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ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley.
Front Plant Sci 2019; 10:1299FP

Abstract

Ataxia Telangiectasia and Rad-3-related protein (ATR) is a DNA damage signaling kinase required for the monitoring of DNA integrity. Together with ATM and SOG1, it is a key player in the transcriptional regulation of DNA damage response (DDR) genes in plants. In this study, we describe the role of ATR in the DDR pathway in barley and the function of the HvATR gene in response to DNA damages induced by aluminum toxicity. Aluminum is the third most abundant element in the Earth's crust. It becomes highly phytotoxic in acidic soils, which comprise more than 50% of arable lands worldwide. At low pH, Al is known to be a genotoxic agent causing DNA damage and cell cycle arrest. We present barley mutants, hvatr.g and hvatr.i, developed by TILLING strategy. The hvatr.g mutant carries a G6054A missense mutation in the ATR gene, leading to the substitution of a highly conserved amino acid in the protein (G1015S). The hvatr.g mutant showed the impaired DDR pathway. It accumulated DNA damages in the nuclei of root meristem cells when grown in control conditions. Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (TUNEL) analysis revealed that 60% of mutant nuclei possessed DNA nicks and breaks, whereas in the wild type only 2% of the nuclei were TUNEL-positive. The high frequency of DNA damages did not lead to the inhibition of the cell cycle progression, but the mutant showed an increased number of cells in the G2/M phase. In response to treatments with different Al doses, hvatr.g showed a high level of tolerance. The retention of root growth, which is the most evident symptom of Al toxicity, was not observed in the mutant, as it was in its parent variety. Furthermore, Al treatment increased the level of DNA damages, but did not affect the mitotic activity and the cell cycle profile in the hvatr.g mutant. A similar phenotype was observed for the hvatr.i mutant, carrying another missense mutation leading to G903E substitution in the HvATR protein. Our results demonstrate that the impaired mechanism of DNA damage response may lead to aluminum tolerance. They shed a new light on the role of the ATR-dependent DDR pathway in an agronomically important species.

Authors+Show Affiliations

Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.Department of Plant Anatomy and Cytology, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.Department of Genetics, Faculty of Biology and Environmental Protection, University of Silesia in Katowice, Katowice, Poland.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31695712

Citation

Szurman-Zubrzycka, Miriam, et al. "ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley." Frontiers in Plant Science, vol. 10, 2019, p. 1299.
Szurman-Zubrzycka M, Nawrot M, Jelonek J, et al. ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley. Front Plant Sci. 2019;10:1299.
Szurman-Zubrzycka, M., Nawrot, M., Jelonek, J., Dziekanowski, M., Kwasniewska, J., & Szarejko, I. (2019). ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley. Frontiers in Plant Science, 10, p. 1299. doi:10.3389/fpls.2019.01299.
Szurman-Zubrzycka M, et al. ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley. Front Plant Sci. 2019;10:1299. PubMed PMID: 31695712.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - ATR, a DNA Damage Signaling Kinase, Is Involved in Aluminum Response in Barley. AU - Szurman-Zubrzycka,Miriam, AU - Nawrot,Malgorzata, AU - Jelonek,Janusz, AU - Dziekanowski,Mariusz, AU - Kwasniewska,Jolanta, AU - Szarejko,Iwona, Y1 - 2019/10/22/ PY - 2019/04/12/received PY - 2019/09/18/accepted PY - 2019/11/8/entrez PY - 2019/11/7/pubmed PY - 2019/11/7/medline KW - ATR KW - DDR pathway KW - TILLING KW - aluminum KW - barley SP - 1299 EP - 1299 JF - Frontiers in plant science JO - Front Plant Sci VL - 10 N2 - Ataxia Telangiectasia and Rad-3-related protein (ATR) is a DNA damage signaling kinase required for the monitoring of DNA integrity. Together with ATM and SOG1, it is a key player in the transcriptional regulation of DNA damage response (DDR) genes in plants. In this study, we describe the role of ATR in the DDR pathway in barley and the function of the HvATR gene in response to DNA damages induced by aluminum toxicity. Aluminum is the third most abundant element in the Earth's crust. It becomes highly phytotoxic in acidic soils, which comprise more than 50% of arable lands worldwide. At low pH, Al is known to be a genotoxic agent causing DNA damage and cell cycle arrest. We present barley mutants, hvatr.g and hvatr.i, developed by TILLING strategy. The hvatr.g mutant carries a G6054A missense mutation in the ATR gene, leading to the substitution of a highly conserved amino acid in the protein (G1015S). The hvatr.g mutant showed the impaired DDR pathway. It accumulated DNA damages in the nuclei of root meristem cells when grown in control conditions. Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling (TUNEL) analysis revealed that 60% of mutant nuclei possessed DNA nicks and breaks, whereas in the wild type only 2% of the nuclei were TUNEL-positive. The high frequency of DNA damages did not lead to the inhibition of the cell cycle progression, but the mutant showed an increased number of cells in the G2/M phase. In response to treatments with different Al doses, hvatr.g showed a high level of tolerance. The retention of root growth, which is the most evident symptom of Al toxicity, was not observed in the mutant, as it was in its parent variety. Furthermore, Al treatment increased the level of DNA damages, but did not affect the mitotic activity and the cell cycle profile in the hvatr.g mutant. A similar phenotype was observed for the hvatr.i mutant, carrying another missense mutation leading to G903E substitution in the HvATR protein. Our results demonstrate that the impaired mechanism of DNA damage response may lead to aluminum tolerance. They shed a new light on the role of the ATR-dependent DDR pathway in an agronomically important species. SN - 1664-462X UR - https://www.unboundmedicine.com/medline/citation/31695712/ATR,_a_DNA_Damage_Signaling_Kinase,_Is_Involved_in_Aluminum_Response_in_Barley L2 - https://doi.org/10.3389/fpls.2019.01299 DB - PRIME DP - Unbound Medicine ER -