A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana
Abstract
Pharmacological inhibition of poly(ADP-ribose) polymerase (PARP) or loss of Arabidopsis thaliana PARG1 (poly(ADP-ribose) glycohydrolase) disrupt a subset of plant defenses. In the present study we examined the impact of altered poly(ADP-ribosyl)ation on early gene expression induced by the microbe-associate molecular patterns (MAMPs) flagellin (flg22) and EF-Tu (elf18). Stringent statistical analyses and filtering identified 178 genes having MAMP-induced mRNA abundance patterns that were altered by either PARP inhibitor 3-aminobenzamide (3AB) or PARG1 knockout. From the identified set of 178 genes, over fifty Arabidopsis T-DNA insertion lines were chosen and screened for altered basal defense responses. Subtle alterations in callose deposition and/or seedling growth in response to those MAMPs were observed in knockouts of At3g55630 (FPGS3, a cytosolic folylpolyglutamate synthetase), At5g15660 (containing an F-box domain), At1g47370 (a TIR-X (Toll-Interleukin Receptor domain)), and At5g64060 (a predicted pectin methylesterase inhibitor). Over-represented GO terms for the gene expression study included "innate immune response" for elf18/parg1, highlighting a subset of elf18-activated defense-associated genes whose expression is altered in parg1 plants. The study also allowed a tightly controlled comparison of early mRNA abundance responses to flg22 and elf18 in wild-type Arabidopsis, which revealed many differences. The PARP inhibitor 3-methoxybenzamide (3MB) was also used in the gene expressionmore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1415065
- Alternate Identifier(s):
- OSTI ID: 1499890
- Grant/Contract Number:
- FG02-02ER15342
- Resource Type:
- Published Article
- Journal Name:
- PLoS ONE
- Additional Journal Information:
- Journal Name: PLoS ONE Journal Volume: 12 Journal Issue: 12; Journal ID: ISSN 1932-6203
- Publisher:
- Public Library of Science
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Briggs, Amy G., Adams-Phillips, Lori C., Keppler, Brian D., Zebell, Sophia G., Arend, Kyle C., Apfelbaum, April A., Smith, Joshua A., Bent, Andrew F., and Davis, ed., Keith R. A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana. United States: N. p., 2017.
Web. doi:10.1371/journal.pone.0190268.
Briggs, Amy G., Adams-Phillips, Lori C., Keppler, Brian D., Zebell, Sophia G., Arend, Kyle C., Apfelbaum, April A., Smith, Joshua A., Bent, Andrew F., & Davis, ed., Keith R. A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana. United States. https://doi.org/10.1371/journal.pone.0190268
Briggs, Amy G., Adams-Phillips, Lori C., Keppler, Brian D., Zebell, Sophia G., Arend, Kyle C., Apfelbaum, April A., Smith, Joshua A., Bent, Andrew F., and Davis, ed., Keith R. Thu .
"A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana". United States. https://doi.org/10.1371/journal.pone.0190268.
@article{osti_1415065,
title = {A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana},
author = {Briggs, Amy G. and Adams-Phillips, Lori C. and Keppler, Brian D. and Zebell, Sophia G. and Arend, Kyle C. and Apfelbaum, April A. and Smith, Joshua A. and Bent, Andrew F. and Davis, ed., Keith R.},
abstractNote = {Pharmacological inhibition of poly(ADP-ribose) polymerase (PARP) or loss of Arabidopsis thaliana PARG1 (poly(ADP-ribose) glycohydrolase) disrupt a subset of plant defenses. In the present study we examined the impact of altered poly(ADP-ribosyl)ation on early gene expression induced by the microbe-associate molecular patterns (MAMPs) flagellin (flg22) and EF-Tu (elf18). Stringent statistical analyses and filtering identified 178 genes having MAMP-induced mRNA abundance patterns that were altered by either PARP inhibitor 3-aminobenzamide (3AB) or PARG1 knockout. From the identified set of 178 genes, over fifty Arabidopsis T-DNA insertion lines were chosen and screened for altered basal defense responses. Subtle alterations in callose deposition and/or seedling growth in response to those MAMPs were observed in knockouts of At3g55630 (FPGS3, a cytosolic folylpolyglutamate synthetase), At5g15660 (containing an F-box domain), At1g47370 (a TIR-X (Toll-Interleukin Receptor domain)), and At5g64060 (a predicted pectin methylesterase inhibitor). Over-represented GO terms for the gene expression study included "innate immune response" for elf18/parg1, highlighting a subset of elf18-activated defense-associated genes whose expression is altered in parg1 plants. The study also allowed a tightly controlled comparison of early mRNA abundance responses to flg22 and elf18 in wild-type Arabidopsis, which revealed many differences. The PARP inhibitor 3-methoxybenzamide (3MB) was also used in the gene expression profiling, but pleiotropic impacts of this inhibitor were observed. This transcriptomics study revealed targets for further dissection of MAMP-induced plant immune responses, impacts of PARP inhibitors, and the molecular mechanisms by which poly(ADP-ribosyl)ation regulates plant responses to MAMPs.},
doi = {10.1371/journal.pone.0190268},
journal = {PLoS ONE},
number = 12,
volume = 12,
place = {United States},
year = {Thu Dec 28 00:00:00 EST 2017},
month = {Thu Dec 28 00:00:00 EST 2017}
}
https://doi.org/10.1371/journal.pone.0190268
Web of Science
Works referenced in this record:
The Role of TIR-NBS and TIR-X Proteins in Plant Basal Defense Responses
journal, June 2013
- Nandety, R. S.; Caplan, J. L.; Cavanaugh, K.
- PLANT PHYSIOLOGY, Vol. 162, Issue 3
Plant pathogens and integrated defence responses to infection
journal, June 2001
- Dangl, Jeffery L.; Jones, Jonathan D. G.
- Nature, Vol. 411, Issue 6839
Poly(ADP-ribose)-Dependent Regulation of DNA Repair by the Chromatin Remodeling Enzyme ALC1
journal, August 2009
- Ahel, D.; Horejsi, Z.; Wiechens, N.
- Science, Vol. 325, Issue 5945
Analysis of knockout mutants reveals non-redundant functions of poly(ADP-ribose)polymerase isoforms in Arabidopsis
journal, October 2015
- Pham, Phuong Anh; Wahl, Vanessa; Tohge, Takayuki
- Plant Molecular Biology, Vol. 89, Issue 4-5
Synthesis and degradation of poly(ADP-ribose) in plants
journal, January 2014
- Bianchi, Anna, Rita
- Frontiers in Bioscience, Vol. 19, Issue 8
UV-B- and oxidative stress-induced increase in nicotinamide and trigonelline and inhibition of defensive metabolism induction by poly(ADP-ribose)polymerase inhibitor in plant tissue
journal, February 1996
- Berglund, Torkel; Kalbin, Georgi; Strid, Åke
- FEBS Letters, Vol. 380, Issue 1-2
Pectin methylesterase inhibitor
journal, February 2004
- Giovane, A.; Servillo, L.; Balestrieri, C.
- Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1696, Issue 2
Plant immunity: towards an integrated view of plant–pathogen interactions
journal, June 2010
- Dodds, Peter N.; Rathjen, John P.
- Nature Reviews Genetics, Vol. 11, Issue 8
BMS-536924 sensitizes human epithelial ovarian cancer cells to the PARP inhibitor, 3-aminobenzamide
journal, November 2009
- Beauchamp, Marie-Claude; Knafo, Ariane; Yasmeen, Amber
- Gynecologic Oncology, Vol. 115, Issue 2
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana
journal, August 2003
- Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J.
- Science, Vol. 301, Issue 5633, p. 653-657
Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine
journal, March 2006
- Li, Y.
- Genome Research, Vol. 16, Issue 3
Activation of Defense Response Pathways by OGs and Flg22 Elicitors in Arabidopsis Seedlings
journal, May 2008
- Denoux, Carine; Galletti, Roberta; Mammarella, Nicole
- Molecular Plant, Vol. 1, Issue 3
Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions
journal, September 2007
- Bent, Andrew F.; Mackey, David
- Annual Review of Phytopathology, Vol. 45, Issue 1
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition
journal, January 2012
- Pajerowska-Mukhtar, Karolina M.; Wang, Wei; Tada, Yasuomi
- Current Biology, Vol. 22, Issue 2
Characteristics of the Inhibition of Induced Tracheary Element Differentiation by 3-Aminobenzamide and Related Compounds
journal, January 1985
- Phillips, R.; Hawkins, S. W.
- Journal of Experimental Botany, Vol. 36, Issue 1
tej Defines a Role for Poly(ADP-Ribosyl)ation in Establishing Period Length of the Arabidopsis Circadian Oscillator
journal, July 2002
- Panda, Satchidananda; Poirier, Guy G.; Kay, Steve A.
- Developmental Cell, Vol. 3, Issue 1
Identification and Mutational Analysis of Arabidopsis FLS2 Leucine-Rich Repeat Domain Residues That Contribute to Flagellin Perception
journal, October 2007
- Dunning, F. Mark; Sun, Wenxian; Jansen, Kristin L.
- The Plant Cell, Vol. 19, Issue 10
Chemical PARP Inhibition Enhances Growth of Arabidopsis and Reduces Anthocyanin Accumulation and the Activation of Stress Protective Mechanisms
journal, May 2012
- Schulz, Philipp; Neukermans, Jenny; Van Der Kelen, Katrien
- PLoS ONE, Vol. 7, Issue 5
New Insights into the Roles of NAD+-Poly(ADP-ribose) Metabolism and Poly(ADP-ribose) Glycohydrolase
journal, September 2016
- Tanuma, Sei-ichi; Sato, Akira; Oyama, Takahiro
- Current Protein & Peptide Science, Vol. 17, Issue 7
Analysis of Poly(ADP-Ribose) Polymerases in Arabidopsis Telomere Biology
journal, February 2014
- Boltz, Kara A.; Jasti, Madhu; Townley, Jennifer M.
- PLoS ONE, Vol. 9, Issue 2
Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance: Inhibition of PARP preserves energy homeostasis
journal, November 2004
- Block, Marc De; Verduyn, Christoph; Brouwer, Dirk De
- The Plant Journal, Vol. 41, Issue 1
Histone ADP-Ribosylation Facilitates Gene Transcription by Directly Remodeling Nucleosomes
journal, April 2012
- Martinez-Zamudio, R.; Ha, H. C.
- Molecular and Cellular Biology, Vol. 32, Issue 13
Radiation-induced mitotic catastrophe in PARG-deficient cells
journal, May 2009
- Ame, J. -C.; Fouquerel, E.; Gauthier, L. R.
- Journal of Cell Science, Vol. 122, Issue 12
A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling
journal, April 2006
- Navarro, L.; Dunoyer, P.; Jay, F.
- Science, Vol. 312, Issue 5772
Single molecule detection of PARP1 and PARP2 interaction with DNA strand breaks and their poly(ADP-ribosyl)ation using high-resolution AFM imaging
journal, December 2015
- Sukhanova, Maria V.; Abrakhi, Sanae; Joshi, Vandana
- Nucleic Acids Research, Vol. 44, Issue 6
cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis
journal, May 2009
- Won, Su-Kyung; Lee, Yong-Ju; Lee, Ha-Yeon
- Plant Physiology, Vol. 150, Issue 3
Poly-(ADP-Ribose) Polymerase-1 Is Necessary for Long-Term Facilitation in Aplysia
journal, July 2009
- Hernandez, A. I.; Wolk, J.; Hu, J. -Y.
- Journal of Neuroscience, Vol. 29, Issue 30
Understanding Plant Immunity as a Surveillance System to Detect Invasion
journal, August 2015
- Cook, David E.; Mesarich, Carl H.; Thomma, Bart P. H. J.
- Annual Review of Phytopathology, Vol. 53, Issue 1
Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases
journal, November 2012
- Lionetti, Vincenzo; Cervone, Felice; Bellincampi, Daniela
- Journal of Plant Physiology, Vol. 169, Issue 16
Microbial Pathogens Trigger Host DNA Double-Strand Breaks Whose Abundance Is Reduced by Plant Defense Responses
journal, April 2014
- Song, Junqi; Bent, Andrew F.
- PLoS Pathogens, Vol. 10, Issue 4
A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis
journal, February 2008
- Wan, Jinrong; Zhang, Xue-Cheng; Neece, David
- The Plant Cell, Vol. 20, Issue 2
AtSKIP18 and AtSKIP31, F-box subunits of the SCF E3 ubiquitin ligase complex, mediate the degradation of 14-3-3 proteins in Arabidopsis
journal, March 2017
- Hong, Jong-Pil; Adams, Eri; Yanagawa, Yuki
- Biochemical and Biophysical Research Communications, Vol. 485, Issue 1
Sequence-specific DNA damage induced by reduced mitomycin C and 7-N-( p -hydroxyphenyl)mitomycin C
journal, January 1984
- Ueda, Kazumitsu; Komano, Tohru
- Nucleic Acids Research, Vol. 12, Issue 17
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias
journal, January 2003
- Bolstad, B. M.; Irizarry, R. A.; Astrand, M.
- Bioinformatics, Vol. 19, Issue 2
Protein Poly(ADP-ribosyl)ation Regulates Arabidopsis Immune Gene Expression and Defense Responses
journal, January 2015
- Feng, Baomin; Liu, Chenglong; de Oliveira, Marcos V. V.
- PLoS Genetics, Vol. 11, Issue 1
Regulation and function of the pepper pectin methylesterase inhibitor (CaPMEI1) gene promoter in defense and ethylene and methyl jasmonate signaling in plants
journal, September 2009
- An, Soo Hyun; Choi, Hyong Woo; Hong, Jeum Kyu
- Planta, Vol. 230, Issue 6
The effect of poly (ADP-ribose) polymerase inhibition on aminoglycoside-induced acute tubular necrosis in rats
journal, January 2016
- Biro, Alexander; Vaknine, Hananya; Cohen-Armon, Malka
- Clinical Nephrology, Vol. 85 (2016), Issue 04
Testing significance relative to a fold-change threshold is a TREAT
journal, January 2009
- McCarthy, D. J.; Smyth, G. K.
- Bioinformatics, Vol. 25, Issue 6
Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors
journal, May 2005
- Jagtap, Prakash; Szabó, Csaba
- Nature Reviews Drug Discovery, Vol. 4, Issue 5
Chimeric receptors of the Arabidopsis thaliana pattern recognition receptors EFR and FLS2
journal, November 2010
- Albert, Markus; Felix, Georg
- Plant Signaling & Behavior, Vol. 5, Issue 11
Poly(ADP-ribose) Polymerase (PARP-1) in Homologous Recombination and as a Target for Cancer Therapy
journal, June 2005
- Helleday, Thomas; Bryant, Helen E.; Schultz, Niklas
- Cell Cycle, Vol. 4, Issue 9
Poly(ADP-ribose) signaling in cell death
journal, December 2013
- Virág, László; Robaszkiewicz, Agnieszka; Rodriguez-Vargas, Jose Manuel
- Molecular Aspects of Medicine, Vol. 34, Issue 6
Poly(ADP‐ribose) polymerases regulate cell division and development in Arabidopsis roots
journal, April 2017
- Liu, Caifeng; Wu, Qiao; Liu, Weiwei
- Journal of Integrative Plant Biology, Vol. 59, Issue 7
Effects of Poly(ADP-Ribose) Polymerase-1 Inhibition in a Neonatal Rodent Model of Hypoxic-Ischemic Injury
journal, January 2017
- Klöfers, Melanie; Kohaut, Jules; Bendix, Ivo
- BioMed Research International, Vol. 2017
NAD+ Depletion Is Necessary and Sufficient forPoly(ADP-Ribose) Polymerase-1-Mediated Neuronal Death
journal, February 2010
- Alano, C. C.; Garnier, P.; Ying, W.
- Journal of Neuroscience, Vol. 30, Issue 8
Discovery of ADP-Ribosylation and Other Plant Defense Pathway Elements Through Expression Profiling of Four Different Arabidopsis–Pseudomonas R-avr Interactions
journal, May 2008
- Adams-Phillips, Lori; Wan, Jinrong; Tan, Xiaoping
- Molecular Plant-Microbe Interactions, Vol. 21, Issue 5
A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana: Sensitivity of A. thaliana to bacterial flagellin
journal, May 1999
- Gómez-Gómez, Lourdes; Felix, Georg; Boller, Thomas
- The Plant Journal, Vol. 18, Issue 3
Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response
journal, January 2009
- Clay, N. K.; Adio, A. M.; Denoux, C.
- Science, Vol. 323, Issue 5910
Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation
journal, May 2006
- Zipfel, Cyril; Kunze, Gernot; Chinchilla, Delphine
- Cell, Vol. 125, Issue 4
Disruption of Poly(ADP-ribosyl)ation Mechanisms Alters Responses of Arabidopsis to Biotic Stress
journal, November 2009
- Adams-Phillips, Lori; Briggs, Amy G.; Bent, Andrew F.
- Plant Physiology, Vol. 152, Issue 1
ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION DEFICIENT2 Expression to Negatively Regulate Plant Innate Immunity in Arabidopsis
journal, August 2009
- Chen, Huamin; Xue, Li; Chintamanani, Satya
- The Plant Cell, Vol. 21, Issue 8
Light-dependent expression of flg22-induced defense genes in Arabidopsis
journal, October 2014
- Sano, Satoshi; Aoyama, Mayu; Nakai, Kana
- Frontiers in Plant Science, Vol. 5
Pattern Recognition Receptors Require N -Glycosylation to Mediate Plant Immunity
journal, December 2009
- Häweker, Heidrun; Rips, Stephan; Koiwa, Hisashi
- Journal of Biological Chemistry, Vol. 285, Issue 7
Modulation of the Poly(ADP-ribosyl)ation Reaction via the Arabidopsis ADP-Ribose/NADH Pyrophosphohydrolase, AtNUDX7, Is Involved in the Response to Oxidative Stress
journal, August 2009
- Ishikawa, Kazuya; Ogawa, Takahisa; Hirosue, Eisuke
- Plant Physiology, Vol. 151, Issue 2
Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells
journal, May 2000
- Tian, Rui-Hua; Zhang, Gui-You; Yan, Chang-Hui
- FEBS Letters, Vol. 474, Issue 1
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks
journal, November 2003
- Shannon, P.
- Genome Research, Vol. 13, Issue 11
Poly(ADP-ribose): novel functions for an old molecule
journal, July 2006
- Schreiber, Valérie; Dantzer, Françoise; Ame, Jean-Christophe
- Nature Reviews Molecular Cell Biology, Vol. 7, Issue 7
Higher plants possess two structurally different poly(ADP-ribose) polymerases
journal, September 1998
- Babiychuk, Elena; Cottrill, Phillippa B.; Storozhenko, Sergei
- The Plant Journal, Vol. 15, Issue 5
Repair and tolerance of oxidative DNA damage in plants
journal, March 2009
- Roldán-Arjona, Teresa; Ariza, Rafael R.
- Mutation Research/Reviews in Mutation Research, Vol. 681, Issue 2-3
Poly(ADP-ribosyl)ation in plants
journal, July 2011
- Briggs, Amy G.; Bent, Andrew F.
- Trends in Plant Science, Vol. 16, Issue 7
Pectin methylesterases: cell wall enzymes with important roles in plant physiology
journal, September 2001
- Micheli, Fabienne
- Trends in Plant Science, Vol. 6, Issue 9
Poly(ADP-ribose) Glycohydrolase Deficiency Sensitizes Mouse ES Cells to DNA Damaging Agents
journal, December 2009
- Fujihara, H.; Ogino, H.; Maeda, D.
- Current Cancer Drug Targets, Vol. 9, Issue 8
Gene expression microarray data from human microvascular endothelial cells supplemented with a low concentration of niacin
journal, March 2016
- Hughes-Large, Jennifer M.; Borradaile, Nica M.
- Data in Brief, Vol. 6
Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction
journal, September 2007
- Vanderauwera, S.; De Block, M.; Van de Steene, N.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 38
The Effect of poly(ADP-ribosyl)ation on Native and H1-depleted Chromatin
journal, May 1989
- Huletsky, A.; de Murcia, G.; Muller, S.
- Journal of Biological Chemistry, Vol. 264, Issue 15
Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance
journal, March 2008
- An, Soo Hyun; Sohn, Kee Hoon; Choi, Hyong Woo
- Planta, Vol. 228, Issue 1
The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants
journal, November 1998
- Amor, Yehudit; Babiychuk, Elena; Inzé, Dirk
- FEBS Letters, Vol. 440, Issue 1-2
Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection
journal, February 2013
- Tintor, N.; Ross, A.; Kanehara, K.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 15
Importance of Poly(ADP-Ribose) Glycohydrolase in the Control of Poly(ADP-Ribose) Metabolism
journal, August 2001
- Davidovic, Laetitia; Vodenicharov, Momchil; Affar, El Bachir
- Experimental Cell Research, Vol. 268, Issue 1
Functional analysis of folate polyglutamylation and its essential role in plant metabolism and development
journal, September 2010
- Mehrshahi, Payam; Gonzalez-Jorge, Sabrina; Akhtar, Tariq A.
- The Plant Journal, Vol. 64, Issue 2, p. 267-279
Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster
journal, December 2003
- Hanai, S.; Kanai, M.; Ohashi, S.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 1
Flagellin Is Not a Major Defense Elicitor in Ralstonia solanacearum Cells or Extracts Applied to Arabidopsis thaliana
journal, June 2004
- Pfund, Christine; Tans-Kersten, Julie; Dunning, F. Mark
- Molecular Plant-Microbe Interactions, Vol. 17, Issue 6
Chromosomal aberrations in PARP-/- mice: Genome stabilization in immortalized cells by reintroduction of poly(ADP-ribose) polymerase cDNA
journal, November 1999
- Simbulan-Rosenthal, C. M.; Haddad, B. R.; Rosenthal, D. S.
- Proceedings of the National Academy of Sciences, Vol. 96, Issue 23
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis
journal, March 2006
- Robatzek, S.
- Genes & Development, Vol. 20, Issue 5
Use of signal thresholds to determine significant changes in microarray data analyses
journal, January 2005
- Xinmin, Li; Kim, Jaejung; Zhou, Jian
- Genetics and Molecular Biology, Vol. 28, Issue 2
The Arabidopsis F-Box Protein CORONATINE INSENSITIVE1 Is Stabilized by SCF COI1 and Degraded via the 26S Proteasome Pathway
journal, February 2013
- Yan, Jianbin; Li, Haiou; Li, Shuhua
- The Plant Cell, Vol. 25, Issue 2
The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases
journal, January 2008
- Hassa, Paul, O.
- Frontiers in Bioscience, Vol. 13, Issue 13
PARP2 Is the Predominant Poly(ADP-Ribose) Polymerase in Arabidopsis DNA Damage and Immune Responses
journal, May 2015
- Song, Junqi; Keppler, Brian D.; Wise, Robert R.
- PLOS Genetics, Vol. 11, Issue 5
Poly(ADP-ribose) (PAR) polymer is a death signal
journal, November 2006
- Andrabi, S. A.; Kim, N. S.; Yu, S. -W.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 48
First-in-Class Chemical Probes against Poly(ADP-ribose) Glycohydrolase (PARG) Inhibit DNA Repair with Differential Pharmacology to Olaparib
journal, October 2016
- James, Dominic I.; Smith, Kate M.; Jordan, Allan M.
- ACS Chemical Biology, Vol. 11, Issue 11
Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality
journal, December 2004
- Koh, D. W.; Lawler, A. M.; Poitras, M. F.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 51