Overexpression of PDH45 or SUV3 helicases in rice leads to delayed leaf senescence-associated events

Protoplasma

Volumn 254, Issue 2, 2017, Pages 1103-1113

  Macovei, Anca ^a,b   Sahoo, Ranjan K ^a   Faè, Matteo ^b   Balestrazzi, Alma ^b   Carbonera, Daniela ^b   Tuteja, Narendra ^a,c  

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

^b UNIVERSITY OF PAVIA   (Italy)

^c AMITY UNIVERSITY   (India)

Author keywords

Pea DNA helicase 45 (PDH45); Rice; Senescence; Suppressor of Var1 3 gene (SUV3); Telomeres

Indexed keywords

CARBON DIOXIDE; CHLOROPHYLL; DNA HELICASE; PLANT DNA; PLANT PROTEIN; PROTEIN BINDING; TELOMERASE;

APOPTOSIS; COMPUTER SIMULATION; DOWN REGULATION; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMIC INSTABILITY; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORYZA; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PLANT STOMA; TELOMERE HOMEOSTASIS; TRANSGENIC PLANT; UPREGULATION;

APOPTOSIS; CARBON DIOXIDE; CHLOROPHYLL; COMPUTER SIMULATION; DNA HELICASES; DNA, PLANT; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOMIC INSTABILITY; ORYZA; PHOTOSYNTHESIS; PLANT LEAVES; PLANT PROTEINS; PLANT STOMATA; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; TELOMERASE; TELOMERE HOMEOSTASIS; UP-REGULATION;

EID: 84984852079     PISSN: 0033183X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00709-016-1017-4     Document Type: Article

References (49)

1. Amiard S, Charbonnel C, Allain E, Depeiges A, White CI, Gallego ME (2010) Distinct roles of the ATR kinase and the Mre11-Ras50-Nbs1 complex in the maintenance of chromosome stability in Arabidopsis. Plant Cell 22:3020–3033. doi:10.1105/tpc.110.078527
2. Amiard S, Da Inez O, Gallego ME, White CI (2014) Responses to telomere erosion in plants. PlosOne 9:e86220. doi:10.1371/journal.pone.0086220
3. Amin M, Elias SM, Hossain A, Ferdousi A, Rahman MS, Tuteja N, Seraj ZI (2012) Over-expression of a DEAD-box helicase, PDH45, confers both seedling and reproductive stage salinity tolerance to rice (Oryza sativa L.). Mol Breed 30:345–354. doi:10.1007/s11032-011-9625-3
4. Balestrazzi A, Donà M, Macove IA, Sabatini ME, Pagano A, Carbonera D (2015) DNA repair and telomere maintenance during seed imbibition: correlation of transcriptional patterns. Telomere Telomerase 2:e496. doi:10.14800/tt.496
5. Barefield C, Karlseder (2012) The BLM helicase contributes to telomere maintenance through processing of late-replication intermediate structures. Nucleic Acids Res 40(15):7358–7367. doi:10.1093/nar/gks407
6. Blasco MA, Lee H-W, Hande MP, Samper E, Lansdorp PM, DePinho RA, Greider CW (1997) Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25–34. doi:10.1016/S0092-8674(01)80006-4
7. Borrás L, Slafer GA, Otegui ME (2004) Seed dry weight response to source-sink manipulations in wheat, maize and soybean: a quantitative reappraisal. Field Crops Res 86:131–146
8. Cawthon RM (2002) Telomere measurement by quantitative PCR. Nucleic Acids Res 30(10):e47. doi:10.1093/nar/30.10.e47
9. Collins K (2006) The biogenesis and regulation of telomerase holoenzymes. Nat Rev Mol Cell Biol 7(7):484–494. doi:10.1038/nrm1961
10. Deng Y, Guo X, Ferguson DO, Chang S (2009) Multiple roles for MRE11 at uncapped telomeres. Nature 460:914–918. doi:10.1038/nature08196
11. Donà M, Confalonieri M, Minio A, Biggiogera M, Buttafava A, Raimondi E, Delledonne M, Ventura L, Sabatini ME, Macovei A, Giraffa G, Carbonera D, Balestrazzi A (2013) RNA-Seq analysis discloses early senescence and nucleolar dysfunction triggered by Tdp1α depletion in Medicago truncatula. J Exp Bot 64:1941–1951. doi:10.1093/jxb/ert063
12. Dvořáčková M, Fojtová M, Fajkus J (2015) Chromatin dynamics of plant telomeres and ribosomal genes. Plant J 83:18–37. doi:10.1111/tpj.12822
13. Fischer RA (2008) The importance of grain or kernel number in wheat: a reply to Sinclair and Jamieson. Filed Crops Res 105:15–21
14. Fitzgerald MS, McKnight TD, Shippen DE (1996) Characterization and developmental patterns of telomerase expression in plants. Proc Natl Acad Sci U S A 93(25):14422–1427
15. Fitzgerald MS, Riha K, Gao F, Ren S, McKnight TD, Shippen DE (1999) Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc Natl Acad Sci U S A 96:14813–1418
16. Gichner T, Mukherjee A, Wagner ED, Plewa MJ (2005) Evaluation of nuclear DNA diffusion assay to detect apoptosis and necrosis. Mutat Res 586:38–46. doi:10.1016/j.mrgentox.2005.05.010
17. Gill SS, Tajrishi M, Madan M, Tuteja N (2013) A DESD-box heliase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. PB1). Plant Mol Biol 82:1–22. doi:10.1007/s11103-013-0031-6
18. Gregersen PL, Culetic A, Boschiam L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622. doi:10.1007/s11103-013-0013-8
19. Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334. doi:10.1139/b79-163
20. Huang YJ, To KY, Yap MN, Chiang WJ, Suen DF, Chen SCG (2001) Cloning and characterization of leaf senescence up-regulated genes in sweet potato. Physiol Plant 113:384–391
21. Hug N, Lingner J (2006) Telomere length homeostasis. Chromosoma 115:413–425
22. Jing HC, Hille J, Dijkwel PP (2003) Aging in plants: conserved strategies and novel pathways. Plant Biol 5:455–464
23. Kakar K, Wandrey M, Czechowski T, Gaertner T, Scheible WR, Stitt M, Torres-Jerez I, Xiao Y, Redman JC, Wu H, Cheung F, Town CD, Udvardi MK (2008) A community resource for high-throughput quantitative RT-PCR analysis of transcription factor gene expression in Medicago truncatula. Plant Methods 4:18. doi:10.1186/1746-4811-4-18
24. Kong Z, Li M, Yang W, Xu W, Xue Y (2006) A novel nuclear-localized CCCH-type zinc finger protein, OsDOS, is involved in delaying leaf senescence in rice. Plant Physiol 141:1376–1388. doi:10.1104/pp.106.082941
25. Lee RH, Wang CH, Huang LT, Chen SCG (2001) Leaf senescence in rice plants: cloning and characterization of senescence up-regulated genes. J Exp Bot 52:1117–1121. doi:10.1093/jexbot/52.358.1117
26. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136. doi:10.1146/annurev.arplant.57.032905.105316
27. Liu X, Li Z, Jiang Z, Zhao Y, Peng J, Jin J, Guo H, Luo J (2011) LSD: a leaf senescence database. Nucleic Acids Res. doi:10.1093/nar/gkq1169
28. Macovei A, Garg B, Raikwar S, Balestrazzi A, Carbonera D, Buttafava A, Jiménez-Bermont JF, Gill SS, Tuteja N (2014) Synergistic exposure of rice seeds to different doses of γ-ray and salinity stress resulted in increased antioxidant enzyme activities and gene-specific modulation of TC-NER pathway. doi:10.1155/2014/676934
29. Malecki M, Jedrzejczak R, Stepien PP, Golik P (2007) In vitro reconstitution and characterization of the yeast mitochondrial degradosome complex unravels tight functional interdependence. J Mol Biol 372:23–36. doi:10.1016/j.jmb.2007.06.074
30. Maser RS, DePinho RA (2002) Connecting chromosomes, crisis, and cancer. Science 297:565–569
31. Mendez-Bermudez A, Hidalgo-Bravo A, Cotton VE, Gravani A, Jeyapalan JN, Royle NJ (2012) The roles of WRN and BLM RecQ helicases in the alternative lengthening of telomeres. Nucleic Acids Res 40:10809–10820. doi:10.1093/nar/gks862
32. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325. doi:10.1093/nar/8.19.4321
33. O’Brien IEW, Baguley BC, Murray BG, Morris BA, Ferguson IB (1998) Early stages of the apoptotic pathway in plant cells are reversible. Plant J 13:803–814
34. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucl Acid Res 9:336. doi:10.1093/nar/30.9.e36
35. Pham XH, Reddy MK, Ehtesham NZ, Matta B, Tuteja N (2000) A DNA helicase from Pisum sativum is homologous to translation initiation factor and stimulates topoisomerase I activity. Plant J 24:219–229. doi:10.1046/j.1365-313x.2000.00869.x
36. Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different models. J Exp Bot 58:435–444. doi:10.1093/jxb/erm258
37. Riha K, Fajkus J, Siroky J, Vyskot B (1998) Developmental control of telomere lengths and telomerase activity in plants. Plant Cell 10:1691–1698. doi:10.1105/tpc.10.10.1691
38. Riha K, McKnight TD, Griffing LR, Shippen DE (2001) Living with genome instability: plant responses to telomere dysfunction. Science 291:1797–1800. doi:10.1126/science.1057110
39. Sahoo RK, Gill SS, Tuteja N (2012) Pea DNA helicase 45 promotes salinity stress tolerance in IR64 rice with improved yield. Plant Sign Behav 7:1–5. doi:10.4161/psb.20915
40. Simeonova E, Sikora A, Charzynska M, Mostowaska A (2000) Aspects of programmed cell death during leaf senescence of mono- and dicotyledonous plants. Protoplasma 214:93–101
41. Singh NP, Muller CH, Berger RE (2003) Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil Steril 80:1420–1430. doi:10.1016/j.fertnstert.2003.04.002
42. Song H, Liu D, Li F, Lu H (2011) Season- and age-associated telomerase activity in Ginkgo biloba L. Mol Biol Rep 38:1799–1805. doi:10.1007/s11033-010-0295-8
43. Szczesny RJ, Borowski LS, Brzezniak LK, Dmochowska A, Gewartowski K, Bartnik E, Stepien PP (2010) Human mitochondrial RNA turnover caught in flagrant: involvement of hSuv3p helicase in RNA surveillance. Nucleic Acids Res 38:279–298. doi:10.1093/nar/gkp903
44. Tuteja N (2003) Plant DNA helicases: the long unwinding road. J Exp Bot 54:2201–2214. doi:10.1093/jxb/erg246
45. Tuteja N, Sahoo RK, Garg B, Tuteja R (2013) OsSUV3 dual helicase functions in salinity stress tolerance by maintaining photosynthesis and antioxidant machinery in rice (Oryza sativa L. cv. IR64). Plant J 76:115–127. doi:10.1111/tpj.12277
46. Van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761. doi:10.1093/jxb/err196
47. Waterworth WM, Drury GE, Bray CM, West CE (2011) Repairing breaks in the plant genome: the importance of keeping it together. New Phytol 192:805–822. doi:10.1111/j.1469-8137.2011.03926.x
48. Watson MJ, Riha K (2010) Comparative biology of telomeres: where plants stand. FEBS Lett 584:3752–3759. doi:10.1016/j.febslet.2010.06.017
49. Zellinger B, Riha K (2007) Composition of plant telomeres. Biochem Biophys Act 1769:399–409. doi:10.1016/j.bbaexp.2007.02.001