Multi-Component Antioxidative System and Robust Carbohydrate Status, the Essence of Plant Arsenic Tolerance

. 2020 Mar 27 ; 9 (4) : . [epub] 20200327

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32230748

Grantová podpora
1018216 Grantová Agentura, Univerzita Karlova
LO 1417 Ministerstvo Školství, Mládeže a Tělovýchovy

Arsenic (As) contaminates the food chain and decreases agricultural production through impairing plants, particularly due to oxidative stress. To better understand the As tolerance mechanisms, two contrasting tobacco genotypes: As-sensitive Nicotiana sylvestris and As-tolerant N.tabacum, cv. 'Wisconsin' were analyzed. The most meaningful differences were found in the carbohydrate status, neglected so far in the As context. In the tolerant genotype, contrary to the sensitive one, net photosynthesis rates and saccharide levels were unaffected by As exposure. Importantly, the total antioxidant capacity was far stronger in the As-tolerant genotype, based on higher antioxidants levels (e.g., phenolics, ascorbate, glutathione) and activities and/or appropriate localizations of antioxidative enzymes, manifested as reverse root/shoot activities in the selected genotypes. Accordingly, malondialdehyde levels, a lipid peroxidation marker, increased only in sensitive tobacco, indicating efficient membrane protection in As-tolerant species. We bring new evidence of the orchestrated action of a broad spectrum of both antioxidant enzymes and molecules essential for As stress coping. For the first time, we propose robust carbohydrate metabolism based on undisturbed photosynthesis to be crucial not only for subsidizing C and energy for defense but also for participating in direct reactive oxygen species (ROS) quenching. The collected data and suggestions can serve as a basis for the selection of plant As phytoremediators or for targeted breeding of tolerant crops.

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Panda S.K., Upadhyay R.K., Nath S. Arsenic stress in plants. J. Agron. Crop Sci. 2010;196:161–174. doi: 10.1111/j.1439-037X.2009.00407.x. DOI

Quaghebeur M., Rengel Z. Arsenic speciation governs arsenic uptake and transport in terrestrial plants. Microchim. Acta. 2005;151:141–152. doi: 10.1007/s00604-005-0394-8. DOI

Panuccio M.R., Logoteta B., Beone G.M., Cagnin M., Cacco G. Arsenic uptake and speciation and the effects of phosphate nutrition in hydroponically grown kikuyu grass (Pennisetum clandestinum Hochst) Environ. Sci. Pollut. Res. 2012;19:3046–3053. doi: 10.1007/s11356-012-0820-5. PubMed DOI

Chakrabarty D., Trivedi P.K., Misra P., Tiwari M., Shri M., Shukla D., Kumar S., Rai A., Pandey A., Nigam D., et al. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere. 2009;74:688–702. doi: 10.1016/j.chemosphere.2008.09.082. PubMed DOI

Finnegan P.M., Chen W. Arsenic toxicity: The effects on plant metabolism. Front. Physiol. 2012;3:182. doi: 10.3389/fphys.2012.00182. PubMed DOI PMC

Mabrouk B., Kaab S.B., Rezgui M., Majdoub N., da Silva J.A.T., Kaab L.B.B. Salicylic acid alleviates arsenic and zinc toxicity in the process of reserve mobilization in germinating fenugreek (Trigonella foenum-graecum L.) seeds. S. Afr. J. Bot. 2019;124:235–243. doi: 10.1016/j.sajb.2019.05.020. DOI

Kumar N., Gautam A., Dubey A.K., Ranjan R., Pandey A., Kumari B., Singh G., Mandotra S., Chauhan P.S., Srikrishna S., et al. GABA mediated reduction of arsenite toxicity in rice seedling through modulation of fatty acids, stress responsive amino acids and polyamines biosynthesis. Ecotoxicol. Environ. Saf. 2019;173:15–27. doi: 10.1016/j.ecoenv.2019.02.017. PubMed DOI

Suriyagoda L.D.B., Dittert K., Lambers H. Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric. Ecosyst. Environ. 2018;253:23–37. doi: 10.1016/j.agee.2017.10.017. DOI

Zhao F., McGrath S.P., Meharg A.A. Arsenic as a food chain contaminant: Mechanisms of plant uptake and metabolism and mitigation strategies. Annu. Rev. Plant Biol. 2010;61:535–559. doi: 10.1146/annurev-arplant-042809-112152. PubMed DOI

Shin H., Shin H.S., Dewbre G.R., Harrison M.J. Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J. 2004;39:629–642. doi: 10.1111/j.1365-313X.2004.02161.x. PubMed DOI

Kamiya T., Islam M.R., Duan G., Uraguchi S., Fujiwara T. Phosphate deficiency signaling pathway is a target of arsenate and phosphate transporter OsPT1 is involved in As accumulation in shoots of rice. Soil Sci. Plant Nutr. 2013;59:580–590. doi: 10.1080/00380768.2013.804390. DOI

Ma J.F., Yamaji N., Mitani N., Xu X.-y., Su Y.-h., Mcgrath S.P., Zhao F.-j. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc. Natl. Acad. Sci. USA. 2008;105:9931–9935. doi: 10.1073/pnas.0802361105. PubMed DOI PMC

Hoffmann M., Mikutta C., Kretzschmar R. Arsenite binding to sulfhydryl groups in the absence and presence of ferrihydrite: A model study. Environ. Sci. Technol. 2014;48:3822–3831. doi: 10.1021/es405221z. PubMed DOI

Naeem M., Aftab T., Ansari A.A., Shabbir A., Masroor M., Khan A., Uddin M. Arsenic exposure modulates physiological attributes and artemisinin biosynthesis in Artemisia annua L. Int. J. Herb. Med. 2019;7:19–26.

Naeem M., Nabi A., Aftab T., Khan M.M.A. Oligomers of carrageenan regulate functional activities and artemisinin production in Artemisia annua L. exposed to arsenic stress. Protoplasma. 2019 doi: 10.1007/s00709-019-01475-y. PubMed DOI

Gupta P., Seth C.S. Nitrate supplementation attenuates As(V) toxicity in Solanum lycopersicum L. cv Pusa Rohini: Insights into As(V) sub-cellular distribution, photosynthesis, nitrogen assimilation, and DNA damage. Plant Physiol. Biochem. 2019;139:44–55. doi: 10.1016/j.plaphy.2019.03.007. PubMed DOI

Gusman G.S., Oliveira J.A., Farnese F.S., Cambraia J. Arsenate and arsenite: The toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol. Plant. 2013;35:1201–1209. doi: 10.1007/s11738-012-1159-8. DOI

Shahid M.A., Balal R.M., Khan N., Zotarelli L., Liu G.D., Sarkhosh A., Fernandez-Zapata J.C., Martinez Nicolas J.J., Garcia-Sanchez F. Selenium impedes cadmium and arsenic toxicity in potato by modulating carbohydrate and nitrogen metabolism. Ecotoxicol. Environ. Saf. 2019;180:588–599. doi: 10.1016/j.ecoenv.2019.05.037. PubMed DOI

Singh R., Jha A.B., Misra A.N., Sharma P. Differential responses of growth, photosynthesis, oxidative stress, metals accumulation and NRAMP genes in contrasting Ricinus communis genotypes under arsenic stress. Environ. Sci. Pollut. Res. 2019;26:31166–31177. doi: 10.1007/s11356-019-06243-2. PubMed DOI

Abbas G., Murtaza B., Bibi I., Shahid M., Niazi N.K., Khan M.I., Amjad M., Hussain M. Arsenic uptake, toxicity, detoxification, and speciation in plants: Physiological, biochemical, and molecular aspects. Int. J. Environ. Res. Public Health. 2018;15:59. doi: 10.3390/ijerph15010059. PubMed DOI PMC

Kofronova M., Maskova P., Lipavska H. Two facets of world arsenic problem solution: Crop poisoning restriction and enforcement of phytoremediation. Planta. 2018;248:19–35. doi: 10.1007/s00425-018-2906-x. PubMed DOI

Dubey R.S., Singh A.K. Salinity induces accumulation of soluble sugars and alters the activity of sugar metabolising enzymes in rice plants. Biol. Plant. 1999;42:233–239. doi: 10.1023/A:1002160618700. DOI

Mishra P., Dubey R.S. Effect of aluminium on metabolism of starch and sugars in growing rice seedlings. Acta Physiol. Plant. 2008;30:265–275. doi: 10.1007/s11738-007-0115-5. DOI

Hartley-Whitaker J., Ainsworth G., Meharg A.A. Copper- and arsenate-induced oxidative stress in Holcus lanatus L. clones with differential sensitivity. Plant Cell Environ. 2001;24:713–722. doi: 10.1046/j.0016-8025.2001.00721.x. DOI

Kumari S., Khan A., Singh P., Dwivedi S.K., Ojha K.K., Srivastava A. Mitigation of As toxicity in wheat by exogenous application of hydroxamate siderophore of Aspergillus origin. Acta Physiol. Plant. 2019;41:107. doi: 10.1007/s11738-019-2902-1. DOI

Kumari A., Pandey N., Pandey-Rai S. Exogenous salicylic acid-mediated modulation of arsenic stress tolerance with enhanced accumulation of secondary metabolites and improved size of glandular trichomes in Artemisia annua L. Protoplasma. 2018;255:139–152. doi: 10.1007/s00709-017-1136-6. PubMed DOI

Karam E.A., Keramat B., Asrar Z., Mozafari H. Study of interaction effect between triacontanol and nitric oxide on alleviating of oxidative stress arsenic toxicity in coriander seedlings. J. Plant Interact. 2017;12:14–20. doi: 10.1080/17429145.2016.1267270. DOI

Matros A., Peshev D., Peukert M., Mock H.P., Van Den Ende W. Sugars as hydroxyl radical scavengers: Proof-of-concept by studying the fate of sucralose in Arabidopsis. Plant J. 2015;82:822–839. doi: 10.1111/tpj.12853. PubMed DOI

Salerno G.L., Curatti L. Origin of sucrose metabolism in higher plants: When, how and why? Trends Plant Sci. 2003;8:63–69. doi: 10.1016/S1360-1385(02)00029-8. PubMed DOI

Ramon M., Rolland F., Sheen J. Sugar sensing and signaling. Arabidopsis Book. 2008;6:e0117. doi: 10.1199/tab.0117. PubMed DOI PMC

Siddiqui H., Sami F., Hayat S. Glucose: Sweet or bitter effects in plants—A review on current and future perspective. Carbohydr. Res. 2020;487 doi: 10.1016/j.carres.2019.107884. PubMed DOI

Solfanelli C., Poggi A., Loreti E., Alpi A., Perata P. Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. Plant Physiol. 2006;140:637–646. doi: 10.1104/pp.105.072579. PubMed DOI PMC

Bolouri-Moghaddam M.R., Le Roy K., Xiang L., Rolland F., Van den Ende W. Sugar signalling and antioxidant network connections in plant cells. FEBS J. 2010;277:2022–2037. doi: 10.1111/j.1742-4658.2010.07633.x. PubMed DOI

Nishikawa F., Kato M., Hyodo H., Ikoma Y., Sugiura M., Yano M. Effect of sucrose on ascorbate level and expression of genes involved in the ascorbate biosynthesis and recycling pathway in harvested broccoli florets. J. Exp. Bot. 2005;56:65–72. doi: 10.1093/jxb/eri007. PubMed DOI

Jha A.B., Dubey R.S. Carbohydrate metabolism in growing rice seedlings under arsenic toxicity. J. Plant Physiol. 2004;161:867–872. doi: 10.1016/j.jplph.2004.01.004. PubMed DOI

Sanglard L.M.V.P., Detmann K.C., Martins S.C.V., Teixeira R.A., Pereira L.F., Sanglard M.L., Fernie A.R., Araújo W.L., DaMatta F.M. The role of silicon in metabolic acclimation of rice plants challenged with arsenic. Environ. Exp. Bot. 2016;123:22–36. doi: 10.1016/j.envexpbot.2015.11.004. DOI

Li C.x., Feng S.l., Shao Y., Jiang L.n., Lu X.y., Hou X.l. Effects of arsenic on seed germination and physiological activities of wheat seedlings. J. Environ. Sci. 2007;19:725–732. doi: 10.1016/S1001-0742(07)60121-1. PubMed DOI

Campos N.V., Araújo T.O., Arcanjo-Silva S., Freitas-Silva L., Azevedo A.A., Nunes-Nesi A. Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress. Physiol. Plant. 2016;157:135–146. doi: 10.1111/ppl.12426. PubMed DOI

Tremlová J., Sehnal M., Száková J., Goessler W., Steiner O., Najmanová J., Horáková T., Tlustoš P. A profile of arsenic species in different vegetables growing in arsenic-contaminated soils. Arch. Agron. Soil Sci. 2017;63:918–927. doi: 10.1080/03650340.2016.1242721. DOI

Strasser B.J. Donor side capacity of Photosystem II probed by chlorophyll a fluorescence transients. Photosynth. Res. 1997;52:147–155. doi: 10.1023/A:1005896029778. DOI

Wellburn A.R. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 1994;144:307–313. doi: 10.1016/S0176-1617(11)81192-2. DOI

Kofronova M., Hrdinova A., Maskova P., Soudek P., Tremlova J., Pinkas D., Lipavska H. Strong antioxidant capacity of horseradish hairy root cultures under arsenic stress indicates the possible use of Armoracia rusticana plants for phytoremediation. Ecotoxicol. Environ. Saf. 2019;174:295–304. doi: 10.1016/j.ecoenv.2019.02.028. PubMed DOI

Hodges D.M., Delong J.M., Forney C.F., Prange R.K., Delong J.M., Hodges D.M., Forney C.F., Prange R.K. Improving the thiobarbituric anthocyanin for estimating lipid peroxidation in plant tissues containing and other interfering. Planta. 1999;207:604–611. doi: 10.1007/s004250050524. DOI

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Habig W.H., Pabst M.J., Jakoby W.B. Glutathione S-Transferases The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 1974;249:7130–7139. PubMed

Hiner a.N., Rodríguez-López J.N., Arnao M.B., Lloyd Raven E., García-Cánovas F., Acosta M. Kinetic study of the inactivation of ascorbate peroxidase by hydrogen peroxide. Biochem. J. 2000;348:321–328. doi: 10.1042/bj3480321. PubMed DOI PMC

Beers R.F., Sizer I.W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 1952;195:133–140. PubMed

Nakano Y., Asada K. Hydrogen peroxide is scavenged by ascorbato specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1987;22:867–880. doi: 10.1093/oxfordjournals.pcp.a076232. DOI

Singleton V.L., Salgues M., Zaya J., Trousdale E. Caftaric acid disappearance and conversion to products of enzymic oxidation in grape must and wine. Am. J. Enol. Vitic. 1985;36:50–56.

Mancinelli A.L., Huangyang C.P., Lindquist P., Anderson O.R., Rabino I. Photocontrol of Anthocyanin Synthesis III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiol. 1975;55:251–257. doi: 10.1104/pp.55.2.251. PubMed DOI PMC

Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980;106:207–212. doi: 10.1016/0003-2697(80)90139-6. PubMed DOI

Mishra S., Alfeld M., Sobotka R., Andresen E., Falkenberg G., Küpper H. Analysis of sublethal arsenic toxicity to Ceratophyllum demersum: Subcellular distribution of arsenic and inhibition of chlorophyll biosynthesis. J. Exp. Bot. 2016;67:4639–4646. doi: 10.1093/jxb/erw238. PubMed DOI PMC

Rai A.N., Srivastava S., Paladi R., Suprasanna P. Calcium supplementation modulates arsenic-induced alterations and augments arsenic accumulation in callus cultures of Indian mustard (Brassica juncea (L.) Czern.) Protoplasma. 2012;249:725–736. doi: 10.1007/s00709-011-0316-z. PubMed DOI

Karimi N., Shayesteh L.S., Ghasmpour H., Alavi M. Effects of arsenic on growth, photosynthetic activity, and accumulation in two new hyperaccumulating populations of Isatis cappadocica desv. J. Plant Growth Regul. 2013;32:823–830. doi: 10.1007/s00344-013-9350-8. DOI

Chandrakar V., Dubey A., Keshavkant S. Modulation of antioxidant enzymes by salicylic acid in arsenic exposed Glycine max L. J. Soil Sci. Plant Nutr. 2016;16:662–676. doi: 10.4067/S0718-95162016005000048. DOI

Marin A.R., Pezeshki S.R., Masschelen P.H., Choi H.S. Effect of dimethylarsenic acid (dmaa) on growth, tissue arsenic, and photosynthesis of rice plants. J. Plant Nutr. 1993;16:865–880. doi: 10.1080/01904169309364580. DOI

Stoeva N., Berova M., Zlatev Z. Physiological response of maize to arsenic contamination. Biol. Plant. 2003;47:449–452. doi: 10.1023/B:BIOP.0000023893.12939.48. DOI

Liu Y., Damaris R.N., Yang P. Proteomics analysis identified a DRT protein involved in arsenic resistance in Populus. Plant Cell Rep. 2017;36:1855–1869. doi: 10.1007/s00299-017-2199-8. PubMed DOI

Malik J.A., Goel S., Sandhir R., Nayyar H. Uptake and distribution of arsenic in chickpea: Effects on seed yield and seed composition. Commun. Soil Sci. Plant Anal. 2011;42:1728–1738. doi: 10.1080/00103624.2011.584593. DOI

Zou J.H., Yu K.L., Zhang Z.G., Jiang W.S., Liu D.H. Antioxidant response system and chlorophyll fluorescence in chromium (VI)—Treated Zea mays L. seedlings. Acta Biol. Crac. Ser. Bot. 2009;51:23–33.

Filek M., Kościelniak J., Łabanowska M., Bednarska E., Bidzińska E. Selenium-induced protection of photosynthesis activity in rape (Brassica napus) seedlings subjected to cadmium stress. Fluorescence and EPR measurements. Photosynth. Res. 2010;105:27–37. doi: 10.1007/s11120-010-9551-y. PubMed DOI

Mishra R.K., Kumar J., Srivastava P.K., Bashri G., Prasad S.M. PSII photochemistry, oxidative damage and anti-oxidative enzymes in arsenate-stressed Oryza sativa L. seedlings. Chem. Ecol. 2017;33:34–50. doi: 10.1080/02757540.2016.1265516. DOI

Tewari A., Singh R., Singh N.K., Rai U.N. Amelioration of municipal sludge by Pistia stratiotes L.: Role of antioxidant enzymes in detoxification of metals. Bioresour. Technol. 2008;99:8715–8721. doi: 10.1016/j.biortech.2008.04.018. PubMed DOI

Sanglard L.M.V.P., Martins S.C.V., Detmann K.C., Silva P.E.M., Lavinsky A.O., Silva M.M., Detmann E., Araújo W.L., DaMatta F.M. Silicon nutrition alleviates the negative impacts of arsenic on the photosynthetic apparatus of rice leaves: An analysis of the key limitations of photosynthesis. Physiol. Plant. 2014;152:355–366. doi: 10.1111/ppl.12178. PubMed DOI

Baker N.R. Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annu. Rev. Plant Biol. 2008;59:89–113. doi: 10.1146/annurev.arplant.59.032607.092759. PubMed DOI

Vernay P., Gauthier-Moussard C., Hitmi A. Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere. 2007;68:1563–1575. doi: 10.1016/j.chemosphere.2007.02.052. PubMed DOI

Stoeva N., Berova M., Zlatev Z. Effect of arsenic on some physiological parameters in bean plants. Biol. Plant. 2005;49:293–296. doi: 10.1007/s10535-005-3296-z. DOI

Vezza M.E., Llanes A., Travaglia C., Agostini E., Talano M.A. Arsenic stress effects on root water absorption in soybean plants: Physiological and morphological aspects. Plant Physiol. Biochem. 2018;123:8–17. doi: 10.1016/j.plaphy.2017.11.020. PubMed DOI

Ismail G.S.M. Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol. Plant. 2012;34:1303–1311. doi: 10.1007/s11738-012-0927-9. DOI

Meharg A.A., Hartley-Whitaker J. Arsenic uptake and metabolism in arsenic resistant and nonresistant plant species. New Phytol. 2002;154:29–43. doi: 10.1046/j.1469-8137.2002.00363.x. DOI

Singh H.P., Batish D.R., Kohli R.K., Arora K. Arsenic-induced root growth inhibition in mung bean (Phaseolus aureus Roxb.) is due to oxidative stress resulting from enhanced lipid peroxidation. Plant Growth Regul. 2007;53:65–73. doi: 10.1007/s10725-007-9205-z. DOI

Armendariz A.L., Talano M.A., Travaglia C., Reinoso H., Wevar Oller A.L., Agostini E. Arsenic toxicity in soybean seedlings and their attenuation mechanisms. Plant Physiol. Biochem. 2016;98:119–127. doi: 10.1016/j.plaphy.2015.11.021. PubMed DOI

Ghosh S., Shaw A.K., Azahar I., Adhikari S., Jana S., Roy S., Kundu A., Sherpa A.R., Hossain Z. Arsenate (AsV) stress response in maize (Zea mays L.) Environ. Exp. Bot. 2016;130:53–67. doi: 10.1016/j.envexpbot.2016.05.003. DOI

Gupta M., Ahmad M.A. Arsenate induced differential response in rice genotypes. Ecotoxicol. Environ. Saf. 2014;107:46–54. doi: 10.1016/j.ecoenv.2014.04.030. PubMed DOI

Cakmak I. Tansley Review No.111: Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000;146:185–205. doi: 10.1046/j.1469-8137.2000.00630.x. PubMed DOI

Pavlík M., Pavlíková D., Staszková L., Neuberg M., Kaliszová R., Száková J., Tlustoš P. The effect of arsenic contamination on amino acids metabolism in Spinacia oleracea L. Ecotoxicol. Environ. Saf. 2010;73:1309–1313. doi: 10.1016/j.ecoenv.2010.07.008. PubMed DOI

Saha J., Majumder B., Mumtaz B., Biswas A.K. Arsenic-induced oxidative stress and thiol metabolism in two cultivars of rice and its possible reversal by phosphate. Acta Physiol. Plant. 2017;39:263. doi: 10.1007/s11738-017-2562-y. DOI

Iannone M.F., Groppa M.D., Benavides M.P. Cadmium induces different biochemical responses in wild type and catalase-deficient tobacco plants. Environ. Exp. Bot. 2015;109:201–211. doi: 10.1016/j.envexpbot.2014.07.008. DOI

Anjum S.A., Tanveer M., Hussain S., Shahzad B., Ashraf U., Fahad S., Hassan W., Jan S., Khan I., Saleem M.F., et al. Osmoregulation and antioxidant production in maize under combined cadmium and arsenic stress. Environ. Sci. Pollut. Res. 2016;23:11864–11875. doi: 10.1007/s11356-016-6382-1. PubMed DOI

Juszczuk I.M., Wiktorowska A., Malusá E., Rychter A.M. Changes in the concentration of phenolic compounds and exudation induced by phosphate deficiency in bean plants (Phaseolus vulgaris L.) Plant Soil. 2004;267:41–49. doi: 10.1007/s11104-005-2569-9. DOI

Dai L.P., Xiong Z.T., Huang Y., Li M.J. Cadmium-induced changes in pigments, total phenolics, and phenylalanine ammonia-lyase activity in fronds of Azolla imbricata. Environ. Toxicol. 2006;21:505–512. doi: 10.1002/tox.20212. PubMed DOI

Kumar A., Prasad M.N.V., Sytar O. Lead toxicity, defense strategies and associated indicative biomarkers in Talinum triangulare grown hydroponically. Chemosphere. 2012;89:1056–1065. doi: 10.1016/j.chemosphere.2012.05.070. PubMed DOI

Duan G.L., Zhou Y., Tong Y.P., Mukhopadhyay R., Rosen B.P., Zhu Y.G. A CDC25 homologue from rice functions as an arsenate reductase. New Phytol. 2007;174:311–321. doi: 10.1111/j.1469-8137.2007.02009.x. PubMed DOI

Kumar A., Pal L., Agrawal V. Glutathione and citric acid modulates lead- and arsenic-induced phytotoxicity and genotoxicity responses in two cultivars of Solanum lycopersicum L. Acta Physiol. Plant. 2017;39:151. doi: 10.1007/s11738-017-2448-z. DOI

Noctor G., Foyer C.H. Ascorbate and glutathionE: Keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998;49:249–279. doi: 10.1146/annurev.arplant.49.1.249. PubMed DOI

Farooq M.A., Islam F., Ali B., Najeeb U., Mao B., Gill R.A., Yan G., Siddique K.H.M., Zhou W. Arsenic toxicity in plants: Cellular and molecular mechanisms of its transport and metabolism. Environ. Exp. Bot. 2016;132:42–52. doi: 10.1016/j.envexpbot.2016.08.004. DOI

Mylona P.V., Polidoros A.N., Scandalios J.G. Modulation of antioxidant responses by arsenic in maize. Free Radic. Biol. Med. 1998;25:576–585. doi: 10.1016/S0891-5849(98)00090-2. PubMed DOI

Ellis D.R., Gumaelius L., Indriolo E., Pickering I.J., Banks J.A., Salt D.E. A novel arsenate reductase from the arsenic hyperaccumulating fern pteris vittata. Plant Physiol. 2006;141:1544–1554. doi: 10.1104/pp.106.084079. PubMed DOI PMC

Sharma I. Arsenic induced oxidative stress in plants. Biologia. 2012;67:447–453. doi: 10.2478/s11756-012-0024-y. DOI

Yeung E.C., Belmonte M.F., Tu L.T.T., Stasolla C. Glutathione modulation of in vitro development. Cell. Dev. Biol. Plant. 2005;41:584–590. doi: 10.1079/IVP2005683. DOI

Xiang C.B., Werner B.L., Christensen E.M., Oliver D.J. The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol. 2001;126:564–574. doi: 10.1104/pp.126.2.564. PubMed DOI PMC

Singh A.P., Dixit G., Kumar A., Mishra S., Singh P.K., Dwivedi S., Trivedi P.K., Chakrabarty D., Mallick S., Pandey V., et al. Nitric oxide alleviated arsenic toxicity by modulation of antioxidants and thiol metabolism in rice (Oryza sativa L.) Front. Plant Sci. 2016;6:1272. doi: 10.3389/fpls.2015.01272. PubMed DOI PMC

Singh N., Ma L.Q., Srivastava M., Rathinasabapathi B. Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci. 2006;170:274–282. doi: 10.1016/j.plantsci.2005.08.013. DOI

Van Den Ende W., Valluru R. Sucrose, sucrosyl oligosaccharides, and oxidative stress: Scavenging and salvaging? J. Exp. Bot. 2009;60:9–18. doi: 10.1093/jxb/ern297. PubMed DOI

Trouvelot S., Héloir M.-C., Poinssot B.T., Gauthier A., Paris F., Guillier C., Combier M., Trdá L., Daire X., Adrian M. Carbohydrates in plant immunity and plant protection: Roles and potential application as foliar sprays. Front. Plant Sci. 2014;5:592. doi: 10.3389/fpls.2014.00592. PubMed DOI PMC

Jiang H.X., Yang L.T., Qi Y.P., Lu Y.B., Huang Z.R., Chen L.S. Root iTRAQ protein profile analysis of two Citrus species differing in aluminum-tolerance in response to long-term aluminum-toxicity. BMC Genom. 2015;16:949. doi: 10.1186/s12864-015-2133-9. PubMed DOI PMC

Wang Z.Q., Xu X.Y., Gong Q.Q., Xie C., Fan W., Yang J.L., Lin Q.S., Zheng S.J. Root proteome of rice studied by iTRAQ provides integrated insight into aluminum stress tolerance mechanisms in plants. J. Proteom. 2014;98:189–205. doi: 10.1016/j.jprot.2013.12.023. PubMed DOI

Richard B., Rivoal J., Spiteri A., Pradet A. Anaerobic stress induces the transcription and tranlslation of sucrose synthase in rice. Plant Physiol. 1991;95:669–674. doi: 10.1104/pp.95.3.669. PubMed DOI PMC

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