A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana

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.

doi:10.1371/journal.pone.0190268

Title: A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana

Journal Article · Thu Dec 28 00:00:00 EST 2017 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0190268· OSTI ID:1415065

; 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.

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.

View Journal Article

Cite

Export

Save

Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FG02-02ER15342

OSTI ID:: 1415065

Alternate ID(s):: OSTI ID: 1499890

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Vol. 12 Journal Issue: 12; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 14 works

Citation information provided by
Web of Science

References (81)

The Role of TIR-NBS and TIR-X Proteins in Plant Basal Defense Responses Nandety, R. S.; Caplan, J. L.; Cavanaugh, K. PLANT PHYSIOLOGY, Vol. 162, Issue 3 https://doi.org/10.1104/pp.113.219162	journal	June 2013
Plant pathogens and integrated defence responses to infection Dangl, Jeffery L.; Jones, Jonathan D. G. Nature, Vol. 411, Issue 6839 https://doi.org/10.1038/35081161	journal	June 2001
Poly(ADP-ribose)-Dependent Regulation of DNA Repair by the Chromatin Remodeling Enzyme ALC1 Ahel, D.; Horejsi, Z.; Wiechens, N. Science, Vol. 325, Issue 5945 https://doi.org/10.1126/science.1177321	journal	August 2009
Analysis of knockout mutants reveals non-redundant functions of poly(ADP-ribose)polymerase isoforms in Arabidopsis Pham, Phuong Anh; Wahl, Vanessa; Tohge, Takayuki Plant Molecular Biology, Vol. 89, Issue 4-5 https://doi.org/10.1007/s11103-015-0363-5	journal	October 2015
Synthesis and degradation of poly(ADP-ribose) in plants Bianchi, Anna, Rita Frontiers in Bioscience, Vol. 19, Issue 8 https://doi.org/10.2741/4294	journal	January 2014
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 Berglund, Torkel; Kalbin, Georgi; Strid, Åke FEBS Letters, Vol. 380, Issue 1-2 https://doi.org/10.1016/0014-5793(96)00027-0	journal	February 1996
Pectin methylesterase inhibitor Giovane, A.; Servillo, L.; Balestrieri, C. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1696, Issue 2 https://doi.org/10.1016/j.bbapap.2003.08.011	journal	February 2004
Plant immunity: towards an integrated view of plant–pathogen interactions Dodds, Peter N.; Rathjen, John P. Nature Reviews Genetics, Vol. 11, Issue 8 https://doi.org/10.1038/nrg2812	journal	June 2010
BMS-536924 sensitizes human epithelial ovarian cancer cells to the PARP inhibitor, 3-aminobenzamide Beauchamp, Marie-Claude; Knafo, Ariane; Yasmeen, Amber Gynecologic Oncology, Vol. 115, Issue 2 https://doi.org/10.1016/j.ygyno.2009.07.009	journal	November 2009
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana Alonso, J. M.; Stepanova, Anna N.; Leisse, Thomas J. Science, Vol. 301, Issue 5633, p. 653-657 https://doi.org/10.1126/science.1086391	journal	August 2003
Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a Relevance Vector Machine Li, Y. Genome Research, Vol. 16, Issue 3 https://doi.org/10.1101/gr.4237406	journal	March 2006
Activation of Defense Response Pathways by OGs and Flg22 Elicitors in Arabidopsis Seedlings Denoux, Carine; Galletti, Roberta; Mammarella, Nicole Molecular Plant, Vol. 1, Issue 3 https://doi.org/10.1093/mp/ssn019	journal	May 2008
Elicitors, Effectors, and R Genes: The New Paradigm and a Lifetime Supply of Questions Bent, Andrew F.; Mackey, David Annual Review of Phytopathology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.phyto.45.062806.094427	journal	September 2007
The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition Pajerowska-Mukhtar, Karolina M.; Wang, Wei; Tada, Yasuomi Current Biology, Vol. 22, Issue 2 https://doi.org/10.1016/j.cub.2011.12.015	journal	January 2012
Characteristics of the Inhibition of Induced Tracheary Element Differentiation by 3-Aminobenzamide and Related Compounds Phillips, R.; Hawkins, S. W. Journal of Experimental Botany, Vol. 36, Issue 1 https://doi.org/10.1093/jxb/36.1.119	journal	January 1985
tej Defines a Role for Poly(ADP-Ribosyl)ation in Establishing Period Length of the Arabidopsis Circadian Oscillator Panda, Satchidananda; Poirier, Guy G.; Kay, Steve A. Developmental Cell, Vol. 3, Issue 1 https://doi.org/10.1016/S1534-5807(02)00200-9	journal	July 2002
Identification and Mutational Analysis of Arabidopsis FLS2 Leucine-Rich Repeat Domain Residues That Contribute to Flagellin Perception Dunning, F. Mark; Sun, Wenxian; Jansen, Kristin L. The Plant Cell, Vol. 19, Issue 10 https://doi.org/10.1105/tpc.106.048801	journal	October 2007
Chemical PARP Inhibition Enhances Growth of Arabidopsis and Reduces Anthocyanin Accumulation and the Activation of Stress Protective Mechanisms Schulz, Philipp; Neukermans, Jenny; Van Der Kelen, Katrien PLoS ONE, Vol. 7, Issue 5 https://doi.org/10.1371/journal.pone.0037287	journal	May 2012
New Insights into the Roles of NAD+-Poly(ADP-ribose) Metabolism and Poly(ADP-ribose) Glycohydrolase Tanuma, Sei-ichi; Sato, Akira; Oyama, Takahiro Current Protein & Peptide Science, Vol. 17, Issue 7 https://doi.org/10.2174/1389203717666160419150014	journal	September 2016
Analysis of Poly(ADP-Ribose) Polymerases in Arabidopsis Telomere Biology Boltz, Kara A.; Jasti, Madhu; Townley, Jennifer M. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0088872	journal	February 2014
Poly(ADP-ribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance: Inhibition of PARP preserves energy homeostasis Block, Marc De; Verduyn, Christoph; Brouwer, Dirk De The Plant Journal, Vol. 41, Issue 1 https://doi.org/10.1111/j.1365-313X.2004.02277.x	journal	November 2004
Histone ADP-Ribosylation Facilitates Gene Transcription by Directly Remodeling Nucleosomes Martinez-Zamudio, R.; Ha, H. C. Molecular and Cellular Biology, Vol. 32, Issue 13 https://doi.org/10.1128/MCB.06667-11	journal	April 2012
Radiation-induced mitotic catastrophe in PARG-deficient cells Ame, J. -C.; Fouquerel, E.; Gauthier, L. R. Journal of Cell Science, Vol. 122, Issue 12 https://doi.org/10.1242/jcs.039115	journal	May 2009
A Plant miRNA Contributes to Antibacterial Resistance by Repressing Auxin Signaling Navarro, L.; Dunoyer, P.; Jay, F. Science, Vol. 312, Issue 5772 https://doi.org/10.1126/science.1126088	journal	April 2006
Single molecule detection of PARP1 and PARP2 interaction with DNA strand breaks and their poly(ADP-ribosyl)ation using high-resolution AFM imaging Sukhanova, Maria V.; Abrakhi, Sanae; Joshi, Vandana Nucleic Acids Research, Vol. 44, Issue 6 https://doi.org/10.1093/nar/gkv1476	journal	December 2015
cis-Element- and Transcriptome-Based Screening of Root Hair-Specific Genes and Their Functional Characterization in Arabidopsis Won, Su-Kyung; Lee, Yong-Ju; Lee, Ha-Yeon Plant Physiology, Vol. 150, Issue 3 https://doi.org/10.1104/pp.109.140905	journal	May 2009
Poly-(ADP-Ribose) Polymerase-1 Is Necessary for Long-Term Facilitation in Aplysia Hernandez, A. I.; Wolk, J.; Hu, J. -Y. Journal of Neuroscience, Vol. 29, Issue 30 https://doi.org/10.1523/JNEUROSCI.1512-09.2009	journal	July 2009
Understanding Plant Immunity as a Surveillance System to Detect Invasion Cook, David E.; Mesarich, Carl H.; Thomma, Bart P. H. J. Annual Review of Phytopathology, Vol. 53, Issue 1 https://doi.org/10.1146/annurev-phyto-080614-120114	journal	August 2015
Methyl esterification of pectin plays a role during plant–pathogen interactions and affects plant resistance to diseases Lionetti, Vincenzo; Cervone, Felice; Bellincampi, Daniela Journal of Plant Physiology, Vol. 169, Issue 16 https://doi.org/10.1016/j.jplph.2012.05.006	journal	November 2012
Microbial Pathogens Trigger Host DNA Double-Strand Breaks Whose Abundance Is Reduced by Plant Defense Responses Song, Junqi; Bent, Andrew F. PLoS Pathogens, Vol. 10, Issue 4 https://doi.org/10.1371/journal.ppat.1004030	journal	April 2014
A LysM Receptor-Like Kinase Plays a Critical Role in Chitin Signaling and Fungal Resistance in Arabidopsis Wan, Jinrong; Zhang, Xue-Cheng; Neece, David The Plant Cell, Vol. 20, Issue 2 https://doi.org/10.1105/tpc.107.056754	journal	February 2008
AtSKIP18 and AtSKIP31, F-box subunits of the SCF E3 ubiquitin ligase complex, mediate the degradation of 14-3-3 proteins in Arabidopsis Hong, Jong-Pil; Adams, Eri; Yanagawa, Yuki Biochemical and Biophysical Research Communications, Vol. 485, Issue 1 https://doi.org/10.1016/j.bbrc.2017.02.046	journal	March 2017
Sequence-specific DNA damage induced by reduced mitomycin C and 7-N-( p -hydroxyphenyl)mitomycin C Ueda, Kazumitsu; Komano, Tohru Nucleic Acids Research, Vol. 12, Issue 17 https://doi.org/10.1093/nar/12.17.6673	journal	January 1984
A comparison of normalization methods for high density oligonucleotide array data based on variance and bias Bolstad, B. M.; Irizarry, R. A.; Astrand, M. Bioinformatics, Vol. 19, Issue 2 https://doi.org/10.1093/bioinformatics/19.2.185	journal	January 2003
Protein Poly(ADP-ribosyl)ation Regulates Arabidopsis Immune Gene Expression and Defense Responses Feng, Baomin; Liu, Chenglong; de Oliveira, Marcos V. V. PLoS Genetics, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pgen.1004936	journal	January 2015
Regulation and function of the pepper pectin methylesterase inhibitor (CaPMEI1) gene promoter in defense and ethylene and methyl jasmonate signaling in plants An, Soo Hyun; Choi, Hyong Woo; Hong, Jeum Kyu Planta, Vol. 230, Issue 6 https://doi.org/10.1007/s00425-009-1021-4	journal	September 2009
The effect of poly (ADP-ribose) polymerase inhibition on aminoglycoside-induced acute tubular necrosis in rats Biro, Alexander; Vaknine, Hananya; Cohen-Armon, Malka Clinical Nephrology, Vol. 85 (2016), Issue 04 https://doi.org/10.5414/CN108697	journal	January 2016
Testing significance relative to a fold-change threshold is a TREAT McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 25, Issue 6 https://doi.org/10.1093/bioinformatics/btp053	journal	January 2009
Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors Jagtap, Prakash; Szabó, Csaba Nature Reviews Drug Discovery, Vol. 4, Issue 5 https://doi.org/10.1038/nrd1718	journal	May 2005
Chimeric receptors of the Arabidopsis thaliana pattern recognition receptors EFR and FLS2 Albert, Markus; Felix, Georg Plant Signaling & Behavior, Vol. 5, Issue 11 https://doi.org/10.4161/psb.5.11.13312	journal	November 2010
Poly(ADP-ribose) Polymerase (PARP-1) in Homologous Recombination and as a Target for Cancer Therapy Helleday, Thomas; Bryant, Helen E.; Schultz, Niklas Cell Cycle, Vol. 4, Issue 9 https://doi.org/10.4161/cc.4.9.2031	journal	June 2005
Poly(ADP-ribose) signaling in cell death Virág, László; Robaszkiewicz, Agnieszka; Rodriguez-Vargas, Jose Manuel Molecular Aspects of Medicine, Vol. 34, Issue 6 https://doi.org/10.1016/j.mam.2013.01.007	journal	December 2013
Poly(ADP‐ribose) polymerases regulate cell division and development in Arabidopsis roots Liu, Caifeng; Wu, Qiao; Liu, Weiwei Journal of Integrative Plant Biology, Vol. 59, Issue 7 https://doi.org/10.1111/jipb.12530	journal	April 2017
Effects of Poly(ADP-Ribose) Polymerase-1 Inhibition in a Neonatal Rodent Model of Hypoxic-Ischemic Injury Klöfers, Melanie; Kohaut, Jules; Bendix, Ivo BioMed Research International, Vol. 2017 https://doi.org/10.1155/2017/2924848	journal	January 2017
NAD+ Depletion Is Necessary and Sufficient forPoly(ADP-Ribose) Polymerase-1-Mediated Neuronal Death Alano, C. C.; Garnier, P.; Ying, W. Journal of Neuroscience, Vol. 30, Issue 8 https://doi.org/10.1523/JNEUROSCI.5552-09.2010	journal	February 2010
Discovery of ADP-Ribosylation and Other Plant Defense Pathway Elements Through Expression Profiling of Four Different Arabidopsis–Pseudomonas R-avr Interactions Adams-Phillips, Lori; Wan, Jinrong; Tan, Xiaoping Molecular Plant-Microbe Interactions, Vol. 21, Issue 5 https://doi.org/10.1094/MPMI-21-5-0646	journal	May 2008
A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana: Sensitivity of A. thaliana to bacterial flagellin Gómez-Gómez, Lourdes; Felix, Georg; Boller, Thomas The Plant Journal, Vol. 18, Issue 3 https://doi.org/10.1046/j.1365-313X.1999.00451.x	journal	May 1999
Glucosinolate Metabolites Required for an Arabidopsis Innate Immune Response Clay, N. K.; Adio, A. M.; Denoux, C. Science, Vol. 323, Issue 5910 https://doi.org/10.1126/science.1164627	journal	January 2009
Perception of the Bacterial PAMP EF-Tu by the Receptor EFR Restricts Agrobacterium-Mediated Transformation Zipfel, Cyril; Kunze, Gernot; Chinchilla, Delphine Cell, Vol. 125, Issue 4 https://doi.org/10.1016/j.cell.2006.03.037	journal	May 2006
Disruption of Poly(ADP-ribosyl)ation Mechanisms Alters Responses of Arabidopsis to Biotic Stress Adams-Phillips, Lori; Briggs, Amy G.; Bent, Andrew F. Plant Physiology, Vol. 152, Issue 1 https://doi.org/10.1104/pp.109.148049	journal	November 2009
ETHYLENE INSENSITIVE3 and ETHYLENE INSENSITIVE3-LIKE1 Repress SALICYLIC ACID INDUCTION DEFICIENT2 Expression to Negatively Regulate Plant Innate Immunity in Arabidopsis Chen, Huamin; Xue, Li; Chintamanani, Satya The Plant Cell, Vol. 21, Issue 8 https://doi.org/10.1105/tpc.108.065193	journal	August 2009
Light-dependent expression of flg22-induced defense genes in Arabidopsis Sano, Satoshi; Aoyama, Mayu; Nakai, Kana Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00531	journal	October 2014
Pattern Recognition Receptors Require N -Glycosylation to Mediate Plant Immunity Häweker, Heidrun; Rips, Stephan; Koiwa, Hisashi Journal of Biological Chemistry, Vol. 285, Issue 7 https://doi.org/10.1074/jbc.M109.063073	journal	December 2009
Modulation of the Poly(ADP-ribosyl)ation Reaction via the Arabidopsis ADP-Ribose/NADH Pyrophosphohydrolase, AtNUDX7, Is Involved in the Response to Oxidative Stress Ishikawa, Kazuya; Ogawa, Takahisa; Hirosue, Eisuke Plant Physiology, Vol. 151, Issue 2 https://doi.org/10.1104/pp.109.140442	journal	August 2009
Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells Tian, Rui-Hua; Zhang, Gui-You; Yan, Chang-Hui FEBS Letters, Vol. 474, Issue 1 https://doi.org/10.1016/S0014-5793(00)01561-1	journal	May 2000
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Poly(ADP-ribose): novel functions for an old molecule Schreiber, Valérie; Dantzer, Françoise; Ame, Jean-Christophe Nature Reviews Molecular Cell Biology, Vol. 7, Issue 7 https://doi.org/10.1038/nrm1963	journal	July 2006
Higher plants possess two structurally different poly(ADP-ribose) polymerases Babiychuk, Elena; Cottrill, Phillippa B.; Storozhenko, Sergei The Plant Journal, Vol. 15, Issue 5 https://doi.org/10.1046/j.1365-313x.1998.00240.x	journal	September 1998
Repair and tolerance of oxidative DNA damage in plants Roldán-Arjona, Teresa; Ariza, Rafael R. Mutation Research/Reviews in Mutation Research, Vol. 681, Issue 2-3 https://doi.org/10.1016/j.mrrev.2008.07.003	journal	March 2009
Poly(ADP-ribosyl)ation in plants Briggs, Amy G.; Bent, Andrew F. Trends in Plant Science, Vol. 16, Issue 7 https://doi.org/10.1016/j.tplants.2011.03.008	journal	July 2011
Pectin methylesterases: cell wall enzymes with important roles in plant physiology Micheli, Fabienne Trends in Plant Science, Vol. 6, Issue 9 https://doi.org/10.1016/S1360-1385(01)02045-3	journal	September 2001
Poly(ADP-ribose) Glycohydrolase Deficiency Sensitizes Mouse ES Cells to DNA Damaging Agents Fujihara, H.; Ogino, H.; Maeda, D. Current Cancer Drug Targets, Vol. 9, Issue 8 https://doi.org/10.2174/156800909790192419	journal	December 2009
Gene expression microarray data from human microvascular endothelial cells supplemented with a low concentration of niacin Hughes-Large, Jennifer M.; Borradaile, Nica M. Data in Brief, Vol. 6 https://doi.org/10.1016/j.dib.2016.01.039	journal	March 2016
Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction Vanderauwera, S.; De Block, M.; Van de Steene, N. Proceedings of the National Academy of Sciences, Vol. 104, Issue 38 https://doi.org/10.1073/pnas.0706668104	journal	September 2007
The Effect of poly(ADP-ribosyl)ation on Native and H1-depleted Chromatin Huletsky, A.; de Murcia, G.; Muller, S. Journal of Biological Chemistry, Vol. 264, Issue 15 https://doi.org/10.1016/S0021-9258(18)81875-0	journal	May 1989
Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance An, Soo Hyun; Sohn, Kee Hoon; Choi, Hyong Woo Planta, Vol. 228, Issue 1 https://doi.org/10.1007/s00425-008-0719-z	journal	March 2008
The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants Amor, Yehudit; Babiychuk, Elena; Inzé, Dirk FEBS Letters, Vol. 440, Issue 1-2 https://doi.org/10.1016/S0014-5793(98)01408-2	journal	November 1998
Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection Tintor, N.; Ross, A.; Kanehara, K. Proceedings of the National Academy of Sciences, Vol. 110, Issue 15 https://doi.org/10.1073/pnas.1216780110	journal	February 2013
Importance of Poly(ADP-Ribose) Glycohydrolase in the Control of Poly(ADP-Ribose) Metabolism Davidovic, Laetitia; Vodenicharov, Momchil; Affar, El Bachir Experimental Cell Research, Vol. 268, Issue 1 https://doi.org/10.1006/excr.2001.5263	journal	August 2001
Functional analysis of folate polyglutamylation and its essential role in plant metabolism and development Mehrshahi, Payam; Gonzalez-Jorge, Sabrina; Akhtar, Tariq A. The Plant Journal, Vol. 64, Issue 2, p. 267-279 https://doi.org/10.1111/j.1365-313X.2010.04336.x	journal	September 2010
Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster Hanai, S.; Kanai, M.; Ohashi, S. Proceedings of the National Academy of Sciences, Vol. 101, Issue 1 https://doi.org/10.1073/pnas.2237114100	journal	December 2003
Flagellin Is Not a Major Defense Elicitor in Ralstonia solanacearum Cells or Extracts Applied to Arabidopsis thaliana Pfund, Christine; Tans-Kersten, Julie; Dunning, F. Mark Molecular Plant-Microbe Interactions, Vol. 17, Issue 6 https://doi.org/10.1094/MPMI.2004.17.6.696	journal	June 2004
Chromosomal aberrations in PARP-/- mice: Genome stabilization in immortalized cells by reintroduction of poly(ADP-ribose) polymerase cDNA Simbulan-Rosenthal, C. M.; Haddad, B. R.; Rosenthal, D. S. Proceedings of the National Academy of Sciences, Vol. 96, Issue 23 https://doi.org/10.1073/pnas.96.23.13191	journal	November 1999
Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis Robatzek, S. Genes & Development, Vol. 20, Issue 5 https://doi.org/10.1101/gad.366506	journal	March 2006
Use of signal thresholds to determine significant changes in microarray data analyses Xinmin, Li; Kim, Jaejung; Zhou, Jian Genetics and Molecular Biology, Vol. 28, Issue 2 https://doi.org/10.1590/S1415-47572005000200002	journal	January 2005
The Arabidopsis F-Box Protein CORONATINE INSENSITIVE1 Is Stabilized by SCF ^COI1 and Degraded via the 26S Proteasome Pathway Yan, Jianbin; Li, Haiou; Li, Shuhua The Plant Cell, Vol. 25, Issue 2 https://doi.org/10.1105/tpc.112.105486	journal	February 2013
The diverse biological roles of mammalian PARPS, a small but powerful family of poly-ADP-ribose polymerases Hassa, Paul, O. Frontiers in Bioscience, Vol. 13, Issue 13 https://doi.org/10.2741/2909	journal	January 2008
PARP2 Is the Predominant Poly(ADP-Ribose) Polymerase in Arabidopsis DNA Damage and Immune Responses Song, Junqi; Keppler, Brian D.; Wise, Robert R. PLOS Genetics, Vol. 11, Issue 5 https://doi.org/10.1371/journal.pgen.1005200	journal	May 2015
Poly(ADP-ribose) (PAR) polymer is a death signal Andrabi, S. A.; Kim, N. S.; Yu, S. -W. Proceedings of the National Academy of Sciences, Vol. 103, Issue 48 https://doi.org/10.1073/pnas.0606526103	journal	November 2006
First-in-Class Chemical Probes against Poly(ADP-ribose) Glycohydrolase (PARG) Inhibit DNA Repair with Differential Pharmacology to Olaparib James, Dominic I.; Smith, Kate M.; Jordan, Allan M. ACS Chemical Biology, Vol. 11, Issue 11 https://doi.org/10.1021/acschembio.6b00609	journal	October 2016
Failure to degrade poly(ADP-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality Koh, D. W.; Lawler, A. M.; Poitras, M. F. Proceedings of the National Academy of Sciences, Vol. 101, Issue 51 https://doi.org/10.1073/pnas.0406182101	journal	December 2004

Similar Records

The effect of poly(ADP-ribosyl)ation inhibition on the porcine cumulus-oocyte complex during in vitro maturation

Journal Article · Sun Jan 29 00:00:00 EST 2017 · Biochemical and Biophysical Research Communications · OSTI ID:1415065

Kim, Duk Hyoun; Lee, Hye Ran; Kim, Min Gyeong; +2 more

PARP-2 regulates cell cycle-related genes through histone deacetylation and methylation independently of poly(ADP-ribosyl)ation

Journal Article · Fri Feb 01 00:00:00 EST 2013 · Biochemical and Biophysical Research Communications · OSTI ID:1415065

Liang, Ya-Chen; Hsu, Chiao-Yu; Yao, Ya-Li; +1 more

Discovery of novel poly(ADP-ribose) glycohydrolase inhibitors by a quantitative assay system using dot-blot with anti-poly(ADP-ribose)

Journal Article · Fri Feb 19 00:00:00 EST 2010 · Biochemical and Biophysical Research Communications · OSTI ID:1415065

Okita, Naoyuki; Ashizawa, Daisuke; Ohta, Ryo; +2 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Title: A transcriptomics approach uncovers novel roles for poly(ADP-ribosyl)ation in the basal defense response in Arabidopsis thaliana

Citation Formats

References (81)

Similar Records

Related Subjects