Abstract
Adventitious rooting (AR) is an obligatory step for vegetative propagation of commercial woody species. Paper industries have interest in Eucalyptus globulus Labill and its hybrids due to low lignin and lipid contents, which facilitate cellulose extraction. However, this species and some of its hybrids are recalcitrant to rooting, often requiring exogenous auxin supply. Here we performed a comparative analysis of proteome changes during AR of E. globulus and the easy-to-root species Eucalyptus grandis W. Hill and the effects of exogenous auxin in different phases of the process (induction and formation), using a label-free quantification method. We identified 398 differentially abundant proteins, which were predicted to be involved in different biological pathways, mainly oxidative stress, energy metabolism and photosynthesis. Notable differences between species included proteins involved in oxidative stress, carbon and secondary metabolism. Exogenous auxin appeared to affect the availability of carbon sources and other phytohormones, besides cell cycle and microtubule—related proteins. Important players were also identified in each phase of AR. This is the first in depth analysis of protein changes during AR in Eucalyptus. The findings can be used in future studies to evaluate rooting competence in different genotypes and provide leads for AR improvement.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abril N, Gion J-M, Kerner R et al (2011) Proteomics research on forest trees, the most recalcitrant and orphan plant species. Phytochemistry 72:1219–1242. https://doi.org/10.1016/j.phytochem.2011.01.005
Abu-Abied M, Szwerdszarf D, Mordehaev I et al (2014) Gene expression profiling in juvenile and mature cuttings of Eucalyptus grandis reveals the importance of microtubule remodeling during adventitious root formation. BMC Genom 15:1–10. https://doi.org/10.1186/1471-2164-15-826
Abu-Abied M, Rogovoy (Stelmakh) O, Mordehaev J et al (2015) Dissecting the contribution of microtubule behaviour in adventitious root induction. J Exp Bot 66:2813–2824. https://doi.org/10.1093/jxb/erv097
Acosta M, Oliveros-Valenzuela MR, Nicolás C, Sánchez-Bravo J (2009) Rooting of carnation cuttings: the auxin signal. Plant Signal Behav 4:234–236. https://doi.org/10.1016/j.plaphy.2008.07.009
Agulló-Antón MÁ, Ferrández-Ayela A, Fernández-García N et al (2014) Early steps of adventitious rooting: morphology, hormonal profiling and carbohydrate turnover in carnation stem cuttings. Physiol Plant 150:446–462. https://doi.org/10.1111/ppl.12114
Ahkami AH, Lischewski S, Haensch KT et al (2009) Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol 181:613–625. https://doi.org/10.1111/j.1469-8137.2008.02704.x
Ahkami A, Scholz U, Steuernagel B et al (2014) Comprehensive transcriptome analysis unravels the existence of crucial genes regulating primary metabolism during adventitious root formation in Petunia hybrida. PLoS ONE 9:e100997. https://doi.org/10.1371/journal.pone.0100997
Álvarez C, Valledor L, Sáez P et al (2016) Proteomic analysis through adventitious rooting of Pinus radiata stem cuttings with different rooting capabilities. Am J Plant Sci 07:1888–1904. https://doi.org/10.4236/ajps.2016.714174
Amzallag GN, Goloubinoff P (2003) An Hsp90 inhibitor, geldanamycin, as a brassinosteroid antagonist: evidence from salt-exposed roots of Vigna radiata. Plant Biol 5:143–150. https://doi.org/10.1055/s-2003-40725
Aumond MLML, de Araujo AT, de Oliveira Junkes CF et al (2017) Events associated with early age-related decline in adventitious rooting competence of Eucalyptus globulus Labill. Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.01734
Beardmore T, Wetzel S, Kalous M (2000) Interactions of airborne methyl jasmonate with vegetative storage protein gene and protein accumulation and biomass partitioning in Populus plants. Can J For Res 30:1106–1113. https://doi.org/10.1139/x00-046
Bedon F, Majada J, Feito I et al (2011) Interaction between environmental factors affects the accumulation of root proteins in hydroponically grown Eucalyptus globulus (Labill.). Plant Physiol Biochem 49:69–76. https://doi.org/10.1016/j.plaphy.2010.09.020
Bedon F, Villar E, Vincent D et al (2012) Proteomic plasticity of two Eucalyptus genotypes under contrasted water regimes in the field. Plant, Cell Environ 35:790–805. https://doi.org/10.1111/j.1365-3040.2011.02452.x
Brinker M, van Zyl L, Liu WB et al (2004) Microarray analyses of gene expression during adventitious root development in Pinus contorta. Plant Physiol 135:1526–1539. https://doi.org/10.1104/pp.103.032235.et
Budzinski IGF, Moon DH, Lindén P et al (2016a) Seasonal variation of carbon metabolism in the cambial zone of Eucalyptus grandis. Front Plant Sci 7:1–17. https://doi.org/10.3389/fpls.2016.00932
Budzinski IGF, Moon DH, Morosini JS et al (2016b) Integrated analysis of gene expression from carbon metabolism, proteome and metabolome, reveals altered primary metabolism in Eucalyptus grandis bark, in response to seasonal variation. BMC Plant Biol 16:1–15. https://doi.org/10.1186/s12870-016-0839-8
Buer CS, Imin N, Djordjevic MA (2010) Flavonoids: new roles for old molecules. J Integr Plant Biol 52:98–111. https://doi.org/10.1111/j.1744-7909.2010.00905.x
Calderan-Rodrigues MJ, Jamet E, Bonassi MBCR et al (2014) Cell wall proteomics of sugarcane cell suspension cultures. Proteomics 14:738–749. https://doi.org/10.1002/pmic.201300132
Celedon PAF, De Andrade A, Meireles KGX et al (2007) Proteomic analysis of the cambial region in juvenile Eucalyptus grandis at three ages. Proteomics 7:2258–2274. https://doi.org/10.1002/pmic.200600989
Chen Q, Guo W, Feng L et al (2015) Data for transcriptome and proteome analysis of Eucalyptus infected with Calonectria pseudoreteaudii. Data Br 3:24–28. https://doi.org/10.1016/j.dib.2014.12.008
Chueca A, Sahrawy M, Pagano EA, López Gorgé J (2002) Chloroplast fructose-1,6-bisphosphatase: structure and function. Photosynth Res 74:235–249. https://doi.org/10.1023/A:1021243110495
Conesa A, Gotz S, Garcia-Gomez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Corrêa LdaR, 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. https://doi.org/10.1007/s10725-004-6125-z
Curir P, VanSumere CF, Termini A et al (1990) Flavonoid accumulation is correlated with adventitious roots formation in Eucalyptus gunnii Hook micropropagated through axillary bud stimulation. Plant Physiol 92:1148–1153. https://doi.org/10.1104/pp.92.4.1148
da Costa CTCT, de Almeida MR, Ruedell CMCM et al (2013) When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 4:1–19. https://doi.org/10.3389/fpls.2013.00133
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. https://doi.org/10.1002/elps.1150070108
de Almeida MR, de Bastiani D, Gaeta MLML et al (2015) Comparative transcriptional analysis provides new insights into the molecular basis of adventitious rooting recalcitrance in Eucalyptus. Plant Sci 239:155–165. https://doi.org/10.1016/j.plantsci.2015.07.022
De Almeida Leonardi G, Carlos NA, Mazzafera P, Balbuena TS (2015) Eucalyptus urograndis stem proteome is responsive to short-term cold stress. Genet Mol Biol 38:191–198. https://doi.org/10.1590/S1415-475738220140235
De Carvalho MCDCG, Caldas DGG, Carneiro RT et al (2008) SAGE transcript profiling of the juvenile cambial region of Eucalyptus grandis. Tree Physiol 28:905–919. https://doi.org/10.1093/treephys/28.6.905
de Klerk G-J, van der Krieken W, de Jong JC (1999) The formation of adventitious roots: new concepts, new possibilities. Vitr Cell Dev Biol Plant 35:189–199. https://doi.org/10.1007/s11627-999-0076-z
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. https://doi.org/10.1007/s10725-010-9555-9
De Santana Costa MG, Mazzafera P, Balbuena TS (2017) Insights into temperature modulation of the Eucalyptus globulus and Eucalyptus grandis antioxidant and lignification subproteomes. Phytochemistry 137:15–23. https://doi.org/10.1016/j.phytochem.2017.01.017
Díaz-Sala C (2014) Direct reprogramming of adult somatic cells toward adventitious root formation in forest tree species: the effect of the juvenile-adult transition. Front Plant Sci 5:1–8. https://doi.org/10.3389/fpls.2014.00310
Druart N, Johansson A, Baba K et al (2007) Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J 50:557–573. https://doi.org/10.1111/j.1365-313X.2007.03077.x
Druege U, Franken P, Hajirezaei MR (2016) Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00381
Fett-Neto AG, Teixeira SL, Da Silva EAM, Sant’ Anna R (1992) Biochemical and morphological changes during in vitro rhizogenesis in cuttings of Sequoia sempervirens (D. Don) Endl. J Plant Physiol 140:720–728. https://doi.org/10.1016/S0176-1617(11)81029-1
Fett-Neto AG, Fett JP, Goulart LWV et al (2001) Distinct effects of auxin and light on adventitious root development in Eucalyptus saligna and Eucalyptus globulus. Tree Physiol 21:457–464. https://doi.org/10.1093/treephys/21.7.457
Goodstein DM, Shu S, Howson R et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:1178–1186. https://doi.org/10.1093/nar/gkr944
Grauvogel C, Brinkmann H, Petersen J (2007) Evolution of the glucose-6-phosphate isomerase: the plasticity of primary metabolism in photosynthetic eukaryotes. Mol Biol Evol 24:1611–1621. https://doi.org/10.1093/molbev/msm075
Guarino C, Conte B, Spada V et al (2014) Proteomic analysis of eucalyptus leaves unveils putative mechanisms involved in the plant response to a real condition of soil contamination by multiple heavy metals in the presence or absence of mycorrhizal/rhizobacterial additives. Environ Sci Technol 48:11487–11496. https://doi.org/10.1021/es502070m
Gutierrez L, Mongelard G, Floková K et al (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527. https://doi.org/10.1105/tpc.112.099119
Han H, Sun X, Xie Y et al (2014) Transcriptome and proteome profiling of adventitious root development in hybrid larch (Larix kaempferi × Larix olgensis). BMC Plant Biol 14:1–13. https://doi.org/10.1186/s12870-014-0305-4
Harris J (2015) Abscisic acid: hidden architect of root system structure. Plants 4:548–572. https://doi.org/10.3390/plants4030548
Heringer AS, Barroso T, Macedo AF et al (2015) Label-free quantitative proteomics of embryogenic and non-embryogenic callus during sugarcane somatic embryogenesis. PLoS ONE 10:e0127803. https://doi.org/10.1371/journal.pone.0127803
Kersting AR, Mizrachi E, Bornberg-Bauer E, Myburg AA (2015) Protein domain evolution is associated with reproductive diversification and adaptive radiation in the genus Eucalyptus. New Phytol 206:1328–1336. https://doi.org/10.1111/nph.13211
Kohler A, Delaruelle C, Martin D et al (2003) The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Lett 542:37–41. https://doi.org/10.1016/S0014-5793(03)00334-X
Landrein B, Hamant O (2013) How mechanical stress controls microtubule behavior and morphogenesis in plants: history, experiments and revisited theories. Plant J 75:324–338. https://doi.org/10.1111/tpj.12188
Lei C, Fan S, Li K et al (2018) iTRAQ-based proteomic analysis reveals potential regulation networks of IBA-induced adventitious root formation in apple. Int J Mol Sci 19:667. https://doi.org/10.3390/ijms19030667
Leslie AD, Mencuccini M, Perks MP, Wilson ER (2019) A review of the suitability of eucalypts for short rotation forestry for energy in the UK. New For. https://doi.org/10.1007/s11056-019-09717-w
Li S-W, Shi R-F, Leng Y (2015) De novo characterization of the mung bean transcriptome and transcriptomic analysis of adventitious rooting in seedlings using RNA-Seq. PLoS ONE 10:e0132969. https://doi.org/10.1371/journal.pone.0132969
Li SW, Leng Y, Shi RF (2017) Transcriptomic profiling provides molecular insights into hydrogen peroxide-induced adventitious rooting in mung bean seedlings. BMC Genom 18:1–23. https://doi.org/10.1186/s12864-017-3576-y
Lischweski S, Muchow A, Guthörl D, Hause B (2015) Jasmonates act positively in adventitious root formation in petunia cuttings. BMC Plant Biol 15:229. https://doi.org/10.1186/s12870-015-0615-1
Liu R, Chen S, Jiang J et al (2013) Proteomic changes in the base of Chrysanthemum cuttings during adventitious root formation. BMC Genom 14:1–14. https://doi.org/10.1186/1471-2164-14-919
Lu N, Xu Z, Meng B et al (2014) Proteomic analysis of etiolated juvenile tetraploid Robinia pseudoacacia branches during different cutting periods. Int J Mol Sci 15:6674–6688. https://doi.org/10.3390/ijms15046674
Lu N, Dai L, Luo Z et al (2017) Characterization of the transcriptome and gene expression of tetraploid black locust cuttings in response to etiolation. Genes (Basel) 8:1–18. https://doi.org/10.3390/genes8120345
Mano J, Belles-Boix E, Babiychuk E, Inzé D et al (2005) Protection against photooxidative injury of tobacco leaves by 2-alkenal reductase. Detoxication of lipid peroxide-derived reactive carbonyls. Plant Physiol 139:1773–1783. https://doi.org/10.1104/pp.105.070391
Melzer E, O’Leary MH (1987) Anapleurotic CO2 fixation by phosphoenolpyruvate carboxylase in C3 plants. Plant Physiol 84:58–60. https://doi.org/10.1104/pp.84.1.58
Min T, Kasahara H, Bedgar DL et al (2003) Crystal structures of pinoresinol-lariciresinol and phenylcoumaran benzylic ether reductases and their relationship to isoflavone reductases. J Biol Chem 278:50714–50723. https://doi.org/10.1074/jbc.M308493200
Mishra BS, Singh M, Aggrawal P, Laxmi A (2009) Glucose and auxin signaling interaction in controlling Arabidopsis thaliana seedlings root growth and development. PLoS ONE 4:e4502. https://doi.org/10.1371/journal.pone.0004502
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Negishi N, Nakahama K, Urata N et al (2014) Hormone level analysis on adventitious root formation in Eucalyptus globulus. New For 45:577–587. https://doi.org/10.1007/s11056-014-9420-1
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. https://doi.org/10.1111/ppl.12171
Park C-J, Seo Y-S (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333. https://doi.org/10.5423/PPJ.RW.08.2015.0150
Peer WA, Murphy AS (2007) Flavonoids and auxin transport: modulators or regulators? Trends Plant Sci 12:556–563. https://doi.org/10.1016/j.tplants.2007.10.003
Péret B, Li G, Zhao J et al (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat Cell Biol 14:991–998. https://doi.org/10.1038/ncb2573
Quan J, Meng S, Guo E et al (2017) De novo sequencing and comparative transcriptome analysis of adventitious root development induced by exogenous indole-3-butyric acid in cuttings of tetraploid black locust. BMC Genom 18:1–14. https://doi.org/10.1186/s12864-017-3554-4
Quecine MC, Leite TF, Bini AP et al (2016) Label-free quantitative proteomic analysis of Puccinia psidii uredospores reveals differences of fungal populations infecting Eucalyptus and guava. PLoS ONE 11:1–19. https://doi.org/10.1371/journal.pone.0145343
Ramirez-Carvajal GA, Morse AM, Dervinis C, Davis JM (2009) The cytokinin type-B response regulator PtRR13 Is a negative regulator of adventitious root development in Populus. Plant Physiol 150:759–771. https://doi.org/10.1104/pp.109.137505
Rasmussen A, Hosseini SA, Hajirezaei MR et al (2015) Adventitious rooting declines with the vegetative to reproductive switch and involves a changed auxin homeostasis. J Exp Bot 66:1437–1452. https://doi.org/10.1093/jxb/eru499
Ravnikar M, Vilhar B, Gogala N (1992) Stimulatory effects of jasmonic acid on potato stem node and protoplast culture. J Plant Growth Regul 11:29–33. https://doi.org/10.1007/BF00193840
Rencoret J, Gutiérrez A, del Río JC (2007) Lipid and lignin composition of woods from different eucalypt species. Holzforschung 61:165–174. https://doi.org/10.1515/HF.2007.030
Rojas-González JA, Soto-Súarez M, García-Díaz Á et al (2015) Disruption of both chloroplastic and cytosolic FBPase genes results in a dwarf phenotype and important starch and metabolite changes in Arabidopsis thaliana. J Exp Bot 66:2673–2689. https://doi.org/10.1093/jxb/erv062
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709. https://doi.org/10.1146/annurev.arplant.57.032905.105441
Ruedell CMCM, de Almeida MR, Schwambach J et al (2013) Pre and post-severance effects of light quality on carbohydrate dynamics and microcutting adventitious rooting of two Eucalyptus species of contrasting recalcitrance. Plant Growth Regul 69:235–245. https://doi.org/10.1007/s10725-012-9766-3
Ruedell CMCM, de Almeida MR, Fett-Neto AGAG (2015) Concerted transcription of auxin and carbohydrate homeostasis-related genes underlies improved adventitious rooting of microcuttings derived from far-red treated Eucalyptus globulus Labill mother plants. Plant Physiol Biochem 97:11–19. https://doi.org/10.1016/j.plaphy.2015.09.005
Samac DA, Litterer L, Temple G et al (2004) Expression of UDP–glucose dehydrogenase reduces cell-wall polysaccharide concentration and increases xylose content in alfalfa stems. Appl Biochem Biotechnol 116:1167–1182. https://doi.org/10.1385/ABAB:116:1-3:1167
Santos BM dos, Balbuena TS (2017) Carbon assimilation in Eucalyptus urophylla grown under high atmospheric CO2 concentrations: a proteomics perspective. J Proteom 150:252–257. https://doi.org/10.1016/j.jprot.2016.09.010
Santos Macedo E, Sircar D, Cardoso HG et al (2012) Involvement of alternative oxidase (AOX) in adventitious rooting of Olea europaea L. microshoots is linked to adaptive phenylpropanoid and lignin metabolism. Plant Cell Rep 31:1581–1590. https://doi.org/10.1007/s00299-012-1272-6
Schwambach J, Fadanelli C, Fett-Neto AG (2005) Mineral nutrition and adventitious rooting in microcuttings of Eucalyptus globulus. Tree Physiol 25:487–494. https://doi.org/10.1093/treephys/25.4.487
Schwambach J, Ruedell CMCM, De Almeida MR et al (2008) Adventitious rooting of Eucalyptus globulus × maidenii mini-cuttings derived from mini-stumps grown in sand bed and intermittent flooding trays: a comparative study. New For 36:261–271. https://doi.org/10.1007/s11056-008-9099-2
Seitz B, Klos C, Wurm M, Tenhaken R (2000) Matrix polysaccharide precursors in Arabidopsis cell walls are synthesized by alternate pathways with organ-specific expression patterns. Plant J 21:537–546. https://doi.org/10.1046/j.1365-313x.2000.00696.x
Serrano L, Rochange F, Semblat JP et al (1996) Genetic transformation of Eucalyptus globulus through biolistics: complementary development of procedures for organogenesis from zygotic embryos and stable transformation of corresponding proliferating tissue. J Exp Bot 47:285–290. https://doi.org/10.1093/jxb/47.2.285
Silva JC, Denny R, Dorschel CA et al (2005) Quantitative proteomic analysis by accurate mass retention time pairs. Anal Chem 77:2187–2200. https://doi.org/10.1021/ac048455k
Sorin C, Negroni L, Balliau T et al (2006) Proteomic analysis of different mutant genotypes of arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiol 140:349–364. https://doi.org/10.1104/pp.105.067868
Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617. https://doi.org/10.1104/pp.15.01360
Thanananta N, Vuttipongchaikij S, Apisitwanich S (2018) Agrobacterium-mediated transformation of a Eucalyptus camaldulensis × E. tereticornis hybrid using peeled nodal-stem segments with yeast HAL2 for improving salt tolerance. New For 49:311–327. https://doi.org/10.1007/s11056-017-9621-5
Tromas A, Braun N, Muller P et al (2009) The AUXIN BINDING PROTEIN 1 is required for differential Auxin responses mediating root growth. PLoS ONE 4:1–11. https://doi.org/10.1371/journal.pone.0006648
Trupiano D, Yordanov Y, Regan S et al (2013) Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta 238:271–282. https://doi.org/10.1007/s00425-013-1890-4
Valdés AE, Irar S, Majada JP et al (2013) Drought tolerance acquisition in Eucalyptus globulus (Labill.): a research on plant morphology, physiology and proteomics. J Proteom 79:263–276. https://doi.org/10.1016/j.jprot.2012.12.019
Vilasboa J, Da Costa CT, Fett-Neto AG (2018) Rooting of eucalypt cuttings as a problem-solving oriented model in plant biology. Prog Biophys Mol Biol. https://doi.org/10.1016/j.pbiomolbio.2018.12.007
Villacorta-Martín C, Sánchez-García AB, Villanova J et al (2015) Gene expression profiling during adventitious root formation in carnation stem cuttings. BMC Genom 16:789. https://doi.org/10.1186/s12864-015-2003-5
Vizcaíno JA, Deutsch EW, Wang R et al (2014) ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32:223–226. https://doi.org/10.1038/nbt.2839
Vizcaíno JA, Csordas A, Del-Toro N et al (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44:D447–D456. https://doi.org/10.1093/nar/gkv1145
Wang J, Feng J, Jia W et al (2015a) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8:145. https://doi.org/10.1186/s13068-015-0331-y
Wang S, Ito T, Uehara M et al (2015b) UDP-d-galactose synthesis by UDP-glucose 4-epimerase 4 is required for organization of the trans-Golgi network/early endosome in Arabidopsis thaliana root epidermal cells. J Plant Res 128:863–873. https://doi.org/10.1007/s10265-015-0737-4
Wang R, Zhang Y, Kieffer M et al (2016) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun 7:1–10. https://doi.org/10.1038/ncomms10269
Wang Z, Hua J, Yin Y et al (2019) An integrated transcriptome and proteome analysis reveals putative regulators of adventitious root formation in Taxodium ‘Zhongshanshan’. Int J Mol Sci 20:1225. https://doi.org/10.3390/ijms20051225
Wei K, Wang L, Cheng H et al (2013) Identification of genes involved in indole-3-butyric acid-induced adventitious root formation in nodal cuttings of Camellia sinensis (L.) by suppression subtractive hybridization. Gene 514:91–98. https://doi.org/10.1016/j.gene.2012.11.008
Wei K, Wang L-Y, Wu L-Y et al (2014) Transcriptome analysis of indole-3-butyric acid-induced adventitious root formation in nodal cuttings of Camellia sinensis (L.). PLoS ONE 9:1–9. https://doi.org/10.1371/journal.pone.0107201
Xu Z-S, Li Z-Y, Chen Y et al (2012) Heat shock protein 90 in plants: molecular mechanisms and roles in stress responses. Int J Mol Sci 13:15706–15723. https://doi.org/10.3390/ijms131215706
Yamauchi Y, Hasegawa A, Mizutani M, Sugimoto Y (2012) Chloroplastic NADPH-dependent alkenal/one oxidoreductase contributes to the detoxification of reactive carbonyls produced under oxidative stress. FEBS Lett 586:1208–1213. https://doi.org/10.1016/j.febslet.2012.03.013
Zelko IN, Mariani TJ, Folz RJ (2002) Superoxide dismutase multigene family: a comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution, and expression. Free Radic Biol Med 33:337–349. https://doi.org/10.1016/S0891-5849(02)00905-X
Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64. https://doi.org/10.1146/annurev-arplant-042809-112308
Zheng Z, Guo Y, Novák O et al (2013) Coordination of auxin and ethylene biosynthesis by the aminotransferase VAS1. Nat Chem Biol 9:244–246. https://doi.org/10.1038/nchembio.1178
Acknowledgements
Seeds used for production of E. globulus and E. grandis microcuttings were a kind gift from Celulose Riograndense S/A (Guaíba, RS, Brazil). This work was funded by Brazilian agencies National Council for Scientific and Technological Development (CNPq-grants 402618/2016-5 and 303560/2017-7) and National Commission for Improvement of Higher Education Personnel (CAPES)-Finance Code 001.
Author information
Authors and Affiliations
Contributions
Conceived and designed the experiments: AGFN. Performed the experiments: MRA, JS, VS. Analyzed the data: MRA, JS. Contributed reagents/materials/analysis tools: JPF, AGFN, VS, JS, ASH. Drafted the paper: MRA. Supervised the study and finalized the manuscript: AGFN. All authors contributed to the preparation, revised and agreed with the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Online Resource 1.
Unchanged proteins during the induction phase. (XLSX 143 kb)
Online Resource 2.
Unchanged proteins during the formation phase. (XLSX 136 kb)
Online Resource 3.
Regulated proteins during the induction phase. (XLSX 99 kb)
Online Resource 4.
Regulated proteins during the formation phase. (XLSX 110 kb)
Online Resource 5.
Identification and classification of regulated proteins during the induction phase. Respective Fold change values and ANOVA results can be accessed in Online Resource 3. (XLSX 27 kb)
Online Resource 6.
Identification and classification of regulated proteins during the formation phase. Respective Fold change values and ANOVA results can be accessed in Online Resource 4. (XLSX 29 kb)
Rights and permissions
About this article
Cite this article
de Almeida, M.R., Schwambach, J., Silveira, V. et al. Proteomic profiles during adventitious rooting of Eucalyptus species relevant to the cellulose industry. New Forests 51, 213–241 (2020). https://doi.org/10.1007/s11056-019-09728-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11056-019-09728-7