Abstract
Crops during their growth period can encounter waterlogging problems which often lead to an oxygen-deficient environment in the rhizosphere and rapid increases in the availability of iron in the soil. Therefore, a hydroponic experimental system was designed to evaluate the response mechanism of sugar beet to single ferrous, hypoxia stress, and interactive ferrous-hypoxia stress through physiological and biochemical analyses. In this study, stress conditions were applied in a factorial design: three ferrous treatments (0.06, 0.48, and 1.92 mmol) and three hypoxia treatments (normal, 4-day hypoxia, and 8-day hypoxia) were set against one another, totaling 9 experimental treatments. We measured morphological indexes, biomass production, root vigor, the electrolytic leakage, chlorophyll content, gas exchange, reactive oxygen species concentration, malonaldehyde concentration, antioxidant enzyme activity, proline, soluble sugar concentration, and plant nutrient contents of sugar beet seedlings under different treatments. Under single stress, the growth of seedlings was inhibited, and interactive stress enhanced this inhibition. Compared to the control, 1.92 mmol Fe and 8 days of hypoxia induced a 16% and 43% reduction in the total plant height of seedlings, respectively, while interactive ferrous-hypoxia stress produced a 51% reduction. Single and interactive stress damaged the roots of seedlings, root vigor reached its lowest under interactive stress, and Fe concentrations increased, but N, P, K, Mn, and Zn decreased. Chlorophyll content decreased under ferrous and interactive stress. At the same time, stresses affected the gas exchange of leaves, and the stomatal conductance, transpiration rate, and intrinsic water use efficiency decreased, resulting in insufficient photosynthetic capacity of the seedlings, and biomass accumulation decreased. Furthermore, the antioxidant enzyme activity and osmotic adjustment substance content of seedlings increased with an increase of the degree of stress. Among these, the POD activity of seedlings grown under 1.92 mmol Fe and hypoxia for 8 days was upregulated by 7.5 and 1.5 times compared with the control, while the interactive stress induced a 10.5 times upregulation. Under single stress, seedling growth was inhibited to varying degrees, while under interactive stress, this inhibition was enhanced. Seedlings also improved their antioxidant capacity to resist the damage caused by stress, but on the whole, stress had a profound effect on the plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad P, Sarwat M, Sharma S (2008) Reactive oxygen species, antioxidants and signaling in plants. J Plant Bio 51:167–173
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase Beta Vulgaris Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
Bai T, Li C, Ma F et al (2010) Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant Soil 327:95–105. https://doi.org/10.1007/s11104-009-0034-x
Balakhnina TI, Bennicelli RP, Stępniewska Z et al (2010) Oxidative damage and antioxidant defense system in leaves of Vicia faba major L. cv. Bartom during soil flooding and subsequent drainage. Plant Soil 327:293–301. https://doi.org/10.1007/s11104-009-0054-6
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375
Board JE (2008) Waterlogging effects on plant nutrient concentrations in soybean. J Plant Nutr 31:828–838. https://doi.org/10.1080/01904160802043122
Bui LT, Giuntoli B, Kosmacz M et al (2015) Constitutively expressed ERF-VII transcription factors redundantly activate the core anaerobic response in Arabidopsis thaliana. Plant Sci 236:37–43. https://doi.org/10.1016/j.plantsci.2015.03.008
Cao X, Wu L, Wu M et al (2020) Abscisic acid mediated proline biosynthesis and antioxidant ability in roots of two different rice genotypes under hypoxic stress. BMC Plant Biol 20:198. https://doi.org/10.1186/s12870-020-02414-3
Chen Y, Lu P, Sun P et al (2017) Interactive salt-alkali stress and exogenous Ca2+ effects on growth and osmotic adjustment of Lolium multiflorum in a coastal estuary. Flora 229:92–99. https://doi.org/10.1016/j.flora.2017.02.018
Connorton JM, Balk J, Rodríguez-Celma J (2017) Iron homeostasis in plants-a brief overview. Metallomics 9:813–823. https://doi.org/10.1039/C7MT00136C
Das U, Rahman MM, Roy ZR et al (2020) Morpho-physiological retardations due to iron toxicity involve redox imbalance rather than photosynthetic damages in tomato. Plant Physiol Bioch 156:55–63. https://doi.org/10.1016/j.plaphy.2020.08.034
de Araújo TO, de Freitas-Silva L, Santana BVN et al (2015) Morphoanatomical responses induced by excess iron in roots of two tolerant grass species. Environ Sci Pollut Res 22:2187–2195. https://doi.org/10.1007/s11356-014-3488-1
de Freitas P, de Carvalho HH, Costa JH et al (2019) Salt acclimation in sorghum plants by exogenous proline: physiological and biochemical changes and regulation of proline metabolism. Plant Cell Rep 38:403–416. https://doi.org/10.1007/s00299-019-02382-5
Delias DS, Da-Silva CJ, Martins AC et al (2021) Iron toxicity increases oxidative stress and impairs mineral accumulation and leaf gas exchange in soybean plants during hypoxia. Environ Sci Pollut Res 29:22427–22438. https://doi.org/10.1007/s11356-021-17397-3
Dhir B, Sharmila P, PardhaSaradhi P et al (2009) Physiological and antioxidant responses of Salvinia natans exposed to chromium-rich wastewater. Ecotoxicol Environ Saf 72:1790–1797. https://doi.org/10.1016/j.ecoenv.2009.03.015
Dietz KJ, Baier M, Krämer U (1999) Free radicals and reactive oxygen species as mediators of heavy metal toxicity in plants. In: Heavy Metal Stress in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-07745-0_4
Dohm JC, Minoche AE, Holtgräwe D et al (2014) The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature 505:546–549. https://doi.org/10.1038/nature12817
dos Santos MS, Sanglard LM, Barbosa ML et al (2020) Silicon nutrition mitigates the negative impacts of iron toxicity on rice photosynthesis and grain yield. Ecotox Environ Saf 189:110008. https://doi.org/10.1016/j.ecoenv.2019.110008
Frei M, Tetteh RN, Razafindrazaka AL et al (2016) Responses of rice to chronic and acute iron toxicity: genotypic differences and biofortification aspects. Plant Soil 408:149–161. https://doi.org/10.1007/s11104-016-2918-x
Frohne T, Rinklebe J, Diaz-Bone RA et al (2011) Controlled variation of redox conditions in a floodplain soil: impact on metal mobilization and biomethylation of arsenic and antimony. Geoderma 160:414–424. https://doi.org/10.1016/j.geoderma.2010.10.012
Geng G, Yang J (2015) Sugar beet production and industry in China. Sugar Tech 17:13–21. https://doi.org/10.1007/s12355-014-0353-y
Geng G, Lv C, Stevanato P et al (2019) Transcriptome analysis of salt-sensitive and tolerant genotypes reveals salt-tolerance metabolic pathways in sugar beet. Int J Mol Sci 20:5910. https://doi.org/10.3390/ijms20235910
Giuntoli B, Shukla V, Maggiorelli F et al (2017) Age-dependent regulation of ERF-VII transcription factor activity in Arabidopsis thaliana. Plant Cell Enviro 40:2333–2346. https://doi.org/10.1111/pce.13037
Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820. https://doi.org/10.1104/pp.104.3.815
Hasanuzzaman M, Bhuyan M, Zulfiqar F et al (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681. https://doi.org/10.3390/antiox9080681
He L, Yu L, Li B et al (2018) The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress. BMC Plant Biol 18:180. https://doi.org/10.1186/s12870-018-1393-3
Hirabayashi Y, Mahendran R, Koirala S et al (2013) Global flood risk under climate change. Nature Clim Change 3:816–821. https://doi.org/10.1038/nclimate1911
Hsu CC, Zhu Y, Arrington JV et al (2018) Universal plant phosphoproteomics workflow and its application to tomato signaling in response to cold stress. Mol Cell Proteomics 17:2068–2080. https://doi.org/10.1074/mcp.TIR118.000702
Jia H, Pan D (2013) On the spatial and temporal patterns of flood and drought hazards of China. Disaster Adv 6:12–18
Koevoets IT, Venema JH, Elzenga JT et al (2016) Roots withstanding their environment: exploiting root system architecture responses to abiotic stress to improve crop tolerance. Front Plant Sci 7:1335. https://doi.org/10.3389/fpls.2016.01335
Lapaz AM, de Camargos LS, Yoshida C et al (2020) Response of soybean to soil waterlogging associated with iron excess in the reproductive stage. Physiol Mol Biol Plants 26:1635–1648. https://doi.org/10.1007/s12298-020-00845-8
Li C, Bai T, Ma F et al (2010) Hypoxia tolerance and adaptation of anaerobic respiration to hypoxia stress in two Malus species. Sci Hortic 124:274–279. https://doi.org/10.1016/j.scienta.2009.12.029
Li CX, Wei H, Geng YH et al (2010) Effects of submergence on photosynthesis and growth of Pterocarya stenoptera (Chinese wingnut) seedlings in the recently-created Three Gorges Reservoir region of China. Wetl Ecol Manag 18:485–494. https://doi.org/10.1007/s11273-010-9181-3
Li J, Sun J, Yang Y et al (2012) Identification of hypoxic-responsive proteins in cucumber roots using a proteomic approach. Plant Physiol Bioch 51:74–80. https://doi.org/10.1016/j.plaphy.2011.10.011
Lu R (2000) Soil agricultural chemical analysis method. Agricultural science and technology press, Beijing
Maathuis FJ (2009) Physiological functions of mineral macronutrients. Cur Opin Plant Biol 12:250–258. https://doi.org/10.1016/j.pbi.2009.04.003
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, San Diego
Mohanty B, Ong BL (2003) Contrasting effects of submergence in light and dark on pyruvate decarboxylase activity in roots of rice lines differing in submergence tolerance. Ann Bot 91:291–300. https://doi.org/10.1093/aob/mcf050
Mukherjee H, Drakeford D, Reid DM (1986) ATPase activity of sunflower root membranes as affected by flooding. Physiol Plant 67:55–60. https://doi.org/10.1111/j.1399-3054.1986.tb01262.x
Müller C, Silveira S, Daloso DM et al (2017) Ecophysiological responses to excess iron in lowland and upland rice cultivars. Chemosphere 189:123–133. https://doi.org/10.1016/j.chemosphere.2017.09.033
Ngoune TL, Mutengwa CS, Ngonkeu ELM et al (2018) Breeding maize for tolerance to acidic soils: a review. Agronomy 8:84. https://doi.org/10.3390/agronomy8060084
Ottow JCG, Benckiser G, Watanabe I (1982) Iron toxicity of rice as a multiple nutrient soil stress. Trop Agric Res Ser 15:167–179
Rodríguez-Gamir J, Ancillo G, González-Mas MC et al (2011) Root signalling and modulation of stomatal closure in flooded citrus seedlings. Plant Physiol Bioch 49:636–645. https://doi.org/10.1016/j.plaphy.2011.03.003
Sairam RK, Dharmar K, Chinnusamy V et al (2009) Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). J Plant Physiol 166:602–616. https://doi.org/10.1016/j.jplph.2008.09.005
Shevyakova NI, Eshinimaeva BT, Paramonova NV et al (2009) Effects of various iron supply on oxidative stress development and ferritin formation in the common ice plants. Russ J Plant Physiol 56:470–479. https://doi.org/10.1134/S1021443709040050
Veen HV, Akman M, Jamar DCL et al (2014) Group VII ethylene response factor diversification and regulation in four species from flood-prone environments. Plant Cell Environ 37:2421–2432. https://doi.org/10.1111/pce.12302
Voesenek L, Colmer T, Pierik R et al (2006) How plants cope with complete submergence. New Phytol 170:213–226. https://doi.org/10.1111/j.1469-8137.2006.01692.x
Wang Y, Stevanato P, Lv C et al (2019) Comparative physiological and proteomic analysis of two sugar beet genotypes with contrasting salt tolerance. J Agric Food Chem 67:6056–6073. https://doi.org/10.1021/acs.jafc.9b00244
Wang Q, Wang L, Chandrasekaran U et al (2021) ABA biosynthesis and signaling cascades under hypoxia stress. Front Plant Sci 12:661228. https://doi.org/10.3389/fpls.2021.661228
Wu LB, Ueda Y, Lai SK et al (2017) Shoot tolerance mechanisms to iron toxicity in rice (Oryza sativa L.). Plant Cell Environ 40:570–584. https://doi.org/10.1111/pce.12733
Xu S, Lin D, Sun H et al (2015) Excess iron alters the fatty acid composition of chloroplast membrane and decreases the photosynthesis rate: a study in hydroponic pea seedlings. Acta Physiol Plant 37:212. https://doi.org/10.1007/s11738-015-1969-6
Yadavalli V, Neelam S, Rao AS et al (2012) Differential degradation of photosystem I subunits under iron deficiency in rice. J Plant Physiol 169:753–759. https://doi.org/10.1016/j.jplph.2012.02.008
Yan K, Zhao S, Cui M et al (2018) Vulnerability of photosynthesis and photosystem I in Jerusalem artichoke (Helianthus tuberosus L.) exposed to waterlogging. Plant Physiol Bioch 125:239–246. https://doi.org/10.1016/j.plaphy.2018.02.017
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217:523–539. https://doi.org/10.1111/nph.14920
Yang CY, Hong CP (2015) The NADPH oxidase Rboh D is involved in primary hypoxia signalling and modulates expression of hypoxia-inducible genes under hypoxic stress. Environ Exp Bot 115:63–72. https://doi.org/10.1016/j.envexpbot.2015.02.008
Yildiztugay E, Ozfidan-Konakci C, Kucukoduk M (2013) Sphaerophysa kotschyana, an endemic species from Central Anatolia: antioxidant system responses under salt stress. J Plant Res 126:729–742. https://doi.org/10.1007/s10265-013-0573-3
Yu J, Zhang Y, Zhong J et al (2019) Water-level alterations modified nitrogen cycling across sediment-water interface in the Three Gorges Reservoir. Environ Sci Pollut Res Int 27:25886–25898. https://doi.org/10.1007/s11356-019-06656-z
Zhang Y, Wang Q, Xu C et al (2016) Iron (Fe2+)-induced toxicity produces morphological and physiological changes in roots in Panax ginseng grown in hydroponics. Environ Toxicol Chem 98:630–637. https://doi.org/10.1080/02772248.2015.1133385
Zhang P, Lyu D, Jia L et al (2017) Physiological and de novo transcriptome analysis of the fermentation mechanism of Cerasus sachalinensis roots in response to short-term waterlogging. BMC Genomics 18:649. https://doi.org/10.1186/s12864-017-4055-1
Zhong J (2017) Roots characteristics among different rice varieties and their effects on plant methane transport rate. Hunan Agricultural University. Chang Sha, China
Funding
This research was supported by the National Natural Science Foundation of China Project (32172055), the Natural Science Foundation of Heilongjiang Province (YQ2020037C), the China Postdoctoral Science Foundation (2020M670944), the Science Foundation for Distinguished Young Scholars of Heilongjiang University, the Initiation Fund for Postdoctoral Research in Heilongjiang Province, the Youth Innovative Talents Training Program of Heilongjiang Regular Universities, and the China Agriculture Research System Fund (CARS-170209).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
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 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
Dong, Y., Wang, G., Stevanato, P. et al. Physiological Response of Sugar Beet Seedlings to Ferrous, Hypoxia, and Interactive Ferrous-Hypoxia Stresses. J Soil Sci Plant Nutr 22, 4249–4261 (2022). https://doi.org/10.1007/s42729-022-01023-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-022-01023-3