Overexpression of bacterial γ-glutamylcysteine synthetase increases toxic metal(loid)s tolerance and accumulation in Crambe abyssinica.


Journal

Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970

Informations de publication

Date de publication:
23 Oct 2024
Historique:
received: 05 07 2024
accepted: 03 10 2024
medline: 24 10 2024
pubmed: 24 10 2024
entrez: 23 10 2024
Statut: epublish

Résumé

Transgenic Crambe abyssinica lines overexpressing γ-ECS significantly enhance tolerance to and accumulation of toxic metal(loid)s, improving phytoremediation potential and offering an effective solution for contaminated soil management. Phytoremediation is an attractive environmental-friendly technology to remove metal(loid)s from contaminated soils and water. However, tolerance to toxic metals in plants is a critical limiting factor. Transgenic Crambe abyssinica lines were developed that overexpress the bacterial γ-glutamylcysteine synthetase (γ-ECS) gene to increase the levels of non-protein thiol peptides such as γ-glutamylcysteine (γ-EC), glutathione (GSH), and phytochelatins (PCs) that mediate metal(loid)s detoxification. The present study investigated the effect of γ-ECS overexpression on the tolerance to and accumulation of toxic As, Cd, Pb, Hg, and Cr supplied individually or as a mixture of metals. Compared to wild-type plants, γ-ECS transgenics (γ-ECS1-8 and γ-ECS16-5) exhibited a significantly higher capacity to tolerate and accumulate these elements in aboveground tissues, i.e., 76-154% As, 200-254% Cd, 37-48% Hg, 26-69% Pb, and 39-46% Cr, when supplied individually. This is attributable to enhanced production of GSH (82-159% and 75-87%) and PC2 (27-33% and 37-65%) as compared to WT plants under AsV and Cd exposure, respectively. The levels of Cys and γ-EC were also increased by 56-67% and 450-794% in the overexpression lines compared to WT plants under non-stress conditions, respectively. This likely enhanced the metabolic pathway associated with GSH biosynthesis, leading to the ultimate synthesis of PCs, which detoxify toxic metal(loid)s through chelation. These findings demonstrate that γ-ECS overexpressing Crambe lines can be used for the enhanced phytoremediation of toxic metals and metalloids from contaminated soils.

Identifiants

pubmed: 39443376
doi: 10.1007/s00299-024-03351-3
pii: 10.1007/s00299-024-03351-3
doi:

Substances chimiques

Glutamate-Cysteine Ligase EC 6.3.2.2
Glutathione GAN16C9B8O
Soil Pollutants 0
gamma-glutamylcysteine M984VJS48P
Phytochelatins 98726-08-0
Metals, Heavy 0
Dipeptides 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

270

Subventions

Organisme : NIEHS NIH HHS
ID : R01ES032686
Pays : United States
Organisme : National Institute of Food and Agriculture
ID : Hatch Project #508

Informations de copyright

© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Al Mamun A, Rahman MM, Huq MA, Rahman MM, Rana MR, Rahman ST, Alam MK (2024) Phytoremediation: a transgenic perspective in omics era. Transgenic Res. 33: 1–20. https://doi.org/10.1007/s11248-024-00393-x
Almotairy H (2024) Mitigating metal/metalloid stress in crops: strategies for sustainable agricultural resilience. https://doi.org/10.5772/intechopen.115044
Anon (1993) Crambe production and utilization. BioOptions, newsletter of the centre for alternative plant and animal products. University of Minnesota, Winter. 1–3
Artus NN (2006) Arsenic and cadmium phytoextraction potential of crambe compared with Indian mustard. J Plant Nutr 29(4):667–679. https://doi.org/10.1080/01904160600564444
doi: 10.1080/01904160600564444
Barathi S, Lee J, Venkatesan R, Vetcher AA (2023) Current status of biotechnological approaches to enhance the phytoremediation of heavy metals in India—a review. Plants 12(22):3816. https://doi.org/10.3390/plants12223816
doi: 10.3390/plants12223816 pubmed: 38005713 pmcid: 10675783
Bennett LE, Burkhead JL, Hale KL, Terry N, Pilon M, Pilon-Smits EA (2003) Analysis of transgenic Indian mustard plants for phytoremediation of metal-contaminated mine tailings. J Environ Qual 32(2):432–440. https://doi.org/10.2134/jeq2003.4320
doi: 10.2134/jeq2003.4320 pubmed: 12708665
Bernardino CA, Mahler CF, Alvarenga P, Castro PM, da Silva EF, Novo LA (2020) Recent advances in phytoremediation of soil contaminated by industrial waste: a road map to a safer environment. Bioremediation Ind Waste Environ Saf Volume I Ind Waste Manag. 207–221. https://doi.org/10.1007/978-981-13-1891-7_10
Bizily SP, Rugh CL, Summers AO, Meagher RB (1999) Phytoremediation of methylmercury pollution: merB expression in Arabidopsis thaliana confers resistance to organomercurials. Proc Natl Acad Sci 96:6808–6813. https://doi.org/10.1073/pnas.96.12.6808
doi: 10.1073/pnas.96.12.6808 pubmed: 10359794 pmcid: 21997
Briffa J, Sinagra E, Blundell R (2020). Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon. https://doi.org/10.1016/j.heliyon.2020.e04691
Chhikara S, Dutta I, Paulose B, Jaiwal PK, Dhankher OP (2012) Development of an Agrobacterium-mediated stable transformation method for industrial oilseed crop Crambe abyssinica ‘BelAnn.’ Ind Crops Prod 37(1):457–465. https://doi.org/10.1016/j.indcrop.2011.07.021
doi: 10.1016/j.indcrop.2011.07.021
Clemens S, Palmgren MG, Krämer U (2002) A long way ahead: understanding and engineering plant metal accumulation. Trends Plant Sci 7(7):309–315. https://doi.org/10.1016/S1360-1385(02)02295-1
doi: 10.1016/S1360-1385(02)02295-1 pubmed: 12119168
Cobbett CS (1999) A family of phytochelatin synthase genes from plant, fungal and animal species. Trends Plant Sci 4(9):335–337. https://doi.org/10.1016/S1360-1385(99)01465-X
doi: 10.1016/S1360-1385(99)01465-X pubmed: 10462763
Cullen JT, McAlister J (2017) Biogeochemistry of lead. Its release to the environment and chemical speciation. Lead Eff Environ Health. 17: 21–48. https://doi.org/10.1515/9783110434330
Dhankher OP, Li Y, Rosen BP, Shi J, Salt D, Senecoff JF, Meagher RB (2002) Engineering tolerance and hyperaccumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nat Biotechnol 20(11):1140–1145. https://doi.org/10.1038/nbt747
doi: 10.1038/nbt747 pubmed: 12368812
Dhankher OP, Pilon-Smits EA, Meagher RB, Doty S (2012) Biotechnological approaches for phytoremediation. In: Plant biotechnology and agriculture. Academic Press. pp. 309–328. https://doi.org/10.1016/B978-0-12-381466-1.00020-1
Eapen S, Singh S, D’souza SF (2007) Advances in development of transgenic plants for remediation of xenobiotic pollutants. Biotechnol Adv 25(5):442–451. https://doi.org/10.1016/j.biotechadv.2007.05.001
doi: 10.1016/j.biotechadv.2007.05.001 pubmed: 17553651
European Union Strategic Research Agenda, part II: Plant for the Future. Stakeholder proposal for a strategic research agenda 2005 including Draft Action Plan 2010 2005.
Fahey RC, Newton GL (1987) Determination of low-molecular-weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography. Methods Enzymol 143:85–96
doi: 10.1016/0076-6879(87)43016-4 pubmed: 3657565
Faizan M, Alam P, Hussain A, Karabulut F, Tonny SH, Cheng SH, Hayat S (2024) Phytochelatins: a key regulator against heavy metal toxicity in plants. Plant Stress. 100355. https://doi.org/10.1016/j.stress.2024.100355
Gisbert C, Ros R, De Haro A, Walker DJ, Bernal MP, Serrano R, Navarro-Aviñó J (2003) A plant genetically modified that accumulates Pb is especially promising for phytoremediation. Biochem Biophys Res Commun 303(2):440–445. https://doi.org/10.1016/S0006-291X(03)00349-8
doi: 10.1016/S0006-291X(03)00349-8 pubmed: 12659836
Hartley-Whitaker J, Ainsworth G, Vooijs R, Bookum WT, Schat H, Meharg AA (2001) Phytochelatins are involved in differential arsenate tolerance in Holcus lanatus. Plant Physiol 126(1):299–306. https://doi.org/10.1104/pp.126.1.299
doi: 10.1104/pp.126.1.299 pubmed: 11351093 pmcid: 102304
Howden R, Andersen CR, Goldsbrough PB, Cobbett CS (1995a) A cadmium-sensitive, glutathione-deficient mutant of Arabidopsis thaliana. Plant Physiol 107(4):1067–1073. https://doi.org/10.1104/pp.107.4.1067
doi: 10.1104/pp.107.4.1067 pubmed: 7770518 pmcid: 157238
Howden R, Goldsbrough PB, Andersen CR, Cobbett CS (1995b) Cadmium-sensitive, cad1 mutants of Arabidopsis thaliana are phytochelatin deficient. Plant Physiol 107(4):1059–1066. https://doi.org/10.1104/pp.107.4.1059
doi: 10.1104/pp.107.4.1059 pubmed: 7770517 pmcid: 157237
Jozefczak M, Remans T, Vangronsveld J, Cuypers A (2012) Glutathione is a key player in metal-induced oxidative stress defenses. Int J Mol Sci 13(3):3145–3175. https://doi.org/10.3390/ijms13033145
doi: 10.3390/ijms13033145 pubmed: 22489146 pmcid: 3317707
Kumar K, Shinde A, Aeron V, Verma A, Arif NS (2023) Genetic engineering of plants for phytoremediation: advances and challenges. J Plant Biochem Biotechnol 32(1):12–30. https://doi.org/10.1007/s13562-022-00776-3
doi: 10.1007/s13562-022-00776-3
Li Y, Dhankher OP, Carreira L, Balish RS, Meagher RB (2005) Arsenic and mercury tolerance and cadmium sensitivity in Arabidopsis plants expressing bacterial γ-glutamylcysteine synthetase. Environ Toxicol Chem Int J 24(6):1376–1386. https://doi.org/10.1897/04-340R.1
doi: 10.1897/04-340R.1
Liu P, Zhang Y, Feng N, Zhu M, Tian J (2020) Potentially toxic element (PTE) levels in maize, soil, and irrigation water and health risks through maize consumption in northern Ningxia, China. BMC Public Health 20:1–13. https://doi.org/10.1186/s12889-020-09845-5
doi: 10.1186/s12889-020-09845-5
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402–408
doi: 10.1006/meth.2001.1262 pubmed: 11846609
Meagher RB (2000) Phytoremediation of toxic elemental and organic pollutants. Curr Opin Plant Biol 3(2):153–162. https://doi.org/10.1016/S1369-5266(99)00054-0
doi: 10.1016/S1369-5266(99)00054-0 pubmed: 10712958
Minocha R, Thangavel P, Dhankher OP, Long S (2008) Separation and quantification of monothiols and phytochelatins from a wide variety of cell cultures and tissues of trees and other plants using high performance liquid chromatography. J Chromatogr A 1207(1–2):72–83. https://doi.org/10.1016/j.chroma.2008.08.023
doi: 10.1016/j.chroma.2008.08.023 pubmed: 18760414
Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP (2016) Potential biotechnological strategies for the cleanup of heavy metals and metalloids. Front Plant Sci 7:183531. https://doi.org/10.3389/fpls.2016.00303
doi: 10.3389/fpls.2016.00303
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiologia plantarum. 15(3)
Niede R, Benbi DK (2022) Integrated review of the nexus between toxic elements in the environment and human health. AIMS Public Health. 9(4): 758. https://doi.org/10.3934/publichealth.2022052
Noctor G, Arisi ACM, Jouanin L, Kunert KJ, Rennenberg H, Foyer CH (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49(321):623–647. https://doi.org/10.1093/jxb/49.321.623
doi: 10.1093/jxb/49.321.623
Pal R, Rai JPN (2010) Phytochelatins: peptides involved in heavy metal detoxification. Appl Biochem Biotechnol 160:945–963. https://doi.org/10.1007/s12010-009-8565-4
doi: 10.1007/s12010-009-8565-4 pubmed: 19224399
Paulose B, Kandasamy S, Dhankher OP (2010) Expression profiling of Crambe abyssinica under arsenate stress identifies genes and gene networks involved in arsenic metabolism and detoxification. BMC Plant Biol 10:1–12. https://doi.org/10.1186/1471-2229-10-108
doi: 10.1186/1471-2229-10-108
Paulose B, Chhikara S, Coomey J, Jung HI, Vatamaniuk O, Dhankher OP (2013) A γ-glutamyl cyclotransferase protects Arabidopsis plants from heavy metal toxicity by recycling glutamate to maintain glutathione homeostasis. Plant Cell 25(11):4580–4595. https://doi.org/10.1105/tpc.113.111815
doi: 10.1105/tpc.113.111815 pubmed: 24214398 pmcid: 3875737
Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiol 122(4):1171–1178. https://doi.org/10.1104/pp.122.4.1171
doi: 10.1104/pp.122.4.1171 pubmed: 10759512 pmcid: 58951
Podgorski JE, Eqani SAMAS, Khanam T, Ullah R, Shen H, Berg M (2017) Extensive arsenic contamination in high-pH unconfined aquifers in the Indus valley. Sci Adv 3(8):e1700935. https://doi.org/10.1126/sciadv.1700935
doi: 10.1126/sciadv.1700935 pubmed: 28845451 pmcid: 5567761
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180(2):169–181. https://doi.org/10.1016/j.plantsci.2010.08.016
doi: 10.1016/j.plantsci.2010.08.016 pubmed: 21421358
Reeves RD, Baker AJ, Jaffré T, Erskine PD, Echevarria G, van Der Ent A (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytologist. 218(2): 407–411. https://www.jstor.org/stable/90019919
Reisinger S, Schiavon M, Terry N, Pilon-Smits EA (2008) Heavy metal tolerance and accumulation in Indian mustard (Brassica juncea L.) expressing bacterial γ-glutamylcysteine synthetase or glutathione synthetase. Int J Phytoremediation. 10(5): 440–454. https://doi.org/10.1080/15226510802100630
Rodríguez-Lado L, Sun G, Berg M, Zhang Q, Xue H, Zheng Q, Johnson CA (2013) Groundwater arsenic contamination throughout China. Science 341(6148):866–868. https://doi.org/10.1126/science.1237484
doi: 10.1126/science.1237484 pubmed: 23970694
Scheerer U, Haensch R, Mendel RR, Kopriva S, Rennenberg H, Herschbach C (2010) Sulphur flux through the sulphate assimilation pathway is differently controlled by adenosine 5′-phosphosulphate reductase under stress and in transgenic poplar plants overexpressing γ-ECS, SO, or APR. J Exp Bot 61(2):609–622
doi: 10.1093/jxb/erp327 pubmed: 19923196
Schmoger ME, Oven M, Grill E (2000) Detoxification of arsenic by phytochelatins in plants. Plant Physiol 122(3):793–802. https://doi.org/10.1104/pp.122.3.793
doi: 10.1104/pp.122.3.793 pubmed: 10712543 pmcid: 58915
Shi S, Wang T, Chen Z, Tang Z, Wu Z, Salt DE, Zhao FJ (2016) OsHAC1; 1 and OsHAC1; 2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiology. 172(3): 1708–1719. https://doi.org/10.1104/pp.16.01332
Sneller FE, van Heerwaarden LM, Koevoets PL, Vooijs R, Schat H, Verkleij JA (2000) Derivatization of phytochelatins from Silene vulgaris, induced upon exposure to arsenate and cadmium: comparison of derivatization with Ellman’s reagent and monobromobimane. J Agric Food Chem 48:4014–4019
doi: 10.1021/jf9903105 pubmed: 10995306
Song WY, Yamaki T, Yamaji N, Ko D, Jung KH, Fujii-Kashino M, Ma JF (2014) A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci 111(44):15699–15704. https://doi.org/10.1073/pnas.1414968111
doi: 10.1073/pnas.1414968111 pubmed: 25331872 pmcid: 4226097
Superfund Releases Green Remediation Strategy and Principles for Greener Cleanup (2010) In EPA.gov. Retrieved 09 May 2024. From https://www.https://www.epa.gov/superfund/superfund-history-printable-version
Upadhyay MK, Shukla A, Yadav P, Srivastava S (2019) A review of arsenic in crops, vegetables, animals and food products. Food Chem 276:608–618. https://doi.org/10.1016/j.foodchem.2018.10.069
doi: 10.1016/j.foodchem.2018.10.069 pubmed: 30409639
Van Aken B (2009) Transgenic plants for enhanced phytoremediation of toxic explosives. Curr Opin Biotechnol 20(2):231–236. https://doi.org/10.1016/j.copbio.2009.01.011
doi: 10.1016/j.copbio.2009.01.011 pubmed: 19278849
Vatamaniuk OK, Bucher EA, Ward JT, Rea PA (2001) A new pathway for heavy metal detoxification in animals: phytochelatin synthase is required for cadmium tolerance incaenorhabditis elegans. J Biol Chem 276(24):20817–20820. https://doi.org/10.1074/jbc.C100152200
doi: 10.1074/jbc.C100152200 pubmed: 11313333
Venegas-Rioseco J, Ginocchio R, Ortiz-Calderón C (2021) Increase in phytoextraction potential by genome editing and transformation: a review. Plants 11(1):86. https://doi.org/10.3390/plants11010086
doi: 10.3390/plants11010086 pubmed: 35009088 pmcid: 8747683
Wang S, Cao Z, Chen Y, Wu R (2017) Enhancement of Cadmium Tolerance in Transgenic Tobacco Plants by transferring a γ-glutamylcysteine synthetase gene. J Agr Agri Aspect. 118
Xiang C, Werner BL, Christensen ELM, Oliver DJ (2001) The biological functions of glutathione revisited in Arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126(2):564–574. https://doi.org/10.1104/pp.126.2.564
doi: 10.1104/pp.126.2.564 pubmed: 11402187 pmcid: 111149
Yan A, Wang Y, Tan SN, Mohd Yusof ML, Ghosh S, Chen Z (2020) Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front Plant Sci 11:359. https://doi.org/10.3389/fpls.2020.00359
doi: 10.3389/fpls.2020.00359 pubmed: 32425957 pmcid: 7203417
Zhakypbek Y, Kossalbayev BD, Belkozhayev AM, Murat T, Tursbekov S, Abdalimov E, Allakhverdiev SI (2024) Reducing heavy metal contamination in soil and water using phytoremediation. Plants. 13(11): 1534
Zhang X, Zhang L, Chen L, Lu Y, An Y (2022) Ectopic expression γ-glutamylcysteine synthetase of Vicia sativa increased cadmium tolerance in Arabidopsis. Gene 823:146358. https://doi.org/10.1016/j.gene.2022.146358
doi: 10.1016/j.gene.2022.146358 pubmed: 35202731
Zhao C, Qiao M, Yu Y, Xia G, Xiang F (2010) The effect of the heterologous expression of Phragmites australis γ-glutamylcysteine synthetase on the Cd2+ accumulation of Agrostis palustris. Plant Cell Environ 33(6):877–887. https://doi.org/10.1111/j.1365-3040.2009.02113.x
doi: 10.1111/j.1365-3040.2009.02113.x pubmed: 20051038
Zhu YL, Pilon-Smits EA, Tarun AS, Weber SU, Jouanin L, Terry N (1999) Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing γ-glutamylcysteine synthetase. Plant Physiol 121(4):1169–1177. https://doi.org/10.1104/pp.121.4.1169
doi: 10.1104/pp.121.4.1169 pubmed: 10594104 pmcid: 59484

Auteurs

Sudesh Chhikara (S)

Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA, 01003, USA.
Department of Biology, Merrimack College, North Andover, MA, USA.

Yogita Singh (Y)

Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA, 01003, USA.

Stephanie Long (S)

USDA Forest Service, Northern Research Station, Durham, NH, 03824, USA.

Rakesh Minocha (R)

USDA Forest Service, Northern Research Station, Durham, NH, 03824, USA.

Craig Musante (C)

Connecticut Agricultural Experiment Station, New Haven, CT, 06511, USA.

Jason C White (JC)

Connecticut Agricultural Experiment Station, New Haven, CT, 06511, USA.

Om Parkash Dhankher (OP)

Stockbridge School of Agriculture, University of Massachusetts, Amherst, MA, 01003, USA. parkash@umass.edu.

Articles similaires

Amaryllidaceae Alkaloids Lycoris NADPH-Ferrihemoprotein Reductase Gene Expression Regulation, Plant Plant Proteins
Drought Resistance Gene Expression Profiling Gene Expression Regulation, Plant Gossypium Multigene Family
Nigeria Environmental Monitoring Solid Waste Waste Disposal Facilities Refuse Disposal
Triticum Transcription Factors Gene Expression Regulation, Plant Plant Proteins Salt Stress

Classifications MeSH