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Overexpression of gamma-glutamyl cyclotransferase 2;1 (CsGGCT2;1) reduces arsenic toxicity and accumulation in Camelina sativa (L.)

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Abstract

Key message

Overexpressing CsGGCT2;1 in Camelina enhances arsenic tolerance, reducing arsenic accumulation by 40–60%. Genetically modified Camelina can potentially thrive on contaminated lands and help safeguard food quality and sustainable food and biofuel production.

Abstract

Environmental arsenic contamination is a serious global issue that adversely affects human health and diminishes the quality of harvested produce. Glutathione (GSH) is known to bind and detoxify arsenic and other toxic metals. A steady level of GSH is maintained within cells via the γ-glutamyl cycle. The γ-glutamyl cyclotransferases (GGCTs) have previously been shown to be involved in GSH degradation and increased tolerance to toxic metals in plants. In this study, we characterized the GGCT2;1 homolog from Camelina sativa for its role in arsenic tolerance and accumulation. Overexpression of CsGGCT2;1 in Camelina under CaMV35S constitutive promoter resulted in strong tolerance to arsenite (AsIII). The overexpression (OE) lines had 2.6–3.5-fold higher shoots and sevenfold to tenfold enhanced root biomass on media supplemented with AsIII, relative to wild-type plants. The CsGGCT2;1 OE lines accumulated 40–60% less arsenic in root and shoot tissues compared to wild-type plants. Further, the OE lines had ~ twofold higher chlorophyll content and 35% lesser levels of malondialdehyde (MDA), an indicator of membrane damage via lipid peroxidation. There was a slight but non-significant increase in 5-oxoproline (5-OP), a product of GSH degradation, in OE lines. However, the transcript levels of Oxoprolinase 1 (OXP1) were upregulated, indicating the accelerated conversion of 5-OP to glutamate, which is further utilized for the resynthesis of GSH to maintain GSH homeostasis. Overall, this research suggests that genetically modified Camelina may have the potential for cultivation on contaminated marginal lands to reduce As accumulation; thereby could help in addressing food safety issues as well as future food and biofuel needs.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Ian Eggleston for helping with the ICP-MS analysis and Dr. Steve Eyles at the University of Massachusetts Mass Spectrometry Core Facility (RRID:SCR_019063) for providing technical expertise for analyzing 5-OP.

Funding

Financial support from the Lotta M. Crabtree fellowship to GS, partial funding support from the National Institute of Health and Environmental Sciences (Grant # R01ES032686) and USDA-NIFA Hatch project (MAS #578) to OPD, and funding from USDA Forest Service, NRS to RM are highly acknowledged.

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Authors and Affiliations

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

    Gurpal Singh, Helen Le, Kenny Ablordeppey & Om Parkash Dhankher

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

    Stephanie Long & Rakesh Minocha

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  1. Gurpal Singh
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  2. Helen Le
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  3. Kenny Ablordeppey
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Contributions

OPD, GS, and KA conceived and designed the study. GS, HL, and KA conducted experiments and collected and analyzed the data. SL and RM helped with HPLC analysis of thiols and amino acids. GS and OPD wrote and revised the manuscript. All authors helped revise the manuscript and provided valuable critical comments.

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Correspondence to Om Parkash Dhankher.

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Communicated by Prakash P. Kumar.

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Singh, G., Le, H., Ablordeppey, K. et al. Overexpression of gamma-glutamyl cyclotransferase 2;1 (CsGGCT2;1) reduces arsenic toxicity and accumulation in Camelina sativa (L.). Plant Cell Rep 43, 14 (2024). https://doi.org/10.1007/s00299-023-03091-w

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