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Endophytic diazotrophic bacteria mitigate water deprivation effects in pineapple explants during acclimatization

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Abstract

We examined physiological and growth promotion traits in water-deprived pineapple explants inoculated with two endophytic diazotrophic bacteria. The following questions were addressed: (i) Is the root inoculation efficient to increase bacteria population associated to pineapple explants? (ii) Are nutrient concentrations improved in pineapple explants in response to endophytic bacteria inoculation? (iii) Can endophytic bacteria improve pineapple explants’ growth and photosynthesis? (iv) Is it possible to mitigate water deprivation negative effects and facilitate pineapple explants’ acclimatization using endophytic diazotrophic bacteria? Pineapple ‘Vitória’ explants grown in vitro were inoculated with two different bacteria species. Therefore, 10 mL of bacteria suspension (108 cells mL−1) of either Burkholderia silvatlantica strain UENF 117111 or Herbaspirillum seropedicae strain HRC54 were applied in the substrate after transplantation. Uninoculated explants received 10 mL of autoclaved DYGS liquid medium (Control treatment). These treatments were subdivided in two water regimes, so that explants were either full-irrigated (FI) or non-irrigated (NI) for 24 days. Thereafter, NI explants were re-irrigated to saturation for two days. We found that: (i) The inoculation was efficient to increase bacteria associated to the plantlets; (ii) Nutrient concentrations were not improved in pineapple explants inoculated with both bacteria species; (iii) B. silvatlantica did not change both growth and photosynthetic capacity of the explants. Nonetheless, H. seropedicae inoculation caused negative effects on growth, whereas Anet was increased; (iv) The use of both bacteria delayed water deprivation effects and maintained the photosynthetic capacity through C3 metabolism intact for longer periods under water deprivation, as well as by recovering Anet after re-irrigation.

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Abbreviations

δ13C:

Carbon isotope composition

Anet :

Net photosynthetic rate

Anet/E:

Water use efficiency

Anet/gs :

Intrinsic water use efficiency

CAM:

Crassulacean acid metabolism

DAIS:

Days after irrigation suspension

E:

Transpiration rates

FI:

Full-irrigated

Fv/Fm :

Maximum quantum yield of primary photochemistry

gs :

Stomatal conductance

NI:

Non-irrigated

PI:

Performance index

PPFD:

Photosynthetic photon flux density

PSII:

Photosystem II

SE:

Standard error

VPD:

Air vapor pressure deficit

References

  • Aguiar N, Medici L, Olivares F, Dobbss L, Torres-Netto A, Silva S, Novotny E, Canellas L (2016) Metabolic profile and antioxidant responses during drought stress recovery in sugarcane treated with humic acids and endophytic diazotrophic bacteria. Ann Appl Biol 168:203–213

    CAS  Google Scholar 

  • Albany NR, Vilchez JA, Garcia L, Jimenez E (2005) Comparative study of morphological parameters of Grand Nain banana (Musa AAA) after in vitro multiplication with growth retardants. Plant Cell Tissue Org Cult 83:357–361

    Google Scholar 

  • Aranjuelo I, Cabrera-Bosquet L, Mottaleb SA, Araus JL, Nogues S (2009) 13C/12C isotope labeling to study carbon partitioning and dark respiration in cereals subjected to water stress. Rapid Commun Mass Spectrom 23:2819–2828

    CAS  PubMed  Google Scholar 

  • Ait Barka E, Belarbi A, Hachet C, Nowak J, Audran JC (2000) Enhancement of in vitro growth and resistance to gray mould of Vitis vinifera co-cultured with plant growth-promoting rhizobacteria. FEMS Microbiol Lett 186:91–95

    Google Scholar 

  • Antony E, Taybi T, Courbot MIC, Smith JAC, Borland AM (2008) Cloning, localization and expression analysis of vacuolar sugar transporters in the CAM plant Ananas comosus (pineapple). J Exp Bot 59(7):1895–1908

    CAS  PubMed  Google Scholar 

  • Aragón C, Carvalho L, González J, Escalona M, Amancio S (2012) The physiology of ex vitro pineapple (Ananas comosus L. Merr. var MD-2) as CAM or C3 is regulated by the environmental conditions. Plant Cell Rep 31:757–769

    PubMed  Google Scholar 

  • Baldani JI, Caruso L, Baldani VLD, Goi SR, Döbereiner J (1997) Recent advances in BNF with non-legume plants. Soil Biol Biochem 29:911–922

    CAS  Google Scholar 

  • Baldani VLD, Baldani JI, Döbereiner J (2000) Inoculation of rice plants with the endophytic diazotrophs Herbapirillum seropedicae and Burkholderia spp. Biol Fert Soils 30:485–491

    Google Scholar 

  • Baldotto LEB, Baldotto MA, Canellas LP, Bressan-Smith R, Olivares FL (2010a) Growth promotion of pineapple ‘Vitória’ by humic acids and Burkholderia spp. during acclimatization. Rev Bras Cienc Solo 34:1593–1600

    CAS  Google Scholar 

  • Baldotto LEB, Baldotto MA, Olivares FL, Viana AP, Bressan-Smith R (2010b) Seleção de bactérias promotoras de crescimento no abacaxizeiro cultivar Vitória durante a aclimatização. Rev Bras Cienc Solo 34:349–360

    CAS  Google Scholar 

  • Barboza SBSC, Graciano-Ribeiro D, Teixeira JB, Portes TA, Souza LAC (2006) Anatomia foliar de plantas micropropagadas de abacaxi. Pesq Agropec Bras 41:185–194

    Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    CAS  PubMed  Google Scholar 

  • Belimov AA, Dodd IC, Hontzeas N, Theobald JC, Safronova VI, Davies WJ (2009) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signalling. New Phytol 181:413–423

    CAS  PubMed  Google Scholar 

  • Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertilizer for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209

    CAS  PubMed  Google Scholar 

  • Biswas B, Gresshoff PM (2014) The role of symbiotic nitrogen fixation in sustainable production of biofuels. Int J Mol Sci 15:7380–7397

    PubMed  PubMed Central  Google Scholar 

  • Campostrini E, Otoni WC (1996) Aclimatização de plantas: abordagens recentes. Embrapa-CNPH, Brasília

    Google Scholar 

  • Canellas LP, Balmori DM, Médici LO, Aguiar NO, Campostrini E, Rosa RCC, Façanha AR, Olivares FL (2012) A combination of humic substances and Herbaspirillum seropedicae inoculation enhances the growth of maize (Zea mays L.). Plant Soil 366:119–132

    Google Scholar 

  • Cassells AC, Walsh C (1994) The influence of gas permeability of the culture lid on calcium uptake and stomatal function in Dianthus microplants. Plant Cell Tissue Org Cult 37:171–178

    Google Scholar 

  • Ceusters N, Valcke R, Frans M, Claes JE, Ende WV, Ceusters J (2019) Performance index and PSII connectivity under drought and contrasting light regimes in the CAM Orchid Phalaenopsis. Front Plant Sci 10:1012

    PubMed  PubMed Central  Google Scholar 

  • Chen C (2016) Cost analysis of plant micropropagation of Phalaenopsis. Plant Cell Tissue Organ Cult 126:167

    Google Scholar 

  • Chen H-Y, Liu J, Pan C, Yu J-W, Wang Q-C (2018) In vitro regeneration of adventitious buds from leaf explants and their subsequent cryopreservation in Highbush blueberry. Plant Cell Tissue Organ Cult 134(2):193–204

    CAS  Google Scholar 

  • Conceição PM, Vieira HD, Canellas LP, Marques Júnior RB, Olivares FL (2008) Recobrimento de sementes de milho com ácidos húmicos e bactérias diazotróficas endofíticas. Nota Científica. Pesqui Agropecu Bras 43:545–548

    Google Scholar 

  • Couto TR, Silva JR, Torres Netto A, Carvelho VS, Campostrini E (2014) Eficiência fotossintética e crescimento de genótipos de abacaxizeiro cultivados in vitro em diferentes qualidades de luz, tipos de frasco de cultivo e concentrações de sacarose. Rev Bras Frutic 36(2):459–466

    Google Scholar 

  • Cui YY, Hahn EJ, Kozai T, Paek KY (2000) Number of air exchanges, sucrose concentration, photosynthetic photon flux, and differences in photoperiod and dark period temperatures affect growth of Rehmannia glutinosa plantlets in vitro. Plant Cell Tissue Org Cult 62:219–226

    CAS  Google Scholar 

  • Deb CR, Imchen T (2010) An effective in vitro hardening technique of tissue culture raised plants. Biotechnology 9(1):79–83

    Google Scholar 

  • Desjardins Y, Dubuc J-F, Badr A (2009) In vitro culture of plants: a stressful activity! Acta Hort 812:29–50

    CAS  Google Scholar 

  • Dimkpa C, Wein T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    CAS  PubMed  Google Scholar 

  • Döbereiner J, Andrade VO, Baldani VLD (1999) Protocolos para Preparo de Meios de Cultura da Embrapa Agrobiologia. Embrapa Agrobiologia, Seropédica

    Google Scholar 

  • Döbereiner J, Da JM (1995) Associative symbioses in tropical grasses: characterization of microorganisms and nitrogen-fixing sites. In: International Symposium on nitrogen fixation, Pullman. p 39.

  • El-Sherif NA (2018) Impact of plant tissue culture on agricultural sustainability. In: Negm A, Abu-hashim M (eds) Sustainability of agricultural environment in Egypt: Part II. The Handbook of environmental chemistry, vol 77. Springer, Cham

    Google Scholar 

  • EMBRAPA (2009) Manual de análises químicas de solos, plantas e fertilizantes, 2nd edn. Revista e Ampliada, Brasília

    Google Scholar 

  • FAOSTAT (2016) FAO data for agriculture: statistics database: https://faostat.fao.org/ faostat/collections?version=extandhasbulk=0andsubset=agricul-ture. Accessed 1 May 2018

  • Flexas J, Bota J, Galmés J, Medrano H, Ribas-Carbo M (2006) Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress. Physiol Planta 127:343–352

    CAS  Google Scholar 

  • Freschi L, Rodrigues MA, Domingues DS, Purgatto E, Sluys MA, Magalhães JR, Kaiser WM, Mercier H (2010) Nitric oxide mediates the hormonal control of crassulacean acid metabolism expression in young pineapple plants. Plant Physiol 154(4):1971–1985

    Google Scholar 

  • Fuchigami LH, Cheng TY, Soeldner A (1981) Abaxial transpiration and water loss in aseptically cultured plum. J Am Soc Hortic Sci 106:519–522

    Google Scholar 

  • Gonçalves S, Martins N, Romano A (2017) Physiological traits and oxidative stress markers during acclimatization of micropropagated plants from two endangered Plantago species: P. algarbiensis Samp. and P. almogravensis Franco. In Vitro Cell Dev Biol Plant 53:249

    Google Scholar 

  • González-Olmedo JL, Fundora Z, Molina LA, Abdulnor J, Desjardins Y, Escalona M (2005) New contributions to propagation of pineapple (Ananas comosus L. Merr.). Vitro Cell Dev B 47:87–90

    Google Scholar 

  • Guo Y-X, Zhao Y-Y, Zhang M, Zhang L-Y (2019) Development of a novel in vitro rooting culture system for the micropropagation of highbush blueberry (Vaccinium corymbosum) seedlings. Plant Cell Tissue Org 139:615–620

    CAS  Google Scholar 

  • Han HS, Lee KD (2005) Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil salinity. Res J Agric Biol Sci 1(3):210–215

    Google Scholar 

  • Honda H, Liu C, Kobayashi T (2003) Large-scale plant micropropagation. In: Sheper T, Zhong JJ (eds) Advances in biochemical engineering biotechnology, vol 50. Springer, Berlin, pp 158–181

    Google Scholar 

  • Houllou-Kido LM, Silva KS, Rivas R, Dias ALF, Alves GD (2009) Viability of Noppalea cochenilifera (cv. IPA Sertania) photoautotrophic micropropagation. Acta Hortic 811:309–313

    CAS  Google Scholar 

  • Jackson ML (1965) Soil chemical analysis. Prentice Hall, New Jersey, p 498

    Google Scholar 

  • James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivares FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth promoting bacterium Herbaspirillum seropedicae Z67. Mol Plant Microb Interact 15:894–906

    CAS  Google Scholar 

  • Jiang F, Hartung W (2008) Long-distance signalling of abscisic acid (ABA): the factors regulating the intensity of the ABA signal. J Exp Bot 59:37–43

    CAS  PubMed  Google Scholar 

  • Jones HG (1992) Plant and microclimate: A quantitative approach to environmental plant physiology, vol 3. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Jones JB Jr, Wolf B, Mills HA (1991) Plant Analysis Handbook: a practical sampling, preparation, analysis, and interpretation guide. Micro-Macro Publishing, Athens, p 213

    Google Scholar 

  • Kirchhof G, Reis VM, Baldani JI, Eckert B, Döbereiner J, Hartmann A (1997) Occurrence, physiological and molecular analysis of endophytic diazotrophic bacteria in gramineous energy plants. Plant Soil 194:45–55

    CAS  Google Scholar 

  • Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 370:773–787

    Google Scholar 

  • Lüttge U (2008) Physiological ecology of tropical plants. Springer, Berlin

    Google Scholar 

  • Malavolta E, Vitti GC, Oliveira SA (1997) Avaliação do estado nutricional das plantas: princípios e aplicações, 2nd edn. Piracicaba, POTAFOS, p 319

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and biossays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Oakes AD, Desmarais T, Powell WA, Maynard CA (2016) Improving rooting and shoot tip survival of micropropagated transgenic American chestnut shoots. HortScience 51(2):171–176

    Google Scholar 

  • Olivares FL, Baldani VLD, Reis VM, Baldani JI, Döbereiner J (1996) Occurrence of the endophytic diazotrophs Herbaspirillum spp. in roots, stems and leaves predominantly of Gramineae. Biol Fertil Soils 21:197–200

    Google Scholar 

  • Olivares FL, James EK, Baldani JI, Döbereiner J (1997) Infection of mottled stripe disease-susceptible and resistant sugar cane varieties by the endophytic diazotroph Herbaspirillum. New Phytol 135:723–737

    Google Scholar 

  • Onofre-Lemus J, Hernández-Lucas I, Girard L, Caballero-Mellado J (2009) ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl Environ Microb 50(20):6581–6590

    Google Scholar 

  • Preece JE, Sutter E (1991) Acclimatization of micropropaget plants to the greenhouse and field. In: Debergh PC, Zimmerman RH (eds) Micropropagation: technology and application. Springer, Netherlands, pp 71–94

    Google Scholar 

  • Radwan TEE, Mohanmed ZK, Reis VM (2005) Aeração e adição de sais na produção de ácido indol acético por bactérias diazotróficas. Pesq Agropec Bras 40:997–1004

    Google Scholar 

  • Rangjaroen C, Rerkasem B, Teaumroong N, Noisangiam R, Lumyong S (2015) Promoting plant growth in a commercial rice cultivar by endophytic diazotrophic bacteria isolated from rice landraces. Ann Microbiol 65(1):253–266

    CAS  Google Scholar 

  • Salazar-Parra C, Aranjuelo I, Pascual I, Erice G, Sanz-Sáez A, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Araus JL, Morales F (2015) Carbon balance, partitioning and photosynthetic acclimation in fruit-bearing grapevine (Vitis vinifera L. cv. Tempranillo) grown under simulated climate change (elevated CO2, elevated temperature and moderate drought) scenarios in temperature gradient greenhouses. J. Plant Physiol 174:97–109

    CAS  PubMed  Google Scholar 

  • Santi C, Bogusz D, Franche C (2013) Biological nitrogen fixation in non-legume plants. Ann Bot 111:743–767

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37

    CAS  PubMed  Google Scholar 

  • Shu S, Guo SR, Sun J, Yuan LY (2012) Effects of salt stress on the structure and function of the photosynthetic apparatus in Cucumis sativus and its protection by exogenous putrescine. Physiol Plant 146:285–296

    CAS  PubMed  Google Scholar 

  • Smith MK, Ko LH, Hamill SD, Sanewski GM, Graham MW (2003) Biotechnology. In: Bartholomew D, Rohrback K, Paull RE (eds) The pineapple: botany, production e uses. International CAB, Australia, pp 57–68

    Google Scholar 

  • Souza FVD, Souza AS, Santos-Serejo JA, Souza EH, Junghans TG, Silva MJ (2009) Micropropagação do Abacaxizeiro e Outras Bromeliáceas. In: Junghans TG, Souza AS (eds) Aspectos Práticos da Micropropagação de Plantas. Embrapa Mandioca e Fruticultura Tropical, Cruz das Almas, pp 177–206

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pather U, Mohanly P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. CRC Press, Ohio, pp 445–483

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, p 321–362

    Google Scholar 

  • Sulieman S (2011) Does GABA increase the efficiency of symbiotic N2 fixation in legumes? Plant Signal Behav 6:32–36

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sutter EG, Hutzell M (1984) Use of humidity tents and antitranspirants in the acclimatization to tissue-cultured plants to the greenhouse. Sci Hortic Amsterdam 23(4):303–312

    Google Scholar 

  • Tegeder M, Masclaux-Daubresse C (2017) Source and sink mechanisms of nitrogen transport and use. New Phytol 217:35–53

    PubMed  Google Scholar 

  • Tombesi S, Nardini A, Frioni T, Soccolini M, Zadra C, Farinelli D, Poni S, Palliotti A (2015) Stomatal closure is induced by hydraulic signals and maintained by ABA in drought-stressed grapevine. Sci Rep 5:1–12

    Google Scholar 

  • Vaz J, Sharma PK (2011) Relationship between xanthophyll cycle and non-photochemical quenching in rice (Oryza sativa L.) plants in response to light stress. Indian J Exp Bot 49:60–67

    Google Scholar 

  • Wetzstein H, Sommer HE (1982) Leaf anatomy of tissue-cultured Liquidambar styraciflua (hamamelidaceae) during acclimatization. Am J Bot 69:1579–1586

    Google Scholar 

  • Winter K, Holtum JAM (2002) How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiol 129:1843–1851

    CAS  PubMed  PubMed Central  Google Scholar 

  • Winter K, Garcia M, Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoe, and Opuntia. J Exp Bot 59:1829–1840

    CAS  PubMed  Google Scholar 

  • Xiao Y, Kozai T (2006) In vitro multiplication of statice plantlet using sugar-free media. Sci Hortic Amsterdam 109(1):71–77

    CAS  Google Scholar 

  • Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agric Res 56:715–721

    Google Scholar 

  • Zawoznik MS, Ameneiros M, Benavides MP, Vázquez S, Groppa MD (2011) Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings. Appl Microb Cell Physiol 90(4):1389–1397

    CAS  Google Scholar 

  • Zhang M, Zhao D, Ma Z, Li X, Xiao Y (2009) Growth and photosynthethetic capability of Momordica grosvenori plantlets grown photoautotrophically in response to light intensity. HortScience 44:757–763

    Google Scholar 

  • Zhu J, Bartholomew D, Goldstein G (1997) Effect of elevated carbon dioxide on the growth and physiological responses of pineapple, a species with Crassulacean acid metabolism. J Am Soc Hortic Sci 122:233–237

    CAS  Google Scholar 

  • Zlatev Z (2009) Drought-induced changes in chlorophyll fluorescence of young wheat plant. Biotechnology 23:437–441

    Google Scholar 

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Acknowledgements

The authors acknowledge Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação Carlos Chagas de Apoio à Pesquisa do Estado do Rio de Janeiro (FAPERJ). We thank Laboratório de Biotecnologia BioMudas for providing us with the explants, and Prof. Carlos Eduardo Rezende for carbon isotope analyses.

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Authors and Affiliations

  1. Centro de Citricultura Sylvio Moreira, Instituto Agronômico, Rodovia Anhanguera, km 158, Cordeirópolis, São Paulo, 13490-970, Brazil

    Jefferson Rangel da Silva

  2. Departamento de Engenharia Sanitária e Meio Ambiente, Universidade Estadual do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

    Alena Torres Netto

  3. Laboratório de Biologia Celular e Tecidual, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil

    Bruna Pintor de Medeiros, Marcus Vinícius Souza Silva & Fábio Lopes Olivares

  4. LMGV, Centro de Ciências e Tecnologias Agropecuárias, Setor de Fisiologia Vegetal, Universidade Estadual Do Norte Fluminense, Campos dos Goytacazes, Rio de Janeiro, Brazil

    Bruna Corrêa da Silva de Deus & Eliemar Campostrini

  5. Laboratório de Ciências Ambientais e Biodiversidade, Departamento de Zootecnia, Univ. Estadual do Maranhão (UEMA), Cidade Universitária Paulo VI, São Luís, MA, 1000, Brazil

    Tiago Massi Ferraz

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  1. Jefferson Rangel da Silva
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da Silva, J.R., Netto, A.T., de Medeiros, B.P. et al. Endophytic diazotrophic bacteria mitigate water deprivation effects in pineapple explants during acclimatization. Theor. Exp. Plant Physiol. 32, 63–77 (2020). https://doi.org/10.1007/s40626-020-00168-9

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