Poly(ADP-Ribose)polymerase activity controls plant growth by promoting leaf cell number

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Schulz, Philipp ^a,b,f   Jansseune, Karel ^a   Degenkolbe, Thomas ^c   Meret, Michael ^c   Claeys, Hannes ^d,e,g   Skirycz, Aleksandra ^d,e   Teige, Markus ^b   Willmitzer, Lothar ^c   Hannah, Matthew A ^a  

^a Bayer Cropscience Belgium   (Belgium)

^b UNIVERSITY OF VIENNA   (Austria)

^c MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^d GHENT UNIVERSITY   (Belgium)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^f FREIE UNIVERSITÄT BERLIN   (Germany)

^g INSTITUTO TECNOLÓGICO VALE   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROPHYLL A; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ARABIDOPSIS THALIANA; ARTICLE; BIOMASS PRODUCTION; CELL COUNT; CELL CYCLE REGULATION; CELL GROWTH; CELL KINETICS; CELL SIZE; ENDOREDUPLICATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GROWTH REGULATION; HYDROPONICS; KINEMATICS; METABOLOMICS; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION STATE; PHENOTYPE; PLANT CELL; PLANT GROWTH; PLANT LEAF; PLANT STRESS; SECONDARY METABOLISM; TIME SERIES ANALYSIS; TRANSCRIPTOMICS;

ARABIDOPSIS; BENZAMIDES; BIOFUELS; BIOMASS; CELL CYCLE; ENZYME INHIBITORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; METABOLIC NETWORKS AND PATHWAYS; PLANT LEAVES; PLANT PROTEINS; POLY(ADP-RIBOSE) POLYMERASES; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84896502953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0090322     Document Type: Article

References (87)

1. Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61: 443-462.
2. Preuss SB, Meister R, Xu Q, Urwin CP, Tripodi FA, et al. (2012) Expression of the Arabidopsis thaliana BBX32 gene in soybean increases grain yield. PLoS ONE 7: e30717.
3. Poupin MJ, Timmermann T, Vega A, Zuñ iga A, González B (2013) Effects of the Plant Growth-Promoting Bacterium Burkholderia phytofirmans PsJN throughout the Life Cycle of Arabidopsis thaliana. PLoS ONE 8: e69435.
4. Skirycz A, De Bodt S, Obata T, De Clercq I, Claeys H, et al. (2010) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiol 152: 226-244.
5. De Block M, Verduyn C, De Brouwer D, Cornelissen M (2005) Poly(ADPribose) polymerase in plants affects energy homeostasis, cell death and stress tolerance. Plant J 41: 95-106.
6. Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448: 938-942. (Pubitemid 47312777)
7. Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57: 675-709. (Pubitemid 44061041)
8. Sulpice R, Pyl E-T, Ishihara H, Trenkamp S, Steinfath M, et al. (2009) Starch as a major integrator in the regulation of plant growth. Proc Natl Acad Sci USA 106: 10348-10353.
9. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, et al. (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 6: 397.
10. Boruc J, Van den Daele H, Hollunder J, Rombauts S, Mylle E, et al. (2010a) Functional modules in the Arabidopsis core cell cycle binary protein-protein interaction network. Plant Cell 22: 1264-1280.
11. Boruc J, Mylle E, Duda M, De Clercq R, Rombauts S, et al. (2010b) Systematic localization of the Arabidopsis core cell cycle proteins reveals novel cell division complexes. Plant Physiol 152: 553-565.
12. Chen YM, Shall S, O'Farrell M (1994) Poly(ADP-ribose) polymerase in plant nuclei. Eur J Biochem 224: 135-142. (Pubitemid 24267114)
13. Lepiniec L, Babiychuk E, Kushnir S, Van Montagu M, Inzé D (1995) Characterization of an Arabidopsis thaliana cDNA homologue to animal poly(ADP-ribose) polymerase. FEBS Lett 364: 103-108.
14. Amor Y, Babiychuk E, Inzé D, Levine A (1998) The involvement of poly(ADPribose) polymerase in the oxidative stress responses in plants. FEBS Lett 440: 1-7. (Pubitemid 28558723)
15. Babiychuk E, Cottrill PB, Storozhenko S, Fuangthong M, Chen Y, et al. (1998) Higher plants possess two structurally different poly(ADP-ribose) polymerases. Plant J 15: 635-645.
16. Willmitzer L (1979) Demonstration of in vitro covalent modification of chromosomal proteins by poly(ADP) ribosylation in plant nuclei. FEBS Lett 108: 13-16.
17. Whitby AJ, Stone PR, Whish WJ (1979) Effect of polyamines and Mg++ on poly(ADP-ribose) synthesis and ADP-ribosylation of histones in wheat. Biochem Biophys Res Commun 90: 1295-1304.
18. Ruf A, Mennissier de Murcia J, de Murcia G, Schulz GE (1996) Structure of the catalytic fragment of poly(AD-ribose) polymerase from chicken. Proc Natl Acad Sci USA 93: 7481-7485. (Pubitemid 26277060)
19. Briggs AG, Bent AF (2011) Poly(ADP-ribosyl)ation in plants. Trends in Plant Science 16: 372-380.
20. Amé J-C, Spenlehauer C, de Murcia G (2004) The PARP superfamily. Bioessays 26: 882-893. (Pubitemid 39128102)
21. Gibson BA, Kraus WL (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat Rev Mol Cell Biol 13: 411-424.
22. Luo X, Kraus WL (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev 26: 417-432.
23. Bürkle A, Virág L (2013) Poly(ADP-ribose): PARadigms and PARadoxes. Molecular Aspects of Medicine. doi: 10.1016/j.mam.2012.12.010.
24. Kraus WL, Hottiger MO (2013) PARP-1 and gene regulation: Progress and puzzles. Mol Aspects Med. doi: 10.1016/j.mam.2013.01.005.
25. Jaspers P, Overmyer K, Wrzaczek M, Vainonen JP, Blomster T, et al. (2010) The RST and PARP-like domain containing SRO protein family: analysis of protein structure, function and conservation in land plants. BMC Genomics 11: 170.
26. Doucet-Chabeaud G, Godon C, Brutesco C, de Murcia G, Kazmaier M (2001) Ionising radiation induces the expression of PARP-1 and PARP-2 genes in Arabidopsis. Mol Genet Genomics 265: 954-963. (Pubitemid 32702168)
27. Vanderauwera S, De Block M, Van de Steene N, van de Cotte B, Metzlaff M, et al. (2007) Silencing of poly(ADP-ribose) polymerase in plants alters abiotic stress signal transduction. Proc Natl Acad Sci USA 104: 15150-15155. (Pubitemid 47619607)
28. Ogawa T, Ishikawa K, Harada K, Fukusaki E, Yoshimura K, et al. (2009) Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57: 289-301.
29. Schulz P, Neukermans J, Van der Kelen K, Mühlenbock P, Van Breusegem F, et al. (2012) Chemical PARP inhibition enhances growth of Arabidopsis and reduces anthocyanin accumulation and the activation of stress protective mechanisms. PLoS ONE 7: e37287
30. Adams-Phillips L, Wan J, Tan X, Dunning FM, Meyers BC, et al. (2008) Discovery of ADP-ribosylation and other plant defense pathway elements through expression profiling of four different Arabidopsis-Pseudomonas R-avr interactions. Mol Plant Microbe Interact 21: 646-657. (Pubitemid 351679743)
31. Adams-Phillips L, Briggs AG, Bent AF (2010) Disruption of poly(ADPribosyl) ation mechanisms alters responses of Arabidopsis to biotic stress. Plant Physiol 152: 267-280.
32. Panda S, Poirier GG, Kay SA (2002) tej defines a role for poly(ADP-ribosyl)ation in establishing period length of the arabidopsis circadian oscillator. Dev Cell 3: 51-61. (Pubitemid 34778395)
33. Phillips R, Hawkins SW (1985) Characteristics of the Inhibition of Induced Tracheary Element Differentiation by 3-Aminobenzamide and Related Compounds. J Exp Bot 36: 119-128.
34. Jia Q, Dulk-Ras A den, Shen H, Hooykaas PJJ, de Pater S (2013) Poly(ADPribose) polymerases are involved in microhomology mediated back-up nonhomologous end joining in Arabidopsis thaliana. Plant Mol Biol. doi: 10.1007/ s11103-013-0065-9.
35. Babiychuk E, Van Montagu M, Kushnir S (2001) N-terminal domains of plant poly(ADP-ribose) polymerases define their association with mitotic chromosomes. Plant J 28: 245-255. (Pubitemid 33066390)
36. Storozhenko S, Inzé D, Van Montagu M, Kushnir S (2001) Arabidopsis coactivator ALY-like proteins, DIP1 and DIP2, interact physically with the DNA-binding domain of the Zn-finger poly(ADP-ribose) polymerase. J Exp Bot 52: 1375-1380. (Pubitemid 32646451)
37. Tian RH, Zhang GY, Yan CH, Dai YR (2000) Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells. FEBS Lett 474: 11-15.
38. Hashida S, Takahashi H, Uchimiya H (2009) The role of NAD biosynthesis in plant development and stress responses. Ann Bot 103: 819-824.
39. Pellny TK, Locato V, Vivancos PD, Markovic J, De Gara L, et al. (2009) Pyridine nucleotide cycling and control of intracellular redox state in relation to poly (ADP-ribose) polymerase activity and nuclear localization of glutathione during exponential growth of Arabidopsis cells in culture. Mol Plant 2: 442-456.
40. Murashige T, Skoog F (1962) A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum 15: 473-497.
41. Skirycz A, Claeys H, De Bodt S, Oikawa A, Shinoda S, et al. (2011) Pause-andstop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23: 1876-1888.
42. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
43. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315. (Pubitemid 38262761)
44. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
45. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1: 387-396.
46. Giavalisco P, Köhl K, Hummel J, Seiwert B, Willmitzer L (2009) 13C isotopelabeled metabolomes allowing for improved compound annotation and relative quantification in liquid chromatography-mass spectrometry-based metabolomic research. Anal Chem 81: 6546-6551.
47. Weckwerth W, Wenzel K, Fiehn O (2004) Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4: 78-83. (Pubitemid 38140876)
48. Cuadros-Inostroza A, Caldana C, Redestig H, Kusano M, Lisec J, et al. (2009) TargetSearch-a Bioconductor package for the efficient preprocessing of GC-MS metabolite profiling data. BMC Bioinformatics 10: 428.
49. Zeeman SC, Umemoto T, Lue WL, Au-Yeung P, Martin C, et al. (1998) A mutant of Arabidopsis lacking a chloroplastic isoamylase accumulates both starch and phytoglycogen. Plant Cell 10: 1699-1712.
50. Carbon S, Ireland A, Mungall CJ, Shu S, Marshall B, et al. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288-289.
51. Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, et al. (2007) The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol 72: 353-363.
52. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, et al. (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939. (Pubitemid 38370342)
53. Küpper JH, van Gool L, Bürkle A (1995) Molecular genetic systems to study the role of poly(ADP-ribosyl)ation in the cellular response to DNA damage. Biochimie 77: 450-455.
54. Ni Z, Kim E-D, Ha M, Lackey E, Liu J, et al. (2009) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457: 327-331.
55. Van Leene J, Boruc J, De Jaeger G, Russinova E, De Veylder L (2011) A kaleidoscopic view of the Arabidopsis core cell cycle interactome. Trends Plant Sci 16: 141-150.
56. Torres Acosta JA, Fowke LC, Wang H (2011) Analyses of phylogeny, evolution, conserved sequences and genome-wide expression of the ICK/KRP family of plant CDK inhibitors. Ann Bot 107: 1141-1157.
57. Jin H, Cominelli E, Bailey P, Parr A, Mehrtens F, et al. (2000) Transcriptional repression by AtMYB4 controls production of UV-protecting sunscreens in Arabidopsis. EMBO J 19: 6150-6161.
58. Gebbie LK, Burn JE, Hocart CH, Williamson RE (2005) Genes encoding ADPribosylation factors in Arabidopsis thaliana L. Heyn.; genome analysis and antisense suppression. J Exp Bot 56: 1079-1091. (Pubitemid 40518582)
59. Yao Y, Ni Z, Du J, Han Z, Chen Y, et al. (2009) Ectopic overexpression of wheat adenosine diphosphate-ribosylation factor, TaARF, increases growth rate in Arabidopsis. J Integr Plant Biol 51: 35-44.
60. Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, et al. (2010) Increased leaf size: different means to an end. Plant Physiol 153: 1261-1279.
61. Inzé D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40: 77-105. (Pubitemid 44956780)
62. Fujikura U, Horiguchi G, Tsukaya H (2007) Dissection of enhanced cell expansion processes in leaves triggered by a defect in cell proliferation, with reference to roles of endoreduplication. Plant Cell Physiol 48: 278-286.
63. Melaragno J, Mehrotra B, Coleman A (1993) Relationship between Endopolyploidy and Cell Size in Epidermal Tissue of Arabidopsis. Plant Cell 5: 1661-1668. (Pubitemid 2021821)
64. Triviño M, Martín-Trillo M, Ballesteros I, Delgado D, de Marcos A, et al. (2013) Timely expression of the Arabidopsis stoma-fate master regulator MUTE is required for specification of other epidermal cell types. Plant J. doi: 10.1111/ tpj.12244.
65. Arabidopsis Interactome Mapping Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333: 601-607.
66. Claeys H, Skirycz A, Maleux K, Inzé D (2012) DELLA signaling mediates stressinduced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol 159: 739-747.
67. Heyman J, Van den Daele H, De Wit K, Boudolf V, Berckmans B, et al. (2011) Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23: 4394-4410.
68. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, et al. (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12: 97-110.
69. Pourcel L, Irani NG, Koo AJK, Bohorquez-Restrepo A, Howe GA, et al. (2013) A chemical complementation approach reveals genes and interactions of flavonoids with other pathways. The Plant Journal 74: 383-397.
70. Ford KA, Casida JE, Chandran D, Gulevich AG, Okrent RA, et al. (2010) Neonicotinoid insecticides induce salicylate-associated plant defense responses. Proc Natl Acad Sci USA 107: 17527-17532.
71. Thielert W (2006) A unique product: The story of the imidacloprid stress shield. Pflanzenschutz-Nachrichten Bayer 59:73-86.
72. Fujiki Y, Yoshikawa Y, Sato T, Inada N, Ito M, et al. (2001) Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol Plant 111: 345-352.
73. Fujiki Y, Nakagawa Y, Furumoto T, Yoshida S, Biswal B, et al. (2005) Response to darkness of late-responsive dark-inducible genes is positively regulated by leaf age and negatively regulated by calmodulin-antagonist- sensitive signalling in Arabidopsis thaliana. Plant Cell Physiol 46: 1741-1746. (Pubitemid 41619492)
74. Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, et al. (2003) Early lightinduced proteins protect Arabidopsis from photooxidative stress. Proc Natl Acad Sci USA 100: 4921-4926. (Pubitemid 36457829)
75. Hannah MA, Caldana C, Steinhauser D, Balbo I, Fernie AR, et al. (2010) Combined Transcript and Metabolite Profiling of Arabidopsis Grown under Widely Variant Growth Conditions Facilitates the Identification of Novel Metabolite-Mediated Regulation of Gene Expression[C][W]. Plant Physiol 152: 2120-2129.
76. Kircher S, Schopfer P (2012) Photosynthetic sucrose acts as cotyledon-derived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc Natl Acad Sci USA 109: 11217-11221.
77. Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15: 282-292.
78. Baroja-Fernández E, Muñoz FJ, Li J, Bahaji A, Almagro G, et al. (2012) Sucrose synthase activity in the sus1/sus2/sus3/sus4 Arabidopsis mutant is sufficient to support normal cellulose and starch production. Proc Natl Acad Sci USA 109: 321-326.
79. Dodd AN, Salathia N, Hall A, Kévei E, Tóth R, et al. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309: 630-633. (Pubitemid 41033650)
80. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci USA 107: 9458-9463.
81. Berglund T, Kalbin G, Strid A, Rydström J, Ohlsson AB (1996) 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. FEBS Lett 380: 188-193. (Pubitemid 26058756)
82. Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, et al. (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15: 573-581.
83. Xiang C, Werner BL, Christensen EM, Oliver DJ (2001) The biological functions of glutathione revisited in arabidopsis transgenic plants with altered glutathione levels. Plant Physiol 126: 564-574. (Pubitemid 32566612)
84. Giacomelli L, Rudella A, van Wijk KJ (2006) High light response of the thylakoid proteome in arabidopsis wild type and the ascorbate-deficient mutant vtc2-2. A comparative proteomics study. Plant Physiol 141: 685-701. (Pubitemid 43974561)
85. Page M, Sultana N, Paszkiewicz K, Florance H, Smirnoff N (2012) The influence of ascorbate on anthocyanin accumulation during high light acclimation in Arabidopsis thaliana: further evidence for redox control of anthocyanin synthesis. Plant Cell Environ 35: 388-404.
86. Banasik M, Komura H, Shimoyama M, Ueda K (1992) Specific inhibitors of poly(ADP-ribose) synthetase and mono(ADP-ribosyl)transferase. J Biol Chem 267: 1569-1575.
87. Murai J, Huang SN, Das BB, Renaud A, Zhang Y, et al. (2012) Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res 72: 5588-5599.