RNA-Seq analysis discloses early senescence and nucleolar dysfunction triggered by Tdp1α depletion in Medicago truncatula

Journal of Experimental Botany

Volumn 64, Issue 7, 2013, Pages 1941-1951

  Donà, Mattia ^a   Confalonieri, Massimo ^a   Minio, Andrea ^b   Biggiogera, Marco ^a   Buttafava, Armando ^c   Raimondi, Elena ^a   Delledonne, Massimo ^b   Ventura, Lorenzo ^c   Sabatini, Maria Elisa ^a   Macovei, Anca ^a,d   Giraffa, Giorgio ^a   Carbonera, Daniela ^a   Balestrazzi, Alma ^a  

^a ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c University of Verona ^*  (Italy)

^d INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

Author keywords

Medicago truncatula; Nucleolus; RNA Seq; Tyrosyl DNA phosphodiesterase

Indexed keywords

PHOSPHODIESTERASE; TYROSYL DNA PHOSPHODIESTERASE; TYROSYL-DNA PHOSPHODIESTERASE; VEGETABLE PROTEIN;

ARTICLE; BARREL MEDIC; CELL AGING; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

CELL AGING; GENE EXPRESSION REGULATION, PLANT; MEDICAGO TRUNCATULA; PHOSPHORIC DIESTER HYDROLASES; PLANT PROTEINS;

EID: 84876969168     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert063     Document Type: Article

References (49)

1. Bahmed KI, Nitiss KC, Nitiss JL 2010. Yeast Tdp1 regulates the fidelity of non homologous end joining. Proceedings of the National Academy of Sciences, USA 107, 4057-4062.
2. Balestrazzi A, Confalonieri M, Macovei A., Carbonera D. 2011a. Seed imbibition in Medicago truncatula Gaertn.: expression profles of DNA repair genes in relation to PEG-mediated stress. Journal of Plant Physiology 168, 706-713.
3. Balestrazzi A, Confalonieri M, Macovei A., Donà M, Carbonera D. 2011b. Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity. Plant Cell Reports 30, 287-295.
4. Balestrazzi A, Locato V, Bottone M.G., De Gara L, Biggiogera M, Pellicciari C., Botti S, Di Gesù D, Donà M, Carbonera D. 2010. Response to UV-C radiation in topo I-deficient carrot cells with low ascorbate levels. Journal of Experimental Botany 61, 575-585.
5. Barthelmes HU, Habermeyer M, Christensen M.O., Mielke C., Interthal H, Pouliot JJ, Boege F, Marko D. 2004. TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerase I and II. Journal of Biological Chemistry 279, 55618-55625.
6. Bochman ML, Sabouri N, Zakian VA 2010. Unwinding the functions of the Pif1 family helicases. DNA Repair 9, 237-249.
7. Boubriak I, Polischuk V, Grodzinsky A., Osborne DJ 2007. Telomeres and seed banks. Cytology and Genomics 41, 18-24.
8. Boulon S, Westman BJ, Hutten S, Boisvert F-M, Lamond AI 2010. The nucleolus under stress. Molecular Cell 40, 216-227.
9. Breeze E, Harrison E, McHattie S., et al 2011. High-resolution temporal profling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. The Plant Cell 23, 873-894.
10. Callard D, Axelos M, Mazzolini L. 1996. Novel molecular markers for late phases of the growth cycle of Arabidopsis thaliana cell-suspension cultures are expressed during organ senescence. Plant Physiology 112, 705-715.
11. Cawthon RH. 2002. Telomere measurement by quantitative PCR. Nucleic Acids Research 15, e47.
12. Cisterna B, Biggiogera M. 2010. Ribosome biogenesis: from structure to dynamics. International Reviews of Cellular and Molecular Biology 284, 67-111.
13. Collins AR. 2004. The comet assay for DNA damage and repair. Molecular Biotechnology 26, 249-261.
14. Confalonieri M, Cammareri M, Biazzi E., Pecchia P, Fevereiro MPS, Balestrazzi A, Tava A, Conicella C. 2009. Enhanced triterpene sapogenin biosynthesis and root nodulation in transgenic barrel medic (Medicago truncatula Gaertn.) expressing a novelamyrin synthase (AsOXA1) gene. Plant Biotechnology Journal 7, 172-182.
15. De Michele R., Formentin E, Todesco M., Toppo S, Carimi F, Zottini M., Barizza E, Ferrarini A, Delledonne M, Fontana P. 2009. Transcriptome analysis of Medicago truncatula leaf senescence: similarities and differences in metabolic and transcriptional regulations as compared with Arabidopsis, nodule senescence and nitric oxide signalling. New Phytologist 181, 563-575.
16. Deng C, Brown JA, You D, Browm JM 2005. Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170, 591-600.
17. De Vos M., Schreiber V, Dantzer F. 2012. The diverse roles and clinical relevance of PARPs in DNA damage repair: current state of the art. Biochemical Pharmacology 84, 137-146.
18. Donati G, Montanaro L, Derenzini M. 2012. Ribosome biogenesis and control of cell proliferation: p53 is not alone. Cancer Research 72, 1602-1607.
19. Ferreyra MLF, Pezza A, Biarc J., Burlingame AL, Casati P. 2010. Plant L10 ribosomal proteins have different roles during developmental and translation under ultraviolet-B stress. Plant Physiology 153, 1878-1894.
20. Hamada T, Kurachi S, Kurachi K. 2010. Heterogeneous nuclear ribonucleoprotein A3 is the liver nuclear protein binding to age related increase element RNA of the Factor IX gene. PloS One 5, e12971.
21. He Y, Gan S. 2002. A gene encoding an acyl hydrolase is involved in leaf senescence in Arabidopsis. The Plant Cell 14, 805-815.
22. Hebeler R, Oeljeklaus S, Reidegeld K.A., et al 2008. Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14N/15N labeling and difference gel electrophoresis. Molecular Cell Proteomics 7, 108-120.
23. Huang PR, Hung SC, Wang TCV. 2010. Telomeric DNA-binding activities of heterogeneous nuclear ribonucleoprotein A3 in vitro and in vivo. Biochimica et Biophysica Acta 1803, 1164-1174.
24. Inamdar KV, Pouliot JJ, Zhou T, Lees-Miller SP, Rasouli-Nia A, Povirk LF 2002. Conversion of phosphoglycolate to phosphate termini on 3'-overhangs of DNA double strand breaks by the human tyrosyl-DNA phosphodiesterase hTdp1. Journal of Biological Chemistry 277, 27162-27168.
25. Interthal H, Pouliot JJ, Champoux JJ 2001. The tyrosyl-DNA phosphodiesterase Tdp1 is a member of the phospholipase D superfamily. Proceedings of the National Academy of Sciences, USA 98, 12009-12014.
26. Jin A, Itahana K, O'Keefe K, Zhang Y. 2004. Inhibition of HDM2 and activation of p53 by ribosomal protein L23. Molecular and Cellular Biology 24, 7669-7680.
27. Kang MR, Muller MJ, Chung IK 2004. Telomeric DNA damage by topoisomerase I. A possible mechanism for cell killing by camptothecin. Journal of Biological Chemistry 279, 12535-12541.
28. Kilian A, Stiff C, Kleinhofs A. 1995. Barley telomeres shorten during differentiation but grow in callus culture. Proceedings of the National Academy of Sciences, USA 92, 9555-9559.
29. Lebedeva NA, Rechkunova NI, Lavrik OI 2011. AP-site cleavage activity of tyrosyl-DNA phosphodiesterase. FEBS Letters 585, 683-686.
30. Lee S-Y, Kim H., Hwang H-J, Jeong Y-M, Na SH, Woo J-C, Kim S-G. 2010. Identification of tyrosyl-DNA phosphodiesterase as a novel DNA damage repair enzyme in Arabidopsis. Plant Physiology 154, 1460-1469.
31. Lotito L, Russo A, Chillemi G., Bueno S, Cavalieri D, Capranico G. 2008. Global transcription regulation by DNA topoisomerase I in exponentially growing Saccharomyces cerevisiae cells: activation of telomere-proximal genes by TOP1 deletion. Journal of Molecular Biology 377, 311-322.
32. Macovei A, Balestrazzi A, Confalonieri M., Carbonera D. 2010. The tyrosyl-DNA phosphodiesterase gene family in Medicago truncatula Gaertn.: bioinformatic investigation and expression profles in response to copper- and PEG-mediated stress. Planta 232, 303-407.
33. Menke M, Meister A, Schubert I. 2000. N-methyl-N-nitrosourea-induced DNA damage detected by the comet assay in Vicia faba nuclei during interphase stages is not restricted to chromatid aberration hotspots. Mutagenesis 15, 503-506.
34. Murai J, Huang SN, Das B.B., Dexheimer TS, Takeda S, Pommier Y. 2012. Tyrosyl-DNA phosphodiesterase I (TDP1) repairs DNA damages induced by topoisomerase I and II and base alkylation in vertebrate cells. Journal of Biological Chemistry 287, 12848-12857.
35. Nemeth A, Langst G. 2011. Genome organization in and around the nucleolus. Trends in Genetics 27, 149-156.
36. Nicot N, Hausman JF, Hoffmann L, Evers D. 2005. Housekeeping gene selection for realtime RT-PCR normalization in potato during biotic and abiotic stress. Journal of Experimental Botany 56, 2907-2914.
37. Pestov DG, Strezoska Z, Lan LF 2001. Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G(1)/S transition. Molecular and Cellular Biology 21, 4246-4255.
38. Preuss SB, Britt AB 2003. A DNA-damage-induced cell cycle checkpoint in Arabidopsis. Genetics 164, 323-334.
39. Sànchez-Pons N., Irar S, Garcìa-Muniz N, Vicient CM. 2011. Transcriptomic and proteomic profling of maize embryos exposed to camptothecin. BMC Plant Biology 11, 91.
40. Singh NP. 2000. A simple method for accurate estimation of apoptotic cells. Experimental Cell Research 256, 328-337.
41. Sprung CN, Li J, Hovan D., McKay MJ, Forrester HB 2011. Alternative transcript initiation and splicing as a response to DNA damage. PLoS One 10, e25758.
42. Thimm O, Blasing O, Gibon Y., Nagel A, Meyer S, Kruger P., Selbig J, Muller LA, Rhee SY, Stitt M. 2004. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914-939.
43. Trapnell C, Pachter L, Salzberg SL 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111.
44. Trapnell C, Williams BA, Pertea G, Mortazavi A., Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 516-520.
45. Ueno M. 2010. Roles of DNA repair proteins in telomere maintenance. Bioscience, Biotechnology, and Biochemistry 74, 1-6.
46. Valero J, Berciano MT, Wernaga E, Lafarga M., Alonso JR 2006. Pre-neurodegeneration of mitral cells in the pcd mutant mouse is associated with DNA damage, transcriptional repression, and reorganization of nucleolar speckles and Cajal bodies. Molecular and Cellular Neuroscience 33, 283-295.
47. Van Attikum H., Grasser SM 2005. The histone code at DNA breaks: a guide to repair? Nature Reviews 6, 757-765.
48. Vos SM, Tretter EM, Schmidt B.H., Berger JM 2011. All tangled up: how cells direct, manage and exploit topoisomerase function. Nature Reviews in Molecular and Cellular Biology 12, 827-841.
49. Whittle CA, Beardmore T, Johnston MO 2001. Is G1 arrest in plant seeds induced by a p53-related pathway? Trends in Plant Science 6, 248-251.