Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice
Tóm tắt
Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and detoxification is still poorly understood. In this study, we found that JA biosynthesis enzymes Allene Oxide Synthases, OsAOS1 and OsAOS2, regulate As accumulation and As tolerance in rice. Evolutionary bioinformatic analysis indicated that AOS1 and AOS2 have evolved from streptophyte algae (e.g. the basal lineage Klebsormidium flaccidum) – sister clade of land plants. Compared to other two AOSs, OsAOS1 and OsAOS2 were highly expressed in all examined rice tissues and their transcripts were highly induced by As in root and shoot. Loss-of-function of OsAOS1 (osaos1–1) showed elevated As concentration in grains, which was likely attributed to the increased As translocation from root to shoot when the plants were subjected to arsenate [As(V)] but not arsenite [As (III)]. However, the mutation of OsAOS2 (osaos2–1) showed no such effect. Moreover, osaos1–1 and osaos2–1 increased the sensitivity of rice plants to both As(V) and As(III). Disrupted expression of genes involved in As accumulation and detoxification, such as OsPT4, OsNIP3;2, and OsOASTL-A1, was observed in both osaos1–1 and osaos2–1 mutant lines. In addition, a As(V)-induced significant decrease in Reactive Oxygen Species (ROS) production was observed in the root of osaos1–1 but not in osaos2–1. Taken together, our results indicate OsAOS1 modulates both As allocation and detoxification, which could be partially attributed to the altered gene expression profiling and ROS homeostasis in rice while OsAOS2 is important for As tolerance.
Tài liệu tham khảo
Abbasi S, Lamb D, Rahman MA et al (2021) Response of phosphorus sensitive plants to arsenate. Environ Technol Innov 24:102008, ISSN 2352-1864. https://doi.org/10.1016/j.eti.2021.102008
Antoniadis V, Shaheen SM, Levizou E, Shahid M, Niazi NK, Vithanage M, Ok YS, Bolan N, Rinklebe J (2019) A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: are they protective concerning health risk assessment? - a review. Environ Int 127:819–847. https://doi.org/10.1016/j.envint.2019.03.039
Azizur Rahman M, Hasegawa H, Mahfuzur Rahman M, Nazrul Islam M, Majid Miah MA, Tasmen A (2007) Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere 67:1072–1079. https://doi.org/10.1016/j.chemosphere.2006.11.061
Cao Y, Sun D, Ai H, Mei H, Liu X, Sun S, Xu G, Liu Y, Chen 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
Chehab EW, Perea JV, Gopalan B, Theg S, Dehesh K (2007) Oxylipin pathway in rice and Arabidopsis. J Integr Plant Biol 49:43–51. https://doi.org/10.1111/j.1744-7909.2006.00405.x
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13:1194–1202. https://doi.org/10.1016/j.molp.2020.06.009
Chen X, Jiang W, Tong T, Chen G, Zeng F, Jang S, Gao W, Li Z, Mak M, Deng F, Chen ZH (2021) Molecular interaction and evolution of jasmonate signaling with transport and detoxification of heavy metals and metalloids in plants. Front Plant Sci 12:665842. https://doi.org/10.3389/fpls.2021.665842
Chen Y, Hua CY, Chen JX, Rathinasabapathi B, Cao Y, Ma LQ (2019) Expressing arsenite antiporter PvACR3;1 in rice (Oryza sativa L.) decreases inorganic arsenic content in rice grains. Environ Sci Technol 53:10062–10069. https://doi.org/10.1021/acs.est.9b02418
Chen Y, Sun SK, Tang Z, Liu G, Moore KL, Maathuis FJM, Miller AJ, McGrath SP, Zhao FJ (2017) 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
Cheng J, Zhang S, Yi Y, Qin Y, Chen ZH, Deng F, Zeng F (2023) Hydrogen peroxide reduces root cadmium uptake but facilitates root-to-shoot cadmium translocation in rice through modulating cadmium transporters. Plant Physiol Biochem 200:107754. https://doi.org/10.1016/j.plaphy.2023.107754
Clemens S, Ma JF (2016) Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol 67:489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
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
Deng F, Liu X, Chen Y, Rathinasabapathi B, Rensing C, Chen J, Bi J, Xiang P, Ma LQ (2020) Aquaporins mediated arsenite transport in plants: molecular mechanisms and applications in crop improvement. Crit Rev Environ Sci Technol 50:1613–1639. https://doi.org/10.1080/10643389.2019.1662704
Deng F, Yamaji N, Ma JF, Lee SK, Jeon JS, Martinoia E et al (2018) Engineering rice with lower grain arsenic. Plant Biotechnol J 16:1691–1699. https://doi.org/10.1111/pbi.12905
Deng F, Yamaji N, Xia J, Ma JF (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol 163:1353–1362. https://doi.org/10.1104/pp.113.226225
Deng F, Yu M, Martinoia E, Song WY (2019) Ideal cereals with lower arsenic and cadmium by accurately enhancing vacuolar sequestration capacity. Front Genet 10:322. https://doi.org/10.3389/fgene.2019.00322
Deng F, Zeng F, Chen G, Feng X, Riaz A, Wu X et al (2021) Metalloid hazards: from plant molecular evolution to mitigation strategies. J Hazard Mater 409:124495. https://doi.org/10.1016/j.jhazmat.2020.124495
Deng F, Zeng F, Shen Q, Abbas A, Cheng J, Jiang W et al (2022) Molecular evolution and functional modification of plant miRNAs with CRISPR. Trends Plant Sci 27:890–907. https://doi.org/10.1016/j.tplants.2022.01.009
Deng M, Wang S, Huang H, Ye D, Zhang X, Wang Y et al (2023) Hydrogen peroxide mediates cadmium accumulation in the root of a high cadmium-accumulating rice (Oryza sativa L.) line. J Hazard Mater 448:130969. https://doi.org/10.1016/j.jhazmat.2023.130969
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, Shao G, Tang Z, Chen H, Wang B, Tang Z et al (2017) Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars. Rice (N Y) 10:9. https://doi.org/10.1186/s12284-017-0149-2
Faizan M, Sehar S, Rajput VD, Faraz A, Afzal S, Minkina T, Sushkova S, Adil MF, Yu F, Alatar AA, Akhter F, Faisal M (2021) Modulation of cellular redox status and antioxidant defense system after synergistic application of zinc oxide nanoparticles and salicylic acid in rice (Oryza sativa) plant under arsenic stress. Plants (Basel) 10(11):2254. https://doi.org/10.3390/plants10112254
Farooq MA, Zhang K, Islam F, Wang J, Athar HUR, Nawaz A et al (2018) Physiological and iTRAQ-based quantitative proteomics analysis of methyl jasmonate-induced tolerance in Brassica napus under arsenic stress. Proteomics 18:e1700290. https://doi.org/10.1002/pmic.201700290
Guan DX, Dai ZH, Sun HJ, Ma LQ (2021) Arsenic and selenium in the plant-soil-human ecosystem: CREST publications during 2018–2021. Crit Rev Environ Sci Technol 1-6. https://doi.org/10.1080/10643389.2021.2010836
Ha SB, Lee BC, Lee DE, Kuk YI, Lee AY, Han O, Back K (2022) Molecular characterization of the gene encoding rice allene oxide synthase and its expression. Biosci Biotechnol Biochem 66(12):2719–2722. https://doi.org/10.1271/bbb.66.2719
Haga K, Iino M (2004) Phytochrome-mediated transcriptional up-regulation of ALLENE OXIDE SYNTHASE in rice seedlings. Plant Cell Physiol 45:119–128. https://doi.org/10.1093/pcp/pch025
Hayashi S, Kuramata M, Abe T, Takagi H, Ozawa K, Ishikawa S (2017) Phytochelatin synthase OsPCS1 plays a crucial role in reducing arsenic levels in rice grains. Plant J 91:840–848. https://doi.org/10.1111/tpj.13612
Hu B, Deng F, Chen G, Chen X, Gao W, Long L, Xia J, Chen ZH (2020) Evolution of abscisic acid signaling for stress responses to toxic metals and metalloids. Front Plant Sci 11:909. https://doi.org/10.3389/fpls.2020.00909
Hu S, Yu K, Yan J, Shan X, Xie D (2023) Jasmonate perception: ligand-receptor interaction, regulation, and evolution. Mol Plant 16:23–42. https://doi.org/10.1016/j.molp.2022.08.011
Huang TL, Nguyen QT, 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
Huang XY, Deng F, Yamaji N, Pinson SRM, Fujii-Kashino M, Danku J, Douglas A, Guerinot ML, Salt DE, Ma JF (2016) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:12138. https://doi.org/10.1038/ncomms12138
Huang Y, Chen H, Reinfelder JR, Liang X, Sun C, Liu C, Li F, Yi J (2019) A transcriptomic (RNA-seq) analysis of genes responsive to both cadmium and arsenic stress in rice root. Sci Total Environ 666:445–460. https://doi.org/10.1016/j.scitotenv.2019.02.281
Hung KT, Hsu YT, Kao CH (2006) Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant 127:293–303. https://doi.org/10.1111/j.1399-3054.2006.00662.x
Jiang W, Tong T, Li W, Huang Z, Chen G, Zeng F, Riaz A, Amoanimaa-Dede H, Pan R, Zhang W, Deng F, Chen ZH (2023) Molecular evolution of plant 14-3-3 proteins and function of Hv14-3-3A in stomatal regulation and drought tolerance. Plant Cell Physiol 63:1857–1872. https://doi.org/10.1093/pcp/pcac034
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
Khanna K, Kohli SK, Kumar P, Ohri P, Bhardwaj R, Alam P, Ahmad P (2022) Arsenic as hazardous pollutant: perspectives on engineering remediation tools. Sci Total Environ 838:155870. https://doi.org/10.1016/j.scitotenv.2022.155870
Koeduka T, Ishizaki K, Mwenda CM, Hori K, Sasaki-Sekimoto Y, Ohta H, Kohchi T, Matsui K (2015) Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family. Planta 242:1175–1186. https://doi.org/10.1007/s00425-015-2355-8
Lei GJ, Sun L, Sun Y, Zhu XF, Li GX, Zheng SJ (2020) Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. J Integr Plant Biol 62:218–227. https://doi.org/10.1111/jipb.12801
Li H, Xu X, Han K, Wang Z, Ma W, Lin Y, Hua H (2022b) Isolation and functional analysis of OsAOS1 promoter for resistance to Nilaparvata lugens Stål infestation in rice. J Cell Physiol 237(3):1833–1844. https://doi.org/10.1002/jcp.30653
Li L, Zheng Q, Jiang W, Xiao N, Zeng F, Chen G, Mak M, Chen ZH, Deng F (2023) Molecular regulation and evolution of cytokinin signaling in plant abiotic stresses. Plant Cell Physiol 63:1787–1805. https://doi.org/10.1093/pcp/pcac071
Li Y, Huang YZ, Bao QL, Huang YC, Zhang SN (2022a) Effects of exogenous jasmonic acid on arsenic accumulation and response to stress in roots of rice seedlings. Environ Sci 43:4831–4838. https://doi.org/10.13227/j.hjkx.202111296
Lu X, Liu S, Zhi S, Chen J, Ye G (2020) Comparative transcriptome profile analysis of rice varieties with different tolerance to zinc deficiency. Plant Biol (Stuttg). https://doi.org/10.1111/plb.13227
Lu Y, Ye X, Guo R, Huang J, Wang W, Tang J, Tan L, Zhu JK, Chu C, Qian Y (2017) Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol Plant 10:1242–1245. https://doi.org/10.1016/j.molp.2017.06.007
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 U S A 105:9931–9935. https://doi.org/10.1073/pnas.0802361105
Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, Villada A, Cambell RC, Sun G, Zhu YG, Feldmann J, Raab A, Zhao FJ, Islam R, Hossain S, Yanai J (2009) Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol 43:1612–1617. https://doi.org/10.1021/es802612a
Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant-Microbe Interact 19:1127–1237. https://doi.org/10.1094/MPMI-19-1127
Mousavi SR, Niknejad Y, Fallah H, Tari DB (2020) Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39:1041–1060. https://doi.org/10.1007/s00299-020-02547-7
Nazir F, Fariduddin Q, Khan TA (2020) Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 252:126486. https://doi.org/10.1016/j.chemosphere.2020.126486
Ning M, Liu SJ, Deng F, Huang L, Li H, Che J, Yamaji N, Hu F, Lei GJ (2023) A vacuolar transporter plays important roles in zinc and cadmium accumulation in rice grain. New Phytol 239:1919–1934. https://doi.org/10.1111/nph.19070
One Thousand Plant Transcriptomes Initiative (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–685. https://doi.org/10.1038/s41586-019-1693-2
Pinson SRM, Tarpley L, Yan W, Yeater K, Lahner B, Yakubova E, Huang XY, Zhang M , Guerinot ML , Salt DE (2015) Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Sci 55:294–311. https://doi.org/10.2135/cropsci2013.10.0656
Podgorski J, Berg M (2020) Global threat of arsenic in groundwater. Science 368:845–850. https://doi.org/10.1126/science.aba1510
Ronzan M, Piacentini D, Fattorini L, Federica DR, Caboni E, Eiche E, Ziegler J, Hause B, Riemann M, 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
Sehar S, Adil MF, Askri SMH, Feng Q, Wei D, Sahito FS, Shamsi IH (2023b) Pan-transcriptomic profiling demarcates serendipita indica-phosphorus mediated tolerance mechanisms in rice exposed to arsenic toxicity. Rice (N Y) 16(1):28. https://doi.org/10.1186/s12284-023-00645-0
Sehar S, Adil MF, Ma Z, Karim MF, Faizan M, Zaidi SSA, Siddiqui MH, Alamri S, Zhou F, Shamsi IH (2023a) Phosphorus and Serendipita indica synergism augments arsenic stress tolerance in rice by regulating secondary metabolism related enzymatic activity and root metabolic patterns. Ecotoxicol Environ Saf 256:114866. https://doi.org/10.1016/j.ecoenv.2023.114866
Sehar S, Feng Q, Adil MF, Sahito FS, Ibrahim Z, Baloch DM, Ullah N, Ouyang Y, Guo Y, Shamsi IH (2022) Tandem application of endophytic fungus Serendipita indica and phosphorus synergistically recuperate arsenic induced stress in rice. Front Plant Sci 13:982668. https://doi.org/10.3389/fpls.2022.982668
Sharma SS, Kumar V, Dietz KJ (2021) Emerging trends in metalloid-dependent signaling in plants. Trends Plant Sci 26:452–471. https://doi.org/10.1016/j.tplants.2020.11.003
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
Smirnoff N, Arnaud D (2019) Hydrogen peroxide metabolism and functions in plants. New Phytol 221:1197–1214. https://doi.org/10.1111/nph.15488
Song WY, Yamaki T, Yamaji N, Ko D, Jung KH, Fujii-Kashino M, An G, Martinoia E, Lee Y, 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
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
Stumpe M, Bode J, Göbel C, Wichard T, Schaaf A, Frank W, Frank M, Reski R, Pohnert G, Feussner I (2006) Biosynthesis of C9-aldehydes in the moss Physcomitrella patens. Biochim Biophys Acta 1761:301–312. https://doi.org/10.1016/j.bbalip.2006.03.008
Su Y, McGrath S, Zhao F (2010) Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant Soil 328:27–34. https://doi.org/10.1007/s11104-009-0074-2
Sun SK, Chen Y, Che J, Konishi N, Tang Z, Miller AJ, Ma JF, Zhao FJ (2018) Decreasing arsenic accumulation in rice by overexpressing OsNIP1;1 and OsNIP3;3 through disrupting arsenite radial transport in roots. New Phytol 219:641–653. https://doi.org/10.1111/nph.15190
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, Zhao F (2021) The roles of membrane transporters in arsenic uptake, translocation and detoxification in plants. Crit Rev Environ Sci Technol 51:2449–2484. https://doi.org/10.1080/10643389.2020.1795053
Verma G, Srivastava D, Narayan S, Shirke PA, Chakrabarty D (2020) Exogenous application of methyl jasmonate alleviates arsenic toxicity by modulating its uptake and translocation in rice (Oryza sativa L.). Ecotoxicol Environ Saf 201:110735. https://doi.org/10.1016/j.ecoenv.2020.110735
Wang J, Song L, Gong X, Xu J, Li M (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci 21. https://doi.org/10.3390/ijms21041446
Wang P, Xu X, Tang Z, Zhang W, Huang XY, Zhao FJ (2018) 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 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
Wasternack C, Feussner I (2018) The oxylipin pathways: biochemistry and function. Annu Rev Plant Biol 69:363–386. https://doi.org/10.1146/annurev-arplant-042817-040440
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
Yamaji N, Ma JF (2021) Metalloid transporters and their regulation in plants. Plant Physiol. https://doi.org/10.1093/plphys/kiab326
Ye M, Song Y, Long J, Wang R, Baerson SR, Pan Z, Zhu-Salzman K, Xie J, Cai K, Luo S, Zeng R (2013) Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA 110(38):E3631–E3639. https://doi.org/10.1073/pnas.1305848110
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
Yu X, Zhang W, Zhang Y, Zhang X, Lang D, Zhang X (2019) The roles of methyl jasmonate to stress in plants. Funct Plant Biol 46:197–212. https://doi.org/10.1071/fp18106
Zhang J, Wysocki R, Li F, Yu M, Martinoia E, Song WY (2023a) Role of ubiquitination in arsenic tolerance in plants. Trends Plant Sci 28:880–892. https://doi.org/10.1016/j.tplants.2023.03.008
Zhang S, Bao Q, Huang Y, Han N (2023b) Exogenous plant hormones alleviate as stress by regulating antioxidant defense system in Oryza sativa L. Environ Sci Pollut Res Int 30:6454–6465. https://doi.org/10.1007/s11356-022-22627-3
Zhang Y, Berman A, Shani E (2023c) Plant hormone transport and localization: signaling molecules on the move. Annu Rev Plant Biol 74:453–479. https://doi.org/10.1146/annurev-arplant-070722-015329
Zhao F, Tang Z, Song J, Huang X, Wang P (2022) Toxic metals and metalloids: uptake, transport, detoxification, phytoremediation and crop improvement for safer food. Mol Plant 15:27–44. https://doi.org/10.1016/j.molp.2021.09.016
Zhao FJ, Ago Y, Mitani N, Li RY, Su YH, Yamaji N, McGrath SP, Ma JF (2010) The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol 186:392–399. https://doi.org/10.1111/j.1469-8137.2010.03192.x
Zhou Y, Guang YL, Li JW, Wang F, Ahammed GJ, Yang YX (2019) The CYP74 gene family in watermelon: genome-wide identification and expression profiling under hormonal stress and root-knot nematode infection. Agronomy-Basel 9. https://doi.org/10.3390/agronomy9120872
Zvobgo G, Sagonda T, Lwalaba JLW, Mapodzeke JM, Muhammad N, Chen G, Shamsi IH, Zhang G (2018) Transcriptomic comparison of two barley genotypes differing in arsenic tolerance exposed to arsenate and phosphate treatments. Plant Physiol Biochem 130:589–603. https://doi.org/10.1016/j.plaphy.2018.08.006