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Front. Plant Sci. | doi: 10.3389/fpls.2018.00270

AtHMA4 drives natural variation in leaf Zn concentration of Arabidopsis thaliana

 Dai-Yin Chao1*,  Zi-Ru Chen1, 2, Lu Kuang1, 3,  Yi-Qun Gao1, 2, Ya-Ling Wang1 and David E. Salt4*
  • 1National Key Laboratory of Plant Molecular Genetics (NKLPMG), CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology,, Shanghai Institutes for Biological Sciences (CAS), China
  • 2University of Chinese Academy of Sciences (UCAS), China
  • 3School of life science,, Jiangsu Normal University, China
  • 44Division of Plant and Crop Sciences, School of Biosciences, Department of Biosciences, University of Nottingham, United Kingdom

Zinc (Zn) is an essential element for plant growth and development, and Zn derived from crop plants in the diet is also important for human health. Here, we report that genetic variation in Heavy Metal-ATPase 4 (HMA4) controls natural variation in leaf Zn content. Investigation of the natural variation in leaf Zn content in a world-wide collection of 349 Arabidopsis thaliana wild collected accessions identified two accessions, Van-0 and Fab-2, which accumulate significantly lower Zn when compared with Col-0. Both quantitative trait loci (QTL) analysis and bulked segregant analysis (BSA) identified HMA4 as a strong candidate accounting for this variation in leaf Zn concentration. Genetic complementation experiments confirmed this hypothesis. Sequence analysis revealed that a 1-bp deletion in the third exon of HMA4 from Fab-2 is responsible for the lose-of-function of HMA4 driving the low Zn observed in Fab-2. Unlike in Fab-2 polymorphisms in the promoter region were found to be responsible for the weak function of HMA4 in Van-0. This is supported by both an expression analysis of HMA4 in Van-0 and through a series of T-DNA insertion mutants which generate truncated HMA4 promoters in the Col-0 background. In addition, we also observed that Fab-2, Van-0 and the hma4-2 null mutant in the Col-0 background show enhanced resistance to a combination of high Zn and high Cd in the growth medium, raising the possibility that variation at HMA4 may play a role in environmental adaptation.

Keywords: Arabidopsis thaliana, BSA, Cadmium, Heavy Metal ATPase 4, natural variation, QTL, Zinc

Received: 30 Nov 2017; Accepted: 15 Feb 2018.

Edited by:

Hatem ROUACHED, Institut National de la Recherche Agronomique (INRA), France

Reviewed by:

Marc Hanikenne, University of Liège, Belgium
Fernando Aleman, The Scripps Research Institute, United States  

Copyright: © 2018 Chao, Chen, Kuang, Gao, Wang and Salt. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Prof. Dai-Yin Chao, Shanghai Institutes for Biological Sciences (CAS), National Key Laboratory of Plant Molecular Genetics (NKLPMG), CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology,, Shanghai, 200032, Shanghai, China, dychao@sibs.ac.cn
Prof. David E. Salt, Department of Biosciences, University of Nottingham, 4Division of Plant and Crop Sciences, School of Biosciences, Loughborough, United Kingdom, David.Salt@nottingham.ac.uk