NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.)
Tobacco plants (Nicotiana tabacum L.) exhibit considerable potential for phytoremediation of soil cadmium (Cd) pollutants, owing to their substantial biomass and efficient metal accumulation capabilities. The reduction of Cd accumulation in tobacco holds promise for minimizing Cd intake in individua...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2024-02-01
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| Series: | Ecotoxicology and Environmental Safety |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651323013891 |
| _version_ | 1797328860597977088 |
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| author | Xueao Zheng Jiarui Jiang Chen Wang Yingpeng Hua Haitao Huang Yalong Xu Pan Wei Jiemeng Tao Peijian Cao Zhengzhong Kang Xuemei Li Qian Gao Qiansi Chen |
| author_facet | Xueao Zheng Jiarui Jiang Chen Wang Yingpeng Hua Haitao Huang Yalong Xu Pan Wei Jiemeng Tao Peijian Cao Zhengzhong Kang Xuemei Li Qian Gao Qiansi Chen |
| author_sort | Xueao Zheng |
| collection | DOAJ |
| description | Tobacco plants (Nicotiana tabacum L.) exhibit considerable potential for phytoremediation of soil cadmium (Cd) pollutants, owing to their substantial biomass and efficient metal accumulation capabilities. The reduction of Cd accumulation in tobacco holds promise for minimizing Cd intake in individuals exposed to cigar smoking. NRAMP transporters are pivotal in the processes of Cd accumulation and resistance in plants; however, limited research has explored the functions of NRAMPs in tobacco plants. In this investigation, we focused on NtNRAMP6c, one of the three homologs of NRAMP6 in tobacco. We observed a robust induction of NtNRAMP6c expression in response to both Cd toxicity and iron (Fe) deficiency, with the highest expression levels detected in the roots. Subsequent subcellular localization and heterologous expression analyses disclosed that NtNRAMP6c functions as a plasma membrane-localized Cd transporter. Moreover, its overexpression significantly heightened the sensitivity of yeast cells to Cd toxicity. Through CRISPR-Cas9-mediated knockout of NtNRAMP6c, we achieved a reduction in Cd accumulation and an enhancement in Cd resistance in tobacco plants. Comparative transcriptomic analysis unveiled substantial alterations in the transcriptional profiles of genes associated with metal ion transport, photosynthesis, and macromolecule catabolism upon NtNRAMP6c knockout. Furthermore, our study employed plant metabolomics and rhizosphere metagenomics to demonstrate that NtNRAMP6c knockout led to changes in phytohormone homeostasis, as well as shifts in the composition and abundance of microbial communities. These findings bear significant biological implications for the utilization of tobacco in phytoremediation strategies targeting Cd pollutants in contaminated soils, and concurrently, in mitigating Cd accumulation in tobacco production destined for cigar consumption. |
| first_indexed | 2024-03-08T06:57:02Z |
| format | Article |
| id | doaj.art-8f241cb96e8e435fbbacf9c28a455ab7 |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-03-08T06:57:02Z |
| publishDate | 2024-02-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-8f241cb96e8e435fbbacf9c28a455ab72024-02-03T06:34:21ZengElsevierEcotoxicology and Environmental Safety0147-65132024-02-01271115885NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.)Xueao Zheng0Jiarui Jiang1Chen Wang2Yingpeng Hua3Haitao Huang4Yalong Xu5Pan Wei6Jiemeng Tao7Peijian Cao8Zhengzhong Kang9Xuemei Li10Qian Gao11Qiansi Chen12Zhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaTechnology Center, China Tobacco Yunnan Industrial Co. LTD, No. 181 Hongjin Road, Kunming, Yunnan Province 650000, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaSchool of Agricultural Sciences, Zhengzhou University, Zhengzhou 450001, ChinaTechnology Center, China Tobacco Yunnan Industrial Co. LTD, No. 181 Hongjin Road, Kunming, Yunnan Province 650000, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaZhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, ChinaTechnology Center, China Tobacco Yunnan Industrial Co. LTD, No. 181 Hongjin Road, Kunming, Yunnan Province 650000, ChinaTechnology Center, China Tobacco Yunnan Industrial Co. LTD, No. 181 Hongjin Road, Kunming, Yunnan Province 650000, China; Corresponding author.Zhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China; Beijing Life Science Academy (BLSA), Beijing 102209, China; Corresponding author at: Zhengzhou Tobacco Research Institute of CNTC, No. 2 Fengyang Street, Zhengzhou, Henan Province 450001, China.Tobacco plants (Nicotiana tabacum L.) exhibit considerable potential for phytoremediation of soil cadmium (Cd) pollutants, owing to their substantial biomass and efficient metal accumulation capabilities. The reduction of Cd accumulation in tobacco holds promise for minimizing Cd intake in individuals exposed to cigar smoking. NRAMP transporters are pivotal in the processes of Cd accumulation and resistance in plants; however, limited research has explored the functions of NRAMPs in tobacco plants. In this investigation, we focused on NtNRAMP6c, one of the three homologs of NRAMP6 in tobacco. We observed a robust induction of NtNRAMP6c expression in response to both Cd toxicity and iron (Fe) deficiency, with the highest expression levels detected in the roots. Subsequent subcellular localization and heterologous expression analyses disclosed that NtNRAMP6c functions as a plasma membrane-localized Cd transporter. Moreover, its overexpression significantly heightened the sensitivity of yeast cells to Cd toxicity. Through CRISPR-Cas9-mediated knockout of NtNRAMP6c, we achieved a reduction in Cd accumulation and an enhancement in Cd resistance in tobacco plants. Comparative transcriptomic analysis unveiled substantial alterations in the transcriptional profiles of genes associated with metal ion transport, photosynthesis, and macromolecule catabolism upon NtNRAMP6c knockout. Furthermore, our study employed plant metabolomics and rhizosphere metagenomics to demonstrate that NtNRAMP6c knockout led to changes in phytohormone homeostasis, as well as shifts in the composition and abundance of microbial communities. These findings bear significant biological implications for the utilization of tobacco in phytoremediation strategies targeting Cd pollutants in contaminated soils, and concurrently, in mitigating Cd accumulation in tobacco production destined for cigar consumption.http://www.sciencedirect.com/science/article/pii/S0147651323013891CadmiumKnockoutMultiomicsNRAMP6Tobacco |
| spellingShingle | Xueao Zheng Jiarui Jiang Chen Wang Yingpeng Hua Haitao Huang Yalong Xu Pan Wei Jiemeng Tao Peijian Cao Zhengzhong Kang Xuemei Li Qian Gao Qiansi Chen NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) Ecotoxicology and Environmental Safety Cadmium Knockout Multiomics NRAMP6 Tobacco |
| title | NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) |
| title_full | NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) |
| title_fullStr | NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) |
| title_full_unstemmed | NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) |
| title_short | NRAMP6c plays a key role in plant cadmium accumulation and resistance in tobacco (Nicotiana tabacum L.) |
| title_sort | nramp6c plays a key role in plant cadmium accumulation and resistance in tobacco nicotiana tabacum l |
| topic | Cadmium Knockout Multiomics NRAMP6 Tobacco |
| url | http://www.sciencedirect.com/science/article/pii/S0147651323013891 |
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