Abstract
Key message
The inoculation of seeds from neotropical tree species with PGPB revealed an active role of inoculant strains in modulating the germination and physiology of seedlings, although the specific responses were subject to specific plant–bacteria and genotype–genotype combinations.
Abstract
Beneficial microbial species encompass different phylogenetic groups, and growth-promoting mechanisms can be direct (nutritional effects) or indirect (resistance against biotic and abiotic stresses). Seed inoculation with plant growth-promoting bacteria (PGPB) can increase the growth and productivity of agricultural crops. However, few studies have been conducted to determine these effects on the seed germination and seedling growth of neotropical tree species. Thus, this study aimed to determine the effects of inoculation with PGPB on the germination, initial development and activities of the enzymes phenylalanine ammonia-lyase and polyphenol oxidase of seedlings of neotropical tree species. Shade-intolerant (Cecropia pachystachya, Heliocarpus popayanensis and Trema micrantha) and shade-tolerant tree species (Cabralea canjerana, Cariniana estrellensis and Trichilia elegans) were inoculated with different species of PGPB (Azospirillum brasilense, Bacillus sp. and Azomonas sp.) and allowed to germinate and grow for 45 days under greenhouse conditions. Inoculation of C. pachystachya with all types of PGPB increased the percentage of germinated seeds (GS) and the vigor index (VI), while the mean time to germination (MTG) decreased. The VI of T. micrantha increased in response to Bacillus sp. and Azomonas sp. inoculation. Cabralea canjerana showed a decreased GS and VI and an increased MTG when inoculated with PGPB and increased activity of phenylalanine ammonia-lyase and polyphenol oxidase when inoculated with Azomonas sp. Inoculation of PGPB interfered with seed germination and seedling physiology, and shade-intolerant species were more likely to benefit from inoculation. Inoculation with PGPB can modulate the seed germination patterns of neotropical tree species, with indications that the ecological group may be involved in the magnitude of the response.
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References
Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Sci 13:630–633
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. JKSUS 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001
Almeida DS (2016) Recuperação ambiental da Mata Atlântica, 3rd edn. EDITUS, Ilhéus
Amaral FP, Pankievicz VCS, Arisi ACM et al (2016) Differential growth responses of Brachypodium distachyon genotypes to inoculation with plant growth promoting rhizobacteria. Plant Mol Biol 90:689–697. https://doi.org/10.1007/s11103-016-0449-8
Ambreetha S, Chinnadurai C, Marimuthu P et al (2018) Plant-associated Bacillus modulates the expression of auxin-responsive genes of rice and modifies the root architecture. Rhizosphere 5:57–66. https://doi.org/10.1016/j.rhisph.2017.12.001
Araújo GC, Sousa NR, Ramos MA et al (2018) Performance of Quercus suber L. at nursery stage—application of two bio-inoculants under two distinct environments. Ann For Sci 75:1–12. https://doi.org/10.1007/s13595-018-0700-3
Arruda IM, Moda-Cirino V, Koltun A et al (2018) Physiological, biochemical and morphoagronomic characterization of drought-tolerant and drought-sensitive bean genotypes under water stress. Physiol Mol Biol Plants 24:1059–1067. https://doi.org/10.1007/s12298-018-0555-y
Ashrafuzzaman M, Hossen FA, Ismail MR et al (2009) Efficiency of plant growth promoting rhizobacteria (PGPR) for the enhancement of rice growth. Afr J Biotechnol 8:1247–1252
Bechara FC, Dickens SJ, Farrer EC et al (2016) Neotropical rainforest restoration: comparing passive, plantation and nucleation approaches. Biodivers Conserv 25:2021–2034. https://doi.org/10.1007/s10531-016-1186-7
Bertoncelli DJ, Alamino DA, Oliveira MC, et al (2015) Biochemical aspects of early development of Physalis under different light conditions. Appl Res Agrotech 8:37–46. https://revistas.unicentro.br/index.php/repaa/article/view/3267
Bever JD, Dickie IA, Facelli E et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004
Bewley JD, Black M (1994) Seeds: physiology of development and germination, 2nd edn. Plenum Press, New York
Brancalion PHS, Chazdon RL (2017) Beyond hectares: four principles to guide reforestation in the context of tropical forest and landscape restoration. Restor Ecol 25:491–496. https://doi.org/10.1111/rec.12519
Brasil (2009) Ministério da Agricultura, Pecuária e Abastecimento. Regras para análise de sementes. Brasília Mapa/ACS 1:1–399
Brevik EC, Cerdà A, Mataix-Solera J et al (2015) The interdisciplinary nature of SOIL. Soil 1:117–129. https://doi.org/10.5194/soil-1-117-2015
Bruto M, Prigent-Combaret C, Muller D et al (2014) Analysis of genes contributing to plant-beneficial functions in plant growth-promoting rhizobacteria and related Proteobacteria. Sci Rep 4:6261. https://doi.org/10.1038/srep06261
Brzezinski C, Zucareli C, Henning F et al (2014) Nitrogênio e inoculação com Azospirillum na qualidade fisiológica e sanitária de sementes de trigo. Rev Cien Agrar 57:257–265. https://doi.org/10.4322/rca.ao1391
Calzavara AK, Paiva PHG, Gabriel LC et al (2018) Associative bacteria influence maize (Zea mays L.) growth, physiology and root anatomy under different nitrogen levels. Plant Biol 4247:0–2. https://doi.org/10.1111/plb.12841
Carvalho N, Raizer J, Fischer E (2017) Passage through Artibeus lituratus (Olfers, 1818) increases germination of Cecropia pachystachya (Urticaceae) seeds. Trop Conserv Sci 10:1–7. https://doi.org/10.1177/1940082917697262
Cassán F, Perrig D, Sgroy V et al (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35. https://doi.org/10.1016/j.ejsobi.2008.08.005
Castro AHF, De Alvarenga AA, Barbosa JPRAD et al (2017) Avaliação sazonal da atividade da fenilalanina amônia-liase e dos teores de fenóis e taninos totais em Stryphnodendron adstringens (Mart.) coville. Ciência Florest 27:1037–1048. https://doi.org/10.5902/1980509828679
Chagas FO, Pessotti RDC, Caraballo-Rodríguez AM et al (2018) Chemical signaling involved in plant–microbe interactions. Chem Soc Rev 47:1652–1704. https://doi.org/10.1039/c7cs00343a
Clarke DA, York PH, Rasheed MA, Northfield TD (2017) Does biodiversity-ecosystem function literature neglect tropical ecosystems? Trends Ecol Evol 32:320–323. https://doi.org/10.1016/j.tree.2017.02.012
Compant S, Samad A, Faist H et al (2019) A review on the plant microbiome: ecology, functions and emerging trends in microbial application. J Adv Res. https://doi.org/10.1016/j.jare.2019.03.004
Costa PB, Campos SB, Albersmeier A et al (2018) Invasion ecology applied to inoculation of plant growth promoting bacteria through a novel SIMPER-PCA approach. Plant Soil 422:467–478. https://doi.org/10.1007/s11104-017-3492-6
Cunha APMA, Alvalá RCS, Kubota PY, Vieira RMSP (2015) Impacts of land use and land cover changes on the climate over northeast Brazil. Atmos Sci Lett 16:219–227. https://doi.org/10.1002/asl2.543
Dalling JW, Davis AS, Schutte BJ, Arnold AE (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. J Ecol 99:89–95. https://doi.org/10.1111/j.1365-2745.2010.01739.x
De Long JR, Fry EL, Veen GF et al (2018) Why are plant–soil feedbacks so unpredictable, and what to do about it? Funct Ecol 33:118–128. https://doi.org/10.1111/1365-2435.13232
Diedhiou AG, Mbaye FK, Mbodj D et al (2016) Field trials reveal ecotype-specific responses to mycorrhizal inoculation in rice. PLoS One 11:1–17. https://doi.org/10.1371/journal.pone.0167014
Dodd IC, Zinovkina NY, Safronova VI et al (2010) Rhizobacterial mediation of plant hormone status. Ann Appl Biol 157:361–379. https://doi.org/10.1111/j.1744-7348.2010.00439.x
Farnden KJF, Robertson JG (1980) Methods for studying enzymes involved in metabolism related to nitrogenase. In: Bergersen JF (ed) Methods for evaluating biological nitrogen fixation. Wiley, Chichester, pp 265–314
Ferraz-Grande FGA, Takaki M (2006) Efeitos da luz, temperatura e estresse de água na germinação de sementes de Caesalpinia peltophoroides BENTH. (Caesalpinoideae). Bragantia 65:37–42. https://doi.org/10.1590/S0006-87052006000100006
Figueiredo GGO, Lopes VR, Filho JCB, et al (2013) Effect of substrates and plant growth promoting bacteria in the germination of sugarcane seeds. Rev Cien Agrar 36:447–454. http://www.scielo.mec.pt/scielo.php?script=sci_arttext&pid=S0871-018X2013000400009&lng=en&nrm=iso
Freitas SR, Hawbaker TJ, Metzger JP (2010) Effects of roads, topography, and land use on forest cover dynamics in the Brazilian Atlantic Forest. For Ecol Manag 259:410–417. https://doi.org/10.1016/j.foreco.2009.10.036
Gallery RE, Dalling JW, Arnold AE (2007) Diversity, host affinity, and distribution of seed-infecting fungi: a case study with Cecropia. Ecology 88:582–588. https://doi.org/10.1890/05-1207
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo) 2012:1–15. https://doi.org/10.6064/2012/963401
Goes KCGP, Fisher MLC, Cattelan AJ et al (2012) Biochemical and molecular characterization of high population density bacteria isolated from sunflower. J Microbiol Biotechnol 22:437–447. https://doi.org/10.4014/jmb.1109.09007
Griffin EA, Carson WP (2015) The ecology and natural history of foliar bacteria with a focus on tropical forests and agroecosystems. Bot Rev 81:105–149. https://doi.org/10.1007/s12229-015-9151-9
Hubbell SP, Foster RB, O’Brien ST et al (1999) Light-gap disturbances, recruitment limitation, and tree diversity in a neotropical forest. Science 283:554–557
Hungria M, Campo RJ, Souza EM et al (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant Soil 331:413–425. https://doi.org/10.1007/s11104-009-0262-0
Kulmatiski A, Beard KH, Stevens JR et al (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992. https://doi.org/10.1111/j.1461-0248.2008.01209.x
Kumar A, Verma JP (2018) Does plant–microbe interaction confer stress tolerance in plants: a review? Microbiol Res 207:41–52. https://doi.org/10.1016/j.micres.2017.11.004
Lambers H, Mougel C, Jaillard B et al (2009) Plant-microbe–soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115. https://doi.org/10.1007/s11104-009-0042-x
Latz E, Eisenhauer N, Scheu S et al (2015) Plant identity drives the expression of biocontrol factors in a rhizosphere bacterium across a plant diversity gradient. Funct Ecol 29:1225–1234. https://doi.org/10.1111/1365-2435.12417
Le Roux JJ, Hui C, Keet JH et al (2017) Co-introduction vs ecological fitting as pathways to the establishment of effective mutualisms during biological invasions. New Phytol 215:1354–1360. https://doi.org/10.1111/nph.14593
Lemanceau P, Barret M, Mazurier S et al (2017) Plant communication with associated microbiota in the spermosphere, rhizosphere and phyllosphere. In: Becard G (ed) How plants communicate with their biotic environment. Elsevier Ltd, New York, pp 101–133
MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85:273–282. https://doi.org/10.1139/O07-018
Mack KM, Eppinga MB, Bever JD (2019) Plant-soil feedbacks promote coexistence and resilience in multi-species communities. PLoS One 14:1–20. https://doi.org/10.1371/journal.pone.0211572
Madadkhah E, Lotfi M, Nabipour A et al (2012) Enzymatic activities in roots of melon genotypes infected with Fusarium oxysporum f. sp. melonis race 1. Sci Hortic (Amsterdam) 135:171–176. https://doi.org/10.1016/j.scienta.2011.11.020
Mangan SA, Herre EA, Bever JD (2010a) Specificity between neotropical tree seedlings and their fungal mutualists leads to plant–soil feedback. Ecology 91:2594–2603. https://doi.org/10.1890/09-0396.1
Mangan SA, Schnitzer SA, Herre EA et al (2010b) Negative plant–soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. https://doi.org/10.1038/nature09273
Masciarelli O, Llanes A, Luna V (2014) A new PGPR co-inoculated with Bradyrhizobium japonicum enhances soybean nodulation. Microbiol Res 169:609–615. https://doi.org/10.1016/j.micres.2013.10.001
Mayer AM (2006) Polyphenol oxidases in plants and fungi: going places? A review. Phytochemistry 67:2318–2331. https://doi.org/10.1016/j.phytochem.2006.08.006
Mei L, Liang Y, Zhang L et al (2014) Induced systemic resistance and growth promotion in tomato by an indole-3-acetic acid-producing strain of Paenibacillus polymyxa. Ann Appl Biol 165:270–279. https://doi.org/10.1111/aab.12135
Moreira WR, Resende RS, Rodrigues FÁ et al (2013) Influência do magnésio na resistência do arroz à mancha parda. Bragantia 72:154–161. https://doi.org/10.1590/S0006-87052013005000027
Moreno M, de Bashan LE, Hernandez JP et al (2017) Success of long-term restoration of degraded arid land using native trees planted 11 years earlier. Plant Soil 421:83–92. https://doi.org/10.1007/s11104-017-3438-z
Muthukumar T, Udaiyan K (2018) Coinoculation of bioinoculants improve Acacia auriculiformis seedling growth and quality in a tropical Alfisol soil. J For Res 29:663–673. https://doi.org/10.1007/s11676-017-0497-1
Nezarat S, Gholami A (2009) Screening plant growth promoting rhizobacteria for improving seed germination, seedling growth and yield of maize. Pak J Biol Sci 12:26–32. https://doi.org/10.3923/pjbs.2009.26.32
Nunes ACP, Santos GA, Santos MA et al (2018) Application of hypergravity in Eucalyptus and Corymbia seeds. Ciência Rural 48:1–7. https://doi.org/10.1590/0103-8478cr20170233
Oliveira ALM, Costa KDR, Ferreira DC et al (2014) Aplicações da biodiversidade bacteriana do solo para a sustentabilidade da agricultura. BBR Biochem Biotechnol Rep 3:56. https://doi.org/10.5433/2316-5200.2014v3n1p56
Oliveira G, Silva M, Marciano T et al (2016) Crescimento inicial do feijoeiro em função do vigor de sementes e inoculação com Bacillus subtilis. Braz J Chem Eng 10:439–448. https://doi.org/10.18011/bioeng2016v10n4p439-448
Oliveira ALM, Santos OJAP, Marcelino PRF et al (2017) Maize inoculation with Azospirillum brasilense Ab-V5 cells enriched with exopolysaccharides and polyhydroxybutyrate results in high productivity under low N fertilizer input. Front Microbiol 8:1–18. https://doi.org/10.3389/fmicb.2017.01873
Orsenigo S, Guzzon F, Abeli T et al (2017) Comparative germination responses to water potential across different populations of Aegilops geniculata and cultivar varieties of Triticum durum and Triticum aestivum. Plant Biol 19:165–171. https://doi.org/10.1111/plb.12528
Palma AC, Laurance SGW (2015) A review of the use of direct seeding and seedling plantings in restoration: what do we know and where should we go? Appl Veg Sci 18:561–568. https://doi.org/10.1111/avsc.12173
Partida-Martínez LP, Heil M (2011) The microbe-free plant: fact or artifact. Front Plant Sci 2:16. https://doi.org/10.1002/9781119053095.ch114
Pearson TRH, Burslem DFRP, Mullins CE, Dalling JW (2002) Germination ecology of neotropical pioneers: interacting effects of environmental conditions and seed size. Ecology 83:2798–2807
Peña-Domene M, Howe HF, Cruz-León E et al (2016) Seed to seedling transitions in successional habitats across a tropical landscape. Oikos 126(3):410–419. https://doi.org/10.1111/oik.03394
Pineda A, Dicke M, Pieterse CMJ et al (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct Ecol 27:574–586. https://doi.org/10.1111/1365-2435.12050
Podile AR, Laxmi VDV (1998) Seed Bacterization with Bacillus subtilis AF 1 Increases phenylalanine ammonialyase and reduces the incidence of fusarial wilt in Pigeonpea. J Phytopathol 146:255–259. https://doi.org/10.1111/j.1439-0434.1998.tb04687.x
Pourcel L, Routaboul JM, Cheynier V et al (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 12:29–36. https://doi.org/10.1016/j.tplants.2006.11.006
Rais A, Jabeen Z, Shair F et al (2017) Bacillus spp., a bio-control agent enhances the activity of antioxidant defense enzymes in rice against Pyricularia oryzae. PLoS One 12:1–17. https://doi.org/10.1371/journal.pone.0187412
Ramachandran A, Radhapriya P (2016) Restoration of degraded soil in the Nanmangalam Reserve forest with native tree species: effect of indigenous plant growth-promoting bacteria. Sci World J. https://doi.org/10.1155/2016/5465841
Ribeiro MC, Metzger JP, Martensen AC et al (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Rickli-Horst HC, Duarte MM, Chirinzane CJ et al (2017) Carposeminal biometry and germination of Cabralea Canjerana (Vell.) Mart. Floresta 47:391–396. https://doi.org/10.5380/rf.v47i4.54128
Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M et al (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008
Sarmiento C, Zalamea P, Dalling JW et al (2017) Soilborne fungi have host affinity and host-specific effects on seed germination and survival in a lowland tropical forest. Proc Natl Acad Sci USA 114:11458–11463. https://doi.org/10.1073/pnas.1706324114
Silva PHM, Bouillet JP, Paula RC (2016) Assessing the invasive potential of commercial Eucalyptus species in Brazil: germination and early establishment. For Ecol Manag 374:129–135. https://doi.org/10.1016/j.foreco.2016.05.007
Singh A, Sarma BK, Upadhyay RS et al (2013) Compatible rhizosphere microbes mediated alleviation of biotic stress in chickpea through enhanced antioxidant and phenylpropanoid activities. Microbiol Res 168:33–40. https://doi.org/10.1016/j.micres.2012.07.001
Souza R, Válio I (2001) Seed size, seed germination, and seedling survival of Brazilian tropical tree species differing in successional status. Biotropica 33:447–457. https://doi.org/10.1646/0006-3606(2001)033%5b0447:sssgas%5d2.0.co;2
Soylu S, Baysal O, Soylu EM (2003) Induction of disease resistance by the plant activator, acibenzolar-S methyl (ASM) against bacterial canker (Clavibacter michiganensis ssp. michiganensis in tomato seedlings. Plant Sci 18:149–156. https://doi.org/10.1016/S0168-9452(03)00302-9
Subhaswaraj P, Jobina R, Parasuraman P et al (2017) Plant growth promoting activity of pink pigmented facultative methylotroph—Methylobacterium extorquens MM2 on Lycopersicon esculentum L. J Appl Biol Biotechnol 5:042–046. https://doi.org/10.7324/JABB.2017.50107
Sunar K, Dey P, Chakraborty U et al (2015) Biocontrol efficacy and plant growth promoting activity of Bacillus altitudinis isolated from Darjeeling hills, India. J Basic Microbiol 55:91–104. https://doi.org/10.1002/jobm.201300227
Tian J, He N, Hale L et al (2018) Soil organic matter availability and climate drive latitudinal patterns in bacterial diversity from tropical to cold temperate forests. Funct Ecol 32:61–70. https://doi.org/10.1111/1365-2435.12952
Tiepo AN, Hertel MF, Rocha SS et al (2018) Enhanced drought tolerance in seedlings of neotropical tree species inoculated with plant growth-promoting bacteria. Plant Physiol Biochem 130:277–288. https://doi.org/10.1016/j.plaphy.2018.07.021
Vanitha SC, Niranjana SR, Umesha S (2009) Role of phenylalanine ammonia lyase and polyphenol oxidase in host resistance to bacterial wilt of Tomato. J Phytopathol 157:552–557. https://doi.org/10.1111/j.1439-0434.2008.01526.x
Vejan P, Abdullah R, Khadiran T et al (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21:1–17. https://doi.org/10.3390/molecules21050573
Venisse JS, Malnoy M, Faize M et al (2002) Modulation of defense pesponses of Malus spp. during compatible and incompatible interactions with Erwinia amylovora. Mol Plant Microbe Interact 15:1204–1212. https://doi.org/10.1094/MPMI.2002.15.12.1204
Vivas M, Rolo V, Wingfield MJ, Slippers B (2019) Maternal environment regulates morphological and physiological traits in Eucalyptus grandis. For Ecol Manag 432:631–636. https://doi.org/10.1016/j.foreco.2018.10
Wang Y, Ohara Y, Nakayashiki H et al (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Interact 18:385–396. https://doi.org/10.1094/MPMI-18-0385
Whitmore TC (1990) An introduction to tropical rain forests. Clarendon Press, Oxford
Widnyana IK, Javandira C (2016) Activities Pseudomonas spp. and Bacillus sp. to stimulate germination and seedling growth of tomato plants. Agric Agric Sci Procedia 9:419–423. https://doi.org/10.1016/j.aaspro.2016.02.158
Yadav DK, Singh D, Kumar N (2017) Induction of defense-related enzymes by Bacillus amyloliquefaciens DSBA-11 in resistant and susceptible cultivars of tomato against bacterial wilt disease. Int J Agric Res 12:172–180. https://doi.org/10.3923/ijar.2017.172.180
Zalamea P-C, Sarmiento C, Arnold AE et al (2015) Do soil microbes and abrasion by soil particles influence persistence and loss of physical dormancy in seeds of tropical pioneers? Front Plant Sci 5:1–14. https://doi.org/10.3389/fpls.2014.0079
Acknowledgements
The authors thank the Laboratory of Biodiversity and Restoration of Ecosystems at the State University of Londrina for making the seeds available and the comments received by the anonymous reviewers, whose suggestions improved the final version of this manuscript.
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This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (HCO: Grant number 524490/2014-5, TVD), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (LMIS, TVD) and FAEPE/UEL—PUBLIC 2018.
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de Souza, N.L., Rocha, S.S., Narezzi, N.T. et al. Differential impacts of plant growth-promoting bacteria (PGPB) on seeds of neotropical tree species with contrasting tolerance to shade. Trees 34, 121–132 (2020). https://doi.org/10.1007/s00468-019-01902-w
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DOI: https://doi.org/10.1007/s00468-019-01902-w