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Volume 25
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10.3390/ijms25179367
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Article

Disruption of Poly(ADP-ribosyl)ation Improves Plant Tolerance to Methyl Viologen-Mediated Oxidative Stress via Induction of ROS Scavenging Enzymes

by
Natalia O. Kalinina
1,2,*,
Nadezhda Spechenkova
1,
Irina Ilina
1,
Viktoriya O. Samarskaya
1,
Polina Bagdasarova
1,
Sergey K. Zavriev
1,
Andrew J. Love
3 and
Michael Taliansky
1,3
1
Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry of the Russian Academy of Sciences, Moscow 117997, Russia
2
Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, Moscow 119234, Russia
3
The James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(17), 9367; https://doi.org/10.3390/ijms25179367
Submission received: 18 July 2024 / Revised: 27 August 2024 / Accepted: 27 August 2024 / Published: 29 August 2024
(This article belongs to the Special Issue Regulatory Mechanism and Network of Abiotic Stress-Response in Plants 2.0)
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Abstract

ADP-ribosylation (ADPRylation) is a mechanism which post-translationally modifies proteins in eukaryotes in order to regulate a broad range of biological processes including programmed cell death, cell signaling, DNA repair, and responses to biotic and abiotic stresses. Poly(ADP-ribosyl) polymerases (PARPs) play a key role in the process of ADPRylation, which modifies target proteins by attaching ADP-ribose molecules. Here, we investigated whether and how PARP1 and PARylation modulate responses of Nicotiana benthamiana plants to methyl viologen (MV)-induced oxidative stress. It was found that the burst of reactive oxygen species (ROS), cell death, and loss of tissue viability invoked by MV in N. benthamiana leaves was significantly delayed by both the RNA silencing of the PARP1 gene and by applying the pharmacological inhibitor 3-aminobenzamide (3AB) to inhibit PARylation activity. This in turn reduced the accumulation of PARylated proteins and significantly increased the gene expression of major ROS scavenging enzymes including SOD (NbMnSOD; mitochondrial manganese SOD), CAT (NbCAT2), GR (NbGR), and APX (NbAPX5), and inhibited cell death. This mechanism may be part of a broader network that regulates plant sensitivity to oxidative stress through various genetically programmed pathways.
Keywords: poly(ADP-ribosyl)ation; poly(ADP-ribosyl) polymerase 1; oxidative stress; methyl viologen; salicylic acid poly(ADP-ribosyl)ation; poly(ADP-ribosyl) polymerase 1; oxidative stress; methyl viologen; salicylic acid

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MDPI and ACS Style

Kalinina, N.O.; Spechenkova, N.; Ilina, I.; Samarskaya, V.O.; Bagdasarova, P.; Zavriev, S.K.; Love, A.J.; Taliansky, M. Disruption of Poly(ADP-ribosyl)ation Improves Plant Tolerance to Methyl Viologen-Mediated Oxidative Stress via Induction of ROS Scavenging Enzymes. Int. J. Mol. Sci. 2024, 25, 9367. https://doi.org/10.3390/ijms25179367

AMA Style

Kalinina NO, Spechenkova N, Ilina I, Samarskaya VO, Bagdasarova P, Zavriev SK, Love AJ, Taliansky M. Disruption of Poly(ADP-ribosyl)ation Improves Plant Tolerance to Methyl Viologen-Mediated Oxidative Stress via Induction of ROS Scavenging Enzymes. International Journal of Molecular Sciences. 2024; 25(17):9367. https://doi.org/10.3390/ijms25179367

Chicago/Turabian Style

Kalinina, Natalia O., Nadezhda Spechenkova, Irina Ilina, Viktoriya O. Samarskaya, Polina Bagdasarova, Sergey K. Zavriev, Andrew J. Love, and Michael Taliansky. 2024. "Disruption of Poly(ADP-ribosyl)ation Improves Plant Tolerance to Methyl Viologen-Mediated Oxidative Stress via Induction of ROS Scavenging Enzymes" International Journal of Molecular Sciences 25, no. 17: 9367. https://doi.org/10.3390/ijms25179367

APA Style

Kalinina, N. O., Spechenkova, N., Ilina, I., Samarskaya, V. O., Bagdasarova, P., Zavriev, S. K., Love, A. J., & Taliansky, M. (2024). Disruption of Poly(ADP-ribosyl)ation Improves Plant Tolerance to Methyl Viologen-Mediated Oxidative Stress via Induction of ROS Scavenging Enzymes. International Journal of Molecular Sciences, 25(17), 9367. https://doi.org/10.3390/ijms25179367

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