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Histomorphology and proteomics during rooting of in vitro shoots in Cariniana legalis (Lecythidaceae), a difficult-to-root endangered species from the Brazilian Atlantic Forest

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Abstract

Rooting is an important step of in vitro propagation that involves auxin signaling and the growth-promoting properties of phenolic compounds. We evaluated the effects of indole-3-butyric acid (IBA) and phloroglucinol (PG) on the in vitro rooting of shoots, histomorphology and proteomic profile during the root development in Cariniana legalis. Micropropagated shoots were incubated in 1/4 Murashige and Skoog culture medium supplemented with IBA (0, 50 and 100 μM) and PG (0 and 30 μM). The root development, histomorphology and proteomic profile were analyzed. IBA was necessary for root induction and the combination of IBA (50 or 100 μM) with 30 μM PG significantly increased the number of roots. The histomorphology of shoots treated with 50 μM IBA + 30 μM PG showed that rooting started at 12 days of induction, with the presence of meristematic-type cells from the callus induced on the base of shoots. The 50 μM IBA + 30 μM PG (IBA + PG) treatment affected the abundance of proteins during the rooting of shoots. The up-accumulation of proteins related to carbohydrate and amino acid metabolic processes in 12-day IBA + PG-treated shoots compared with 0-day shoots (before root induction) was associated with the rooting promoted by IBA + PG. The down-accumulation of proteins involved in secondary metabolic processes in 12-day IBA + PG-treated shoots compared with 12-day with no plant growth regulators (PGR) shoots was related to the lack of rooting in with no PGR shoots, while the increased accumulation of antioxidant proteins was related to rooting in 12-day IBA + PG-treated shoots compared with no PGR shoots. This is the first work to demonstrate the effect of IBA + PG on the proteomic profile and histomorphology during the rooting of an economically and ecologically important endangered species, which is difficult to root in vitro.

Key message

Indole-3-butyric acid improved the in vitro rooting changing the proteomic profile and histomorphology in micropropagated shoot of Cariniana legalis, an endangered species from Atlantic Forest, which is difficult-to-root.

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Abbreviations

DTT:

Dithiothreitol

eIF5A:

Eukaryotic translation initiation factor

HSP:

Heat shock proteins

IBA:

Indole-3-butyric acid

IAA:

Indole-3-acetic acid

LED:

Light-emitting diode

MS:

Murashige and Skoog (plant culture medium)

PG:

Phloroglucinol

TCA:

Trichloroacetic acid

References

  • Ahkami AH, Lischewski S, Haensch KT, Porfirova S, Hofmann J, Rolletschek H, Melzer M, Franken P, Hause B, Druege U, Hajirezaei MR (2009) Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol 181:613–625

    Article  CAS  PubMed  Google Scholar 

  • Ahmed Laskar A, Younus H (2019) Aldehyde toxicity and metabolism: the role of aldehyde dehydrogenases in detoxification, drug resistance and carcinogenesis. Drug Metabol Rev 51:42–64

    Article  CAS  Google Scholar 

  • Altamura M (1996) Root histogenesis in herbaceous and woody explants cultured in vitro: a critical review. Agronomie 16:589–602

    Article  Google Scholar 

  • Altamura M, Capitani F, Serafini-Fracassini D, Torrigiani P, Falasca G (1991) Root histogenesis from tobacco thin cell layers. Protoplasma 161:31–42

    Article  Google Scholar 

  • Álvarez C, Valledor L, Sáez P, Sánchez-Olate M, Ríos D (2016) Proteomic analysis through adventitious rooting of Pinus radiata stem cuttings with different rooting capabilities. Am J Plant Sci 7:1888–1904

    Article  CAS  Google Scholar 

  • Anjum NA et al (2016) Catalase and ascorbate peroxidase-representative H2 O2-detoxifying heme enzymes in plants. Environ Sci Pollut Res 23:19002–19029

    Article  CAS  Google Scholar 

  • Aragão VPM, Silveira V, Santa Catarina C (2017) Micropropagation of Cariniana legalis (Martius) O. Kuntze, An Endangered Hardwood Tree From The Brazilian Atlantic Forest. Plant Cell Cult Micro 13:41–50

    Google Scholar 

  • Araujo WL, Nunes-Nesi A, Nikoloski Z, Sweetlove LJ, Fernie AR (2012) Metabolic control and regulation of the tricarboxylic acid cycle in photosynthetic and heterotrophic plant tissues. Plant Cell Environ 35:1–21

    Article  CAS  PubMed  Google Scholar 

  • Aulkemeyer P, Ebner R, Heilenmann G, Jahreis K, Schmid K, Wrieden S, Lengeler J (1991) Molecular analysis of two fructokinases involved in sucrose metabolism of enteric bacteria. Mol Microbiol 5:2913–2922

    Article  CAS  PubMed  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld J-P (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blakesley D, Weston G, Hall J (1991) The role of endogenous auxin in root initiation. Plant Growth Regul 10:341–353

    Article  CAS  Google Scholar 

  • Brinker M, van Zyl L, Liu W, Craig D, Sederoff RR, Clapham DH, von Arnold S (2004) Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol 135:1526–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111

    Article  CAS  PubMed  Google Scholar 

  • Burrieza HP, Rizzo AJ, Vale EM, Silveira V, Maldonado S (2019) Shotgun proteomic analysis of quinoa seeds reveals novel lysine-rich seed storage globulins. Food Chem 293:299–306

    Article  CAS  PubMed  Google Scholar 

  • Carvalho PER (2005) Jequitibá-rosa. Circular Técnica. Colombo, Paraná, Embrapa Florestas, p 10

    Google Scholar 

  • Chen H-C, Song J, Williams CM, Shuford CM, Liu J, Wang JP, Li Q, Shi R, Gokce E, Ducoste J (2013) Monolignol pathway 4-coumaric acid: Coenzyme A ligases in Populus trichocarpa: novel specificity, metabolic regulation, and simulation of coenzyme a ligation fluxes. Plant Physiol 161:1501–1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa L, Stein R, Fett-Neto A (2012) Adventitious rooting of detached Arabidopsis thaliana leaves. Biol Plant 56:25–30

    Article  CAS  Google Scholar 

  • Corrêa LdR, Paim DC, Schwambach J, Fett-Neto AG (2005) Carbohydrates as regulatory factors on the rooting of Eucalyptus saligna Smith and Eucalyptus globulus Labill. Plant Growth Regul 45:63–73

    Article  CAS  Google Scholar 

  • Da Costa CT, De Almeida MR, Ruedell CM, Schwambach J, Maraschin FDS, Fett-Neto AG (2013) When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 4:133

    Article  PubMed  PubMed Central  Google Scholar 

  • da Silva JAT, Dobránszki J, Ross S (2013) Phloroglucinol in plant tissue culture. In Vitro Cell Dev Biol-Plant 49:1–16

    Article  CAS  Google Scholar 

  • Damerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54

    Article  CAS  Google Scholar 

  • De Klerk G-J, van der Krieken W, de Jong JC (1999) Review the formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Dev Biol Plant 35:189–199

    Article  Google Scholar 

  • De Klerk G-J, Guan H, Huisman P, Marinova S (2011) Effects of phenolic compounds on adventitious root formation and oxidative decarboxylation of applied indoleacetic acid in Malus ‘Jork 9.’ Plant Growth Regul 63:175–185

    Article  CAS  Google Scholar 

  • de Mello T, de Oliveir Goncalves E, Alexandre RS, Schmildt ER, Otoni WC (2020) Establishment and in vitro morphogenesis of sapucaia explants (Lecythidaceae). Vitro Cell Dev Biol Plant. 10:20. https://doi.org/10.1007/s11627-020-10091-y

    Article  CAS  Google Scholar 

  • Deisenroth C, Zhang Y (2010) Ribosome biogenesis surveillance: probing the ribosomal protein-Mdm2-p53 pathway. Oncogene 29:4253–4260

    Article  CAS  PubMed  Google Scholar 

  • Dewir YH, Murthy HN, Ammar MH, Alghamdi SS, Al-Suhaibani NA, Alsadon AA, Paek KY (2016) In vitro rooting of leguminous plants: Difficulties, alternatives, and strategies for improvement. Hortic Environ Biotechnol 57:311–322

    Article  CAS  Google Scholar 

  • Dias PC, de Oliveira LS, Xavier A, Wendling I (2012) Estaquia e miniestaquia de espécies florestais lenhosas do Brasil. Pesq Flor Bras 32:453–462

    Article  Google Scholar 

  • Diaz-Vivancos P, de Simone A, Kiddle G, Foyer CH (2015) Glutathione-linking cell proliferation to oxidative stress. Free Radical Biol Med 89:1154–1164

    Article  CAS  Google Scholar 

  • Distler U, Kuharev J, Navarro P, Levin Y, Schild H, Tenzer S (2014) Drift time-specific collision energies enable deep-coverage data-independent acquisition proteomics. Nat Methods 11:167–170

    Article  CAS  PubMed  Google Scholar 

  • Distler U, Kuharev J, Navarro P, Tenzer S (2016) Label-free quantification in ion mobility-enhanced data-independent acquisition proteomics. Nat Protoc 11:795

    Article  CAS  PubMed  Google Scholar 

  • Do C-T, Pollet B, Thévenin J, Sibout R, Denoue D, Barrière Y, Lapierre C, Jouanin L (2007) Both caffeoyl Coenzyme A 3-O-methyltransferase 1 and caffeic acid O-methyltransferase 1 are involved in redundant functions for lignin, flavonoids and sinapoyl malate biosynthesis in Arabidopsis. Planta 226:1117–1129

    Article  CAS  PubMed  Google Scholar 

  • Drew RA, Simpson BW, Osborne WJ (1991) Degradation of exogenous indole-3-butyric acid and riboflavin and their influence on rooting response of papaya in vitro. Plant Cell Tiss Org Cult 26:29–34

    Article  CAS  Google Scholar 

  • Epstein E, Ludwig-Müller J (1993) Indole-3-butyric acid in plants: occurrence, synthesis, metabolism and transport. Physiol Plant 88:382–389

    Article  CAS  Google Scholar 

  • Geigenberger P (2003) Regulation of sucrose to starch conversion in growing potato tubers. J Exp Bot 54:457–465

    Article  CAS  PubMed  Google Scholar 

  • Geneve RL (1991) Patterns of adventitious root formation in English ivy. Plant Growth Regul 10:215–220

    Article  CAS  Google Scholar 

  • Giannino D, Frugis G, Ticconi C, Florio S, Mele G, Santini L, Cozza R, Bitonti M, Innocenti A, Mariotti D (2000) Isolation and molecular characterisation of the gene encoding the cytoplasmic ribosomal protein S28 in Prunus persica [L.] Batsch. Mol Gen Genet 263:201–212

    Article  CAS  PubMed  Google Scholar 

  • Han H, Sun X, Xie Y, Feng J, Zhang S (2014) Transcriptome and proteome profiling of adventitious root development in hybrid larch (Larix kaempferi × Larix olgensis). BMC Plant Biol 14:305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Heringer AS, Santa-Catarina C, Silveira V (2018) Insights from proteomic studies into plant somatic embryogenesis. Proteomics 18:1–9

    Article  CAS  Google Scholar 

  • Hernandez-Valladares M, Aasebo E, Mjaavatten O, Vaudel M, Bruserud O, Berven F, Selheim F (2016) Reliable FASP-based procedures for optimal quantitative proteomic and phosphoproteomic analysis on samples from acute myeloid leukemia patients. Biol Proc Online 18:13

    Article  CAS  Google Scholar 

  • Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468

    Article  CAS  PubMed  Google Scholar 

  • Hoad S, Leakey R (1996) Effects of pre-severance light quality on the vegetative propagation of Eucalyptus grandis W. Hill ex Maiden Trees 10:317–324

    Google Scholar 

  • Husain MK, Anis M, Shahzad A (2008) In vitro propagation of a multipurpose leguminous tree (Pterocarpus marsupium Roxb.) using nodal explants. Acta Physiol Plant 30:353–359

    Article  CAS  Google Scholar 

  • Ikeuchi M, Ogawa Y, Iwase A, Sugimoto K (2016) Plant regeneration: cellular origins and molecular mechanisms. J Dev 143:1442–1451

    Article  CAS  Google Scholar 

  • Ikeuchi M, Iwase A, Rymen B, Lambolez A, Kojima M, Takebayashi Y, Heyman J, Watanabe S, Seo M, De Veylder L (2017) Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol 175:1158–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IUCN (2020) The IUCN Red List of Threatened Species. Version 2020-1. https://www.iucnredlist.org. Accessed 1st may 2020

  • Jasik J, De Klerk G-J (1997) Anatomical and ultrastructural examination of adventitious root formation in stem slices of apple. Biol Plant 39:79–90

    Article  Google Scholar 

  • Jenner C, Siwek K, Hawker J (1993) The synthesis of [14C] starch from [14C] sucrose in isolated wheat grains is dependent upon the activity of soluble starch synthase. Funct Plant Biol 20:329–335

    Article  CAS  Google Scholar 

  • Klopotek Y, Haensch K-T, Hause B, Hajirezaei M-R, Druege U (2010) Dark exposure of petunia cuttings strongly improves adventitious root formation and enhances carbohydrate availability during rooting in the light. Plant Physiol 167:547–554

    Article  CAS  Google Scholar 

  • Koprivova A, Mugford ST, Kopriva S (2010) Arabidopsis root growth dependence on glutathione is linked to auxin transport. Plant Cell Rep 29:1157–1167

    Article  CAS  PubMed  Google Scholar 

  • Lerin J, Aragão VPM, Reis RS, Silveira V, Santa-Catarina C (2019) Proteomic profile and polyamine contents are modulated by light source to promote in vitro shoot development in Cariniana legalis (Martius) O. Kuntze (Lecythidaceae). Plant Cell Tiss Org Cult 137:329–342

    Article  CAS  Google Scholar 

  • Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S-W, Leng Y, Shi R-F (2017) Transcriptomic profiling provides molecular insights into hydrogen peroxide-induced adventitious rooting in mung bean seedlings. BMC Genomics 18:188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lipecka J, Chhuon C, Bourderioux M, Bessard MA, van Endert P, Edelman A, Guerrera IC (2016) Sensitivity of mass spectrometry analysis depends on the shape of the filtration unit used for filter aided sample preparation (FASP). Proteomics 16:1852–1857

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Chen S, Jiang J, Zhu L, Zheng C, Han S, Gu J, Sun J, Li H, Wang H (2013) Proteomic changes in the base of chrysanthemum cuttings during adventitious root formation. BMC Genomics 14:919

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Sheng L, Xu Y, Li J, Yang Z, Huang H, Xu L (2014) WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26:1081–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lloyd G, McCown B (1981) Commercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Int Plant Propag Societ 30:421–427

    Google Scholar 

  • MacDonald MJ, D’Cunha GB (2007) A modern view of phenylalanine ammonia lyase. Biochem Cell Biol 85:273–282

    Article  CAS  PubMed  Google Scholar 

  • Mendoza-Cozatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29:653–671

    Article  CAS  PubMed  Google Scholar 

  • Millán-Orozco L, Corredoira E, San José MdC (2011) In vitro rhizogenesis: histoanatomy of Cedrela odorata (Meliaceae) microcuttings. Rev Biol Trop 59:447–453

    PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nanjo Y, Skultety L, Uváčková Lu, Kn K, Hajduch M, Komatsu S (2012) Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. J Proteome Res 11:372–385

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    Article  CAS  PubMed  Google Scholar 

  • Oliveira LSd, Dias PC, Brondani GE (2013) Micropropagação de espécies florestais brasileiras. Pes Florest Bras 33:439–453

    Article  Google Scholar 

  • Pacurar DI, Perrone I, Bellini C (2014) Auxin is a central player in the hormone cross-talks that control adventitious rooting. Physiol Plant 151:83–96

    Article  CAS  PubMed  Google Scholar 

  • Parveen S, Shahzad A (2010) TDZ-induced high frequency shoot regeneration in Cassia sophera Linn. via cotyledonary node explants. Physiol Mol Biol Plant 16:201–206

    Article  Google Scholar 

  • Parveen S, Shahzad A, Saema S (2010) In vitro plant regeneration system for Cassia siamea Lam., a leguminous tree of economic importance. Agroforest Syst 80:109–116

    Article  Google Scholar 

  • Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563

    Article  CAS  PubMed  Google Scholar 

  • Peer WA, Bandyopadhyay A, Blakeslee JJ, Makam SN, Chen RJ, Masson PH, Murphy AS (2004) Variation in expression and protein localization of the PIN family of auxin efflux facilitator proteins in flavonoid mutants with altered auxin transport in Arabidopsis thaliana. Plant Cell 16:1898–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez LP, Montesinos YP, Olmedo JG, Rodriguez RB, Sánchez RR, Montenegro ON, Escriba RCR, Daniels D, Gómez-Kosky R (2016) Effect of phloroglucinol on rooting and in vitro acclimatization of papaya (Carica papaya L. var. Maradol Roja). In Vitro Cell Dev Biol Plant 52:196–203

    Article  CAS  Google Scholar 

  • R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Rapaka VK, Bessler B, Schreiner M, Druege U (2005) Interplay between initial carbohydrate availability, current photosynthesis, and adventitious root formation in Pelargonium cuttings. Plant Sci 168:1547–1560

    Article  CAS  Google Scholar 

  • Rêgo GM (2002) Jequitibá-rosa (Cariniana legalis): espécie em extinção da floresta Atlântica. Circular técnico, Embrapa Tabuleiros Costeiros, Aracaju, Embrapa Tabuleiros Costeiros, p 2p

    Google Scholar 

  • Ren B, Chen Q, Hong S, Zhao W, Feng J, Feng H, Zuo J (2013) The Arabidopsis eukaryotic translation initiation factor eIF5A-2 regulates root protoxylem development by modulating cytokinin signaling. Plant Cell 25:3841–3857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro M, Catenacci FS, Smith NP, Cabello NB (2017) Lecythidaceae in Flora do Brasil 2020 em construção. Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/reflora/floradobrasil/FB8543. Accessed 22 July 2019

  • Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R (2012) The AINTEGUMENTA LIKE1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riis B, Rattan SI, Clark BF, Merrick WC (1990) Eukaryotic protein elongation factors. Trends Biochem Sci 15:420–424

    Article  PubMed  Google Scholar 

  • Rogers LA, Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164:17–30

    Article  CAS  PubMed  Google Scholar 

  • Rylott EL, Gilday AD, Graham IA (2003) The gluconeogenic enzyme phosphoenolpyruvate carboxykinase in Arabidopsis is essential for seedling establishment. Plant Physiol 131:1834–1842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeiahagh H, Mousavi M, Wiedow C, Bassett H, Pathirana R (2019) Effect of cytokinins and sucrose concentration on the efficiency of micropropagation of ‘Zes006’ Actinidia chinensis var. chinensis, a red-fleshed kiwifruit cultivar. Plant Cell Tiss Org Cult 138:1–10

    Article  CAS  Google Scholar 

  • Saibil H (2013) Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 14:630–642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sang YL, Cheng ZJ, Zhang XS (2018) Plant stem cells and de novo organogenesis. New Phytol 218:1334–1339

    Article  PubMed  Google Scholar 

  • Santelia D, Henrichs S, Vincenzetti V, Sauer M, Bigler L, Klein M, Bailly A, Lee Y, Friml J, Geisler M (2008) Flavonoids redirect PIN-mediated polar auxin fluxes during root gravitropic responses. J Biol Chem 283:31218–31226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shu W, Zhou H, Jiang C, Zhao S, Wang L, Li Q, Yang Z, Groover A, Lu MZ (2019) The auxin receptor TIR 1 homolog (Pag FBL 1) regulates adventitious rooting through interactions with Aux/IAA 28 in Populus. Plant Biotech J 17:338–349

    Article  CAS  Google Scholar 

  • Sousa KR, Aragão VPM, Reis RS, Macedo AF, Vieira HD, de Souza CLM, Floh EIS, Silveira V, Santa-Catarina C (2016) Polyamine, amino acid, and carbohydrate profiles during seed storage of threatened woody species of the Brazilian Atlantic Forest may be associated with seed viability maintenance. Braz J Bot 39:985–995

    Article  Google Scholar 

  • Stevens ME, Pijut PM (2018) Rapid in vitro shoot multiplication of the recalcitrant species Juglans nigra L. In Vitro Cell Dev Biol-Plant 54:309–317

    Article  CAS  Google Scholar 

  • Sukumar P, Maloney GS, Muday GK (2013) Localized induction of the ATP-binding cassette B19 auxin transporter enhances adventitious root formation in Arabidopsis. Plant Physiol 162:1392–1405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tahiri A, Delporte F, Muhovski Y, Ongena M, Thonart P, Druart P (2016) Change in ATP-binding cassette B1/19, glutamine synthetase and alcohol dehydrogenase gene expression during root elongation in Betula pendula Roth and Alnus glutinosa L. Gaertn in response to leachate and leonardite humic substances. Plant Physiol Biochem 98:25–38

    Article  CAS  PubMed  Google Scholar 

  • Takahashi H, Saito K (1996) Subcellular localization of spinach cysteine synthase isoforms and regulation of their gene expression by nitrogen and sulfur. Plant Physiol 112:273–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang Z, Du W, Du X, Ban Y, Cheng J (2016) iTRAQ protein profiling of adventitious root formation in mulberry hardwood cuttings. Plant Grow Regul 35:618–631

    Article  CAS  Google Scholar 

  • Thangjam R, Sahoo L (2012) In vitro regeneration and Agrobacterium tumefaciens-mediated genetic transformation of Parkia timoriana (DC.) Merr.: a multipurpose tree legume. Acta Physiol Plant 34:1207–1215

    Article  CAS  Google Scholar 

  • Thompson GM, Cano VS, Valentini SR (2003) Mapping eIF5A binding sites for Dys1 and Lia1: in vivo evidence for regulation of eIF5A hypusination. FEBS Lett 555:464–468

    Article  CAS  PubMed  Google Scholar 

  • Thompson JE, Hopkins MT, Taylor C, Wang T-W (2004) Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development. Trends Plant Sci 9:174–179

    Article  CAS  PubMed  Google Scholar 

  • Timperio AM, Egidi MG, Zolla L (2008) Proteomics applied on plant abiotic stresses: role of heat shock proteins (HSP). J Prot 71:391–411

    Article  CAS  Google Scholar 

  • Tyburski J, Tretyn A (2010) Glutathione and glutathione disulfide affect adventitious root formation and growth in tomato seedling cuttings. Acta Physiol Plant 32:411–417

    Article  CAS  Google Scholar 

  • Vahdati K, Leslie C, Zamani Z, McGranahan G (2004) Rooting and acclimatization of in vitro-grown shoots from mature trees of three Persian walnut cultivars. HortScience 39:324–327

    Article  Google Scholar 

  • Van Lijsebettens M, Vanderhaeghen R, De Block M, Bauw G, Villarroel R, Van Montagu M (1994) An S18 ribosomal protein gene copy at the Arabidopsis PFL locus affects plant development by its specific expression in meristems. EMBO J 13:3378–3388

    Article  PubMed  PubMed Central  Google Scholar 

  • Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153:895–905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vernoux T, Wilson RC, Seeley KA, Reichheld J-P, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inzé D (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Hua J, Yin Y, Gu C, Yu C, Shi Q, Guo J, Xuan L, Yu F (2019) An integrated transcriptome and proteome analysis reveals putative regulators of adventitious root formation in Taxodium ‘Zhongshanshan.’ Inter J Mol Sci 20:1225

    Article  CAS  Google Scholar 

  • Xu A, Chen KY (2001) Hypusine is required for a sequence-specific interaction of eukaryotic initiation factor 5A with postsystematic evolution of ligands by exponential enrichment RNA. J Biol Chem 276:2555–2561

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Cai X-T, Wang Y, Xing L, Chen Q, Xiang C-B (2014) HDG11 upregulates cell-wall-loosening protein genes to promote root elongation in Arabidopsis. J Exp Bot 65:4285–4295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Peer WA (2017) Auxin homeostasis: the DAO of catabolism. J Exp Bot 68:3145–3154

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Wu J, Yuan D, Zhang D, Huang Z, Xiao L, Yang C (2014) Perturbation of auxin homeostasis caused by mitochondrial FtSH4 gene-mediated peroxidase accumulation regulates Arabidopsis architecture. Mol Plant 7:856–873

    Article  CAS  PubMed  Google Scholar 

  • Zhou J, Wu H, Collet G (1992) Histological study of initiation and development in vitro of adventitious roots in minicuttings of apple rootstocks of M 26 and EMLA 9. Physiol Plant 84:433–440

    Article  Google Scholar 

  • Zhou T, Song YC, Feng MQ, Tan RX (2011) Cloning, expression and biochemical characterization of UDP-glucose 6-dehydrogenase, a key enzyme in the biosynthesis of an anti-tumor polysaccharide from the marine fungus Phoma herbarum YS4108. Process Biochem 46:2263–2268

    Article  CAS  Google Scholar 

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Acknowledgements

Funding for this work was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (444,453/2014-8 and 307596/2016-8) and the Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro (FAPERJ) (E26/201.247/2015; E26/202.969/2016; E26/202.533/2019). This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001. TRO acknowledges the scholarship funded by FAPERJ. JL and YRSR are thankful for the scholarship provided by CAPES—Finance Code 001.

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CSC and JL conceived the study, designed the experiments and wrote the manuscript. JL was responsible for the in vitro cultures. JL, YRSR and CSC were responsible for the histological experiments and analyses. JL, TRO and VS were responsible for the proteomic analyses. All authors have read and approved the final manuscript.

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Correspondence to Claudete Santa-Catarina.

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Communicated by Ranjith Pathirana.

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Lerin, J., Ribeiro, Y.R.d.S., de Oliveira, T.d.R. et al. Histomorphology and proteomics during rooting of in vitro shoots in Cariniana legalis (Lecythidaceae), a difficult-to-root endangered species from the Brazilian Atlantic Forest. Plant Cell Tiss Organ Cult 144, 325–344 (2021). https://doi.org/10.1007/s11240-020-01955-7

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  • DOI: https://doi.org/10.1007/s11240-020-01955-7

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