels. In the present study, trembling aspen, green alder, tamarack, and white spruce were grown in liquid culture and subjected to treatments with three pH levels (5, 7, 9) and three NaCl levels (0, 30, 60 mM) in a factorial design. After 50 days of treatment, total dry weight, gas exchange, foliar elemental, and chlorophyll concentrations were measured. Trembling aspen exhibited less than 50% survival for all pH 9 treatments, whereas green alder was sensitive to any increases in pH or NaCl. Tamarack and white spruce showed high survival and tolerance to pH levels of 9 and NaCl levels of 60 mM. However, some decreases in physiological variables were observed. All species showed decreases in total dry weight, foliar nitrogen and chlorophyll concentrations, net photosynthesis, and transpiration rates from elevated root zone pH and NaCl levels, potentially due to a deliberate downregulation of metabolism. Also, measuring chlorophyll concentration may provide a reliable indicator of seedling health. This study recommends reclamation sites with moderately high soil pH and NaCl be planted with trembling aspen, tamarack, or white spruce. Overplanting of trembling aspen may be needed to compensate for anticipated lower survival rates at pH 9. Biostimulants, such as beneficial bacteria, biochar, mycorrhizal fungi, and seaweed extracts, may be useful in reversing symptoms of plant stress.
Similar content being viewed by others
Data availability
Data for this study can be made available by the author upon request.
References
Arif Y, Singh P, Siddiqui H, Bajguz A, Hayat S (2020) Salinity induced physiological and biochemical changes in plants: an omic approach towards salt stress tolerance. Plant Physiol Biochem 156:64–77. https://doi.org/10.1016/j.plaphy.2020.08.042
Aslam M, Huffaker RC, Rains DW (1984) Early effects of salinity on nitrate assimilation in barley seedlings. Plant Physiol 76:321–325. https://doi.org/10.1104/pp.76.2.321
Berkowitz N, Speight JG (1975) The oil sands of Alberta. Fuel 54(3):138–149. https://doi.org/10.1016/0016-2361(75)90001-0
Bowman DC, Cramer GR, Devitt DA (2006) Effect of salinity and nitrogen status on nitrogen uptake by tall fescue turf. J Plant Nutr 29(8):1481–1490. https://doi.org/10.1080/01904160600837584
Busch FA (2013) Current methods for estimating the rate of photorespiration in leaves. Plant Biol 15(4):648–655. https://doi.org/10.1111/j.1438-8677.2012.00694.x
Calvo-Polanco M, Jones MD, Zwiazek JJ (2009) Effects of pH on NaCl tolerance of American elm (Ulmus americana) seedlings inoculated with Hebeloma crustuliniforme and Laccaria bicolor. Acta Physiol Plant 31(3):515–522. https://doi.org/10.1007/s11738-008-0260-5
Choi WG, Toyota M, Kim SH, Hilleary R, Gilroy S (2014) Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants. PNAS 111(17):6497–6502. https://doi.org/10.1073/pnas.1319955111
Dai Q, Chung KH (1996) Hot water extraction process mechanism using model oil sands. Fuel 75(2):220–226. https://doi.org/10.1016/0016-2361(95)00218-9
Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York
Fageria NK, Dos Santos AB, Moraes MF (2010) Influence of urea and ammonium sulfate on soil acidity indices in lowland rice production. Commun Soil Sci Plant Anal 41(13):1565–1575. https://doi.org/10.1080/00103624.2010.485237
Franklin JA, Renault S, Croser C, Zwiazek JJ, MacKinnon M (2002a) Jack pine growth and elemental composition are affected by saline tailings water. J Environ Qual 31(2):648–653. https://doi.org/10.2134/jeq2002.6480
Franklin JA, Zwiazek JJ, Renault S, Croser C (2002b) Growth and elemental composition of jack pine (Pinus banksiana) seedlings treated with sodium chloride and sodium sulfate. Trees 16(4):325–330. https://doi.org/10.1007/s00468-002-0175-5
Gangwar P, Singh R, Trivedi M, Tiwari RK (2020) Sodic soil: management and reclamation strategies. Environmental concerns and sustainable development. Springer, Singapore, pp 175–190
Geilfus C (2017) The pH of the apoplast: dynamic factor with functional impact under stress. Mol Plant 10(11):1371–1386. https://doi.org/10.1016/j.molp.2017.09.018
Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171(3):1606–1615. https://doi.org/10.1104/pp.16.00434
Government of Alberta (2010) Environmental Protection and Enhancement Act (Chapter E-13. 3). Queen’s printer, Government of Alberta, Edmonton, AB, p 152
Griffin TS (2008) Nitrogen availability. In: Schepers JS, Raun W (eds) Nitrogen in agricultural systems. ASA-CSSA-SSSA, Madison, pp 613–646
Hawkins HJ, Lewis OAM (1993) Effect of NaCl salinity, nitrogen form, calcium and potassium concentration on nitrogen uptake and kinetics in Triticum aestivum L. cv. ‘Gamtoos.’ New Phytol 124:171–177. https://doi.org/10.1111/j.1469-8137.1993.tb03807.x
Howat D (2000) Acceptable salinity, sodicity and pH values for boreal forest reclamation. Alberta Environment, Environmental Sciences Division, Edmonton, Alberta. Report # ESD/LM/00-2. ISBN 0-7785-1173-1
Hundare A, Joshi V, Joshi N (2022) Salicylic acid attenuates salinity-induced growth inhibition in in vitro raised ginger (Zingiber officinale Roscoe) plantlets by regulating ionic balance and antioxidative system. Plant Stress. https://doi.org/10.1016/j.stress.2022.100070
Jiang K, Moe-Lange J, Hennet L, Feldman LJ (2016) Salt stress affects the redox status of Arabidopsis root meristems. Front Plant Sci 7:81. https://doi.org/10.3389/fpls.2016.00081
Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20(9):586–594. https://doi.org/10.1016/j.tplants.2015.06.008
Kamaluddin M, Zwiazek JJ (2004) Effects of root medium pH on water transport in paper birch (Betula papyrifera) seedlings in relation to root temperature and abscisic acid treatments. Tree Physiol 24(10):1173–1180. https://doi.org/10.1093/treephys/24.10.1173
Kessler S, Barbour SL, Van Rees KC, Dobchuk BS (2010) Salinization of soil over saline-sodic overburden from the oil sands in Alberta. Can J Soil Sci 90(4):637–647. https://doi.org/10.4141/cjss10019
Kosegarten H, Hoffmann B, Mengel K (2001) The paramount influence of nitrate in increasing apoplastic pH of young sunflower leaves to induce Fe deficiency chlorosis, and the re-greening effect brought about by acidic foliar sprays. J Plant Nutr Soil Sci 164(2):155–163. https://doi.org/10.1002/1522-2624(200104)164:2%3C155::AID-JPLN155%3E3.0.CO;2-F
Kumagai E, Araki T, Hamaoka N, Ueno O (2011) Ammonia emission from rice leaves in relation to photorespiration and genotypic differences in glutamine synthetase activity. Ann Bot 108(7):1381–1386. https://doi.org/10.1093/aob/mcr245
Lauer N (2022) Recovery of trembling aspen, tamarack, and white spruce seedlings from NaCl stress following winter dormancy: implications for increased foliar potassium, necrosis, and sodium management as stress resistance mechanisms. Trees 36(5):1633–1648. https://doi.org/10.1007/s00468-022-02318-9
Lauer N (2023) Linking whole-plant responses to cell physiology in glycophyres exposed to NaCl stress. Acta Physiol Plant 45(2):36. https://doi.org/10.1007/s11738-023-03515-w
LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89(2):371–379. https://doi.org/10.1890/06-2057.1
Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69(1):1–24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Legendre P, Legendre L (2012) Redundancy analysis (RDA). Numerical ecology. Elsevier, Québec, Canada, pp 579–594
Mace JE, Amrhein C, Oster JD (1999) Comparison of gypsum and sulfuric acid for sodic soil reclamation. Arid Soil Res Rehabil 13(2):171–188. https://doi.org/10.1080/089030699263401
Masliyah J, Zhou ZJ, Xu Z, Czarnecki J, Hamza H (2004) Understanding water-based bitumen extraction from Athabasca oil sands. Can J Chem Eng 82(4):628–654. https://doi.org/10.1002/cjce.5450820403
Maynard DG, Mallett KI, Myrholm CL (1997) Sodium carbonate inhibits emergence and growth of greenhouse-grown white spruce. Can J Soil Sci 77(1):99–105. https://doi.org/10.4141/S96-048
Miller GW, Pushnik JC, Welkie GW (1984) Iron chlorosis, a world-wide problem, the relation of chlorophyll biosynthesis to iron. J Plant Nutr 7(1–5):1–22. https://doi.org/10.1080/01904168409363172
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Muñoz-Huerta RF, Guevara-Gonzalez RG, Contreras-Medina LM, Torres-Pacheco I, Prado-Olivarez J, Ocampo-Velazquez RV (2013) A review of methods for sensing the nitrogen status in plants: advantages, disadvantages and recent advances. Sensors 13(8):10823–10843. https://doi.org/10.3390/s130810823
Oster JD (1982) Gypsum usage in irrigated agriculture: a review. Fertil Res 3(1):73–89. https://doi.org/10.1007/BF01063410
Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349. https://doi.org/10.1016/j.ecoenv.2004.06.010
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22(6):4056–4075. https://doi.org/10.1007/s11356-014-3739-1
Pei ZM, Murata Y, Benning G, Thomine S, Klüsener B, Allen GJ, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734. https://doi.org/10.1038/35021067
Reddy MP, Vora AB (1986) Changes in pigment composition, Hill reaction activity and saccharides metabolism in Bajra (Pennisetum typhoides S and H) leaves under NaCl salinity. Photosynthetica (praha) 20(1):50–55
Renault S (2005) Tamarack response to salinity: effects of sodium chloride on growth and ion, pigment, and soluble carbohydrate levels. Can J for Res 35(12):2806–2812. https://doi.org/10.1139/x05-194
Renault S, Paton E, Nilsson G, Zwiazek JJ, MacKinnon MD (1999) Responses of boreal plants to high salinity oil sands tailings water. J Environ Qual 28(6):1957–1962. https://doi.org/10.2134/jeq1999.00472425002800060035x
Rhoades C, Oskarsson H, Binkley D, Stottlemyer B (2001) Alder (Alnus crispa) effects on soils in ecosystems of the Agashashok River Valley, Northwest Alaska. Ecoscience 8(1):89–95. https://doi.org/10.1080/11956860.2001.11682634
Rodakowska E et al (2009) Signaling and Cell Walls. In: Mancuso S, Baluka F (eds) Signaling in plants signaling and communication in plants. Springer, Berlin, Heidelberg
Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hortic 103(1):93–99. https://doi.org/10.1016/j.scienta.2004.04.009
Sestak Z, Catský J, Jarvis PG (1971) Plant photosynthetic production. Manual of methods. Dr. W. Junk Publishers, The Hague
Shabala S, Munns R (2012) Salinity stress: physiological constraints and adaptive mechanisms. Plant Stress Physiol 1(1):59–93. https://doi.org/10.1079/9781780647296.0024
Sible CN, Seebauer JR, Below FE (2021) Plant biostimulants: a categorical review, their implications for row crop production, and relation to soil health indicators. Agronomy 11(7):1297
Siemens JA, Zwiazek JJ (2011) Hebeloma crustuliniforme modifies root hydraulic responses of Trembling aspen (Populus tremuloides) seedlings to changes in external pH. Plant Soil 345(1–2):247–256. https://doi.org/10.1007/s11104-011-0776-0
Sinfield JV, Fagerman D, Colic O (2010) Evaluation of sensing technologies for on-the-go detection of macro-nutrients in cultivated soils. Comput Electron Agric 70(1):1–18. https://doi.org/10.1016/j.compag.2009.09.017
Solis CA, Yong MT, Venkataraman G, Milham P, Zhou M, Shabala L, Chen ZH (2021) Sodium sequestration confers salinity tolerance in an ancestral wild rice. Physiol Plant 172(3):1594–1608. https://doi.org/10.1111/ppl.13352
Sukhov V (2016) Electrical signals as mechanism of photosynthesis regulation in plants. Photosynth Res 130(1–3):373–387. https://doi.org/10.1007/s11120-016-0270-x
Sukhov V, Sukhova E, Vodeneev V (2019) Long-distance electrical signals as a link between the local action of stressors and the systemic physiological responses in higher plants. Prog Biophys Mol Biol 146:63–84. https://doi.org/10.1016/j.pbiomolbio.2018.11.009
Svitsev MV, Ponnamoreva SA, Kuznetsova EA (1973) Effect of salinization and herbicides on chlorophyllase activity in tomato leaves. Fiziol Rastenii 20(1):62–65. https://doi.org/10.1016/j.tplants.2009.11.009
Tang C, Zheng SJ, Qiao YF, Wang GH, Han XZ (2006) Interactions between high pH and iron supply on nodulation and iron nutrition of Lupinus albus L. genotypes differing in sensitivity to iron deficiency. Plant Soil 279(1–2):153–162. https://doi.org/10.1007/s11104-005-0616-1
Tenhaken R (2015) Cell wall remodeling under abiotic stress. Front Plant Sci 5:771. https://doi.org/10.3389/fpls.2014.00771
Tremblay N, Fallon E, Ziadi N (2011) Sensing of crop nitrogen status: Opportunities, tools, limitations, and supporting information requirements. HortTechnology 21(3):274–281. https://doi.org/10.21273/HORTTECH.21.3.274
Volkmar KM, Hu Y, Steppuhn H (1998) Physiological responses of plants to salinity: a review. Can J Plant Sci 78(1):19–27. https://doi.org/10.4141/P97-020
Ward MR, Asiam M, Huffaker RC (1986) Enhancement of nitrate uptake and growth of barley seedlings by calcium under saline conditions. Plant Physiol 80:520–524. https://doi.org/10.1104/pp.80.2.520
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25(2):195–210. https://doi.org/10.1046/j.0016-8025.2001.00824.x
Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B Biol Sci 355(1402):1517–1529. https://doi.org/10.1098/rstb.2000.0712
Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47(1):79–86. https://doi.org/10.1007/s11099-009-0013-8
Zarcinas BA, Cartwright B, Spouncer LR (1987) Nitric acid digestion and multi-element analysis of plant material by inductively coupled plasma spectrometry. Soil Sci Plant Anal 18(1):131–146. https://doi.org/10.1080/00103628709367806
Zhang W, Zwiazek JJ (2016) Effects of root medium pH on root water transport and apoplastic pH in red-osier dogwood (Cornus sericea) and paper birch (Betula papyrifera) seedlings. Plant Biol 18(6):1001–1007. https://doi.org/10.1111/plb.12483
Zhang W, Calvo-Polanco M, Chen ZC, Zwiazek JJ (2013) Growth and physiological responses of Trembling aspen (Populus tremuloides), White spruce (Picea glauca) and Tamarack (Larix laricina) seedlings to root zone pH. Plant Soil 373(1–2):775–786. https://doi.org/10.1007/s11104-013-1843-5
Acknowledgements
I am grateful to Dr. Simon Landhäusser and Dr. Barb Thomas for providing feedback during the initial document drafting stages. I am also thankful for the help and support from lab members, including Ale Equiza, Seong Hee Lee, Wenquing Zhang, Frank Tan, Deyu Mu, Hao Xu, and Samantha Olivier. This research was funded by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC) and Total E&P Canada Ltd.
Funding
This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) and Total E&P Canada Ltd and Canadian Network for Research and Innovation in Machining Technology.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares no competing interests.
Additional information
Communicated by Baoshan Wang .
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lauer, N. Elevated root zone pH and NaCl leads to decreased foliar nitrogen, chlorophyll, and physiological performance in trembling aspen (Populus tremuloides), green alder (Alnus alnobetula), tamarack (Larix laricina), and white spruce (Picea glauca). Trees 37, 1041–1054 (2023). https://doi.org/10.1007/s00468-023-02404-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-023-02404-6