Abstract
Purpose
Calcium (Ca2+) is a major structural plant nutrient whose low mobility in the phloem causes deleterious nutritional disorders in non-transpiring organs. Since strontium (Sr2+) and Ca2+ share many chemical properties, Sr2+ is frequently used as a tracer to study Ca2+ cycles in ecosystems. However, the level of agreement between Sr2+ and Ca2+ distribution pattern in plants is debatable, and several studies have reported toxic effects of Sr2+. Therefore, we investigated Sr2+ and Ca2+ uptake rates and distribution pattern to determine how reliably Sr2+ can be used as a tracer of Ca2+ in tomato plants (Solanum lycopersicum L.).
Methods
We conducted six independent experiments of various duration: from a few hours to several weeks, in hydroponic and perlite substrate. We treated plants with either Ca2+ or Sr2+ at equivalent concentrations and monitored their accumulation in shoot and fruits.
Results
Under short-term exposure (hours), Ca2+ and Sr2+ uptake and distribution within the plant were comparable, while the long-term exposure (days and weeks) to 4 mM Sr2+ reduced transpiration and biomass accumulation. The toxic effect of Sr2+ was more prominent when growth conditions were favourable. Nonetheless, Sr2+ accumulated similarly to Ca2+ in shoot and fruit. Surprisingly, Sr2+ deposition in tomato fruit cell walls prevented blossom end rot (BER) to the same degree as Ca2+.
Conclusion
Sr2+ can credibly be used as a tracer of Ca2+ uptake and allocation in the short-term, making Sr2+ a powerful tool to study the factors governing Ca2+ allocation to plant organs, primarily fruit Ca2+ delivery.
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Availability of data and material
The datasets generated during and/or analysed during the current study are available from the corresponding author on a reasonable request.
Code availability
Not relevant to the study.
References
Åberg G, Jacks G, Wickman T, Hamilton PJ (1990) Strontium isotopes in trees as an indicator for calcium availability. CATENA 17:1–11. https://doi.org/10.1016/0341-8162(90)90011-2
Achary VMM, Parinandi NL, Panda BB (2013) Mutation Research / Genetic Toxicology and Environmental Mutagenesis Calcium channel blockers protect against aluminium-induced DNA damage and block adaptive response to genotoxic stress in plant cells. Mutat Res - Genet Toxicol Environ Mutagen 751:130–138. https://doi.org/10.1016/j.mrgentox.2012.12.008
Anthon GE, Barrett DM (2006) Characterization of the temperature activation of pectin methylesterase in green beans and tomatoes. J Agric Food Chem 54:204–211. https://doi.org/10.1021/jf051877q
Bowen HJM, Dymond JA (1956) The Uptake of Calcium and Strontium by Plants from Soils and Nutrient Solutions. J Exp Bot 7:264–272. http://www.jstor.org/stable/23686486
Brambilla M, Fortunati P, Carini F (2002) Foliar and root uptake of 134Cs, 85Sr and 65Zn in processing tomato plants (Lycopersicon esculentum Mill.). J Environ Radioact 60:351–363. https://doi.org/10.1016/S0265-931X(01)00109-6
Burger A, Lichtscheidl I (2019) Strontium in the environment: Review about reactions of plants towards stable and radioactive strontium isotopes. Sci Total Environ 653:1458–1512. https://doi.org/10.1016/j.scitotenv.2018.10.312
Burger A, Weidinger M, Adlassnig W et al (2019a) Response of Plantago major to cesium and strontium in hydroponics: Absorption and effects on morphology, physiology and photosynthesis. Environ Pollut 254:113084. https://doi.org/10.1016/j.envpol.2019.113084
Burger A, Weidinger M, Adlassnig W et al (2019b) Response of Arabidopsis halleri to cesium and strontium in hydroponics: Extraction potential and effects on morphology and physiology. Ecotoxicol Environ Saf 184:109625. https://doi.org/10.1016/j.ecoenv.2019.109625
Capo RC, Stewart BW, Chadwick OA (1998) Strontium isotopes as tracers of earth surface processes: theory and methods. Geoderma 82:197–225
Coelho I, Castanheira I, Bordado JM et al (2017) Recent developments and trends in the application of strontium and its isotopes in biological related fields. TrAC - Trends Anal Chem 90:45–61. https://doi.org/10.1016/j.trac.2017.02.005
Dasch AA, Blum JD, Eagar C et al (2006) The relative uptake of Ca and Sr into tree foliage using a whole-watershed calcium addition. Biogeochemistry 80:21–41. https://doi.org/10.1007/s10533-005-6008-z
de Freitas ST, do Amarante CV, Labavitch JM, Mitcham EJ (2010) Cellular approach to understand bitter pit development in apple fruit. Postharvest Biol Technol 57:6–13. https://doi.org/10.1016/j.postharvbio.2010.02.006
de Freitas ST, Handa AK, Wu Q et al (2012a) Role of pectin methylesterases in cellular calcium distribution and blossom-end rot development in tomato fruit. Plant J 71:824–835. https://doi.org/10.1111/j.1365-313X.2012.05034.x
de Freitas ST, Jiang CZ, Mitcham EJ (2012b) Mechanisms Involved in Calcium Deficiency Development in Tomato Fruit in Response to Gibberellins. J Plant Growth Regul 31:221–234. https://doi.org/10.1007/s00344-011-9233-9
de Freitas ST, Mitcham EJ (2012) Factors involved in fruit calcium deficiency disorders. Hortic Rev (am Soc Hortic Sci) 40:107–146. https://doi.org/10.1002/9781118351871.ch3
Demidchik V, Davenport RJ, Tester M (2002) Nonselective cation channels in plants. Annu Rev Plant Biol 53:67–107. https://doi.org/10.1146/annurev.arplant.53.091901.161540
Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: From salt stress to signalling and development. New Phytol 175:387–404. https://doi.org/10.1111/j.1469-8137.2007.02128.x
Demidchik V, Shabala S, Isayenkov S et al (2018) Calcium transport across plant membranes: mechanisms and functions. New Phytol 220:49–69. https://doi.org/10.1111/nph.15266
Drouet T, Herbauts J (2008) Evaluation of the mobility and discrimination of Ca, Sr and Ba in forest ecosystems: Consequence on the use of alkaline-earth element ratios as tracers of Ca. Plant Soil 302:105–124. https://doi.org/10.1007/s11104-007-9459-2
Drouet T, Herbauts J, Gruber W, Demaiffe D (2005) Strontium isotope composition as a tracer of calcium sources in two forest ecosystems in Belgium. Geoderma 126:203–223. https://doi.org/10.1016/j.geoderma.2004.09.010
Gerasopoulos D, Drogoudi PD (2005) Summer-pruning and preharvest calcium chloride sprays affect storability and low temperature breakdown incidence in kiwifruit. Postharvest Biol Technol 36:303–308. https://doi.org/10.1016/j.postharvbio.2005.01.005
Gilliham M, Dayod M, Hocking BJ et al (2011) Calcium delivery and storage in plant leaves: Exploring the link with water flow. J Exp Bot 62:2233–2250. https://doi.org/10.1093/jxb/err111
González-Fontes A, Navarro-Gochicoa MT, Ceacero CJ et al (2017) Understanding calcium transport and signaling, and its use efficiency in vascular plants. Elsevier Inc
Gould JM, Sternglass EJ, Sherman JD et al (2000) Strontium-90 in deciduous teeth as a factor in early childhood cancer. Int J Heal Serv 30:515–539. https://doi.org/10.2190/FTL4-HNG0-BELK-5EMH
Hagassou D, Francia E, Ronga D, Buti M (2019) Blossom end-rot in tomato (Solanum lycopersicum L.): A multi-disciplinary overview of inducing factors and control strategies. Sci Hortic (amsterdam) 249:49–58. https://doi.org/10.1016/j.scienta.2019.01.042
Ho LC, White PJ (2005) A cellular hypothesis for the induction of blossom-end rot in tomato fruit. Ann Bot 95:571–581. https://doi.org/10.1093/aob/mci065
Hocking B, Tyerman SD, Burton RA, Gilliham M (2016) Fruit Calcium: Transport and Physiology. Front Plant Sci 7:569. https://doi.org/10.3389/fpls.2016.00569
Kalcsits L, van der Heijden G, Reid M, Mullin K (2017) Calcium absorption during fruit development in ‘honeycrisp’ apple measured using 44ca as a stable isotope tracer. HortScience 52:1804–1809. https://doi.org/10.21273/HORTSCI12408-17
Kanter U, Hauser A, Michalke B et al (2010) Caesium and strontium accumulation in shoots of Arabidopsis thaliana: Genetic and physiological aspects. J Exp Bot 61:3995–4009. https://doi.org/10.1093/jxb/erq213
Katayama H, Banba N, Sugimura Y et al (2013) Subcellular compartmentation of strontium and zinc in mulberry idioblasts in relation to phytoremediation potential. Environ Exp Bot 85:30–35. https://doi.org/10.1016/j.envexpbot.2012.06.001
Kondo K, Kawabata H, Ueda S et al (2003) Distribution of aquatic plants and absorption of radionuclides by plants through the leaf surface in brackish Lake Obuchi, Japan, bordered by nuclear fuel cycle facilities. J Radioanal Nucl Chem 257:305–312. https://doi.org/10.1023/A:1024775511376
Kumar A, Singh UM, Manohar M, Gaur VS (2015) Calcium transport from source to sink: understanding the mechanism(s) of acquisition, translocation, and accumulation for crop biofortification. Acta Physiol Plant 37. https://doi.org/10.1007/s11738-014-1722-6
Laszlo JA (1994) Changes in soybean fruit Ca2+ (Sr2+) and K+ (Rb+) transport ability during development. Plant Physiol 104:937–944. https://doi.org/10.1104/pp.104.3.937
Lide DR (2005) CRC Handbook of Chemistry and Physics. CRC Press, Boca Raton, FL, Internet Version, p 2005
Marschner P (2011) Marschner’s Mineral Nutrition of Higher Plants: Third Edition. Academic Press
Martins V, Garcia A, Costa C et al (2018) Calcium- and hormone-driven regulation of secondary metabolism and cell wall enzymes in grape berry cells. J Plant Physiol 231:57–67. https://doi.org/10.1016/j.jplph.2018.08.011
Mayorga-Gómez A, Nambeesan SU, Coolong T, Díaz-Pérez JC (2020) Temporal Relationship between Calcium and Fruit Growth and Development in Bell Pepper (Capsicum annuum L.). HortScience 55:906–913. https://doi.org/10.21273/hortsci14892-20
McGonigle TP, Grant CA (2015) Variation in potassium and calcium uptake with time and root depth. Can J Plant Sci 95:771–777. https://doi.org/10.4141/cjps-2014-227
Moyen C, Bonmort J, Roblin G (2011) Early Sr2+-induced effects on membrane potential, proton pumping- and ATP hydrolysis-activities of plasma membrane vesicles from maize root cells. Environ Exp Bot 70:289–296. https://doi.org/10.1016/j.envexpbot.2010.10.005
Moyen C, Roblin G (2010) Uptake and translocation of strontium in hydroponically grown maize plants, and subsequent effects on tissue ion content, growth and chlorophyll a/b ratio: comparison with Ca effects. Environ Exp Bot 68:247–257. https://doi.org/10.1016/j.envexpbot.2009.12.004
Moyen C, Roblin G (2013) Occurrence of interactions between individual Sr2+- and Ca2+-effects on maize root and shoot growth and Sr2+, Ca2+ and Mg2+ contents, and membrane potential: Consequences on predicting Sr2+-impact. J Hazard Mater 260:770–779. https://doi.org/10.1016/j.jhazmat.2013.06.029
Nagata T (2019) Effect of strontium on the growth, ion balance, and suberin induction in solanum lycopersicum. Plant Root 13:9–14. https://doi.org/10.3117/plantroot.13.9
Palta JP (2010) Improving potato tuber quality and production by targeted calcium nutrition: the discovery of tuber roots leading to a new concept in potato nutrition. Potato Res 53:267–275. https://doi.org/10.1007/s11540-010-9163-0
Parvin K, Nahar K, Hasanuzzaman M et al (2019) Calcium-mediated growth regulation and abiotic stress tolerance in plants
Peek S, Clementz MT (2012) Sr/Ca and Ba/Ca variations in environmental and biological sources: A survey of marine and terrestrial systems. Geochim Cosmochim Acta 95:36–52. https://doi.org/10.1016/j.gca.2012.07.026
Pett-Ridge JC, Derry LA, Barrows JK (2009) Ca/Sr and87Sr/86Sr ratios as tracers of Ca and Sr cycling in the Rio Icacos watershed, Luquillo Mountains, Puerto Rico. Chem Geol 267:32–45. https://doi.org/10.1016/j.chemgeo.2008.11.022
Pongrac P, Vogel-Mikuš K, Regvar M et al (2013) On the distribution and evaluation of Na, Mg and Cl in leaves of selected halophytes. Nucl Instruments Methods Phys Res Sect B Beam Interact with Mater Atoms 306:144–149. https://doi.org/10.1016/j.nimb.2012.12.057
Rosen C, Bierman P, Telias A et al (2019) Foliar applied strontium as a tracer for calcium transport in apple trees. HortScience 39:853C – 853. https://doi.org/10.21273/hortsci.39.4.853c
Seligmann R, Wengrowicz U, Tirosh D et al (2009) Calcium translocation and whole plant transpiration: spatial and temporal measurements using radio-Strontium as tracer. In: International Plant Nutrition Collquium. UC Davis: Department of Plant Sciences https://escholarship.org/uc/item/6fx7b4bg
Seregin IV, Kozhevnikova AD (2004) Strontium transport, distribution, and toxic effects on maize seedling growth. Russ J Plant Physiol 51:215–221. https://doi.org/10.1023/B:RUPP.0000019217.89936.e7
Shear CB, Faust M (1970) Calcium Transport in Apple Trees. Plant Physiol 45:670–674. https://doi.org/10.1104/pp.45.6.670
Song WP, Chen W, Yi JW et al (2018) Ca distribution pattern in litchi fruit and pedicel and impact of Ca channel inhibitor, La3+. Front Plant Sci 8:1–11. https://doi.org/10.3389/fpls.2017.02228
Soudek P, Valenová Š, Vavříková Z, Vaněk T (2006) 137Cs and 90Sr uptake by sunflower cultivated under hydroponic conditions. J Environ Radioact 88:236–250. https://doi.org/10.1016/j.jenvrad.2006.02.005
Storey R, Leigh RA (2004) Processes modulating calcium distribution in citrus leaves. An investigation using x-ray microanalysis with strontium as a tracer. Plant Physiol 136:3838–3848. https://doi.org/10.1104/pp.104.045674
Sugita R, Kobayashi NI, Hirose A et al (2016) Visualization of uptake of mineral elements and the dynamics of photosynthates in arabidopsis by a newly developed Real-Time Radioisotope Imaging System (RRIS). Plant Cell Physiol 57:743–753. https://doi.org/10.1093/pcp/pcw056
Tan J, Ben-Gal A, Shtein I et al (2020) Root structural plasticity enhances salt tolerance in mature olives. Environ Exp Bot 179:104224. https://doi.org/10.1016/j.envexpbot.2020.104224
Taylor MD, Locascio SJ (2004) Blossom-End Rot: A Calcium Deficiency. J Plant Nutr 27:123–139. https://doi.org/10.1081/PLN-120027551
Thor K (2019) Calcium—nutrient and messenger. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00440
van der Heijden G, Legout A, Pollier B et al (2014) The dynamics of calcium and magnesium inputs by throughfall in a forest ecosystem on base poor soil are very slow and conservative: Evidence from an isotopic tracing experiment (26Mg and 44Ca). Biogeochemistry 118:413–442. https://doi.org/10.1007/s10533-013-9941-2
Von Fircks Y, Rosén K, Sennerby-Forsse L (2002) Uptake and distribution of 137Cs and 90Sr in Salix viminalis plants. J Environ Radioact 63:1–14. https://doi.org/10.1016/S0265-931X(01)00131-X
Vriese K, De Costa A, Beeckman T, Vanneste S ( 2018) Pharmacological strategies for manipulating plant Ca2+ signalling. Int J Mol Sci 19. https://doi.org/10.3390/ijms19051506
Watanabe T, Broadley MR, Jansen S et al (2007) Evolutionary control of leaf element composition in plants: Rapid report. New Phytol 174:516–523. https://doi.org/10.1111/j.1469-8137.2007.02078.x
Watanabe T, Maejima E, Yoshimura T et al (2016) The ionomic study of vegetable crops. PLoS One 11. https://doi.org/10.1371/journal.pone.0160273
White PJ (2001) The pathways of calcium movement to the xylem. J Exp Bot 52:891–899. https://doi.org/10.1093/jexbot/52.358.891
White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511. https://doi.org/10.1093/aob/mcg164
Wu HC, Bulgakov VP, Jinn TL (2018) Pectin methylesterases: Cell wall remodeling proteins are required for plant response to heat stress. Front Plant Sci 871:1–21. https://doi.org/10.3389/fpls.2018.01612
Acknowledgements
We thank Adi Bier Kushmaro, Yonatan Weizman and Natalie Toren for the technical assistance. We also thank Dr Moshe Halpern for the English language editing and Dr Asher Bar-Tal for the pre-review of our work. We are grateful to the Ben-Gurion University of the Negev and to the Israeli vegetable board for partially funding the research.
Funding
The Ben-Gurion University of the Negev, through the scholarship received by Petar Jovanović, and the “Israeli vegetable board”, partly funded the current research.
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Jovanović, P., Rachmilevitch, S., Roitman, N. et al. Strontium as a tracer for calcium: uptake, transport and partitioning within tomato plants. Plant Soil 466, 303–316 (2021). https://doi.org/10.1007/s11104-021-05024-6
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DOI: https://doi.org/10.1007/s11104-021-05024-6