The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize

The persistent nature of lead (Pb) and cadmium (Cd) in the environment severely affects plant growth and yield. Conversely, plants acquire zinc (Zn) from the soil for their vital physiological and biochemical functions. However, the interplay and coordination between essential and toxic metals for t...

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Main Authors: Sarfraz Shafiq, Asim Ali, Yasar Sajjad, Qudsia Zeb, Muhammad Shahzad, Abdul Rehman Khan, Rashid Nazir, Emilie Widemann
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/21/18/6959
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author Sarfraz Shafiq
Asim Ali
Yasar Sajjad
Qudsia Zeb
Muhammad Shahzad
Abdul Rehman Khan
Rashid Nazir
Emilie Widemann
author_facet Sarfraz Shafiq
Asim Ali
Yasar Sajjad
Qudsia Zeb
Muhammad Shahzad
Abdul Rehman Khan
Rashid Nazir
Emilie Widemann
author_sort Sarfraz Shafiq
collection DOAJ
description The persistent nature of lead (Pb) and cadmium (Cd) in the environment severely affects plant growth and yield. Conversely, plants acquire zinc (Zn) from the soil for their vital physiological and biochemical functions. However, the interplay and coordination between essential and toxic metals for their uptake and translocation and the putative underlying epigenetic mechanisms have not yet been investigated in maize. Here, we report that the presence of Zn facilitates the accumulation and transport of Pb and Cd in the aerial parts of the maize plants. Moreover, the Zn, Pb, and Cd interplay specifically interferes with the uptake and translocation of other divalent metals, such as calcium and magnesium. Zn, Pb, and Cd, individually and in combinations, differentially regulate the expression of DNA methyltransferases, thus alter the DNA methylation levels at the promoter of <i>Zinc-regulated transporters, Iron-regulated transporter-like Protein</i> (<i>ZIP</i>) genes to regulate their expression. Furthermore, the expression of histone deacetylases (<i>HDACs</i>) varies greatly in response to individual and combined metals, and <i>HDACs</i> expression showed a negative correlation with <i>ZIP</i> transporters. Our study highlights the implication of DNA methylation and histone acetylation in regulating the metal stress tolerance dynamics through Zn transporters and warns against the excessive use of Zn fertilizers in metal contaminated soils.
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spelling doaj.art-fbb54760564c44e9916d930fa02eaec12023-11-20T14:40:21ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672020-09-012118695910.3390/ijms21186959The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in MaizeSarfraz Shafiq0Asim Ali1Yasar Sajjad2Qudsia Zeb3Muhammad Shahzad4Abdul Rehman Khan5Rashid Nazir6Emilie Widemann7Department of Anatomy and Cell Biology, University of Western Ontario, 1151 Richmond St, London, ON N6A5B8, CanadaDepartment of Biotechnology, COMSATS University Islamabad, Abbottabad Campus, University Road, Tobe Camp, Abbottabad 22060, PakistanDepartment of Biotechnology, COMSATS University Islamabad, Abbottabad Campus, University Road, Tobe Camp, Abbottabad 22060, PakistanDepartment of Environmental Sciences, COMSATS University Islamabad, Abbottabad Campus, University Road, tobe Camp, Abbottabad 22060, PakistanDepartment of Environmental Sciences, COMSATS University Islamabad, Abbottabad Campus, University Road, tobe Camp, Abbottabad 22060, PakistanDepartment of Biotechnology, COMSATS University Islamabad, Abbottabad Campus, University Road, Tobe Camp, Abbottabad 22060, PakistanDepartment of Environmental Sciences, COMSATS University Islamabad, Abbottabad Campus, University Road, tobe Camp, Abbottabad 22060, PakistanDepartment of Biology, University of Western Ontario, 1151 Richmond St, London, ON N6A5B8, CanadaThe persistent nature of lead (Pb) and cadmium (Cd) in the environment severely affects plant growth and yield. Conversely, plants acquire zinc (Zn) from the soil for their vital physiological and biochemical functions. However, the interplay and coordination between essential and toxic metals for their uptake and translocation and the putative underlying epigenetic mechanisms have not yet been investigated in maize. Here, we report that the presence of Zn facilitates the accumulation and transport of Pb and Cd in the aerial parts of the maize plants. Moreover, the Zn, Pb, and Cd interplay specifically interferes with the uptake and translocation of other divalent metals, such as calcium and magnesium. Zn, Pb, and Cd, individually and in combinations, differentially regulate the expression of DNA methyltransferases, thus alter the DNA methylation levels at the promoter of <i>Zinc-regulated transporters, Iron-regulated transporter-like Protein</i> (<i>ZIP</i>) genes to regulate their expression. Furthermore, the expression of histone deacetylases (<i>HDACs</i>) varies greatly in response to individual and combined metals, and <i>HDACs</i> expression showed a negative correlation with <i>ZIP</i> transporters. Our study highlights the implication of DNA methylation and histone acetylation in regulating the metal stress tolerance dynamics through Zn transporters and warns against the excessive use of Zn fertilizers in metal contaminated soils.https://www.mdpi.com/1422-0067/21/18/6959phytotoxcityheavy metals interplayZn transporters (<i>ZIP</i>)DNA methylationhistone deacetylasesmaize
spellingShingle Sarfraz Shafiq
Asim Ali
Yasar Sajjad
Qudsia Zeb
Muhammad Shahzad
Abdul Rehman Khan
Rashid Nazir
Emilie Widemann
The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
International Journal of Molecular Sciences
phytotoxcity
heavy metals interplay
Zn transporters (<i>ZIP</i>)
DNA methylation
histone deacetylases
maize
title The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
title_full The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
title_fullStr The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
title_full_unstemmed The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
title_short The Interplay between Toxic and Essential Metals for Their Uptake and Translocation Is Likely Governed by DNA Methylation and Histone Deacetylation in Maize
title_sort interplay between toxic and essential metals for their uptake and translocation is likely governed by dna methylation and histone deacetylation in maize
topic phytotoxcity
heavy metals interplay
Zn transporters (<i>ZIP</i>)
DNA methylation
histone deacetylases
maize
url https://www.mdpi.com/1422-0067/21/18/6959
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