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Lindberg, S. & Premkumar, A. (2024). Ion Changes and Signaling under Salt Stress in Wheat and Other Important Crops. Plants , 13(1), Article ID 46.
Open this publication in new window or tab >>Ion Changes and Signaling under Salt Stress in Wheat and Other Important Crops
2024 (English)In: Plants , E-ISSN 2223-7747, Vol. 13, no 1, article id 46Article, review/survey (Refereed) Published
Abstract [en]

High concentrations of sodium (Na+), chloride (Cl-), calcium (Ca2+), and sulphate (SO42-) are frequently found in saline soils. Crop plants cannot successfully develop and produce because salt stress impairs the uptake of Ca2+, potassium (K+), and water into plant cells. Different intracellular and extracellular ionic concentrations change with salinity, including those of Ca2+, K+, and protons. These cations serve as stress signaling molecules in addition to being essential for ionic homeostasis and nutrition. Maintaining an appropriate K+:Na+ ratio is one crucial plant mechanism for salt tolerance, which is a complicated trait. Another important mechanism is the ability for fast extrusion of Na+ from the cytosol. Ca2+ is established as a ubiquitous secondary messenger, which transmits various stress signals into metabolic alterations that cause adaptive responses. When plants are under stress, the cytosolic-free Ca2+ concentration can rise to 10 times or more from its resting level of 50-100 nanomolar. Reactive oxygen species (ROS) are linked to the Ca2+ alterations and are produced by stress. Depending on the type, frequency, and intensity of the stress, the cytosolic Ca2+ signals oscillate, are transient, or persist for a longer period and exhibit specific signatures. Both the influx and efflux of Ca2+ affect the length and amplitude of the signal. According to several reports, under stress Ca2+ alterations can occur not only in the cytoplasm of the cell but also in the cell walls, nucleus, and other cell organelles and the Ca2+ waves propagate through the whole plant. Here, we will focus on how wheat and other important crops absorb Na+, K+, and Cl- when plants are under salt stress, as well as how Ca2+, K+, and pH cause intracellular signaling and homeostasis. Similar mechanisms in the model plant Arabidopsis will also be considered. Knowledge of these processes is important for understanding how plants react to salinity stress and for the development of tolerant crops.

Keywords
cereals, chloride, cytosolic Ca2+, K+, Na+, pH, salt stress, signaling, wheat
National Category
Botany
Identifiers
urn:nbn:se:su:diva-226569 (URN)10.3390/plants13010046 (DOI)001141503400001 ()38202354 (PubMedID)2-s2.0-85181943401 (Scopus ID)
Available from: 2024-02-14 Created: 2024-02-14 Last updated: 2025-08-28Bibliographically approved
Awad-Allah, E. F. A., Elsokkary, I. H. & Lindberg, S. M. (2023). Phosphorus protects against cadmium-induced phytotoxicity by stimulating plasma membrane H+-ATPase activity. Journal of plant nutrition, 46(16), 3918-3932
Open this publication in new window or tab >>Phosphorus protects against cadmium-induced phytotoxicity by stimulating plasma membrane H+-ATPase activity
2023 (English)In: Journal of plant nutrition, ISSN 0190-4167, E-ISSN 1532-4087, Vol. 46, no 16, p. 3918-3932Article in journal (Refereed) Published
Abstract [en]

Proper plant nutrition can be an effective strategy to alleviate the phytotoxicity and damaging effects of Cd stress on plants and to avoid its entry into the food chain. This study aimed to investigate effects of phosphorus concentrations, and pH levels in the nutrient solution on Cd uptake, growth, photosynthetic characters, total phytochelatins (PCs), and plasma membrane ATPase activity of sugar beet (Beta vulgaris L.) plants grown in sand culture. Two successive experimental studies were carried out under controlled conditions. In the first study, 10-day-old sugar beet seedlings were irrigated with a half-strength Hoagland and Arnon nutrient solution, adjusted to different pH (3.5, 5.0, 6.0, 7.0, or 8.0), and containing 0, 0.15, or 0.30 mg Cd L−1 as CdCl2. In the second study, 10-day-old sugar beet seedlings were irrigated with the same nutrient solution (pH 6), but combined with different phosphorus concentrations (0, 10, 25 and 50 µg P ml−1 as KH2PO4) and Cd levels (0, 0.15, and 0.30 mg Cd L−1 as CdCl2). The first study revealed that pH had a strong influence on Cd uptake by sugar beet roots. Cd stress significantly decreased sugar beet growth and Mg2+-ATPase activity, whereas it increased total phytochelatins (PCs). Second study indicated an antagonistic effect between P and Cd. Furthermore, phosphorus had the potential to stimulate Mg2+-ATPase activity and synthesis of photosynthetic pigments and to promote growth of sugar beet seedlings. Cadmium induced phytotoxicity in sugar beet seedlings can be alleviated by a proper pH and phosphorus nutrition.

Keywords
ATPase activity, circadian rhythms, pH levels, phytotoxicity, total phytochelatins
National Category
Botany
Identifiers
urn:nbn:se:su:diva-229765 (URN)10.1080/01904167.2023.2220709 (DOI)001003225200001 ()2-s2.0-85161569611 (Scopus ID)
Available from: 2024-06-04 Created: 2024-06-04 Last updated: 2024-06-04Bibliographically approved
Morgan, S. H., Kader, M. A. & Lindberg, S. (2022). Cytosolic Sodium Influx in Mesophyll Protoplasts of Arabidopsis thaliana, wt, sos1:1 and nhx1 Differs and Induces Different Calcium Changes. Plants , 11(24), Article ID 3439.
Open this publication in new window or tab >>Cytosolic Sodium Influx in Mesophyll Protoplasts of Arabidopsis thaliana, wt, sos1:1 and nhx1 Differs and Induces Different Calcium Changes
2022 (English)In: Plants , E-ISSN 2223-7747, Vol. 11, no 24, article id 3439Article in journal (Refereed) Published
Abstract [en]

The sodium influx into the cytosol of mesophyll protoplasts from Arabidopsis thaliana cv. Columbia, wild type, was compared with the influx into sos1-1 and nhx1 genotypes, which lack the Na+/H+ antiporter in the plasma membrane and tonoplast, respectively. Changes in cytosolic sodium and calcium concentrations upon a 100 mM NaCl addition were detected by use of epifluorescence microscopy and the sodium-specific fluorescent dye SBFI, AM, and calcium sensitive Fura 2, AM, respectively. There was a smaller and mainly transient influx of Na+ in the cytosol of the wild type compared with the sos1-1 and nhx1 genotypes, in which the influx lasted for a longer time. Sodium chloride addition to the protoplasts’ medium induced a significant increase in cytosolic calcium concentration in the wild type at 1.0 mM external calcium, and to a lesser extent in nhx1, however, it was negligible in the sos1-1 genotype. LiCl inhibited the cytosolic calcium elevation in the wild type. The results suggest that the salt-induced calcium elevation in the cytosol of mesophyll cells depends on an influx from both internal and external stores and occurs in the presence of an intact Na+/H+ antiporter at the plasma membrane. The Arabidopsis SOS1 more effectively regulates sodium homeostasis than NHX1.

Keywords
Arabidopsis, cytosolic Ca2+ and Na+, epifluorescence ratio microscopy, influx, salt stress
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-213823 (URN)10.3390/plants11243439 (DOI)000904341600001 ()36559553 (PubMedID)2-s2.0-85144927881 (Scopus ID)
Available from: 2023-01-20 Created: 2023-01-20 Last updated: 2025-08-28Bibliographically approved
Premkumar, A., Javed, M. T., Pawlowski, K. & Lindberg, S. M. (2022). Silicate Inhibits the Cytosolic Influx of Chloride in Protoplasts of Wheat and Affects the Chloride Transporters, TaCLC1 and TaNPF2.4/2.5. Plants , 11(9), Article ID 1162.
Open this publication in new window or tab >>Silicate Inhibits the Cytosolic Influx of Chloride in Protoplasts of Wheat and Affects the Chloride Transporters, TaCLC1 and TaNPF2.4/2.5
2022 (English)In: Plants , E-ISSN 2223-7747, Vol. 11, no 9, article id 1162Article in journal (Refereed) Published
Abstract [en]

Chloride is an essential nutrient for plants, but high concentrations can be harmful. Silicon ameliorates both abiotic and biotic stresses in plants, but it is unknown if it can prevent cellular increase of chloride. Therefore, we investigated the influx of Cl ions in two wheat cultivars different in salt sensitivity, by epifluorescence microscopy and a highly Cl-sensitive dye, MQAE, N-[ethoxycarbonylmethyl]-6-methoxy-quinolinium bromide, in absence and presence of potassium silicate, K2SiO3. The Cl-influx was higher in the salt-sensitive cv. Vinjett, than in the salt-tolerant cv. S-24, and silicate pre-treatment of protoplasts inhibited the Cl-influx in both cultivars, but more in the sensitive cv. Vinjett. To investigate if the Cl-transporters TaCLC1 and TaNPF2.4/2.5 are affected by silicate, expression analyses by RT-qPCR were undertaken of TaCLC1 and TaNPF 2.4/2.5 transcripts in the absence and presence of 100 mM NaCl, with and without the presence of K2SiO3. The results show that both transporter genes were expressed in roots and shoots of wheat seedlings, but their expressions were differently affected by silicate. The TaNPF2.4/2.5 expression in leaves was markedly depressed by silicate. These findings demonstrate that less chloride accumulates in the cytosol of leaf mesophyll by Si treatment and increases salt tolerance.

Keywords
chloride, cytosolic uptake, silicate, TaCLC1, TaNPF 2.4/2.5, wheat
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-205111 (URN)10.3390/plants11091162 (DOI)000796178300001 ()35567163 (PubMedID)2-s2.0-85128753291 (Scopus ID)
Available from: 2022-06-01 Created: 2022-06-01 Last updated: 2025-08-28Bibliographically approved
Tanwir, K. & Lindberg, S. (2020). Ecophysiology and Stress Responses of Aquatic Macrophytes Under Metal/Metalloid Toxicity. In: Mirza Hasanuzzaman (Ed.), Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I: General Consequences and Plant Responses (pp. 485-511). Springer
Open this publication in new window or tab >>Ecophysiology and Stress Responses of Aquatic Macrophytes Under Metal/Metalloid Toxicity
2020 (English)In: Plant Ecophysiology and Adaptation under Climate Change: Mechanisms and Perspectives I: General Consequences and Plant Responses / [ed] Mirza Hasanuzzaman, Springer, 2020, p. 485-511Chapter in book (Refereed)
Abstract [en]

Many metal elements are essential for plant growth at low concentrations but their excessive levels in the rhizosphere may cause phytotoxicity depending upon the fact that metals are easily absorbed and translocated in soil–plant systems. Nonessential metals/metalloids, i.e., Pb, Cr, Cd, As, Hg, etc., initiate a series of consecutive and/or parallel events at morphological, physiological, and molecular levels in aquatic plants depending on the nature of element and plant species. This chapter emphasizes the responses of aquatic macrophytes to metals/metalloids, with possible implementation in phytoremediation techniques. Metal-triggered growth inhibition, alterations in enzyme activities, inhibition of photosynthesis, changes in nutrient acquisition and metabolism, and the formation of free radicals are the major components reviewed in this book chapter. Discussion about the metal toxicity avoidance strategies like fluctuations in rhizospheric environments, plasma membrane exclusion, cell wall immobilization, phytochelatin-based sequestration and compartmentalization processes, stress proteins, and metallothioneins is also within the scope of this chapter. Metal tolerance in aquatic plants is more likely involved in an integrated network of multiple response processes generally described as “fan-shaped response” rather than several isolated functions described above. Plant tolerance to metals/metalloids is mainly determined from its transport across plasma membrane and tonoplast in plant. The appropriate understanding of metal-triggered ecophysiological responses of aquatic plants may make it promising to use them for treatment of metal polluted waters and soils.

Place, publisher, year, edition, pages
Springer, 2020
Keywords
Aquatic plants, Defense mechanisms, Ecophysiological responses, Metals/metalloids, Phytofilteration, Phytostabilization, Tolerance
National Category
Biological Sciences
Research subject
Plant Physiology
Identifiers
urn:nbn:se:su:diva-188877 (URN)10.1007/978-981-15-2156-0_16 (DOI)978-981-15-2155-3 (ISBN)978-981-15-2158-4 (ISBN)978-981-15-2156-0 (ISBN)
Projects
Cadmium uptake and tolerance mechanisms in plants
Available from: 2021-01-13 Created: 2021-01-13 Last updated: 2022-02-25Bibliographically approved
Yemelyanov, V. V., Lastochkin, V. V., Chirkova, T., Lindberg, S. M. & Shishova, M. F. (2020). Indoleacetic Acid Levels in Wheat and Rice Seedlings under Oxygen Deficiency and Subsequent Reoxygenation. Biomolecules, 10(2), Article ID 276.
Open this publication in new window or tab >>Indoleacetic Acid Levels in Wheat and Rice Seedlings under Oxygen Deficiency and Subsequent Reoxygenation
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2020 (English)In: Biomolecules, E-ISSN 2218-273X, Vol. 10, no 2, article id 276Article in journal (Refereed) Published
Abstract [en]

The lack of oxygen and post-anoxic reactions cause significant alterations of plant growth and metabolism. Plant hormones are active participants in these alterations. This study focuses on auxin-a phytohormone with a wide spectrum of effects on plant growth and stress tolerance. The indoleacetic acid (IAA) content in plants was measured by ELISA. The obtained data revealed anoxia-induced accumulation of IAA in wheat and rice seedlings related to their tolerance of oxygen deprivation. The highest IAA accumulation was detected in rice roots. Subsequent reoxygenation was accompanied with a fast auxin reduction to the control level. A major difference was reported for shoots: wheat seedlings contained less than one-third of normoxic level of auxin during post-anoxia, while IAA level in rice seedlings rapidly recovered to normoxic level. It is likely that the mechanisms of auxin dynamics resulted from oxygen-induced shift in auxin degradation and transport. Exogenous IAA treatment enhanced plant survival under anoxia by decreased electrolyte leakage, production of hydrogen peroxide and lipid peroxidation. The positive effect of external IAA application coincided with improvement of tolerance to oxygen deprivation in the 35S:iaaM x 35S:iaaH lines of transgene tobacco due to its IAA overproduction.

Keywords
auxin, oxygen deficiency, post-anoxia, rice, tobacco, wheat
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-181106 (URN)10.3390/biom10020276 (DOI)000522138500079 ()32054127 (PubMedID)
Available from: 2020-04-27 Created: 2020-04-27 Last updated: 2022-03-23Bibliographically approved
Yemelyanov, V. V., Chirkova, T. V., Shishova, M. F. & Lindberg, S. M. (2020). Potassium Efflux and Cytosol Acidification as Primary Anoxia-Induced Events in Wheat and Rice Seedlings. Plants , 9(9), Article ID 1216.
Open this publication in new window or tab >>Potassium Efflux and Cytosol Acidification as Primary Anoxia-Induced Events in Wheat and Rice Seedlings
2020 (English)In: Plants , E-ISSN 2223-7747, Vol. 9, no 9, article id 1216Article in journal (Refereed) Published
Abstract [en]

Both ion fluxes and changes of cytosolic pH take an active part in the signal transduction of different environmental stimuli. Here we studied the anoxia-induced alteration of cytosolic K+ concentration, [K+]cyt, and cytosolic pH, pHcyt, in rice and wheat, plants with different tolerances to hypoxia. The [K+]cyt and pHcyt were measured by fluorescence microscopy in single leaf mesophyll protoplasts loaded with the fluorescent potassium-binding dye PBFI-AM and the pH-sensitive probe BCECF-AM, respectively. Anoxic treatment caused an efflux of K+ from protoplasts of both plants after a lag-period of 300–450 s. The [K+]cyt decrease was blocked by tetraethylammonium (1 mM, 30 min pre-treatment) suggesting the involvement of plasma membrane voltage-gated K+ channels. The protoplasts of rice (a hypoxia-tolerant plant) reacted upon anoxia with a higher amplitude of the [K+]cyt drop. There was a simultaneous anoxia-dependent cytosolic acidification of protoplasts of both plants. The decrease of pHcyt was slower in wheat (a hypoxia-sensitive plant) while in rice protoplasts it was rapid and partially reversible. Ion fluxes between the roots of intact seedlings and nutrient solutions were monitored by ion-selective electrodes and revealed significant anoxia-induced acidification and potassium leakage that were inhibited by tetraethylammonium. The K+ efflux from rice was more distinct and reversible upon reoxygenation when compared with wheat seedlings.

Keywords
anoxic signaling, potassium, pH, acidification, fluorescence microscopy, Triticum aestivum, Oryza sativa
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-187817 (URN)10.3390/plants9091216 (DOI)000580224800001 ()32948036 (PubMedID)
Available from: 2020-12-16 Created: 2020-12-16 Last updated: 2025-08-28Bibliographically approved
Premkumar, A., Lindberg, S., Lager, I., Rasmussen, U. & Schulz, A. (2019). Arabidopsis PLDs with C2-domain function distinctively in hypoxia. Physiologia Plantarum, 167(1), 90-110
Open this publication in new window or tab >>Arabidopsis PLDs with C2-domain function distinctively in hypoxia
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2019 (English)In: Physiologia Plantarum, ISSN 0031-9317, E-ISSN 1399-3054, Vol. 167, no 1, p. 90-110Article in journal (Refereed) Published
Abstract [en]

Hypoxia (oxygen deprivation) causes metabolic disturbances at physiological, biochemical and genetic levels and results in decreased plant growth and development. Phospholipase D (PLD)-mediated signaling was reported for abiotic and biotic stress signaling events in plants. To investigate the participatory role of PLDs also in hypoxia signaling, we used wild type of Arabidopsis thaliana and 10 pld isoform mutants containing C2-domain. Hypoxia-induced changes in three major signaling players, namely, cytosolic free calcium (Ca-cyt(2+)), reactive oxygen species (ROS) and phosphatidic acid (PA), were determined in mesophyll protoplasts. The Ca-cyt(2+) and ROS levels were monitored by fluorescence microscopy and confocal imaging, while PA levels were quantified by an enzymatic method. Our findings reveal that the elevations of cytosolic calcium and PA are reduced in all the 10 mutants dysfunctional in PLD isoforms. The hypoxia-related changes in both calcium and ROS show different kinetic patterns depending on the type of PLD studied. Pharmacological experiments confirm that both external and internal sources contribute to calcium and ROS accumulation under hypoxia. PLD alpha 1-3, PLD beta 1 and PLD gamma 1-3 are likely involved in calcium signaling under hypoxia as well as in PA production, while all investigated PLDs, except for PLD gamma 3, take part in ROS elevation.

National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-171939 (URN)10.1111/ppl.12874 (DOI)000478917400008 ()30417386 (PubMedID)
Available from: 2019-09-06 Created: 2019-09-06 Last updated: 2022-05-10Bibliographically approved
Gul, M., Wakeel, A., Steffens, D. & Lindberg, S. (2019). Potassium-induced decrease in cytosolic Na+ alleviates deleterious effects of salt stress on wheat (Triticum aestivum L.). Plant Biology, 21(5), 825-831
Open this publication in new window or tab >>Potassium-induced decrease in cytosolic Na+ alleviates deleterious effects of salt stress on wheat (Triticum aestivum L.)
2019 (English)In: Plant Biology, ISSN 1435-8603, E-ISSN 1438-8677, Vol. 21, no 5, p. 825-831Article in journal (Refereed) Published
Abstract [en]

Accumulation of NaCl in soil causes osmotic stress in plants, and sodium (Na+) and chloride (Cl-) cause ion toxicity, but also reduce the potassium (K+) uptake by plant roots and stimulate the K+ efflux through the cell membrane. Thus, decreased K+/Na+ ratio in plant tissue lead us to hypothesise that elevated levels of K+ in nutrient medium enhance this ratio in plant tissue and cytosol to improve enzyme activation, osmoregulation and charge balance. In this study, wheat was cultivated at different concentrations of K+ (2.2, 4.4 or 8.8 mm) with or without salinity (1, 60 or 120 mm NaCl) and the effects on growth, root and shoot Na+ and K+ distribution and grain yield were determined. Also, the cytosolic Na+ concentration was investigated, as well as photosynthesis rate and water potential. Salinity reduced fresh weight of both shoots and roots and dry weight of roots. The grain yield was significantly reduced under Na+ stress and improved with elevated K+ fertilisation. Elevated K+ level during cultivation prevented the accumulation of Na+ into the cytosol of both shoot and root protoplasts. Wheat growth at vegetative stage was transiently reduced at the highest K+ concentration, perhaps due to plants' efforts to overcome a high solute concentration in the plant tissue, nevertheless grain yield was increased at both K+ levels. In conclusion, a moderately elevated K+ application to wheat seedlings reduces tissue as well as cytosolic Na+ concentration and enhances wheat growth and grain yield by mitigating the deleterious effects of Na+ toxicity.

Keywords
Cytosolic Na+, grain yield, potassium fertilisation, salinity, wheat
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-171940 (URN)10.1111/plb.12999 (DOI)000478947900005 ()31034750 (PubMedID)
Available from: 2019-09-13 Created: 2019-09-13 Last updated: 2022-02-26Bibliographically approved
Shahid, M., Javed, M. T., Masood, S., Akram, M. S., Azeem, M., Ali, Q., . . . Lindberg, S. (2019). Serratia sp. CP-13 augments the growth of cadmium (Cd)-stressed Linum usitatissimum L. by limited Cd uptake, enhanced nutrient acquisition and antioxidative potential. Journal of Applied Microbiology, 126(6), 1708-1721
Open this publication in new window or tab >>Serratia sp. CP-13 augments the growth of cadmium (Cd)-stressed Linum usitatissimum L. by limited Cd uptake, enhanced nutrient acquisition and antioxidative potential
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2019 (English)In: Journal of Applied Microbiology, ISSN 1364-5072, E-ISSN 1365-2672, Vol. 126, no 6, p. 1708-1721Article in journal (Refereed) Published
Abstract [en]

Aims: The current study was aimed to evaluate the beneficial effects and bioremediation potential of a Cd-tolerant bacterial strain, Serratia sp. CP-13, on the physiological and biochemical functions of Linum usitatissimum L., under Cd stress.

Methods and Results: The bacterial strain was isolated from the wastewater collection point of Chakera, Faisalabad, Pakistan, as this place contains industrial wastewater of the Faisalabad region. The Serratia sp. CP-13, identified through 16S rRNA gene sequence analysis, exhibited a significant phyto-beneficial potential in terms of in vitro inorganic phosphate solubilization, indole-3-acetic acid production and 1-aminocyclopropane-1-carboxylic acid deaminase activity. Effects of Serratia sp. CP-13 inoculation on L. usitatissimum were evaluated by growing the plants in CdCl2 (0, 5 or 10 mg kg(-1) dry soil)-spiked soil. Without inoculation of Serratia sp. CP-13, Cd stress significantly reduced the plant biomass as well as the quantity of proteins and photosynthetic pigments due to enhanced H2O2, malondialdehyde (MDA) contents and impaired nutrient homeostasis. Subsequently, Serratia sp. CP-13 increased the plant fresh and dry biomass, plant antioxidation capacity, whereas it decreased the lipid peroxidation under Cd stress. In parallel, Serratia sp. inoculation assisted the Cd-stressed plants to maintain an optimum level of nutrients (K, Ca, P, Mg, Fe and Mn).

Conclusions: The isolated bacterial strain (Serratia sp. CP-13) when applied to Cd-stressed L. usitatissimum inhibited the Cd uptake, reduced Cd-induced lipid peroxidation, maintained the optimum level of nutrients and thereby, enhanced L. usitatissimum growth. The analysis of bio-concentration and translocation factor revealed that L. usitatissimum with Serratia sp. CP-13 inoculation sequestered Cd in plant rhizospheric zone.

Significance and Impact of the Study: Serratia sp. CP-13 inoculation is a potential candidate for the development of low Cd-accumulating linseed and could be used for phytostabilization of Cd-contaminated rhizosphere/soil colloids.

Keywords
antioxidants, cadmium tolerance, linseed, nutrient uptake, PGPB, Serratia, wastewater
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-169227 (URN)10.1111/jam.14252 (DOI)000467570600007 ()30882965 (PubMedID)
Available from: 2019-06-19 Created: 2019-06-19 Last updated: 2022-02-26Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-0860-9406

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