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A genome-wide co-expression network analysis revealed ZmNRAMP6-mediated regulatory pathway involved in maize tolerance to lead stress

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Abstract

Key message

A metal transporter ZmNRAMP6 was identified by using a trait-associated co-expression network analysis at a genome-wide level. ZmNRAMP6 confers maize sensitivity to Pb by accumulating it to maize shoots. ZmNRAMP6 knockout detains Pb in roots, activates antioxidant enzymes, and improves Pb tolerance.

Abstract

Lead (Pb) is one of the most toxic heavy metal pollutants, which can penetrate plant cells via root absorption and thus cause irreversible damages to the human body through the food chain. To identify the key gene responsible for Pb tolerance in maize, we performed a trait-associated co-expression network analysis at a genome-wide level, using two maize lines with contrasting Pb tolerances. Finally, ZmNRAMP6 that encodes a metal transporter was identified as the key gene among the Pb tolerance-associated co-expression module. Heterologous expression of ZmNRAMP6 in yeast verified its role in Pb transport. Combined Arabidopsis overexpression and maize mutant analysis suggested that ZmNRAMP6 conferred plant sensitivity to Pb stress by mediating Pb distribution across the roots and shoots. Knockout of ZmNRAMP6 caused Pb retention in the roots and activation of the antioxidant enzyme system, resulting in an increased Pb tolerance in maize. ZmNRAMP6 was likely to transport Pb from the roots to shoots and environment. An integration of yeast one-hybrid and dual-luciferase reporter assay uncovered that ZmNRAMP6 was negatively regulated by a known Pb tolerance-related transcript factor ZmbZIP54. Collectively, knockout of ZmNRAMP6 will aid in the bioremediation of contaminated soil and food safety guarantee of forage and grain corn.

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Data availability

All raw data generated of 42 samples used in this study were deposited in Genome Sequence Archive (GSA) in National Genomics Data Center (NGDC) database with the accession number CRA004789.

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Acknowledgements

This work is supported by the National Key Research and Development Program of China (2021YFF1000300), the National Natural Science Foundation of China (32072073 and 32101777), and the Sichuan Science and Technology Program (2021JDTD0004 and 2021YJ0476).

Funding

This work is supported by the National Key Research and Development Program of China (2021YFF1000300), the National Natural Science Foundation of China (32072073 and 32101777), and the Sichuan Science and Technology Program (2021JDTD0004 and 2021YJ0476).

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Authors and Affiliations

Authors

Contributions

YS: conceived the project. YS, PL, and LM: supervised the study. LJ, PL, PL, QL, FH, ZC, MZ, and CZ: conducted the experiments. PL and LJ: analyzed the data. YS, PL, and LJ: wrote the manuscript with contributions from LM and GY. GP: provided the maize materials. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yaou Shen.

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Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationship that could be construed as a potential conflict of interest.

Human and animal rights

This study does not include human or animal subjects.

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Communicated by Ian D. Godwin.

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Liu, P., Jiang, L., Long, P. et al. A genome-wide co-expression network analysis revealed ZmNRAMP6-mediated regulatory pathway involved in maize tolerance to lead stress. Theor Appl Genet 136, 122 (2023). https://doi.org/10.1007/s00122-023-04371-5

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  • DOI: https://doi.org/10.1007/s00122-023-04371-5

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