Strontium-induced mineral imbalance, cell death, and reactive oxygen species generation in Arabidopsis thaliana
Strontium (Sr) is a known non-essential element for plants. However, its toxic effects at high concentration on plants remain unclear. Here the effects of Sr on the growth and phytotoxicity were investigated in Arabidopsis thaliana. The plants grown on a medium containing 10-mM Sr showed reduced roo...
Saved in:
| Published in | Plant Root Vol. 17; pp. 36 - 44 |
|---|---|
| Main Author | |
| Format | Journal Article |
| Language | English |
| Published |
Japanese Society for Root Research
2023
|
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Strontium (Sr) is a known non-essential element for plants. However, its toxic effects at high concentration on plants remain unclear. Here the effects of Sr on the growth and phytotoxicity were investigated in Arabidopsis thaliana. The plants grown on a medium containing 10-mM Sr showed reduced root fresh weight (FW) and root elongation, which suggested that high Sr concentration could inhibit root growth. Assessment of Sr in the shoots and roots indicated that its concentrations increased in a dose-dependent manner. Sr treatment caused reduced calcium (Ca) levels in a dose-dependent manner, while photosynthetic pigments were also reduced. Evans blue staining of shoots and roots treated with 10-mM Sr revealed that cell death was induced by Sr accumulation. Addition of potassium iodide (KI), a reduction compound, in Sr containing agar medium to determine the relationship between reactive oxygen species (ROS) and Sr toxicity showed that it could alleviate the Sr toxicity to growth. The 3,3'-Diaminobenzidine (DAB) detection of ROS production in the leaves and roots treated with 1- and 10-mM Sr confirmed that cell death was induced by ROS. |
|---|---|
| AbstractList | Strontium (Sr) is a known non-essential element for plants. However, its toxic effects at high concentration on plants remain unclear. Here the effects of Sr on the growth and phytotoxicity were investigated in Arabidopsis thaliana. The plants grown on a medium containing 10-mM Sr showed reduced root fresh weight (FW) and root elongation, which suggested that high Sr concentration could inhibit root growth. Assessment of Sr in the shoots and roots indicated that its concentrations increased in a dose-dependent manner. Sr treatment caused reduced calcium (Ca) levels in a dose-dependent manner, while photosynthetic pigments were also reduced. Evans blue staining of shoots and roots treated with 10-mM Sr revealed that cell death was induced by Sr accumulation. Addition of potassium iodide (KI), a reduction compound, in Sr containing agar medium to determine the relationship between reactive oxygen species (ROS) and Sr toxicity showed that it could alleviate the Sr toxicity to growth. The 3,3'-Diaminobenzidine (DAB) detection of ROS production in the leaves and roots treated with 1- and 10-mM Sr confirmed that cell death was induced by ROS. |
| Author | Nagata, Takeshi |
| Author_xml | – sequence: 1 fullname: Nagata, Takeshi organization: Faculty of Science and Engineering, Setsunan University |
| BookMark | eNpVkM1OwzAQhC1UJNrCmasfoGntOHbSY6n4kypxAM7Rxt60rhK7sg2ib09QUQWnndXMN4eZkJHzDgm55WwuOC8Xhw5cCt6nOS_nQl2QMa8qnqlSFqM_-opMYtwzppaSyzHxrwPjkv3oM-vMh0ZDe-swQEdt38DQqXFGNXYdNQhpN6PgDA0IOtlPpP7ruEVH4wG1xUgHPaDJeketo6sAjTX-EG2kaQedBQfX5LKFLuLN752S94f7t_VTtnl5fF6vNpnOlVAZGG1KyVqpWykwB4NlzlBxJYWEKmcGlFQtIpdV1VSmkaIt2mZZqKoAVgIXU7I49ergYwzY1odgewjHmrP6Z6_6vFc9PEINxN2J2McEWzznISSrO_yfZyfobOodhBqd-AbNon5J |
| Cites_doi | 10.1093/pcp/pcw027 10.1104/pp.15.00346 10.1080/18811248.2007.9711867 10.3117/plantroot.8.72 10.1016/j.cell.2008.02.001 10.11648/j.plant.20210903.12 10.1016/j.tplants.2016.08.002 10.5511/plantbiotechnology.19.0531b 10.1111/tpj.12388 10.1002/jpln.19721320211 10.1007/s00253-010-2572-9 10.1016/j.ecoenv.2019.109625 10.3390/plants8010008 10.1016/j.jenvrad.2004.01.037 10.1016/j.bbamcr.2015.02.017 10.3390/ijms22084094 10.1007/s12374-015-0256-9 10.1080/18811248.2007.9711851 10.3390/molecules21010090 10.1093/jxb/erq213 10.1080/15592324.2018.1460048 10.1271/bbb.120928 10.3117/plantroot.13.9 10.1021/jf501257r 10.3390/molecules24213825 10.3117/plantroot.11.1 10.4172/2168-9652.1000207 10.1146/annurev.arplant.55.031903.141701 10.1021/jf5058777 10.1007/s00425-011-1372-5 10.1111/j.1399-3054.1962.tb08052.x 10.1242/dev.136465 10.1094/CCHEM.1999.76.3.350 10.1111/j.1365-313X.2006.02837.x 10.1080/15592324.2015.1017698 10.1104/pp.110.162982 10.1016/j.plaphy.2014.03.037 10.1130/0016-7606(1961)72[175:DOTEIS]2.0.CO;2 10.1016/j.jplph.2018.12.003 10.1134/S1021443712060052 10.1104/pp.65.3.478 10.1016/j.jplph.2013.05.017 10.1016/j.crvi.2013.10.007 10.1080/13510002.2021.2002001 10.1080/15592324.2018.1451708 10.1104/pp.15.00961 |
| ContentType | Journal Article |
| Copyright | 2023 Japanese Society for Root Research |
| Copyright_xml | – notice: 2023 Japanese Society for Root Research |
| DBID | AAYXX CITATION |
| DOI | 10.3117/plantroot.17.36 |
| DatabaseName | CrossRef |
| DatabaseTitle | CrossRef |
| DatabaseTitleList | |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Botany |
| EISSN | 1881-6754 |
| EndPage | 44 |
| ExternalDocumentID | 10_3117_plantroot_17_36 article_plantroot_17_0_17_36_article_char_en |
| GroupedDBID | 123 29O 2WC 5VS 7.U ABDBF ALMA_UNASSIGNED_HOLDINGS CS3 E3Z ECGQY ESX GROUPED_DOAJ JSF JSH KQ8 M~E OK1 RJT RZJ TKC TR2 TUS AAYXX CITATION |
| ID | FETCH-LOGICAL-c2636-adcd750f5cf53e2ade720e616535a820da656fee1588b8db53f4fb94684a07a13 |
| ISSN | 1881-6754 |
| IngestDate | Fri Aug 23 04:04:27 EDT 2024 Tue Mar 26 04:03:21 EDT 2024 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | false |
| IsScholarly | true |
| Language | English |
| LinkModel | OpenURL |
| MergedId | FETCHMERGED-LOGICAL-c2636-adcd750f5cf53e2ade720e616535a820da656fee1588b8db53f4fb94684a07a13 |
| OpenAccessLink | https://www.jstage.jst.go.jp/article/plantroot/17/0/17_36/_article/-char/en |
| PageCount | 9 |
| ParticipantIDs | crossref_primary_10_3117_plantroot_17_36 jstage_primary_article_plantroot_17_0_17_36_article_char_en |
| PublicationCentury | 2000 |
| PublicationDate | 2023 2023-00-00 |
| PublicationDateYYYYMMDD | 2023-01-01 |
| PublicationDate_xml | – year: 2023 text: 2023 |
| PublicationDecade | 2020 |
| PublicationTitle | Plant Root |
| PublicationTitleAlternate | Plant Root |
| PublicationYear | 2023 |
| Publisher | Japanese Society for Root Research |
| Publisher_xml | – name: Japanese Society for Root Research |
| References | Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J, Denoux C, Hayes T, Gerrish C, Davies DR, Ausubel F.M, Bolwell G.P 2006 Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 47: 851-863. Turekian KK, Wedepohl KH 1961 Distribution of the elements in some major units of the Earth's crust. Geol. Soc. Am. Bull. 72: 175-192. Sowa I, Wojciak-Kosior M, Strzemski M, Dresler S, Szwerc W, Blicharski T, Szymczak G, Kocjan R 2014 Biofortification of Soy (Glycine max (L.) Merr.) with strontium ions. J. Agric. Food Chem. 62: 5248-5252. Gardner JL, Al-Hamdani SH 1997 Interactive effects of aluminium and humic substances on Salvinia. J. Aquat. Plant Manage. 35: 30-34. Hanaka A, Dresler S, Wójciak-Kosior M, Strzemski M, Kováčik J, Latalski M, Zawiślak G, Sowa I 2019 The impact of long-and short-term strontium treatment on metabolites and minerals in Glycine max. Molecules 23: 3825. Nagata T 2014 Expression analysis of new Metallothionein2-like protein under mercury stress in tomato seedling. Plant Root 8: 72-81. Adamakis IDS, Panteris E, Eleftheriou EP 2011 The fatal effect of tungsten on Pisum sativum L., root cells: Indications for endoplasmic reticulum stress-induced programmed cell death. Planta 234: 21-34. Hossain MS, Ye W, Hossain MA, Okuma E, Uraji M, Nakamura Y, Mori IC, Murata Y 2013 Glucosinolate degradation products, isothiocyanates, nitriles, and thiocyanates, induce stomatal closure accompanied by peroxidase-mediated reactive oxygen species production in Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 77: 977-983. Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA 2015 The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol. 169: 1397-1404. Cha JY, Barman DN, Kim MG, Kim WY 2015 Stress defense mechanisms of NADPH-dependent thioredoxin reductases (NTRs) in plants. Plant Signal. Behav. 10: e1017698. Wojciak-Kosior M, Sowa I, Blicharski T, Strzemski M, Dresler S, Szymczak G, Wnorowski A, Kocjan R, Świeboda R 2016 The stimulatory effect of strontium ions on phytoestrogens content in Glycine max (L.) Merr. Molecules 21: 90-98. Meena D, Singh SK, Chaudhuri SK 2013 Effect of Sr2+ on mitotic activity and chromosomal behavior in root meristem of Allium cepa L. Int. J. Agric. Env. Biotech. 6: 197-201. Kalingan M, Rajagopal S, Venkatachalam R 2016 Effect of metal stress due to strontium and the mechanisms of tolerating it by Amaranthus caudatus Linn. Biochem. Physiol. 5: 207-212. Filippi A, Zancani M, Petrussa E, Braidot E 2019 Caspase-3-like activity and proteasome degradation in grapevine suspension cell cultures undergoing silver-induced programmed cell death. J. Plant Physiol. 233: 42-51. Nagata T 2019 Effect of strontium on the growth, ion balance, and suberin induction in Solanum lycopersicum. Plant Root 13: 9-14. Goto F, Enomoto Y, Shoji K, Shimada H, Yoshihara T 2019 Copper treatment of peach leaves causes lesion formation similar to the biotic stress response. Plant Biotechnol. 36: 135-142. Hasegawa J, Sakamoto Y, Nakagami S, Aida M, Sawa S, Matsunaga S 2016 Three-dimensional imaging of plant organs using a simple and rapid transparency technique. Plant Cell Physiol. 57: 462-472. Hassanien SE, Ramadan AM, Azeiz AZ, Mohammed RA, Hassan SM, Shokry AM, Atef A, Kamal KB, Rabah S, Sabir JS, Abuzinadah OA, El-Domyati FM, Martin GB, Bahieldin A 2013 Thymoquinone causes multiple effects, including cell death, on dividing plant cells. Comptes Rendus Biol. 336: 546-56. Hashem AM, Moore S, Chen S, Hu C, Zhao Q, Elesawi IE, Feng Y, Topping JF, Liu J, Lindsey K, Chen C 2021 Putrescine Depletion affects Arabidopsis root meristem size by modulating auxin and cytokinin signaling and ROS accumulation. Int. J. Mol. Sci. 22: 4094. Apel K, Hirt H 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55: 373-399. Abdel-Aal el-SM, Huncl P 1999 A rapid method for quantifying total anthocyanins in blue aleurone and purple pericarp wheats. Cereal Chem. 76: 350-354. Chu Q, Watanabe T, Sha Z, Osaki M, Shinano T 2015 Interactions between Cs, Sr, and other nutrients and trace element accumulation in Amaranthus shoot in response to variety effect. J. Agric. Food Chem. 63: 2355-2363. Tsukada H, Takeda A, Takahashi T, Hasegawa H, Hisamatsu S, Inaba J 2005 Uptake and distribution of 90Sr and stable Sr in rice plants. J Environ. Radioact. 81: 221-231. Xu J, Yin H, Li Y, Liu X 2010 Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum. Plant Physiol. 154: 1319-1334. Jin T, Wang X, Deng Z, Liu X, Liang D 2021 ROS-induced dramatic lipid changes in Arabidopsis. Redox Rep. 26: 190-196. Mittler, R. 2017 ROS are good. Trends Plant Sci. 22: 11-19. Murashige T, Skoog F 1962 A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol. Plant 15: 473-497. Uchida S, Tagami K, Hirai I 2007b Soil-to-plant transfer factors of stable elements and naturally occurring radionuclides (2) rice collected in Japan. J. Nuclear Sci. Tech. 44: 779-790. Kanter U, Hauser A, Michalke B, Dräxl S, Schäffner RA 2010 Caesium and strontium accumulation in shoots of Arabidopsis thaliana: genetic and physiological aspects. J. Exp. Bot. 61: 3995-4009. Dutta S, Mitra M, Agarwal P, Mahapatra K, De S, Sett U, Roy S 2018 Oxidative and genotoxic damages in plants in response to heavy metal stress and maintenance of genome stability. Plant Signal Behav. 13: e1460048. Uchida S, Tagami K, Hirai I 2007a Soil-to-plant transfer factors of stable elements and naturally occurring radionuclides (1) upland field crops collected in Japan. J. Nuclear Sci. Tech. 44: 628-640. Di Mambro R, Sabatini S, Dello Ioio R 2018 Patterning the Axes: A Lesson from the Root. Plants (Basel) 8: 8. Himschoot E, Beeckman T, Friml J, Vanneste S 2015 Calcium is an organizer of cell polarity in plants. Biochim. Biophys. Acta. 1853: 2168-2172. Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K, Michael AJ, Tohge T, Yamazaki M, Saito K 2014 Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 77: 367- 379. Moran R, Porath D 1980 Chlorophyll determination in intact tissues using N,N-dimethyl formamide. Plant Physiol. 65: 478-489. Agency for Toxic Substances and Disease Registry (ATSDR) 2014 Toxicological profile for strontium Atlanta, GA: U.S. Department of Health and Human Services, Public Health Service. Kirisiuk Y, Mackievic V, Zvanarou S, Przhevalskaya D, Leschenka Y, Demidchik V 2016 The effect of copper nanoparticles on growth, cell viability and signaling processes of wheat plants. Plant Signalling & Behavior 4th International Symposium Proceedings, p123. Dinneny JR, Benfey PN 2008 Plant stem cell niches: standing the test of time. Cell 132: 553-557. Nagata T 2015 Growth inhibition and IRT1 induction of Arabidopsis thaliana in response to bismuth. J. Plant Biol. 58: 311-317. Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F, Bennett MJ, Périlleux C, Beeckman T, Draye X 2016 RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 14: 3328-3339. Zhang Y, De Stefano R, Robine M, Butelli E, Bulling K, Hill L, Rejzek M, Martin C, Schoonbeek HJ 2015 Different reactive oxygen species scavenging properties of flavonoids determine their abilities to extend the shelf life of tomato. Plant Physiol. 169: 1568-1583. Nishimura M, Nagata T 2021 Phytotoxicity and iron homeostasis disturbance of bismuth on IRT1 promoter knockout Arabidopsis thaliana. Plant 9: 48-57. Nagata T, Morita H, Akizawa T, Pan-Hou H 2010 Development of a transgenic tobacco plant for phytoremediation of methylmercury pollution. Appl. Microbiol. Biotechnol. 87: 781-786. Nagata T 2017 Effect of Pseudomonas fluorescens inoculation on the improvement of iron deficiency in tomato. Plant Root 11: 1-9. Burger A, Weidinger M, Adlassnig W, Puschenreiter M, Lichtscheidl I 2019 Response of Arabidopsis halleri to cesium and strontium in hydroponics: extraction potential and effects on morphology and physiology. Ecotoxicol. and Environ. Safe. 184: 109625. Xu H, Xu W, Xi H, Ma W, He Z, Ma M 2013 The ER luminal binding protein (BiP) alleviates Cd2+-induced programmed cell death through endoplasmic reticulum stress-cell death signalling pathway in tobacco cells. J. Plant Physiol. 170: 1434-1441. Xu Z, Rothstein SJ 2018 ROS-Induced anthocyanin production provides feedback protection by scavenging ROS and maintaining photosynthetic capacity in Arabidopsis. Plant Signal. Behav. 13: e1451708. Bussler W, Epstein E 1972 Mineral nutrition of plants: Principles and perspectives. J. Plant Nut. Soil Sci. 132: 158-159. Chen M, Tang YL, Ao J, Wang D 2012 Effects of strontium on photosynthetic characteristics of oilseed rape seedlings. Russian J. Plant Physiol. 59: 772-780. Huang W, Yang X, Yao S, LwinOo T, He H, Wang A, Li C, He L 2014 Reactive oxygen species burst induced by aluminum stress triggers mitochondria-dependent programmed cell death in peanut root tip cells. Plant Physiol. Biochem. 82: 76-84. 44 45 46 47 48 49 50 10 11 12 13 14 15 16 17 18 19 1 2 3 4 5 6 7 8 9 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 |
| References_xml | – ident: 18 doi: 10.1093/pcp/pcw027 – ident: 50 doi: 10.1104/pp.15.00346 – ident: 45 doi: 10.1080/18811248.2007.9711867 – ident: 32 doi: 10.3117/plantroot.8.72 – ident: 12 doi: 10.1016/j.cell.2008.02.001 – ident: 38 doi: 10.11648/j.plant.20210903.12 – ident: 29 doi: 10.1016/j.tplants.2016.08.002 – ident: 16 doi: 10.5511/plantbiotechnology.19.0531b – ident: 37 doi: 10.1111/tpj.12388 – ident: 7 doi: 10.1002/jpln.19721320211 – ident: 36 doi: 10.1007/s00253-010-2572-9 – ident: 6 doi: 10.1016/j.ecoenv.2019.109625 – ident: 13 doi: 10.3390/plants8010008 – ident: 42 doi: 10.1016/j.jenvrad.2004.01.037 – ident: 21 doi: 10.1016/j.bbamcr.2015.02.017 – ident: 19 doi: 10.3390/ijms22084094 – ident: 33 doi: 10.1007/s12374-015-0256-9 – ident: 44 doi: 10.1080/18811248.2007.9711851 – ident: 46 doi: 10.3390/molecules21010090 – ident: 26 doi: 10.1093/jxb/erq213 – ident: 14 doi: 10.1080/15592324.2018.1460048 – ident: 22 doi: 10.1271/bbb.120928 – ident: 35 doi: 10.3117/plantroot.13.9 – ident: 41 doi: 10.1021/jf501257r – ident: 27 – ident: 17 doi: 10.3390/molecules24213825 – ident: 34 doi: 10.3117/plantroot.11.1 – ident: 25 doi: 10.4172/2168-9652.1000207 – ident: 4 doi: 10.1146/annurev.arplant.55.031903.141701 – ident: 10 doi: 10.1021/jf5058777 – ident: 2 doi: 10.1007/s00425-011-1372-5 – ident: 31 doi: 10.1111/j.1399-3054.1962.tb08052.x – ident: 39 doi: 10.1242/dev.136465 – ident: 28 – ident: 1 doi: 10.1094/CCHEM.1999.76.3.350 – ident: 5 doi: 10.1111/j.1365-313X.2006.02837.x – ident: 8 doi: 10.1080/15592324.2015.1017698 – ident: 48 doi: 10.1104/pp.110.162982 – ident: 23 doi: 10.1016/j.plaphy.2014.03.037 – ident: 3 – ident: 43 doi: 10.1130/0016-7606(1961)72[175:DOTEIS]2.0.CO;2 – ident: 15 doi: 10.1016/j.jplph.2018.12.003 – ident: 11 – ident: 9 doi: 10.1134/S1021443712060052 – ident: 30 doi: 10.1104/pp.65.3.478 – ident: 47 doi: 10.1016/j.jplph.2013.05.017 – ident: 20 doi: 10.1016/j.crvi.2013.10.007 – ident: 24 doi: 10.1080/13510002.2021.2002001 – ident: 49 doi: 10.1080/15592324.2018.1451708 – ident: 40 doi: 10.1104/pp.15.00961 |
| SSID | ssj0069515 |
| Score | 2.2794466 |
| Snippet | Strontium (Sr) is a known non-essential element for plants. However, its toxic effects at high concentration on plants remain unclear. Here the effects of Sr... |
| SourceID | crossref jstage |
| SourceType | Aggregation Database Publisher |
| StartPage | 36 |
| SubjectTerms | Arabidopsis thaliana calcium cell death reactive oxygen species (ROS) strontium |
| Title | Strontium-induced mineral imbalance, cell death, and reactive oxygen species generation in Arabidopsis thaliana |
| URI | https://www.jstage.jst.go.jp/article/plantroot/17/0/17_36/_article/-char/en |
| Volume | 17 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| ispartofPNX | Plant Root, 2023, Vol.17, pp.36-44 |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lb9QwELZg2wMXxFOUl3zggJSmbPyKI05doKqQ6AG2Um-RHTs0RbtZlaxE-fXMxEmaXThQuFhRNrFX_qyZbybzIOQVqDAPatvFzhUsFk7qWGdGxiIrrCkZT63HBOdPJ-r4VHw8k2fXXVHb7JLGHhQ__5hX8i-owj3AFbNkb4DsMCncgGvAF0ZAGMa_wvgL-rGbar2IwbJe45f8RdVWkY6qhcWYxeAhR-d85JDr9bGawBRbORfVP65g9gjzLcFkxn7KvjsS6Ae5NLZy9QprljTnrUPEjMksNjxqos91PYTOnJivJtDRufnmv59XY6dCyPgNoh5UNLa-3AgaxYmGSMCgOIK01DqJweIQG-I0HclDrkaaNRR63JbZPGkLPa3wL4OxgF2SD_hWdexW33bbnA9P5kmaT3HgKu9_xFw1OBq3yQ5LMykmZOdw9n521CtnBYRShgpPuO6brVU3yMnuBfDzPravpRvze-RuZyfQw7DgfXLLLx-Q3VkNXP7qIal_Q552yNMB-X2KuNMW930KqNMedRpQpx3q9Bp1Wi3pCHXao_6InB59mL87jrvWGXHBFFexcYUDLljKopTcM-N8yqZeJUpyaYD0OQM8vvQ-kVpb7azkpShtJpQWZpqahD8mk2W99E8ILVU6dSLTPtMMaxFprosEDWXJnJSG7ZHX_Z7lq1AhJQfLErd3Eyqu9sjbsKfDgzfB9Ol_vf2M3MGDHrxnz8mkuVz7F8AnG_uyOyO_AGsQiPA |
| link.rule.ids | 315,786,790,4043,27954,27955,27956 |
| linkProvider | EBSCOhost |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Strontium-induced+mineral+imbalance%2C+cell+death%2C+and+reactive+oxygen+species+generation+in+Arabidopsis+thaliana&rft.jtitle=Plant+Root&rft.au=Nagata%2C+Takeshi&rft.date=2023&rft.pub=Japanese+Society+for+Root+Research&rft.eissn=1881-6754&rft.volume=17&rft.spage=36&rft.epage=44&rft_id=info:doi/10.3117%2Fplantroot.17.36&rft.externalDocID=article_plantroot_17_0_17_36_article_char_en |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1881-6754&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1881-6754&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1881-6754&client=summon |