Abstract
Main conclusion
A critical investigation into arsenic uptake and transportation, its phytotoxic effects, and defense strategies including complex signaling cascades and regulatory networks in plants.
Abstract
The metalloid arsenic (As) is a leading pollutant of soil and water. It easily finds its way into the food chain through plants, more precisely crops, a common diet source for humans resulting in serious health risks. Prolonged As exposure causes detrimental effects in plants and is diaphanously observed through numerous physiological, biochemical, and molecular attributes. Different inorganic and organic As species enter into the plant system via a variety of transporters e.g., phosphate transporters, aquaporins, etc. Therefore, plants tend to accumulate elevated levels of As which leads to severe phytotoxic damages including anomalies in biomolecules like protein, lipid, and DNA. To combat this, plants employ quite a few mitigation strategies such as efficient As efflux from the cell, iron plaque formation, regulation of As transporters, and intracellular chelation with an array of thiol-rich molecules such as phytochelatin, glutathione, and metallothionein followed by vacuolar compartmentalization of As through various vacuolar transporters. Moreover, the antioxidant machinery is also implicated to nullify the perilous outcomes of the metalloid. The stress ascribed by the metalloid also marks the commencement of multiple signaling cascades. This whole complicated system is indeed controlled by several transcription factors and microRNAs. This review aims to understand, in general, the plant–soil–arsenic interaction, effects of As in plants, As uptake mechanisms and its dynamics, and multifarious As detoxification mechanisms in plants. A major portion of this article is also devoted to understanding and deciphering the nexus between As stress-responsive mechanisms and its underlying complex interconnected regulatory networks.
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References
Abbas G, Murtaza B, Bibi I, Shahid M, Niazi NK, Khan MI, Amjad M, Hussain M, Natasha (2018) Arsenic uptake, toxicity, detoxification, and speciation in plants: physiological, biochemical, and molecular aspects. Int J Environ Res Public Health 15:59. https://doi.org/10.3390/ijerph15010059
Abercrombie JM, Halfhill MD, Ranjan P, Rao MR, Saxton AM, Yuan JS, Stewart CN (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8:87. https://doi.org/10.1186/1471-2229-8-87
Abiri R, Shaharuddin NA, Maziah M, Yusof ZN, Atabaki N, Sahebi M, Valdiani A, Kalhori N, Azizi P, Hanafi MM (2017) Role of ethylene and the APETALA 2/ethylene response factor superfamily in rice under various abiotic and biotic stress conditions. Environ Exp Bot 134:33–44. https://doi.org/10.1016/j.envexpbot.2016.10.015
Adhikary A, Kumar R, Pandir R, Bhardwaj P, Wusirika R, Kumar S (2019) Pseudomonas citronellolis; a multi-metal resistant and potential plant growth promoter against arsenic (V) stress in chickpea. Plant Physiol Biochem 142:179–192. https://doi.org/10.1016/j.plaphy.2019.07.006
Agency for toxic substances and disease registry (2019) https://www.atsdr.cdc.gov/spl/index.html. Accessed on 26.01.2020
Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813. https://doi.org/10.3389/fpls.2016.00813
Ahmad P, Alam P, Balawi TH, Altalayan FH, Ahanger MA, Ashraf M (2020) Sodium nitroprusside (SNP) improves tolerance to arsenic (As) toxicity in Vicia faba through the modifications of biochemical attributes, antioxidants, ascorbate-glutathione cycle and glyoxalasecycle. Chemosphere 244:125480. https://doi.org/10.1016/j.chemosphere.2019.125480
Ahmad A, Khan WU, Shah AA, Yasin NA, Naz S, Ali A, Tahir A, Batool AI (2021) Synergistic effects of nitric oxide and silicon on promoting plant growth, oxidative stress tolerance and reduction of arsenic uptake in Brassica juncea. Chemosphere 262:128384. https://doi.org/10.1016/j.chemosphere.2020.128384
Ali W, Isner JC, Isayenkov SV, Liu W, Zhao FJ, Maathuis FJ (2012) Heterologous expression of the yeast arsenite efflux system ACR3 improves Arabidopsis thaliana tolerance to arsenic stress. New Phytol 194:716–723. https://doi.org/10.1111/j.1469-8137.2012.04092.x
Anjum SA, Tanveer M, Hussain S, Ashraf U, Khan I, Wang L (2017) Alteration in growth, leaf gas exchange, and photosynthetic pigments of maize plants under combined cadmium and arsenic stress. Water Air Soil Pollut 228:13. https://doi.org/10.1007/s11270-016-3187-2
Ashraf MA, Umetsu K, Ponomarenko O, Saito M, Aslam M, Antipova O, Dolgova N, Kiani CD, Nezhati S, Tanoi K, Minegishi K, Nagatsu K, Kamiya T, Fujiwara T, Luschnig C, Tanino K, Pickering I, George GN, Rahman A (2020) PIN FORMED 2 modulates the transport of arsenite in Arabidopsis thaliana. Plant Commun 1(3):100009. https://doi.org/10.1016/j.xplc.2019.100009
Awasthi S, Chauhan R, Srivastava S, Tripathi RD (2017) The journey of arsenic from soil to grain in rice. Front Plant Sci 8:1007. https://doi.org/10.3389/fpls.2017.01007
Barozzi F, Papadia P, Stefano G, Renna L, Brandizzi F, Migoni D, Fanizzi FP, Piro G, Di Sansebastiano GP (2019) Variation in membrane trafficking linked to SNARE AtSYP51 interaction with aquaporin NIP1; 1. Front Plant Sci 9:1949. https://doi.org/10.3389/fpls.2018.01949
Baud S, Lepiniec L (2009) Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Biochem 47(6):448–455. https://doi.org/10.1016/j.plaphy.2008.12.006
Bayle V, Arrighi JF, Creff A, Nespoulous C, Vialaret J, Rossignol M, Gonzalez E, Paz-Ares J, Nussaume L (2011) Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23:1523–1535. https://doi.org/10.1105/tpc.110.081067
Betti C, Della Rovere F, Piacentini D, Fattorini L, Falasca G, Altamura MM (2021) Jasmonates, ethylene and brassinosteroids control adventitious and lateral rooting as stress avoidance responses to heavy metals and metalloids. Biomolecules 11(1):77. https://doi.org/10.3390/biom11010077
Bhat JA, Ahmad P, Corpas FJ (2021) Main nitric oxide (NO) hallmarks to relieve arsenic stress in higher plants. J Hazard Mater 406:124289. https://doi.org/10.1016/j.jhazmat.2020.124289
Bianucci E, Godoy A, Furlan A, Peralta JM, Hernández LE, Carpena-Ruiz RO, Castro S (2018) Arsenic toxicity in soybean alleviated by a symbiotic species of Bradyrhizobium. Symbiosis 74:167–176. https://doi.org/10.1007/s13199-017-0499-y
Bienert GP, Thorsen M, Schüssler MD, Nilsson HR, Wagner A, Tamás MJ, Jahn TP (2008) A subgroup of plant aquaporins facilitate the bi-directional diffusion of As(OH) 3 and Sb(OH) 3 across membranes. BMC Biol 6:26. https://doi.org/10.1186/1741-7007-6-26
Boorboori MR, Gao Y, Wang H, Fang C (2021) Usage of Si, P, Se, and Ca decrease arsenic concentration/toxicity in rice, a review. Appl Sci 11(17):8090. https://doi.org/10.3390/app11178090
Bücker-Neto L, Paiva AL, Machado RD, Arenhart RA, Margis-Pinheiro M (2017) Interactions between plant hormones and heavy metals responses. Genet Mol Biol 40:373–386. https://doi.org/10.1590/1678-4685-GMB-2016-0087
Cai Y, Su J, Ma LQ (2004) Low molecular weight thiols in arsenic hyperaccumulator Pteris vittata upon exposure to arsenic and other trace elements. Environ Pollut 129:69–78. https://doi.org/10.1016/j.envpol.2003.09.020
Cao Y, Sun D, Ai H, Mei H, Liu X, Sun S, Xu G, Liu Y, Ma LQ (2017) Knocking out OsPT4 gene decreases arsenate uptake by rice plants and inorganic arsenic accumulation in rice grains. Environ Sci Technol 51:12131–12138. https://doi.org/10.1021/acs.est.7b03028
Cao Y, Feng H, Sun D, Xu G, Rathinasabapathi B, Chen Y, Ma LQ (2019) Heterologous expression of Pteris vittata phosphate transporter PvPht1;3 enhances arsenic translocation to and accumulation in tobacco shoots. Environ Sci Technol 53:10636–10644. https://doi.org/10.1021/acs.est.9b02082
Castrillo G, Sánchez-Bermejo E, de Lorenzo L, Crevillén P, Fraile-Escanciano A, Mohan TC, Mouriz A, Catarecha P, Sobrino-Plata J, Olsson S, del Puerto YL, Mateos I, Rojo E, Hernández LE, Jarillo JA, Piñeiro M, Paz-Ares J, Leyva A (2013) WRKY6 transcription factor restricts arsenate uptake and transposon activation in Arabidopsis. Plant Cell 25:2944–2957. https://doi.org/10.1105/tpc.113.114009
Catarecha P, Segura MD, Franco-Zorrilla JM, García-Ponce B, Lanza M, Solano R, Paz-Ares J, Leyva A (2007) A mutant of the Arabidopsis phosphate transporter PHT1;1 displays enhanced arsenic accumulation. Plant Cell 19:1123–1133. https://doi.org/10.1105/tpc.106.041871
Chandrakar V, Yadu B, Meena RK, Dubey A, Keshavkant S (2017) Arsenic-induced genotoxic responses and their amelioration by diphenylene iodonium, 24-epibrassinolide and proline in Glycine max L. Plant Physiol Biochem 112:74–86. https://doi.org/10.1016/j.plaphy.2016.12.023
Chandrakar V, Pandey N, Keshavkant S (2018) Plant responses to arsenic toxicity: morphology and physiology. In: Hasanuzzaman M, Nahar K, Fujita M (eds) Mechanisms of arsenic toxicity and tolerance in plants. Springer, Singapore, pp 27–48. https://doi.org/10.1007/978-981-13-1292-2_2
Chao DY, Chen Y, Chen J, Shi S, Chen Z, Wang C, Danku JM, Zha FJ, Salt DE (2014) Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12:e1002009. https://doi.org/10.1371/journal.pbio.1002009
Chen J, Liu Y, Ni J, Wang Y, Bai Y, Shi J, Gan J, Wu Z, Wu P (2011) OsPHF1 regulates the plasma membrane localization of low-and high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol 157:269–278. https://doi.org/10.1104/pp.111.181669
Chen YS, Xu WZ, Shen HL, Yan HL, Xu WX, He ZY, Ma M (2013) Engineering arsenic tolerance and hyperaccumulation in plants for phytoremediation by a Pvacr3 transgenic approach. Environ Sci Technol 47:9355–9362. https://doi.org/10.1021/es4012096
Chen Y, Han YH, Cao Y, Zhu YG, Rathinasabapathi B, Ma LQ (2017a) Arsenic transport in rice and biological solutions to reduce arsenic risk from rice. Front Plant Sci 8:268. https://doi.org/10.3389/fpls.2017.00268
Chen Y, Sun SK, Tang Z, Liu GD, Moore KL, Maathuis FJM, Miller AJ, McGrath SP, Zhao FJ (2017b) The Nodulin 26-like intrinsic membrane protein OsNIP3;2 is involved in arsenite uptake by lateral roots in rice. J Exp Bot 68:3007–3016. https://doi.org/10.1093/jxb/erx165
Chen Y, Hua CY, Jia MR, Fu JW, Liu X, Han YH, Liu Y, Rathinasabapathi B, Cao Y, Ma LQ (2017c) Heterologous expression of Pteris vittata arsenite antiporter PvACR3;1 reduces arsenic accumulation in plant shoots. Environ Sci Technol 51:10387–10395. https://doi.org/10.1021/acs.est.7b03369
Chen C, Li LY, Huang K, Zhang J, Xie WY, Lu Y, Dong XZ, Zhao FJ (2019) Sulfate-reducing bacteria and methanogens are involved in arsenic methylation and demethylation in paddy soils. ISME J 13:2523–2535. https://doi.org/10.1038/s41396-019-0451-7
Costa de Oliveira A, Batista BL, Pegoraro C, Venske E, Viana VE (2020) Mechanisms of arsenic uptake, transport. In: Srivastava S (ed) Arsenic in drinking water and food. Springer, Singapore, pp 371–389. https://doi.org/10.1007/978-981-13-8587-2_14
Cuypers A, Hendrix S, Amaral dos Reis R, De Smet S, Deckers J, Gielen H, Jozefczak M, Loix C, Vercampt H, Vangronsveld J, Keunen E (2016) Hydrogen peroxide, signaling in disguise during metal phytotoxicity. Front Plant Sci 7:470. https://doi.org/10.3389/fpls.2016.00470
Das J, Sarkar P (2018) Remediation of arsenic in mung bean (Vigna radiata) with growth enhancement by unique arsenic-resistant bacterium Acinetobacter lwoffii. Sci Total Environ 624:1106–1118. https://doi.org/10.1016/j.scitotenv.2017.12.157
Das N, Bhattacharya S, Bhattacharyya S, Maiti MK (2018) Expression of rice MATE family transporter OsMATE2 modulates arsenic accumulation in tobacco and rice. Plant Mol Biol 98:101–120. https://doi.org/10.1007/s11103-018-0766-1
Demidchik V (2015) Mechanisms of oxidative stress in plants: from classical chemistry to cell biology. Environ Exp Bot 109:212–228. https://doi.org/10.1016/j.envexpbot.2014.06.021
Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801. https://doi.org/10.1104/pp.106.093971
Di X, Zheng F, Norton GJ, Beesley L, Zhang Z, Lin H, Zhi S, Liu X, Ding Y (2021) Physiological responses and transcriptome analyses of upland rice following exposure to arsenite and arsenate. Environ Exp Bot 183:104366. https://doi.org/10.1016/j.envexpbot.2020.104366
Dietrich D, Hammes U, Thor K, Suter-Grotemeyer M, Flückiger R, Slusarenko AJ, Ward JM, Rentsch D (2004) AtPTR1, a plasma membrane peptide transporter expressed during seed germination and in vascular tissue of Arabidopsis. Plant J 40:488–499. https://doi.org/10.1111/j.1365-313X.2004.02224.x
DiTusa SF, Fontenot EB, Wallace RW, Silvers MA, Steele TN, Elnagar AH, Dearman KM, Smith AP (2016) A member of the phosphate transporter 1 (Pht1) family from the arsenic-hyperaccumulating fern Pteris vittata is a high-affinity arsenate transporter. New Phytol 209:762–772. https://doi.org/10.1111/nph.13472
Duan G, Kamiya T, Ishikawa S, Arao T, Fujiwara T (2012) Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell Physiol 53:154–163. https://doi.org/10.1093/pcp/pcr161
Duan G, Liu W, Chen X, Hu Y, Zhu Y (2013) Association of arsenic with nutrient elements in rice plants. Metallomics 5(7):784–792. https://doi.org/10.1039/c3mt20277a
Duan GL, Hu Y, Schneider S, McDermott J, Chen J, Sauer N, Rosen BP, Daus B, Liu Z, Zhu YG (2015) Inositol transporters AtINT2 and AtINT4 regulate arsenic accumulation in Arabidopsis seeds. Nat Plants 2:1–6. https://doi.org/10.1038/nplants.2015.202
Duquesnoy I, Champeau GM, Evray G, Ledoigt G, Piquet-Pissaloux A (2010) Enzymatic adaptations to arsenic-induced oxidative stress in Zea mays and genotoxic effect of arsenic in root tips of Vicia faba and Zea mays. CR Biol 333:814–824. https://doi.org/10.1016/j.crvi.2010.07.004
Farmer EE, Mueller MJ (2013) ROS-mediated lipid peroxidation and RES-activated signaling. Annu Rev Plant Biol 64:429–450. https://doi.org/10.1146/annurev-arplant-050312-120132
Farnese FS, Oliveira JA, Gusman GS, Leão GA, Silveira NM, Silva PM, Ribeiro C, Cambraia J (2014) Effects of adding nitroprusside on arsenic stressed response of Pistia stratiotes L. under hydroponic conditions. Int J Phytoremediation 16(2):123–137. https://doi.org/10.1080/15226514.2012.759532
Farnese FS, Oliveira JA, Paiva EA, Menezes-Silva PE, da Silva AA, Campos FV, Ribeiro C (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516. https://doi.org/10.3389/fpls.2017.00516
Farooq MA, Gill RA, Ali B, Wang J, Islam F, Ali S, Zhou W (2016a) Subcellular distribution, modulation of antioxidant and stress-related genes response to arsenic in Brassica napus L. Ecotoxicology 25:350–366. https://doi.org/10.1007/s10646-015-1594-6
Farooq MA, Gill RA, Islam F, Ali B, Liu H, Xu J, He S, Zhou W (2016b) Methyl jasmonate regulates antioxidant defense and suppresses arsenic uptake in Brassica napus L. Front Plant Sci 7:468. https://doi.org/10.3389/fpls.2016.00468
Finnegan P, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3:182. https://doi.org/10.3389/fphys.2012.00182
Fu SF, Chen PY, Nguyen QTT, Huang LY, Zeng GR, Huang TL, Lin CY, Huang HJ (2014) Transcriptome profiling of genes and pathways associated with arsenic toxicity and tolerance in Arabidopsis. BMC Plant Biol 14:94. https://doi.org/10.1186/1471-2229-14-94
Gangwar S, Singh VP, Tripathi DK, Chauhan DK, Prasad SM, Maurya JN (2014) Plant responses to metal stress: the emerging role of plant growth hormones in toxicity alleviation. In: Ahmad P, Rasool S (eds) Emerging technologies and management of crop stress tolerance, a sustainable approach, vol 2. Academic Press, pp 215–248. https://doi.org/10.1016/B978-0-12-800875-1.00010-7
Garg N, Singla P (2011) Arsenic toxicity in crop plants: physiological effects and tolerance mechanisms. Environ Chem Lett 9:303–321. https://doi.org/10.1007/s10311-011-0313-7
Gautam A, Pandey AK, Dubey RS (2020) Unravelling molecular mechanisms for enhancing arsenic tolerance in plants: a review. Plant Gene 23:100240. https://doi.org/10.1016/j.plgene.2020.100240
Ghori NH, Ghori T, Hayat MQ, Imadi SR, Gul A, Altay V, Ozturk M (2019) Heavy metal stress and responses in plants. Int J Environ Sci Technol 16(3):1807–1828. https://doi.org/10.1007/s13762-019-02215-8
Ghosh S, Saha J, Biswas AK (2013) Interactive influence of arsenate and selenate on growth and nitrogen metabolism in wheat (Triticum aestivum L.) seedlings. Acta Physiol Plant 35:1873–1885. https://doi.org/10.1007/s11738-013-1225-x
Ghosh S, Singh K, Shaw AK, Azahar I, Adhikari S, Ghosh U, Basu U, Roy S, Saha S, Sherpa AR, Hossain Z (2017) Insights into the miRNA-mediated response of maize leaf to arsenate stress. Environ Exp Bot 137:96–109. https://doi.org/10.1016/j.envexpbot.2017.01.015
Ghosh PK, Maiti TK, Pramanik K, Ghosh SK, Mitra S, De TK (2018) The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity. Chemosphere 211:407–419. https://doi.org/10.1016/j.chemosphere.2018.07.148
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. https://doi.org/10.1016/j.plaphy.2010.08.016
González E, Solano R, Rubio V, Leyva A, Paz-Ares J (2005) Phosphate transporter traffic facilitator1 is a plant-specific SEC12-related protein that enables the endoplasmic reticulum exit of a high-affinity phosphate transporter in Arabidopsis. Plant Cell 17:3500–3512. https://doi.org/10.1105/tpc.105.036640
Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494. https://doi.org/10.1071/FP05016
Gunes A, Inal A, Bagci EG, Kadioglu YK (2010) Combined effect of arsenic and phosphorus on mineral element concentrations of sunflower. Commun Soil Sci Plant Anal 41(3):361–372. https://doi.org/10.1080/00103620903462357
Gupta P, Seth CS (2019) 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 139:44–55. https://doi.org/10.1016/j.plaphy.2019.03.007
Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74:1201–1208. https://doi.org/10.1016/j.chemosphere.2008.11.023
Gusman GS, Oliveira JA, Farnese FS, Cambraia J (2013a) Arsenate and arsenite: the toxic effects on photosynthesis and growth of lettuce plants. Acta Physiol Plant 35:1201–1209. https://doi.org/10.1007/s11738-012-1159-8
Gusman GS, Oliveira JA, Farnese FS, Cambraia J (2013b) Mineral nutrition and enzymatic adaptation induced by arsenate and arsenite exposure in lettuce plants. Plant Physiol Biochem 71:307–314. https://doi.org/10.1016/j.plaphy.2013.08.006
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596. https://doi.org/10.1007/s10646-013-1050-4
He Z, Yan H, Chen Y, Shen H, Xu W, Zhang H, Shi L, Zhu YG, Ma M (2016) An aquaporin PvTIP4;1 from Pteris vittata may mediate arsenite uptake. New Phytol 209:746–761. https://doi.org/10.1111/nph.13637
Huang TL, Nguyen QTT, Fu SF, Lin CY, Chen YC, Huang HJ (2012) Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol 80:587–608. https://doi.org/10.1007/s11103-012-9969-z
Hussain MM, Bibi I, Niazi NK, Shahid M, Iqbal J, Shakoor MB, Ahmad A, Shah NS, Bhattacharya P, Mao K, Bundschuh J (2021) Arsenic biogeochemical cycling in paddy soil-rice system: Interaction with various factors, amendments and mineral nutrients. Sci Total Environ 773:145040. https://doi.org/10.1016/j.scitotenv.2021.145040
Indriolo E, Na G, Ellis D, Salt DE, Banks JA (2010) A vacuolar arsenite transporter necessary for arsenic tolerance in the arsenic hyperaccumulating fern Pteris vittata is missing in flowering plants. Plant Cell 22:2045–2057. https://doi.org/10.1105/tpc.109.069773
Isayenkov SV, Maathuis FJ (2008) The Arabidopsis thaliana aquaglyceroporin AtNIP7; 1 is a pathway for arsenite uptake. FEBS Lett 582:1625–1628. https://doi.org/10.1016/j.febslet.2008.04.022
Islam E, Khan MT, Irem S (2015) Biochemical mechanisms of signaling: perspectives in plants under arsenic stress. Ecotoxicol Environ Saf 114:126–133. https://doi.org/10.1016/j.ecoenv.2015.01.017
Jalmi SK, Bhagat PK, Verma D, Noryang S, Tayyeba S, Singh K, Sharma D, Sinha AK (2018) Traversing the links between heavy metal stress and plant signaling. Front Plant Sci 9:12. https://doi.org/10.3389/fpls.2018.00012
Jha AB, Dubey RS (2004a) Carbohydrate metabolism in growing rice seedlings under arsenic toxicity. J Plant Physiol 161(7):867–872. https://doi.org/10.1016/j.jplph.2004.01.004
Jha AB, Dubey RS (2004b) Arsenic exposure alters activity behaviour of key nitrogen assimilatory enzymes in growing rice plants. Plant Growth Regul 43:259–268. https://doi.org/10.1023/B:GROW.0000045995.49365.df
Ji R, Zhou L, Liu J, Wang Y, Yang L, Zheng Q, Zhang C, Zhang B, Ge H, Yang Y, Zhao F (2017) Calcium-dependent protein kinase CPK31 interacts with arsenic transporter AtNIP1; 1 and regulates arsenite uptake in Arabidopsis thaliana. PLoS ONE 12:e0173681. https://doi.org/10.1371/journal.pone.0173681
Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P, Xu G (2011) The phosphate transporter gene OsPht1;8 is involved in phosphate homeostasis in rice. Plant Physiol 156:1164–1175. https://doi.org/10.1104/pp.111.175240
Jonak C, Ökrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424. https://doi.org/10.1016/S1369-5266(02)00285-6
Jung HI, Kong MS, Lee BR, Kim TH, Chae MJ, Lee EJ, Jung GB, Lee CH, Sung JK, Kim YH (2019) Exogenous glutathione increases arsenic translocation into shoots and alleviates arsenic-induced oxidative stress by sustaining ascorbate-glutathione homeostasis in rice seedlings. Front Plant Sci 10:1089. https://doi.org/10.3389/fpls.2019.01089
Kamiya T, Tanaka M, Mitani N, Ma JF, Maeshima M, Fujiwara T (2009) NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284:2114–2120. https://doi.org/10.1074/jbc.M806881200
Kamiya T, Islam R, Duan G, Uraguchi S, Fujiwara T (2013) 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 59:580–590. https://doi.org/10.1080/00380768.2013.804390
Katsuhara M, Sasano S, Horie T, Matsumoto T, Rhee J, Shibasaka M (2014) Functional and molecular characteristics of rice and barley NIP aquaporins transporting water, hydrogen peroxide and arsenite. Plant Biotechnol 31:213–219. https://doi.org/10.5511/plantbiotechnology.14.0421a
Kaur S, Singh HP, Batish DR, Negi A, Mahajan P, Rana S, Kohli RK (2012) Arsenic (As) Inhibits radicle emergence and elongation in Phaseolus aureus by altering starch-metabolizing enzymes vis-à-vis disruption of oxidative metabolism. Biol Trace Elem Res 146(3):360–368. https://doi.org/10.1007/s12011-011-9258-8
Kofroňová M, Hrdinová A, Mašková P, Soudek P, Tremlova J, Pinkas D, Lipavská H (2019) Strong antioxidant capacity of horseradish hairy root cultures under arsenic stress indicates the possible use of Armoracia rusticana plants for phytoremediation. Ecotoxicol Environ Saf 174:295–304. https://doi.org/10.1016/j.ecoenv.2019.02.028
Komarova NY, Thor K, Gubler A, Meier S, Dietrich D, Weichert A, Grotemeyer MS, Tegeder M (2008) Rentsch D AtPTR1 and AtPTR5 transport dipeptides in planta. Plant Physiol 148:856–869. https://doi.org/10.1104/pp.108.123844
Krishnamurthy A, Rathinasabapathi B (2013) Auxin and its transport play a role in plant tolerance to arsenite-induced oxidative stress in Arabidopsis thaliana. Plant Cell Environ 36:1838–1849. https://doi.org/10.1111/pce.12093
Kumar S, Trivedi PK (2016) Heavy metal stress signaling in plants. In: Ahmad P (ed) Plant metal interaction. Elsevier, pp 585–603. https://doi.org/10.1016/B978-0-12-803158-2.00025-4
Kumar K, Gupta D, Mosa KA, Ramamoorthy K, Sharma P (2019) Arsenic transport, metabolism, and possible mitigation strategies in plants. In: Srivastava S, Srivastava A, Suprasanna P (eds) Plant-metal interactions. Springer Nature, Switzerland, pp 141–168. https://doi.org/10.1007/978-3-030-20732-8_8
Kumari A, Pandey N, Pandey-Rai S (2018) 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 255:139–152. https://doi.org/10.1007/s00709-017-1136-6
Lakshmanan V, Shantharaj D, Li G, Seyfferth AL, Sherrier DJ, Bais HP (2015) A natural rice rhizospheric bacterium abates arsenic accumulation in rice (Oryza sativa L.). Planta 242:1037–1050. https://doi.org/10.1007/s00425-015-2340-2
LeBlanc MS, McKinney EC, Meagher RB, Smith AP (2013) Hijacking membrane transporters for arsenic phytoextraction. J Biotechnol 163:1–9. https://doi.org/10.1016/j.jbiotec.2012.10.013
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143. https://doi.org/10.1016/j.envpol.2012.03.012
Li WX, Chen TB, Huang ZC, Lei M, Liao XY (2006) Effect of arsenic on chloroplast ultrastructure and calcium distribution in arsenic hyperaccumulator Pteris vittata L. Chemosphere 62:803–809. https://doi.org/10.1016/j.chemosphere.2005.04.055
Li RY, Ago Y, Liu WJ, Mitani N, Feldmann J, McGrath SP, Ma JF, Zhao FJ (2009) The rice aquaporin Lsi1 mediates uptake of methylated arsenic species. Plant Physiol 150:2071–2080. https://doi.org/10.1104/pp.109.140350
Li N, Wang J, Song WY (2016) Arsenic uptake and translocation in plants. Plant Cell Physiol 57:4–13. https://doi.org/10.1093/pcp/pcv143
Li J, Zhao Q, Xue B, Wu H, Song G, Zhang X (2019a) Arsenic and nutrient absorption characteristics and antioxidant response in different leaves of two ryegrass (Lolium perenne) species under arsenic stress. PLoS ONE 14:e0225373. https://doi.org/10.1371/journal.pone.0225373
Li Y, Wang X, Zhang H, Wang S, Ye X, Shi L, Xu F, Ding G (2019b) Molecular identification of the phosphate transporter family 1 (PHT1) genes and their expression profiles in response to phosphorus deprivation and other abiotic stresses in Brassica napus. PLoS ONE 14:e0220374. https://doi.org/10.1371/journal.pone.0220374
Lin A, Zhang X, Zhu YG, Zhao FJ (2007) Arsenate-induced toxicity: Effects on antioxidative enzymes and DNA damage in Vicia faba. Environ Toxicol Chem 27:413–419. https://doi.org/10.1897/07-266R.1
Lindsay ER, Maathuis FJ (2016) Arabidopsis thaliana NIP 7;1 is involved in tissue arsenic distribution and tolerance in response to arsenate. FEBS Lett 590:779–786. https://doi.org/10.1002/1873-3468.12103
Liu Q, Zhang H (2012) Molecular identification and analysis of arsenite stress-responsive miRNAs in rice. J Agric Food Chem 60:6524–6536. https://doi.org/10.1021/jf300724t
Lomax C, Liu WJ, Wu L, Xue K, Xiong J, Zhou J, McGrath SP, Meharg AA, Miller AJ, Zhao FJ (2012) Methylated arsenic species in plants originate from soil microorganisms. New Phytol 193:665–672. https://doi.org/10.1111/j.1469-8137.2011.03956.x
Luan M, Zhao F, Han X, Sun G, Yang Y, Liu J, Shi J, Fu A, Lan W, Luan S (2019) Vacuolar phosphate transporters contribute to systemic phosphate homeostasis vital for reproductive development in Arabidopsis. Plant Physiol 179:640–655. https://doi.org/10.1104/pp.18.01424
Ma JF, Yamaji N, Mitani N, Xu XY, Su YH, McGrath SP, Zhao FJ (2008) Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105:9931–9935. https://doi.org/10.1073/pnas.0802361105
Maghsoudi K, Arvin MJ, Ashraf M (2020) Mitigation of arsenic toxicity in wheat by the exogenously applied salicylic acid, 24-epi-brassinolide and silicon. J Soil Sci Plant Nutr 20(2):577–588. https://doi.org/10.1007/s42729-019-00147-3
Maglovski M, Gerši Z, Rybanský Ľ, Bardáčová M, Moravčíková J, Bujdoš M, Dobrikova A, Apostolova E, Kraic J, Blehová A, Matušíková I (2019) Effects of nutrition on wheat photosynthetic pigment responses to arsenic stress. Pol J Environ Stud 28:1821–1829. https://doi.org/10.15244/pjoes/89584
Malik JA, Goel S, Sandhir R, Nayyar H (2011) Uptake and distribution of arsenic in chickpea: effects on seed yield and seed composition. Commun Soil Sci Plant Anal 42(14):1728–1738. https://doi.org/10.1080/00103624.2011.584593
Mano JI (2012) Reactive carbonyl species: their production from lipid peroxides, action in environmental stress, and the detoxification mechanism. Plant Physiol Biochem 59:90–97. https://doi.org/10.1016/j.plaphy.2012.03.010
Mano JI, Biswas M, Sugimoto K (2019) Reactive carbonyl species: a missing link in ROS signaling. Plants 8:391. https://doi.org/10.3390/plants8100391
Mansour NM, Sawhney M, Tamang DG, Vogl C, Saier MH Jr (2007) The bile/arsenite/riboflavin transporter (BART) superfamily. FEBS J 274:612–629. https://doi.org/10.1111/j.1742-4658.2006.05627.x
Maurel C, Boursiac Y, Luu DT, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358. https://doi.org/10.1152/physrev.00008.2015
Meng YL, Liu ZJ, Rosen BP (2004) As(III) and Sb(III) uptake by GlpF and efflux by ArsB in Escherichia coli. J Biol Chem 279:18334–18341. https://doi.org/10.1074/jbc.M400037200
Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489. https://doi.org/10.1111/j.1399-3054.2008.01090.x
Mishra S, Srivastava S, Tripathi RD, Trivedi PK (2008) Thiol metabolism and antioxidant systems complement each other during arsenate detoxification in Ceratophyllum demersum L. Aquat Toxicol 86:205–215. https://doi.org/10.1016/j.aquatox.2007.11.001
Mishra S, Srivastava S, Dwivedi S, Tripathi RD (2013) Investigation of biochemical responses of Bacopa monnieri L. upon exposure to arsenate. Environ Toxicol 28:419–430. https://doi.org/10.1002/tox.20733
Mishra S, Alfeld M, Sobotka R, Andresen E, Falkenberg G, Küpper H (2016) Analysis of sublethal arsenic toxicity to Ceratophyllum demersum: subcellular distribution of arsenic and inhibition of chlorophyll biosynthesis. J Exp Bot 67(15):4639–4646. https://doi.org/10.1093/jxb/erw238
Mishra S, Dwivedi S, Mallick S, Tripathi RD (2019) Redox homeostasis in plants under arsenic stress. In: Panda S, Yamamoto Y (eds) Redox homeostasis in plants. Signaling and communication in plants, Springer Nature, Switzerland, pp 179–198. https://doi.org/10.1007/978-3-319-95315-1_9
Mitani-Ueno N, Yamaji N, Zhao FJ, Ma JF (2011) The aromatic/arginine selectivity filter of NIP aquaporins plays a critical role in substrate selectivity for silicon, boron, and arsenic. J Exp Bot 62(12):4391–4398. https://doi.org/10.1093/jxb/err158
Mohamed HI, Latif HH, Hanafy RS (2016) Influence of nitric oxide application on some biochemical aspects, endogenous hormones, minerals and phenolic compounds of Vicia faba plant grown under arsenic stress. Gesunde Pflanzen 68(2):99–107. https://doi.org/10.1007/s10343-016-0363-7
Mohan TC, Castrillo G, Navarro C, Zarco-Fernández S, Ramireddy E, Mateo C, Zamarreño AM, Paz-Ares J, Muñoz R, García-Mina JM, Hernández LE (2016) Cytokinin determines thiol-mediated arsenic tolerance and accumulation. Plant Physiol 171(2):1418–1426. https://doi.org/10.1104/pp.16.00372
Mondal S, Pramanik K, Ghosh SK, Pal P, Mondal T, Soren T, Maiti TK (2021) Unraveling the role of plant growth-promoting rhizobacteria in the alleviation of arsenic phytotoxicity: a review. Microbiol Res 250:126809. https://doi.org/10.1016/j.micres.2021.126809
Mosa KA, Kumar K, Chhikara S, Mcdermott J, Liu Z, Musante C, White JC, Dhankher OP (2012) Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants. Transgenic Res 21:1265–1277. https://doi.org/10.1007/s11248-012-9600-8
Mostofa MG, Rahman MM, Nguyen KH, Li W, Watanabe Y, Tran CD, Zhang M, Itouga M, Fujita M, Tran LS (2021) Strigolactones regulate arsenate uptake, vacuolar-sequestration and antioxidant defense responses to resist arsenic toxicity in rice roots. J Hazard Mater 415:125589. https://doi.org/10.1016/j.jhazmat.2021.125589
Nabi A, Naeem M, Aftab T, Khan MM, Ahmad P (2021) A comprehensive review of adaptations in plants under arsenic toxicity: Physiological, metabolic and molecular interventions. Environ Pollut 290:118029. https://doi.org/10.1016/j.envpol.2021.118029
Nadarajah KK (2020) ROS homeostasis in abiotic stress tolerance in plants. Int J Mol Sci 21(15):5208. https://doi.org/10.3390/ijms21155208
Nagarajan VK, Jain A, Poling MD, Lewis AJ, Raghothama KG, Smith AP (2011) Arabidopsis Pht1; 5 mobilizes phosphate between source and sink organs and influences the interaction between phosphate homeostasis and ethylene signaling. Plant Physiol 156:1149–1163. https://doi.org/10.1104/pp.111.174805
Niazi NK, Bibi I, Fatimah A, Shahid M, Javed MT, Wang H, Ok YS, Bashir S, Murtaza B, Saqib ZA, Shakoor MB (2017) Phosphate-assisted phytoremediation of arsenic by Brassica napus and Brassica juncea: morphological and physiological response. Int J Phytoremediat 19:670–678. https://doi.org/10.1080/15226514.2016.1278427
Nussaume L, Kanno S, Javot H, Marin E, Nakanishi TM, Thibaud MC (2011) Phosphate import in plants: focus on the PHT1 transporters. Front Plant Sci 2:83. https://doi.org/10.3389/fpls.2011.00083
Pan D, Liu C, Yi J, Li X, Li F (2021) Different effects of foliar application of silica sol on arsenic translocation in rice under low and high arsenite stress. J Environ Sci 105:22–32. https://doi.org/10.1016/j.jes.2020.12.034
Pandey C, Gupta M (2015) Selenium and auxin mitigates arsenic stress in rice (Oryza sativa L.) by combining the role of stress indicators, modulators and genotoxicity assay. J Hazard Mater 287:384–391. https://doi.org/10.1016/j.jhazmat.2015.01.044
Pandey AK, Gedda MR, Verma AK (2020) Effect of Arsenic stress on expression pattern of a rice specific miR156j at various developmental stages and their allied co-expression target networks. Front Plant Sci 11:752. https://doi.org/10.3389/fpls.2020.00752
Parvin K, Nahar K, Hasanuzzaman M, Bhuyan MHMB, Fujita M (2019) Calcium-mediated growth regulation and abiotic stress tolerance in plants. In: Hasanuzzaman M, Hakeem K, Nahar K, Alharby H (eds) Plant abiotic stress tolerance. Springer Nature, Switzerland, pp 291–331. https://doi.org/10.1007/978-3-030-06118-0_13
Petrov VD, Van Breusegem F (2012) Hydrogen peroxide—a central hub for information flow in plant cells. AoB Plants. https://doi.org/10.1093/aobpla/pls014
Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227. https://doi.org/10.1016/j.plantsci.2015.06.002
Quaghebeur M, Rengel Z (2005) Arsenic speciation governs arsenic uptake and transport in terrestrial plants. Microchim Acta 151:141–152. https://doi.org/10.1007/s00604-005-0394-8
Rahman MS, Jamal MA, Biswas PK, Rahman SM, Sharma SP, Saha SK, Hong ST, Islam MR (2020) Arsenic remediation in bangladeshi rice varieties with enhance plant growth by unique arsenic-resistant bacterial isolates. Geomicrobiol J 37:130–142. https://doi.org/10.1080/01490451.2019.1666938
Rai A, Bhardwaj A, Misra P, Bag SK, Adhikari B, Tripathi RD, Trivedi PK, Chakrabarty D (2015) Comparative transcriptional profiling of contrasting rice genotypes shows expression differences during arsenic stress. Plant Genome 8:1–14. https://doi.org/10.3835/plantgenome2014.09.0054
Raja V, Majeed U, Kang H, Andrabi KI, John R (2017) Abiotic stress: Interplay between ROS, hormones and MAPKs. Environ Exp Bot 137:142–157. https://doi.org/10.1016/j.envexpbot.2017.02.010
Rao KP, Vani G, Kumar K, Wankhede DP, Misra M, Gupta M, Sinha AK (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82. https://doi.org/10.1016/j.abb.2010.11.006
Remy E, Cabrito TR, Batista RA, Teixeira MC, Sá-Correia I, Duque P (2012) The Pht1; 9 and Pht1; 8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. New Phytol 195:356–371. https://doi.org/10.1111/j.1469-8137.2012.04167.x
Rodríguez-Ruiz M, Aparicio-Chacón MV, Palma JM, Corpas FJ (2019) Arsenate disrupts ion balance, sulfur and nitric oxide metabolisms in roots and leaves of pea (Pisum sativum L.) plants. Environ Exp Bot 161:143–156. https://doi.org/10.1016/j.envexpbot.2018.06.028
Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9(12):606–613. https://doi.org/10.1016/j.tplants.2004.10.009
Ronzan M, Piacentini D, Fattorini L, Caboni E, Eiche E, Ziegler J, Hause B, Riemann B, Betti C, Altamura MM, Falasca G (2019) Auxin-jasmonate crosstalk in Oryza sativa L. root system formation after cadmium and/or arsenic exposure. Environ Exp Bot 165:59–69. https://doi.org/10.1016/j.envexpbot.2019.05.013
Sachdev S, Ansari SA, Ansari MI, Fujita M, Hasanuzzaman M (2021) Abiotic stress and reactive oxygen species: Generation, signaling, and defense mechanisms. Antioxidants 10(2):277. https://doi.org/10.3390/antiox10020277
Saifullah DS, Naeem A, Iqbal M, Farooq MA, Bibi S, Rengel Z (2018) Opportunities and challenges in the use of mineral nutrition for minimizing arsenic toxicity and accumulation in rice: a critical review. Chemosphere 194:171–188. https://doi.org/10.1016/j.chemosphere.2017.11.149
Saini S, Kaur N, Pati PK (2021) Phytohormones: Key players in the modulation of heavy metal stress tolerance in plants. Ecotoxicol Environ Saf 223:112578. https://doi.org/10.1016/j.ecoenv.2021.112578
Seyfferth AL, Webb SM, Andrews JC, Fendorf S (2010) Arsenic localization, speciation, and co-occurrence with iron on rice (Oryza sativa L.) roots having variable Fe coatings. Environ Sci Technol 44:8108–8113. https://doi.org/10.1021/es101139z
Shaibur MR, Kitajima N, Huq SI, Kawai S (2009a) Arsenic–iron interaction: effect of additional iron on arsenic-induced chlorosis in barley grown in water culture. Soil Sci Plant Nutr 55(6):739–746. https://doi.org/10.1111/j.1747-0765.2009.00414.x
Shaibur MR, Kitajima N, Sugawara R, Kondo T, Huq SI, Kawai S (2009b) Effect of arsenic on phytosiderophores and mineral nutrition of barley seedlings grown in iron-depleted medium. Soil Sci Plant Nutr 55(2):283–293. https://doi.org/10.1111/j.1747-0765.2009.00360.x
Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447–453. https://doi.org/10.2478/s11756-012-0024-y
Sharma D, Tiwari M, Lakhwani D, Tripathi RD, Trivedi PK (2015) Differential expression of microRNAs by arsenate and arsenite stress in natural accessions of rice. Metallomics 7:174–187. https://doi.org/10.1039/C4MT00264D
Sharma SS, Kumar V, Dietz KJ (2021) Emerging trends in metalloid-dependent signaling in plants. Trends Plant Sci 26(5):452–471. https://doi.org/10.1016/j.tplants.2020.11.003
Sharma A, Ramakrishnan M, Khanna K, Landi M, Prasad R, Bhardwaj R, Zheng B (2022) Brassinosteroids and metalloids: regulation of plant biology. J Hazard Mater 424:127518. https://doi.org/10.1016/j.jhazmat.2021.127518
Shi S, Wang T, Chen Z, Tang Z, Wu Z, Salt DE, Chao DY, Zhao FJ (2016) OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol 172:1708–1719. https://doi.org/10.1104/pp.16.01332
Shin H, Shin HS, Dewbre GR, Harrison MJ (2004) 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 39:629–642. https://doi.org/10.1111/j.1365-313X.2004.02161.x
Shri M, Kumar S, Chakrabarty D, Trivedi PK, Mallick S, Misra P, Shukla D, Mishra S, Srivastava S, Tripathi RD, Tuli R (2009) Effect of arsenic on growth, oxidative stress, and antioxidant system in rice seedlings. Ecotoxicol Environ Saf 72:1102–1110. https://doi.org/10.1016/j.ecoenv.2008.09.022
Shri M, Singh PK, Kidwai M, Gautam N, Dubey S, Verma G, Chakrabarty D (2019) Recent advances in arsenic metabolism in plants: current status, challenges and highlighted biotechnological intervention to reduce grain arsenic in rice. Metallomics 11:519–532. https://doi.org/10.1039/C8MT00320C
Shukla P, Singh S, Dubey P, Singh A, Singh AK (2015) Nitric oxide mediated amelioration of arsenic toxicity which alters the alternative oxidase (Aox1) gene expression in Hordeum vulgare L. Ecotoxicol Environ Saf 120:59–65. https://doi.org/10.1016/j.ecoenv.2015.05.030
Shukla T, Khare R, Kumar S, Lakhwani D, Sharma D, Asif MH, Trivedi PK (2018) Differential transcriptome modulation leads to variation in arsenic stress response in Arabidopsis thaliana accessions. J Hazard Mater 351:1–10. https://doi.org/10.1016/j.jhazmat.2018.02.031
Siddiqui MH, Alamri S, Khan MN, Corpas FJ, Al-Amri AA, Alsubaie QD, Ali HM, Kalaji HM, Ahmad P (2020) Melatonin and calcium function synergistically to promote the resilience through ROS metabolism under arsenic-induced stress. J Hazard Mater 398:122882. https://doi.org/10.1016/j.jhazmat.2020.122882
Singh N, Ma LQ, Srivastava M, Rathinasabapathi B (2006) Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Sci 170:274–282. https://doi.org/10.1016/j.plantsci.2005.08.013
Singh AP, Dixit G, Mishra S, Dwivedi S, Tiwari M, Mallick S, Pandey V, Trivedi PK, Chakrabarty D, Tripathi RD (2015) Salicylic acid modulates arsenic toxicity by reducing its root to shoot translocation in rice (Oryza sativa L.). Front Plant Sci 6:340. https://doi.org/10.3389/fpls.2015.00340
Singh S, Parihar P, Singh R, Singh VP, Prasad SM (2016) Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Front Plant Sci 6:1143. https://doi.org/10.3389/fpls.2015.01143
Singh PK, Indoliya Y, Chauhan AS, Singh SP, Singh AP, Dwivedi S, Tripathi RD, Chakrabarty D (2017) Nitric oxide mediated transcriptional modulation enhances plant adaptive responses to arsenic stress. Sci Rep 7:1–13. https://doi.org/10.1038/srep42530
Singh R, Upadhyay AK, Singh DP (2018) Regulation of oxidative stress and mineral nutrient status by selenium in arsenic treated crop plant Oryza sativa. Ecotoxicol Environ Saf 148:105–113. https://doi.org/10.1016/j.ecoenv.2017.10.008
Singh A, Kumar A, Yadav S, Singh IK (2019) Reactive oxygen species-mediated signaling during abiotic stress. Plant Gene 18:100173. https://doi.org/10.1016/j.plgene.2019.100173
Singh R, Parihar P, Prasad SM (2020a) Interplay of calcium and nitric oxide in improvement of growth and arsenic-induced toxicity in mustard seedlings. Sci Rep 10(1):1–2. https://doi.org/10.1038/s41598-020-62831-0
Singh R, Parihar P, Prasad SM (2020b) Sulphur and calcium attenuate arsenic toxicity in Brassica by adjusting ascorbate–glutathione cycle and sulphur metabolism. Plant Growth Regul 91(2):221–235. https://doi.org/10.1007/s10725-020-00601-8
Song WY, Park J, Mendoza-Cózatl DG, Suter-Grotemeyer M, Shim D, Hörtensteiner S, Geisler M, Weder B, Rea PA, Rentsch D, Schroeder JI, Lee Y, Martinoia E (2010) Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107:21187–21192. https://doi.org/10.1073/pnas.1013964107
Song WY, Yamaki T, Yamaji N, Ko D, Jung K, Fujii-Kashino M, An G, Martinoia E, Lee YS, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci U S A 111:15699–15704. https://doi.org/10.1073/pnas.1414968111
Souri Z, Karimi N, Farooq MA, Sandalio LM (2020) Nitric oxide improves tolerance to arsenic stress in Isatis cappadocica desv shoots by enhancing antioxidant defenses. Chemosphere 239:124523. https://doi.org/10.1016/j.chemosphere.2019.124523
Srivastava S, Singh N (2014) Mitigation approach of arsenic toxicity in chickpea grown in arsenic amended soil with arsenic tolerant plant growth promoting Acinetobacter sp. Ecol Eng 70:146–153. https://doi.org/10.1016/j.ecoleng.2014.05.008
Srivastava S, Suprasanna P (2021) MicroRNAs: tiny, powerful players of metal stress responses in plants. Plant Physiol Biochem 166:928–938. https://doi.org/10.1016/j.plaphy.2021.07.004
Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Trivedi PK, Tandon PK (2007) Phytochelatins and antioxidant systems respond differentially during arsenite and arsenate stress in Hydrilla verticillata (Lf) Royle. Environ Sci Technol 41:2930–2936. https://doi.org/10.1021/es062167j
Srivastava S, Suprasanna P, D’Souza SF (2011) Redox state and energetic equilibrium determine the magnitude of stress in Hydrilla verticillata upon exposure to arsenate. Protoplasma 248:805–815. https://doi.org/10.1007/s00709-010-0256-z
Srivastava S, Srivastava AK, Sablok G, Deshpande TU, Suprasanna P (2015) Transcriptomics profiling of Indian mustard (Brassica juncea) under arsenate stress identifies key candidate genes and regulatory pathways. Front Plant Sci 6:646. https://doi.org/10.3389/fpls.2015.00646
Srivastava S, Sinha P, Sharma YK (2017) Status of photosynthetic pigments, lipid peroxidation and anti-oxidative enzymes in Vigna mungo in presence of arsenic. J Plant Nutr 40:298–306. https://doi.org/10.1080/01904167.2016.1240189
Sun S, Gu M, Cao Y, Huang X, Zhang X, Ai P, Zhao J, Fan X, Xu G (2012) A constitutive expressed phosphate transporter, OsPht1;1, modulates phosphate uptake and translocation in phosphate-replete rice. Plant Physiol 159:1571–1581. https://doi.org/10.1104/pp.112.196345
Sun SK, Chen Y, Che J, Konishi N, Tang Z, Miller AJ, Ma JF, Zhao FJ (2018) Decreasing arsenic accumulation in rice by overexpressing OsNIP 1;1 and OsNIP 3;3 through disrupting arsenite radial transport in roots. New Phytol 219:641–653. https://doi.org/10.1111/nph.15190
Sun D, Feng H, Li X, Ai H, Sun S, Chen Y, Xu G, Rathinasabapathi B, Cao Y, Ma LQ (2019) Expression of new Pteris vittata phosphate transporter PvPht1;4 reduces arsenic translocation from the roots to shoots in tobacco plants. Environ Sci Technol 54:1045–1053. https://doi.org/10.1021/acs.est.9b05486
Surgun-Acar Y, Zemheri-Navruz F (2019) 24-Epibrassinolide promotes arsenic tolerance in Arabidopsis thaliana L. by altering stress responses at biochemical and molecular level. J Plant Physiol 238:12–19. https://doi.org/10.1016/j.jplph.2019.05.002
Sytar O, Kumari P, Yadav S, Brestic M, Rastogi A (2019) Phytohormone priming: regulator for heavy metal stress in plants. J Plant Growth Regul 38(2):739–752. https://doi.org/10.1007/s00344-018-9886-8
Takano J, Wada M, Ludewig U, Schaaf G, Von Wirén N, Fujiwara T (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18:1498–1509. https://doi.org/10.1105/tpc.106.041640
Tang Z, Zhao FJ (2021) The roles of membrane transporters in arsenic uptake, translocation and detoxification in plants. Crit Rev Env Sci Tec 51(21):2449–2484. https://doi.org/10.1080/10643389.2020.1795053
Tang Z, Chen Y, Chen F, Ji Y, Zhao FJ (2017) OsPTR7 (OsNPF8. 1), a putative peptide transporter in rice, is involved in dimethylarsenate accumulation in rice grain. Plant Cell Physiol 58:904–913. https://doi.org/10.1093/pcp/pcx029
Tang Z, Chen Y, Miller AJ, Zhao FJ (2019) The C-type ATP-binding cassette transporter OsABCC7 is involved in the root-to-shoot translocation of arsenic in rice. Plant Cell Physiol 60:1525–1535. https://doi.org/10.1093/pcp/pcz054
Tang Z, Wang Y, Gao A, Ji Y, Yang B, Wang P, Tang Z, Zhao FJ (2020) Dimethylarsinic acid is the causal agent inducing rice straighthead disease. J Exp Bot 71:5631–5644. https://doi.org/10.1093/jxb/eraa253
Thakur S, Choudhary S, Dubey P, Bhardwaj P (2019) Comparative transcriptome profiling reveals the reprogramming of gene networks under arsenic stress in Indian mustard. Genome 62:833–847. https://doi.org/10.1139/gen-2018-0152
Thakur S, Choudhary S, Majeed A, Singh A, Bhardwaj P (2020) Insights into the molecular mechanism of arsenic phytoremediation. J Plant Growth Regul 39:532–543. https://doi.org/10.1007/s00344-019-10019-w
Tiwari M, Sharma D, Dwivedi S, Singh M, Tripathi RD, Trivedi PK (2014) Expression in Arabidopsis and cellular localization reveal involvement of rice NRAMP, OsNRAMP1, in arsenic transport and tolerance. Plant Cell Environ 37:140–152. https://doi.org/10.1111/pce.12138
Tripathi P, Tripathi RD (2019) Metabolome modulation during arsenic stress in plants. In: Srivastava S, Srivastava A, Suprasanna P (eds) Plant-metal interactions. Springer Nature, Switzerland, pp 119–140. https://doi.org/10.1007/978-3-030-20732-8_7
Tripathi RD, Srivastava S, Mishra S, Singh N, Tuli R, Gupta DK, Maathuis FJ (2007) Arsenic hazards: strategies for tolerance and remediation by plants. Trends Biotechnol 25:158–165. https://doi.org/10.1016/j.tibtech.2007.02.003
Tripathi P, Mishra A, Dwivedi S, Chakrabarty D, Trivedi PK, Singh RP, Tripathi RD (2012) Differential response of oxidative stress and thiol metabolism in contrasting rice genotypes for arsenic tolerance. Ecotoxicol Environ Saf 79:189–198. https://doi.org/10.1016/j.ecoenv.2011.12.019
Tripathi P, Singh RP, Sharma YK, Tripathi RD (2015) Arsenite stress variably stimulates pro-oxidant enzymes, anatomical deformities, photosynthetic pigment reduction, and antioxidants in arsenic-tolerant and sensitive rice seedlings. Environ Toxicol Chem 34:1562–1571. https://doi.org/10.1002/etc.2937
Verma PK, Verma S, Meher AK, Pande V, Mallick S, Bansiwal AK, Tripathi RD, Dhankher OP, Chakrabarty D (2016) Overexpression of rice glutaredoxins (OsGrxs) significantly reduces arsenite accumulation by maintaining glutathione pool and modulating aquaporins in yeast. Plant Physiol Biochem 106:208–217. https://doi.org/10.1016/j.plaphy.2016.04.052
Vithanage M, Dabrowska BB, Mukherjee AB, Sandhi A, Bhattacharya P (2012) Arsenic uptake by plants and possible phytoremediation applications: a brief overview. Environ Chem Lett 10:217–224. https://doi.org/10.1007/s10311-011-0349-8
Wang H, Xu Q, Kong YH, Chen Y, Duan JY, Wu WH, Chen YF (2014) Arabidopsis WRKY45 transcription factor activates phosphate transporter1;1 expression in response to phosphate starvation. Plant Physiol 164:2020–2029. https://doi.org/10.1104/pp.113.235077
Wang P, Zhang W, Mao C, Xu G, Zhao FJ (2016) The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. J Exp Bot 67:6051–6059. https://doi.org/10.1093/jxb/erw362
Wang FZ, Chen MX, Yu LJ, Xie LJ, Yuan LB, Qi H, Xiao M, Guo W, Chen Z, Yi K, Zhang J, Qiu R, Shu W, Xiao S, Chen QF (2017) OsARM1, an R2R3 MYB transcription factor, is involved in regulation of the response to arsenic stress in rice. Front Plant Sci 8:1868. https://doi.org/10.3389/fpls.2017.01868
Wang C, Na G, Bermejo ES, Chen Y, Banks JA, Salt DE, Zhao FJ (2018a) Dissecting the components controlling root-to-shoot arsenic translocation in Arabidopsis thaliana. New Phytol 217(1):206–218. https://doi.org/10.1111/nph.14761
Wang P, Xu X, Tang Z, Zhang W, Huang XY, Zhao FJ (2018b) OsWRKY28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice. Front Plant Sci 9:1330. https://doi.org/10.3389/fpls.2018.01330
Wang J, Kerl CF, Hu P, Martin M, Mu T, Brüggenwirth L, Wu G, Said-Pullicino D, Romani M, Wu L, Planer-Friedrich B (2020) Thiolated arsenic species observed in rice paddy pore waters. Nat Geosci 13:282–287. https://doi.org/10.1038/s41561-020-0533-1
Wanke D, Üner Kolukisaoglu H (2010) An update on the ABCC transporter family in plants: many genes, many proteins, but how many functions? Plant Biol 12:15–25. https://doi.org/10.1111/j.1438-8677.2010.00380.x
Williams PN, Islam S, Islam R, Jahiruddin M, Adomako E, Soliaman AR, Rahman GK, Lu Y, Deacon C, Zhu YG, Meharg AA (2009) Arsenic limits trace mineral nutrition (selenium, zinc, and nickel) in Bangladesh rice grain. Environ Sci Technol 43(21):8430–8436. https://doi.org/10.1021/es901825t
Wu Z, Ren H, McGrath SP, Wu P, Zhao FJ (2011) Investigating the contribution of the phosphate transport pathway to arsenic accumulation in rice. Plant Physiol 157:498–508. https://doi.org/10.1104/pp.111.178921
Xie MY, Tian ZH, Yang XL, Liu BH, Yang J, Lin HH (2019) The role of OsNLA1 in regulating arsenate uptake and tolerance in rice. J Plant Physiol 236:15–22. https://doi.org/10.1016/j.jplph.2019.02.013
Xie Q, Yu Q, Jobe TO, Pham A, Ge C, Guo Q, Liu J, Liu H, Zhang H, Zhao Y, Xue S (2021) An amiRNA screen uncovers redundant CBF and ERF34/35 transcription factors that differentially regulate arsenite and cadmium responses. Plant Cell Environ 44(5):1692–1706. https://doi.org/10.1111/pce.14023
Xu W, Dai W, Yan H, Li S, Shen H, Chen Y, Xu H, Sun Y, He Z, Ma M (2015) Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8:722–733. https://doi.org/10.1016/j.molp.2015.01.005
Xu J, Shi S, Wang L, Tang Z, Lv T, Zhu X, Ding X, Wang Y, Zhao FJ, Wu Z (2017) OsHAC4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytol 215:1090–1101. https://doi.org/10.1111/nph.14572
Xu B, Yu JY, Xie T, Li YL, Liu MJ, Guo JX, Li HL, Yu Y, Zheng CY, Chen YH, Wang G (2018) Brassinosteroids and iron plaque affect arsenic and cadmium uptake by rice seedlings grown in hydroponic solution. Biol Plant 62:362–368. https://doi.org/10.1007/s10535-018-0784-5
Xu B, Yu J, Zhong Y, Guo Y, Ding J, Chen Y, Wang G (2019) Influence of Br 24 and Gr24 on the accumulation and uptake of Cd and As by rice seedlings grown in nutrient solution. Pol J Environ Stud 28(5):3951–3958. https://doi.org/10.15244/pjoes/95036
Xu B, Chen J, Yu J, Guo Y, Cai Q, Wu Y, Li Y, Xie T, Chen Y, Wang G (2020) Effects of 24-epibrassinolide and 28-homobrassinolide on iron plaque formation and the uptake of As and Cd by rice seedlings (Oryza sativa L.) in solution culture. Environ Technol Innov 19:100802. https://doi.org/10.1016/j.eti.2020.100802
Yadav G, Srivastava PK, Parihar P, Tiwari S, Prasad SM (2016) Oxygen toxicity and antioxidative responses in arsenic stressed Helianthus annuus L. seedlings against UV-B. J Photochem Photobiol B 165:58–70. https://doi.org/10.1016/j.jphotobiol.2016.10.011
Yamaji N, Ma JF (2021) Metalloid transporters and their regulation in plants. Plant Physiol 187(4):1929–1939. https://doi.org/10.1093/plphys/kiab326
Yan G, Chen X, Du S, Deng Z, Wang L, Chen S (2019) Genetic mechanisms of arsenic detoxification and metabolism in bacteria. Curr Genet 65:329–338. https://doi.org/10.1007/s00294-018-0894-9
Yang J, Gao MX, Hu H, Ding XM, Lin HW, Wang L, Xu JM, Mao CZ, Zhao FJ, Wu ZC (2016) OsCLT1, a CRT-like transporter 1, is required for glutathione homeostasis and arsenic tolerance in rice. New Phytol 211:658–670. https://doi.org/10.1111/nph.13908
Yang J, Wang L, Mao C, Lin H (2017) Characterization of the rice NLA family reveals a key role for OsNLA1 in phosphate homeostasis. Rice 10:1–6. https://doi.org/10.1186/s12284-017-0193-y
Yao L, Huang L, He Z, Zhou C, Lu W, Bai C (2016) Delivery of roxarsone via chicken diet→ chicken→ chicken manure→ soil→ rice plant. SciTotal Environ 566:1152–1158. https://doi.org/10.1016/j.scitotenv.2016.05.157
Ye Y, Li P, Xu T, Zeng L, Cheng D, Yang M, Luo J, Lian X (2017) OsPT4 contributes to arsenate uptake and transport in rice. Front Plant Sci 8:2197. https://doi.org/10.3389/fpls.2017.02197
Yoshinari A, Hosokawa T, Amano T, Beier MP, Kunieda T, Shimada T, Hara-Nishimura I, Naito S, Takano J (2019) Polar localization of the borate exporter BOR1 requires AP2-dependent endocytosis. Plant Physiol 179(4):1569–1580. https://doi.org/10.1104/pp.18.01017
Yu LJ, Luo YF, Liao B, Xie LJ, Chen L, Xiao S, Li JT, Hu SN, Shu WS (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol 195:97–112. https://doi.org/10.1111/j.1469-8137.2012.04154.x
Yue W, Ying Y, Wang C, Zhao Y, Dong C, Whelan J, Shou H (2017) OsNLA1, a RING-type ubiquitin ligase, maintains phosphate homeostasis in Oryza sativa via degradation of phosphate transporters. Plant J 90:1040–1051. https://doi.org/10.1111/tpj.13516
Zhao FJ, Wang P (2020) Arsenic and cadmium accumulation in rice and mitigation strategies. Plant Soil 446(1):1–21. https://doi.org/10.1007/s11104-019-04374-6
Zhao FJ, Ma JF, Meharg AA, McGrath SP (2009) Arsenic uptake and metabolism in plants. New Phytol 181:777–794. https://doi.org/10.1111/j.1469-8137.2008.02716.x
Zhao FJ, McGrath SP, Meharg AA (2010a) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559. https://doi.org/10.1146/annurev-arplant-042809-112152
Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010b) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. The New Phytol 186:392–399. https://doi.org/10.1111/j.1469-8137.2010.03192.x
Zheng MZ, Li G, Sun GX, Shim H, Cai C (2013) Differential toxicity and accumulation of inorganic and methylated arsenic in rice. Plant Soil 365:227–238. https://doi.org/10.1007/s11104-012-1376-3
Acknowledgements
Authors are thankful to the Council of Scientific and Industrial Research (CSIR), India, for financial assistance [vide letter No. 38 (1469)/18/EMR-II, dated 04.04.2018]. KP gratefully acknowledges University Grants Commission (UGC), New Delhi, for UGC—Dr. D. S. Kothari Post-Doctoral Fellowship [No.F.4-2/2006 (BSR)/BL/19-20/0072 dated October 21, 2019].
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Mondal, S., Pramanik, K., Ghosh, S.K. et al. Molecular insight into arsenic uptake, transport, phytotoxicity, and defense responses in plants: a critical review. Planta 255, 87 (2022). https://doi.org/10.1007/s00425-022-03869-4
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DOI: https://doi.org/10.1007/s00425-022-03869-4