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Identification and characterization of eight metallothionein genes involved in heavy metal tolerance from the ectomycorrhizal fungus Laccaria bicolor

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Abstract

Metallothioneins (MTs) are small, cysteine-rich, heavy metal-binding proteins involved in metal homeostasis and detoxification. The increasing numbers of available genomic sequences of ectomycorrhizal (ECM) fungi enable deeper insights into the characteristics of MT genes in these fungi that form the most important symbiosis with the host trees in forest ecosystems. The aim of this study was to establish a comprehensive, genome-wide inventory of MT genes from the ECM fungus Laccaria bicolor. Eight MT genes in L. bicolor were cloned, and the expression patterns of their transcripts at various developmental stages based on expressed sequence tag (EST) counts were analyzed. The expression levels of four MTs were significantly increased during symbiosis stages. Quantitative real-time PCR (qRT-PCR) analysis revealed that transcripts of LbMT1 were dominant in free-living mycelia and strongly induced by excessive copper (Cu), cadmium (Cd), and hydrogen peroxide (H2O2). To determine whether these eight MTs functioned as metal chelators, we expressed them in the Cu- and Cd-sensitive yeast mutants, cup1∆ and yap1∆, respectively. All LbMT proteins provided similar levels of Cu(II) or Cd(II) tolerance, but did not affect by H2O2. Our findings provide novel data on the evolution and diversification of fungal MT gene duplicates, a valuable resource for understanding the vast array of biological processes in which these proteins are involved.

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Acknowledgments

We thank Prof. F. Martin (INRA, France) and Prof. A. G. Pardo (University of Quilmes, Argentina) for providing the fungus material Laccaria bicolor S238N. We thank Prof. Dennis J. Thiele (Duke University, USA) for the gift of yeast strains DTY3 and DTY4 and Prof. Shusuke Kuge (Tohoku Pharmaceutical University, Japan) for strains W303B and WYU. We thank Prof. Z. H. Ren (Shandong Agricultural University, China) for the gift of the vector P424-GPD.

Funding

This study was supported by the National Natural Science Foundation of China (31901180; 31800525; 41571307); the China Agriculture Research System of MOF and MARA (CARS-10-B24, CARS-23-A03); China Postdoctoral Science Foundation (2019M651845); and Special Fund Project of Fundamental Scientific Research Funds for Central Universities of Nanjing Agricultural University (KYQN202061).

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  1. College of Life Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Binhao Liu, Pengcheng Dong, Xinzhe Zhang, Zhihang Feng, Liang Shi, Yan Xia, Chen Chen, Zhenguo Shen & Yahua Chen

  2. Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource, Nanjing Agricultural University, Nanjing, 210095, China

    Liang Shi, Zhenguo Shen & Yahua Chen

  3. Jiangsu Coastal Area Institute of Agricultural Sciences, Yancheng, 224002, Jiangsu, China

    Zhugui Wen

  4. Asian Natural Environmental Science Center, The University of Tokyo, 1-1-8 Midoricho, Nishitokyo, Tokyo, 188-0002, Japan

    Chunlan Lian & Yahua Chen

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  1. Binhao Liu
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Contributions

Binhao Liu, Pengcheng Dong, and Zhihang Feng involved in cloning of MTs in L. bicolor, organ-specific expression count and promoter analysis, sequence alignment and phylogenetic analysis, real-time quantitative PCR of L. bicolor MT genes, and yeast complementation assay. Xinzhe Zhang tested the heavy metal tolerance of L. bicolor. Binhao Liu, Pengcheng Dong, Yan Xia, and Zhenguo Shen were four major contributors in writing the manuscript. Liang Shi, Chen Chen, Zhugui Wen, Chunlan Lian, and Yahua Chen provided experimental programs and ideas. All authors read and approved the final manuscript.

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Correspondence to Yahua Chen.

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Liu, B., Dong, P., Zhang, X. et al. Identification and characterization of eight metallothionein genes involved in heavy metal tolerance from the ectomycorrhizal fungus Laccaria bicolor. Environ Sci Pollut Res 29, 14430–14442 (2022). https://doi.org/10.1007/s11356-021-16776-0

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