Abstract
Arabis paniculata has been reported as a hyperaccumulator and functions in cadmium (Cd) tolerance and accumulation. However, the genes involved in Cd stress resistance in A. paniculata are still unknown. In this work, genes of the natural resistance-associated macrophage proteins (NRAMPs) were characterized in A. paniculata, and their evolutionary relationship and expression patterns were analysed. Expression profiles indicated that ApNRAMPs showed large differences in response to Cd stress. It was highly induced by Cd in root and shoot tissues. To investigate the function of ApNRAMP4 under Cd stress, ApNRAMP4 was cloned and expressed in yeast and Arabidopsis. The results indicated that yeast and Arabidopsis expressing ApNRAMP4 showed normal growth under Cd stress. In addition, transgenic yeast and Arabidopsis showed the ability to concentrate Cd. Under 20 μM CdCl2, Cd concentrations in wild type (WT) and transgenic yeast were 3.11 and 5.92 mg/kg, respectively. Cd concentrations in root tissues of WT and transgenic Arabidopsis were 0.18 and 0.54 mg/kg, respectively. In shoot tissues of WT and transgenic Arabidopsis, Cd concentrations were 0.13 and 0.49 mg/kg, respectively. This report provides genomic information on hyperaccumulator A. paniculata. In addition, the present work identified key NRAMP genes that may serve as resources for heavy metal phytoremediation.
References
Alejandro S., Cailliatte R., Alcon C., Dirick L., Domergue F., Correia D. et al. 2017 Intracellular distribution of manganese by the trans-Golgi network transporter NRAMP2 is critical for photosynthesis and cellular redox homeostasis. Plant Cell 29, 3068–3084.
Cailliatte R., Schikora A., Briat J. F., Mari S. and Curie C. 2010 High-affinity manganese uptake by the metal transporter NRAMP1 is essential for Arabidopsis growth in low manganese conditions. Plant Cell 22, 904–917.
Dias M. C., Monteiro C., Moutinho-Pereira J., Correia C., Gonçalves B. and Santos C. 2013 Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiol. Plant. 35, 1281–1289.
Ehsan S., Ali S., Noureen S., Mahmood K., Farid M., Ishaque W. et al. 2014 Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxcol. Environ. Safe. 106, 164–172.
Hou W. Q., Feng W., Yu G. H., Du X. Y. and Ren M. J. 2017 Cloning and functional analysis of a novel x-type high-molecular-weight glutenin subunit with altered cysteine residues from Aegilops umbellulata. Crop Pasture Sci. 68, 409–414.
Khan A., Khan S., Alam M., Khan M. A., Aamir M., Qamar Z. et al. 2016 Toxic metal interactions affect the bioaccumulation and dietary intake of macro- and micro-nutrients. Chemosphere 146, 121–128.
Livak J. and Schmitten T. D. 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25, 402–408.
Lanquar V., Ramos M. S., Lelievre F., Barbier-Brygoo H., Krieger-Liszkay A., Kramer U. et al. 2010 Export of vacuolar manganese by AtNRAMP3 and AtNRAMP4 is required for optimal photosynthesis and growth under manganese deficiency. Plant Physiol. 152, 1986–1999.
Maser P., Thomine S., Schroeder J. I., Ward J. M., Hirschi K., Sze H., Talke I. N. et al. 2001 Phylogenetic relationships within cation transporter families of Arabidopsis. Plant Physiol. 126, 1646–1667.
Meena M., Aamir M., Kumar V., Swapnil P. and Upadhyay R. S. 2018 Evaluation of morpho-physiological growth parameters of tomato in response to Cd induced toxicity and characterization of metal sensitive NRAMP3 transporter protein. Environ. Exp. Bot. 148, 144–167.
Oono Y., Yazawa T., Kanamori H., Sasaki H., Mori S., Handa H. et al. 2016 Genome-wide transcriptome analysis of cadmium stress in rice. Biomed. Res. Int. 9739505.
Peng F., Wang C., Zhu J. S., Zeng J., Kang H. Y., Fan X. et al. 2018 Expression of TpNRAMP5, a metal transporter from Polish wheat (Triticum polonicum L.), enhances the accumulation of Cd, Co and Mn in transgenic Arabidopsis plants. Planta 247, 1395–1406.
Schutzendubel A., Schwanz P., Teichmann T., Gross K., Langenfeld-Heyser R., Godbold D. L. et al. 2001 Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol. 127, 887–898.
Takahashi R., Ishimaru Y., Senoura T., Shimo H., Ishikawa S., Arao T. et al. 2011 The OsNRAMP1 iron transporter is involved in Cd accumulation in rice. J. Exp. Bot. 62, 4843–4850.
Tang T., Liu P. L., Zheng G. W. and Li W. Q. 2016 Two phases of response to long-term moderate heat: variation in thermotolerance between Arabidopsis thaliana and its relative Arabis paniculata. Phytochem. 122, 81–90.
Tang Y. T., Qiu R. L., Zeng X. W., Yi R. R., Yu F. M. and Zhou X. Y. 2009 Lead, zinc, cadmium hyperaccumulation and growth stimulation in Arabis paniculata Franch. Environ. Exp. Bot. 66, 126–134.
Wang C., Chen X., Yao Q., Long D., Fan X., Kang H. Y. et al. 2019 Overexpression of TtNRAMP6 enhances the accumulation of Cd in Arabidopsis. Gene 696, 225–232.
Xia J., Yamaji N., Kasai T. and Ma J. F. 2010 Plasma membrane localized transporter for aluminum in rice. Proc. Natl. Acad. Sci. USA 107, 18381–18385.
Zhao X. Y., Qi C. H., Jiang H., Zhong M. S., You C. X., Li Y. Y. et al. 2019 MdHIR4 transcription and translation levels associated with disease in apple are regulated by MdWRKY31. Plant Mol. Biol. 101, 149–162.
Zhang J., Zhang M., Song H. Y., Zhao J. Q., Shabala S., Tian S. K. et al. 2020 A novel plasma membrane-based NRAMP transporter contributes to Cd an Zn hyperaccumulation in Sedum alfredii Hance. Environ. Exp. Bot. 176, 104121.
Acknowledgements
This work was supported by Guizhou Normal University (2018-5769-16) and Open Project of Key Laboratory of Biology and Genetic Improvement of Oil Crops, Ministry of Agriculture and Rural Affairs, China (KF2019005). We thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Corresponding editor: Manoj Prasad
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhu, B., Gan, C., Gu, L. et al. Identification of NRAMP4 from Arabis paniculata enhance cadmium tolerance in transgenic Arabidopsis. J Genet 100, 89 (2021). https://doi.org/10.1007/s12041-021-01339-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12041-021-01339-6