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Induced Tolerance to Salinity Stress by Halotolerant Bacteria Bacillus aryabhattai H19-1 and B. mesonae H20-5 in Tomato Plants

  • Yoo, Sung-Je (Division of Agricultural Microbiology, National Institute of Agricultural Science, Rural Development Administration) ;
  • Weon, Hang-Yeon (Division of Agricultural Microbiology, National Institute of Agricultural Science, Rural Development Administration) ;
  • Song, Jaekyeong (Division of Agricultural Microbiology, National Institute of Agricultural Science, Rural Development Administration) ;
  • Sang, Mee Kyung (Division of Agricultural Microbiology, National Institute of Agricultural Science, Rural Development Administration)
  • Received : 2019.04.15
  • Accepted : 2019.06.19
  • Published : 2019.07.28

Abstract

Salinity is one of the major abiotic stresses that cause reduction of plant growth and crop productivity. It has been reported that plant growth-promoting bacteria (PGPB) could confer abiotic stress tolerance to plants. In a previous study, we screened bacterial strains capable of enhancing plant health under abiotic stresses and identified these strains based on 16s rRNA sequencing analysis. In this study, we investigated the effects of two selected strains, Bacillus aryabhattai H19-1 and B. mesonae H20-5, on responses of tomato plants against salinity stress. As a result, they alleviated decrease in plant growth and chlorophyll content; only strain H19-1 increased carotenoid content compared to that in untreated plants under salinity stress. Strains H19-1 and H20-5 significantly decreased electrolyte leakage, whereas they increased $Ca^{2+}$ content compared to that in the untreated control. Our results also indicated that H20-5-treated plants accumulated significantly higher levels of proline, abscisic acid (ABA), and antioxidant enzyme activities compared to untreated and H19-1-treated plants during salinity stress. Moreover, strain H20-5 upregulated 9-cisepoxycarotenoid dioxygenase 1 (NCED1) and abscisic acid-response element-binding proteins 1 (AREB1) genes, otherwise strain H19-1 downregulated AREB1 in tomato plants after the salinity challenge. These findings demonstrated that strains H19-1 and H20-5 induced ABA-independent and -dependent salinity tolerance, respectively, in tomato plants, therefore these strains can be used as effective bio-fertilizers for sustainable agriculture.

Keywords

References

  1. Bano A, Fatima M. 2009. Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol. Fert. Soils 45: 405-413. https://doi.org/10.1007/s00374-008-0344-9
  2. Jha Y, Subramanian RB, Patel S. 2011. Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol. Plant. 33: 797-802. https://doi.org/10.1007/s11738-010-0604-9
  3. Munns R, Gilliham M. 2015. Salinity tolerance of crops - what is the cost? New Phytol. 208: 668-673. https://doi.org/10.1111/nph.13519
  4. Ruan CJ, da Silva JAT, Mopper S, Qin P, Lutts S. 2010. Halophyte improvement for a salinized world. Crit. Rev. Plant Sci. 29: 329-359. https://doi.org/10.1080/07352689.2010.524517
  5. Lakhdar A, Rabhi M, Ghnay a T, Montemurro F, Jedidi N, Abdelly C. 2009. Effectiveness of compost use in salt-affected soil. J. Hazard Mater. 171: 29-37. https://doi.org/10.1016/j.jhazmat.2009.05.132
  6. Tester M, Langridge P. 2010. Breeding technologies to increase crop production in a changing world. Science 327: 818-822. https://doi.org/10.1126/science.1183700
  7. Moreno-Limon S, Maiti RK, Nunez-Gonzalez A, Star JV, Foroughbakhch R, Gamez-Gonzalez H. 2000. Genotypic variability in bean cultivars (Phaseolus vulgaris L.) for resistance to salinity at the seedling stage. Ind. Agric. 44: 1-12.
  8. Mano Y, Takeda K. 2001. Genetic resources of salt tolerance at germination and the seedling stage in wheat. Jpn. J. Crop. Sci. 70: 215-220. https://doi.org/10.1626/jcs.70.215
  9. Athar H, Ashraf M. 2009. Strategies for crop improvement against salinity and drought stress: an overview. In Salinity and Water Stress. pp. 1-16: Springer.
  10. Li HW, Zang BS, Deng XW, Wang XP. 2011. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta 234: 1007-1018. https://doi.org/10.1007/s00425-011-1458-0
  11. Munoz-Mayor A, Pineda B, Garcia-Abellan JO, Anton T, Garcia-Sogo B, Sanchez-Bel P, et al. 2012. Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J. Plant Physiol. 169: 459-468. https://doi.org/10.1016/j.jplph.2011.11.018
  12. Chen L, Liu Y, Wu G, Veronican Njeri K, Shen Q, Zhang N, et al. 2016. Induced maize salt tolerance by rhizosphere inoculation of Bacillus amyloliquefaciens SQR9. Physiol. Plant. 158: 34-44. https://doi.org/10.1111/ppl.12441
  13. Bhardwaj D, Ansari MW, Sahoo RK, Tuteja N. 2014. Biofertilizers function as key player in sustainable agriculture by improving soil fertility, plant tolerance and crop productivity. Microb. Cell Fact. 13: 66. https://doi.org/10.1186/1475-2859-13-66
  14. Esitken A, Yildiz HE, Ercisli S, Donmez MF, Turan M, Gunes A. 2010. Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci. Hortic. 124: 62-66. https://doi.org/10.1016/j.scienta.2009.12.012
  15. Fernandez O, Theocharis A, Bordiec S, Feil R, Jacquens, L Clement C, et al. 2012. Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol. Plant Microbe Interact. 25: 496-504. https://doi.org/10.1094/MPMI-09-11-0245
  16. Jha Y, Subramanian RB. 2014. PGPR regulate caspase-like activity, programmed cell death, and antioxidant enzyme activity in paddy under salinity. Physiol. Mol. Biol. Plants 20: 201-207. https://doi.org/10.1007/s12298-014-0224-8
  17. Meena RK, Singh RK, Pal Singh N, Meena SK, Meena VS. 2015. Isolation of low temperature surviving plant growth - promoting rhizobacteria (PGPR) from pea (Pisum sativum L.) and documentation of their plant growth promoting traits. Biocatal. Agric. Biotechnol. 4: 806-811. https://doi.org/10.1016/j.bcab.2015.08.006
  18. Glick BR. 2014. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 169: 30-39. https://doi.org/10.1016/j.micres.2013.09.009
  19. Damodaran T, Sah V, Rai RB, Sharma DK, Mishra VK, Jha SK, et al. 2013. Isolation of salt tolerant endophytic and rhizospheric bacteria by natural selection and screening for promising plant growth-promoting rhizobacteria (PGPR) and growth vigour in tomato under sodic environment. Afr. J. Microbiol. Res. 7: 5082-5089.
  20. Qu L, Huang, Y, Zhu C, Zeng H, Shen C, Liu C, et al. 2015. Rhizobia-inoculation enhances the soybean's tolerance to salt stress. Plant Soil 400: 209-222. https://doi.org/10.1007/s11104-015-2728-6
  21. Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A. 2016. Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci. Rep. 6: 34768. https://doi.org/10.1038/srep34768
  22. Yang J, Kloepper JW, Ryu CM. 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14: 1-4. https://doi.org/10.1016/j.tplants.2008.10.004
  23. Sang MK, Dutta S, Park K. 2015. Influence of commercial antibiotics on biocontrol of soft rot and plant growth promotion in Chinese cabbages by Bacillus vallismortis EXTN-1 and BS07M. Res. Plant Dis. 21: 225-260.
  24. Polonenko DR, Mayfield CI, Dumbroff EB. 1981. Microbial responses to salt-induced osmotic stress. Plant Soil 59: 269-285. https://doi.org/10.1007/BF02184200
  25. Lichtenthaler HK. 1987. Chlorophyll fluorescence signatures of leaves during the autumnal chlorophyll breakdown. J. Plant Physiol. 131: 101-110. https://doi.org/10.1016/S0176-1617(87)80271-7
  26. Lutts S, Kinet JM, Bouharmont J. 1996. NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann. Bot. 78: 389-398. https://doi.org/10.1006/anbo.1996.0134
  27. Shukla PS, Agarwal PK, Jha B. 2012. Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul. 31: 195-206. https://doi.org/10.1007/s00344-011-9231-y
  28. Iseki K, Marubodee R, Ehara H, Tomooka N. 2017. A rapid quantification method for tissue $Na^+$ and $K^+$ concentrations in salt-tolerant and susceptible accessions in Vigna vexillata (L.) A. Rich. Plant Prod. Sci. 20: 144-148. https://doi.org/10.1080/1343943X.2016.1251826
  29. Bates LS, Waldren RP, Teare I. 1973. Rapid determination of free proline for water-stress studies. Plant Soil 39: 205-207. https://doi.org/10.1007/BF00018060
  30. Yemm EW, Willis AJ. 1954. The estimation of carbohydrates in plant extracts by anthrone. Biochem. J. 57: 508-514. https://doi.org/10.1042/bj0570508
  31. Chen Z, Cuin TA, Zhou M, Twomey A, Naidu BP, Shabala S. 2007. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance. J. Exp. Bot. 58: 4245-4255. https://doi.org/10.1093/jxb/erm284
  32. Iovieno P, Punzo P, Guida G, Mistretta C, Van Oosten MJ, Nurcato R, et al. 2016. Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front. Plant Sci. 7: 371.
  33. Lovdal T, Lillo C. 2009. Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Anal. Biochem. 387: 238-242. https://doi.org/10.1016/j.ab.2009.01.024
  34. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  35. Halo BA, Khan AL, Waqas M, Al-Harrasi A, Hussain J, Ali L, et al. 2015. Endophytic bacteria (Sphingomonas sp. LK11) and gibberellin can improve Solanum lycopersicum growth and oxidative stress under salinity. J. Plant Interact. 10: 117-125. https://doi.org/10.1080/17429145.2015.1033659
  36. Chatterjee P, Samaddar S, Anandham R, Kang Y, Kim K, Selvakumar G, et al. 2017. Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front. Plant Sci. 8: 705. https://doi.org/10.3389/fpls.2017.00705
  37. Yoo SJ, Shin DJ, Weon HY, Song J, Sang MK. 2018. Selection of bacteria for enhancement of tolerance to salinity and temperature stresses in tomato plants. Korean J. Org. Agric. 26: 463-475. https://doi.org/10.11625/KJOA.2018.26.3.463
  38. Turan S, Tripathy BC. 2015. Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiol. Plant. 153: 477-491. https://doi.org/10.1111/ppl.12250
  39. Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, et al. 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 38: 102. https://doi.org/10.1007/s11738-016-2113-y
  40. Amirjani MR. 2011. Effect of salinity stress on growth, sugar content, pigments and enzyme activity of rice. Int. J. Bot. 7: 73-81. https://doi.org/10.3923/ijb.2011.73.81
  41. Ruiz-Sola MA, Arbona V, Gomez-Cadenas A, Rodriguez-Concepcion M, Rodriguez-Villalon A. 2014. A root specific induction of carotenoid biosynthesis contributes to ABA production upon salt stress in Arabidopsis. PLoS One 9: e90765. https://doi.org/10.1371/journal.pone.0090765
  42. Baha N, Bekki A. 2015. An approach of improving plant salt tolerance of Lucerne (Medicago sativa) grown under salt stress: use of Bio-inoculants. J. Plant Growth. Regul. 34: 169-182. https://doi.org/10.1007/s00344-014-9455-8
  43. Sukweenadhi J, Balusamy SR, Kim YJ, Lee CH, Kim YJ, Koh SC, et al. 2018. A growth-promoting bacteria, Paenibacillus yonginensis DCY84T enhanced salt stress tolerance by activating defense-related systems in Panax ginseng. Front. Plant Sci. 9: 813. https://doi.org/10.3389/fpls.2018.00813
  44. Bajji M, Kinet JM, Lutts S. 2001. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regul. 36: 61-70. https://doi.org/10.1023/A:1014732714549
  45. Demidchik V, Straltsova D, Medvedev SS, Pozhvanov GA, Sokolik A, Yurin V. 2014. Stress-induced electrolyte leakage: the role of $K^+$-permeable channels and involvement in programmed cell death and metabolic adjustment. J. Exp. Bot. 65: 1259-1270. https://doi.org/10.1093/jxb/eru004
  46. El-Esawi MA, Alaraidh IA, Alsahli AA, Alzahrani SM, Ali HM, Alayafi AA, et al. 2018. Serratia liquefaciens KM4 improves salt stress tolerance in maize by regulating redox potential, ion homeostasis, leaf gas exchange and stress-related gene expression. Int. J. Mol. Sci. 19(11): pii.3310.
  47. Rabhi NEH, Silini A, Cherif-Silini H, Yahiaoui B, Lekired A, Robineau M, et al. 2018. Pseudomonas knackmussii MLR6, a rhizospheric strain isolated from halophyte, enhances salt tolerance in Arabidopsis thaliana. J. Appl. Microbiol. 125: 1836-1851. https://doi.org/10.1111/jam.14082
  48. Sapre S, Gontia-Mishra I, Tiwari S. 2018. Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol. Res. 206: 25-32. https://doi.org/10.1016/j.micres.2017.09.009
  49. Singh RP, Jha P, Jha PN. 2015. The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J. Plant physiol. 184: 57-67. https://doi.org/10.1016/j.jplph.2015.07.002
  50. Sharma S, Kulkarni J, Jha B. 2016. Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Front. Microbiol. 7: 1600.
  51. Shabala S, Shabala S, Cuin TA, Pang J, Percey W, Chen Z, et al. 2010. Xylem ionic relations and salinity tolerance in barley. Plant J. 61: 839-853. https://doi.org/10.1111/j.1365-313X.2009.04110.x
  52. Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, et al. 2007. SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19: 1415-1431. https://doi.org/10.1105/tpc.106.042291
  53. Ranty B, Aldon D, Cotelle V, Galaud JP, Thuleau P, Mazars C. 2016. Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. Front. Plant Sci. 7: 327.
  54. Nayyar H. 2003. Variation in osmoregulation in differentially drought-sensitive wheat genotypes involves calcium. Biol. Plant. 47: 541-547. https://doi.org/10.1023/B:BIOP.0000041059.10703.11
  55. Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, et al. 2013. Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One 8: e62085. https://doi.org/10.1371/journal.pone.0062085
  56. Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, et al. 2015. Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol. Biochem. 94: 104-113. https://doi.org/10.1016/j.plaphy.2015.05.014
  57. Li H, Lei P, Pang X, Li S, Xu H, Xu Z, et al. 2017. Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl. Soil Ecol. 119: 26-34. https://doi.org/10.1016/j.apsoil.2017.05.033
  58. Upadhyay SK, Singh JS, Saxena AK, Singh DP. 2012. Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biol. 14: 605-611. https://doi.org/10.1111/j.1438-8677.2011.00533.x
  59. Kerepesi I, Galiba G. 2000. Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop. Sci. 40: 482-487. https://doi.org/10.2135/cropsci2000.402482x
  60. Singh RP, Jha PN. 2016. A halotolerant bacterium Bacillus licheniformis HSW-16 augments induced systemic tolerance to salt stress in wheat plant (Triticum aestivum). Front. Plant Sci. 7: 1890.
  61. Das K and Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front. Environ. Sci. 2.
  62. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 59: 651-681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
  63. Hussain S, Khaliq A, Matloob A, Wahid MA, Afzal I. 2013. Germination and growth response of three wheat cultivars to NaCl salinity. Soil Environ. 32: 36-43.
  64. Azevedo-Neto AD, Prisco JT, Eneas-Filho J, de Abreu CEB, Gomes-Filho E. 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot. 56: 87-94. https://doi.org/10.1016/j.envexpbot.2005.01.008
  65. Islam F, Yasmeen T, Arif MS, Ali S, Ali B, Hameed S, et al. 2016. Plant growth promoting bacteria confer salt tolerance in Vigna radiata by up-regulating antioxidant defense and biological soil fertility. Plant Growth Regul. 80: 23-36. https://doi.org/10.1007/s10725-015-0142-y
  66. Akram MS, Shahid M, Tariq M, Azeem M, Javed MT, Saleem S, et al. 2016. Deciphering Staphylococcus sciuri SAT-17 mediated anti-oxidative defense mechanisms and growth modulations in salt stressed maize (Zea mays L.). Front. Microbiol. 7: 867.
  67. Shi H, Zhu JK. 2002. Regulation of expression of the vacuolar $Na^+/H^+$ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol. Biol. 50: 543-550. https://doi.org/10.1023/A:1019859319617
  68. Saavedra X, Modrego A, Rodriguez D, Gonzalez-Garcia MP, Sanz L, Nicolas G, et al. 2010. The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol. 152: 133-150. https://doi.org/10.1104/pp.109.146381
  69. Gomez-Cadenas A, Arbona V, Jacas J, Primo-Millo E, Talon M. 2003. Abscisic acid reduces leaf abscission and increases salt tolerance in citrus plants. J. Plant Growth Regul. 21: 234-240. https://doi.org/10.1007/s00344-002-0013-4
  70. Yoshida R, Umezawa T, Mizoguchi T, Takahashi S, Takahashi F, Shinozaki K. 2006. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis. J. Biol. Chem. 281: 5310-5318. https://doi.org/10.1074/jbc.M509820200
  71. Naz R, Bano A. 2015. Molecular and physiological responses of sunflower (Helianthus annuus L.) to PGPR and SA under salt stress. Pak. J. Bot. 47: 35-42.
  72. Zhou C, Zhu L, Xie,Y, Li F, Xiao X, Ma Z, et al. 2017. Bacillus licheniformis SA03 confers increased saline-alkaline tolerance in chrysanthemum plants by induction of abscisic acid accumulation. Front. Plant Sci. 8: 1143. https://doi.org/10.3389/fpls.2017.01143
  73. Sun L, Sun Y, Zhang M, Wang L, Ren J, Cui M, et al. 2012. Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiol. 158: 283-298. https://doi.org/10.1104/pp.111.186866
  74. Iuchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K. 2000. A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol. 123: 553-562. https://doi.org/10.1104/pp.123.2.553
  75. Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, et al. 2000. Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J. 23: 363-374. https://doi.org/10.1046/j.1365-313x.2000.00789.x
  76. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. USA 97: 11632-11637. https://doi.org/10.1073/pnas.190309197
  77. Yanez M, Caceres S, Orellana S, Bastias A, Verdugo I, Ruiz-Lara S, et al. 2009. An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep. 28: 1497-1507. https://doi.org/10.1007/s00299-009-0749-4
  78. Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT. 2010. A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231: 1459-1473. https://doi.org/10.1007/s00425-010-1147-4
  79. Orellana S, Yanez M, Espinoza A, Verdugo I, Gonzalez E, Ruiz-Lara S, et al. 2010. The transcription factor SlAREB1 confers drought, salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant cell Environ. 33: 2191-2208. https://doi.org/10.1111/j.1365-3040.2010.02220.x

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