Skip to main content

Advertisement

SpringerLink
Log in

AaMps1 protein inhibition regulates the protein profile, nitric oxide, carbohydrate and polyamine contents in embryogenic suspension cultures of Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae)

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

The Monopolar Spindle 1 (Mps1) protein is a dual-specificity kinase that plays a critical role in the progression of the cell cycle. Studies on biochemical changes promoted by Mps1 protein inhibition are important for the development of somatic embryogenesis in plants; however, such work has not been previously performed for Araucaria angustifolia. We analyzed the effects of Mps1 protein inhibition on differential protein regulation and the effects of such differential regulation on the carbohydrate, nitric oxide (NO) and polyamine (PA) contents in embryogenic suspension cultures of this species. A proteomic analysis by the shotgun method was performed using mass spectrometry. The PA and carbohydrate contents were determined by high-performance liquid chromatography, while NO was analyzed by fluorescence microscopy. A total of 1518 proteins were identified, and 157 and 162 proteins were down- and up-regulated, respectively, in embryogenic suspension cultures incubated with 10 µM Mps1 inhibitor. Inhibition of the AaMps1 protein affected the abundance of proteins related to cell cycle division by reducing the accumulation of both cell division control protein 48 and NAP1-related protein 2. In addition, the abundance of the sucrose synthase 3 protein was down-regulated, which reduced sucrose contents. Moreover, a significant reduction in endogenous NO and free putrescine contents was observed in the embryogenic suspension cultures treated with the Mps1 inhibitor. These results show that AaMps1 protein inhibition affects the metabolism of proteins, carbohydrates, NO and PAs, which ultimately interferes in the development of somatic embryogenesis in A. angustifolia.

Key Message

The inhibition of AaMps1 during somatic embryogenesis of Araucaria angustifolia modulates the abundance of proteins and the contents of nitric oxide, carbohydrate and polyamines.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

HSP:

Heat shock protein

LEA:

Late embryogenesis abundant

Mps1:

Monopolar spindle 1

NO:

Nitric oxide

PAs:

Polyamines

PEMs:

Pro-embryogenic masses

Put:

Putrescine

ROS:

Reactive oxygen species

Spd:

Spermidine

Spm:

Spermine

References

  • Alm K, Oredsson S (2009) Cells and polyamines do it cyclically. Essays Biochem 46:63–76. https://doi.org/10.1042/bse0460005

    Article  CAS  PubMed  Google Scholar 

  • Al-Madhoun AS, Sanmartin M, Kanellis AK (2003) Expression of ascorbate oxidase isoenzymes in cucurbits and during development and ripening of melon fruit. Postharvest Biol Technol 27(2):137–146

    Article  CAS  Google Scholar 

  • Aragão VPM, de Souza Ribeiro YR, Reis RS, Macedo AF, Floh EIS, Silveira V, Santa-Catarina C (2016) In vitro organogenesis of Cedrela fissilis Vell. (Meliaceae): the involvement of endogenous polyamines and carbohydrates on shoot development. Plant Cell Tissue Org Cult 124(3):611–620. https://doi.org/10.1007/s11240-015-0919-8

    Article  CAS  Google Scholar 

  • Balbuena TS, Silveira V, Junqueira M, Dias LLC, Santa-Catarina C, Shevchenko A, Floh EIS (2009) Changes in the 2-DE protein profile during zygotic embryogenesis in the Brazilian pine (Araucaria angustifolia). J Proteomics 72(3):337–352. https://doi.org/10.1016/j.jprot.2009.01.011

    Article  CAS  PubMed  Google Scholar 

  • Bechtold U, Richard O, Zamboni A, Gapper C, Geisler M, Pogson B, Karpinski S, Mullineaux PM (2008) Impact of chloroplastic-and extracellular-sourced ROS on high light-responsive gene expression in Arabidopsis. J Exp Bot 59(2):121–133

    Article  CAS  PubMed  Google Scholar 

  • Becker MG, Chan A, Mao X, Girard IJ, Lee S, Mohamed E, Stasolla C, Belmonte MF (2014) Vitamin C deficiency improves somatic embryo development through distinct gene regulatory networks in Arabidopsis. J Exp Bot 65(20):5903–5918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becwar MR, Noland TL, Wyckoff JL (1989) Maturation, germination, and conversion of norway spruce (Picea abies L.) somatic embryos to plants. In Vitro Cell Dev Biol Plant 25(6):575–580

    Article  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39. https://doi.org/10.1146/annurev.arplant.59.032607.092830

    Article  CAS  PubMed  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16(1):1–18. https://doi.org/10.1146/annurev.cellbio.16.1.1

    Article  CAS  PubMed  Google Scholar 

  • Calderan-Rodrigues MJ, Jamet E, Bonassi MBCR, Guidetti-Gonzalez S, Begossi AC, Setem LV, Franceschini LM, Fonseca JG, Labate CA (2014) Cell wall proteomics of sugarcane cell suspension cultures. Proteomics 14(6):738–749

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142(2):775–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

    Article  CAS  PubMed  Google Scholar 

  • De Oliveira EAG, Romeiro NC, da Silva Ribeiro E, Santa-Catarina C, Oliveira AEA, Silveira V, de Souza Filho GA, Venancio TM, Cruz MAL (2012) Structural and functional characterization of the protein kinase Mps1 in Arabidopsis thaliana. PLoS ONE 7(9):e45707. https://doi.org/10.1371/journal.pone.0045707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong A, Liu Z, Zhu Y, Yu F, Li Z, Cao K, Shen W-H (2005) Interacting proteins and differences in nuclear transport reveal specific functions for the NAP1 family proteins in plants. Plant Physiol 138(3):1446–1456. https://doi.org/10.1104/pp.105.060509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • dos Santos ALW, Elbl P, Navarro BV, de Oliveira LF, Salvato F, Balbuena TS, Floh EIS (2016) Quantitative proteomic analysis of Araucaria angustifolia (Bertol.) Kuntze cell lines with contrasting embryogenic potential. J Proteomics 130:180–189

    Article  PubMed  Google Scholar 

  • Douétts-Peres JC, Cruz MAL, Reis RS, Heringer AS, de Oliveira EAG, Elbl PM, Floh EIS, Silveira V, Santa-Catarina C (2016a) Mps1 (monopolar spindle 1) protein inhibition affects cellular growth and pro-embryogenic masses morphology in embryogenic cultures of Araucaria angustifolia (Araucariaceae). PLoS ONE. https://doi.org/10.1371/journal.pone.0153528

    Article  PubMed  PubMed Central  Google Scholar 

  • Douétts-Peres JC, Silveira V, Cruz ML, Santa-Catarina C (2016b) Isolating and measuring the growth and morphology of pro-embryogenic masses in Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae). Bio-protocol 6(23):e2031. https://doi.org/10.21769/bioprotoc.2031

    Article  Google Scholar 

  • Dutra NT, Silveira V, de Azevedo IG, Gomes-Neto LR, Facanha AR, Steiner N, Guerra MP, Floh EIS, Santa-Catarina C (2013) Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. Physiol Plant 148(1):121–132. https://doi.org/10.1111/j.1399-3054.2012.01695.x

    Article  CAS  PubMed  Google Scholar 

  • Elbl P, Campos R, Lira B, Andrade S, Jo L, Dos-Santos A, Coutinho L, Floh E, Rossi M (2015a) Erratum to: Comparative transcriptome analysis of early somatic embryo formation and seed development in Brazilian pine, Araucaria angustifolia (Bertol.) Kuntze. Plant Cell Tissue Org Cult 120(3):917. https://doi.org/10.1007/s11240-015-0730-6

    Article  Google Scholar 

  • Elbl P, Lira BS, Andrade SCS, Jo L, dos Santos ALW, Coutinho LL, Floh EIS, Rossi M (2015b) Comparative transcriptome analysis of early somatic embryo formation and seed development in Brazilian pine, Araucaria angustifolia (Bertol.) Kuntze. Plant Cell Tissue Org 120(3):903–915

    Article  CAS  Google Scholar 

  • Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63(9):3367–3377. https://doi.org/10.1093/Jxb/Err379

    Article  CAS  PubMed  Google Scholar 

  • Farias-Soares FL, Steiner N, Schmidt EC, Pereira MLT, Rogge-Renner GD, Bouzon ZL, Floh ESI, Guerra MP (2014) The transition of proembryogenic masses to somatic embryos in Araucaria angustifolia (Bertol.) Kuntze is related to the endogenous contents of IAA, ABA and polyamines. Acta Physiol Plant 36(7):1853–1865. https://doi.org/10.1007/s11738-014-1560-6

    Article  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61(1):243–282

    Article  CAS  PubMed  Google Scholar 

  • Fraga HPF, Vieira LN, Heringer AS, Puttkammer CC, Silveira V, Guerra MP (2016) DNA methylation and proteome profiles of Araucaria angustifolia (Bertol.) Kuntze embryogenic cultures as affected by plant growth regulators supplementation. Plant Cell Tissue Org Cult 125(2):353–374. https://doi.org/10.1007/s11240-016-0956-y

    Article  CAS  Google Scholar 

  • Galland R, Blervacq A-S, Blassiau C, Smagghe B, Decottignies J-P, Hilbert J-L (2007) Glutathione-S-transferase is detected during somatic embryogenesis in chicory. Plant Signal Behav 2(5):343–348

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghosh S, Pal A (2012) Identification of differential proteins of mungbean cotyledons during seed germination: a proteomic approach. Acta Physiol Plant 34(6):2379–2391

    Article  CAS  Google Scholar 

  • Gonzalez-Reyes JA, Hidalgo A, Caler JA, Palos R, Navas P (1994) Nutrient uptake changes in ascorbate free radical-stimulated onion roots. Plant Physiol 104(1):271–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan Y, Li S-G, Fan X-F, Su Z-H (2016) Application of somatic embryogenesis in woody plants. Front Plant Sci 7:938. https://doi.org/10.3389/fpls.2016.00938

    Article  PubMed  PubMed Central  Google Scholar 

  • Heringer AS, Santa-Catarina C, Silveira V (2018) Insights from proteomic studies into plant somatic embryogenesis. Proteomics. https://doi.org/10.1002/pmic.201700265

    Article  PubMed  Google Scholar 

  • Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kämper J, Sonnewald U, Voll LM (2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol 152(1):293–308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Møller IM, Song S-Q (2012) Proteomics of desiccation tolerance during development and germination of maize embryos. J Proteomics 75(4):1247–1262

    Article  CAS  PubMed  Google Scholar 

  • Iraqi D, Tremblay FM (2001) The role of sucrose during maturation of black spruce (Picea mariana) and white spruce (Picea glauca) somatic embryos. Physiol Plant 111(3):381–388. https://doi.org/10.1034/j.1399-3054.2001.1110316.x

    Article  CAS  PubMed  Google Scholar 

  • Iraqi D, Le Quy V, Lamhamedi MS, Tremblay FM (2005) Sucrose utilization during somatic embryo development in black spruce: involvement of apoplastic invertase in the tissue and of extracellular invertase in the medium. J Plant Physiol 162(1):115–124

    Article  CAS  PubMed  Google Scholar 

  • Jo L, Dos Santos AL, Bueno CA, Barbosa HR, Floh EI (2014) Proteomic analysis and polyamines, ethylene and reactive oxygen species levels of Araucaria angustifolia (Brazilian pine) embryogenic cultures with different embryogenic potential. Tree Physiol 34(1):94–104

    Article  CAS  PubMed  Google Scholar 

  • Kimura S, Suzuki T, Yanagawa Y, Yamamoto T, Nakagawa H, Tanaka I, Hashimoto J, Sakaguchi K (2001) Characterization of plant proliferating cell nuclear antigen (PCNA) and flap endonuclease-1 (FEN-1), and their distribution in mitotic and meiotic cell cycles. Plant J 28(6):643–653

    Article  CAS  PubMed  Google Scholar 

  • Krajňáková J, Häggman H, Gömöry D (2009) Effect of sucrose concentration, polyethylene glycol and activated charcoal on maturation and regeneration of Abies cephalonica somatic embryos. Plant Cell Tissue Org Cult 96(3):251–262

    Article  Google Scholar 

  • Lipavska H, Konradova H (2004) Somatic embryogenesis in conifers: the role of carbohydrate metabolism. In Vitro Cell Dev Biol Plant 40(1):23–30. https://doi.org/10.1079/Ivp2003482

    Article  CAS  Google Scholar 

  • Lu J, Vahala J, Pappinen A (2011) Involvement of ethylene in somatic embryogenesis in Scots pine (Pinus sylvestris L.). Plant Cell Tissue Org Cult 107(1):25–33

    Article  CAS  Google Scholar 

  • Maki H, Ando S, Kodama H, Komamine A (1991) Polyamines and the cell cycle of Catharanthus roseus cells in culture. Plant Physiol 96(4):1008–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maldonado-Cervantes E, Huerta-Ocampo JA, Montero-Morán GM, Barrera-Pacheco A, Espitia-Rangel E, de la Rosa AB (2014) Characterization of Amaranthus cruentus L. seed proteins by 2-DE and LC/MS–MS: identification and cloning of a novel late embryogenesis-abundant protein. J Cereal Sci 60(1):172–178

    Article  CAS  Google Scholar 

  • Meskaoui AE, Tremblay FM (2001) Involvement of ethylene in the maturation of black spruce embryogenic cell lines with different maturation capacities. J Exp Bot 52(357):761–769

    Article  PubMed  Google Scholar 

  • Musacchio A, Salmon ED (2007) The spindle-assembly checkpoint in space and time. Nat Rev Mol Cell Biol 8(5):379–393

    Article  CAS  PubMed  Google Scholar 

  • Nanjo Y, Skultety L, Uváčková Lu, Kn Klubicová, Hajduch M, Komatsu S (2011) Mass spectrometry-based analysis of proteomic changes in the root tips of flooded soybean seedlings. J Proteome Res 11(1):372–385

    Article  PubMed  Google Scholar 

  • Navarro BV, Elbl P, De Souza AP, Jardim V, de Oliveira LF, Macedo AF, dos Santos ALW, Buckeridge MS, Floh EIS (2017) Carbohydrate-mediated responses during zygotic and early somatic embryogenesis in the endangered conifer, Araucaria angustifolia. PLoS ONE 12(7):e0180051. https://doi.org/10.1371/journal.pone.0180051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noah AM, Niemenak N, Sunderhaus S, Haase C, Omokolo DN, Winkelmann T, Braun H-P (2013) Comparative proteomic analysis of early somatic and zygotic embryogenesis in Theobroma cacao L. J Proteomics 78:123–133. https://doi.org/10.1016/j.jprot.2012.11.007

    Article  CAS  PubMed  Google Scholar 

  • Osti RZ, Andrade JBR, Souza JP, Silveira V, Balbuena TS, Guerra MP, Franco DW, Floh EIS, Santa-Catarina C (2010) Nitrosyl ethylenediaminetetraacetate ruthenium(II) complex promotes cellular growth and could be used as nitric oxide donor in plants. Plant Sci 178(5):448–453. https://doi.org/10.1016/j.plantsci.2010.02.006

    Article  CAS  Google Scholar 

  • Ötvös K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Szucs A, Bottka S, Dudits D, Fehér A (2005) Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J 43(6):849–860. https://doi.org/10.1111/j.1365-313X.2005.02494.x

    Article  CAS  PubMed  Google Scholar 

  • Park S, Rancour DM, Bednarek SY (2008) In planta analysis of the cell cycle-dependent localization of AtCDC48A and its critical roles in cell division, expansion, and differentiation. Plant Physiol 148(1):246–258. https://doi.org/10.1104/pp.108.121897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reis RS, de Moura Vale E, Heringer AS, Santa-Catarina C, Silveira V (2016) Putrescine induces somatic embryo development and proteomic changes in embryogenic callus of sugarcane. J Proteomics 130:170–179

    Article  CAS  PubMed  Google Scholar 

  • Riou-Khamlichi C, Menges M, Healy JS, Murray JA (2000) Sugar control of the plant cell cycle: differential regulation of Arabidopsis D-type cyclin gene expression. Mol Cell Biol 20(13):4513–4521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson AR, Dauwe R, Ukrainetz NK, Cullis IF, White R, Mansfield SD (2009) Predicting the regenerative capacity of conifer somatic embryogenic cultures by metabolomics. Plant Biotechnol J 7(9):952–963

    Article  CAS  PubMed  Google Scholar 

  • Santa-Catarina C, Silveira V, Balbuena TS, Viana AM, Estelita MEM, Handro W, Floh EI (2006) IAA, ABA, polyamines and free amino acids associated with zygotic embryo development of Ocotea catharinensis. Plant Growth Regul 49:237–247

    Article  CAS  Google Scholar 

  • Santa-Catarina C, Silveira V, Scherer GFE, Floh EIS (2007) Polyamine and nitric oxide levels relate with morphogenetic evolution in somatic embryogenesis of Ocotea catharinensis. Plant Cell Tissue Org Cult 90(1):93–101. https://doi.org/10.1007/s11240-007-9259-7

    Article  CAS  Google Scholar 

  • Saruhan N, Terzi R, Saglam A, Kadioglu A (2009) The relationship between leaf rolling and ascorbate-glutathione cycle enzymes in apoplastic and symplastic areas of Ctenanthe setosa subjected to drought stress. Biol Res 42(3):315–326

    Article  CAS  PubMed  Google Scholar 

  • Sharifi G, Ebrahimzadeh H, Ghareyazie B, Gharechahi J, Vatankhah E (2012) Identification of differentially accumulated proteins associated with embryogenic and non-embryogenic calli in saffron (Crocus sativus L.). Proetome Sci 10(1):3

    Article  CAS  Google Scholar 

  • Silveira V, Santa-Catarina C, Tun NN, Scherer GFE, Handro W, Guerra MP, Floh EIS (2006) Polyamine effects on the endogenous polyamine contents, nitric oxide release, growth and differentiation of embryogenic suspension cultures of Araucaria angustifolia (Bert.) O. Ktze. Plant Sci 171(1):91–98. https://doi.org/10.1016/j.plantsci.2006.02.015

    Article  CAS  Google Scholar 

  • Silveira V, Santa-Catarina C, Balbuena TS, Moraes FMS, Ricart CAO, Sousa MV, Guerra MP, Handro W, Floh EIS (2008) Endogenous abscisic acid and protein contents during seed development of Araucaria angustifolia. Biol Plant 52(1):101–104. https://doi.org/10.1007/s10535-008-0018-3

    Article  CAS  Google Scholar 

  • Steiner N, Santa-Catarina C, Silveira V, Floh EIS, Guerra MP (2007) Polyamine effects on growth and endogenous hormones levels in Araucaria angustifolia embryogenic cultures. Plant Cell Tissue Org Cult 89(1):55–62. https://doi.org/10.1007/s11240-007-9216-5

    Article  CAS  Google Scholar 

  • Steiner N, Farias-Soares FL, Schmidt ÉC, Pereira ML, Scheid B, Rogge-Renner GD, Bouzon ZL, Schmidt D, Maldonado S, Guerra MP (2016) Toward establishing a morphological and ultrastructural characterization of proembryogenic masses and early somatic embryos of Araucaria angustifolia (Bert.) O. Kuntze. Protoplasma 253(2):487–501. https://doi.org/10.1007/s00709-015-0827-0

    Article  CAS  PubMed  Google Scholar 

  • Strzalka W, Ziemienowicz A (2011) Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Ann Bot 107(7):1127–1140

    Article  CAS  PubMed  Google Scholar 

  • Strzalka W, Kaczmarek A, Naganowska B, Ziemienowicz A (2010) Identification and functional analysis of PCNA1 and PCNA-like1 genes of Phaseolus coccineus. J Exp Bot 61(3):873–888

    Article  CAS  PubMed  Google Scholar 

  • Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4(10):401–407

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Wu Y, Zou H, Su S, Li S, Shan X, Xi J, Yuan Y (2013) Comparative proteomic analysis of the H99 inbred maize (Zea mays L.) line in embryogenic and non-embryogenic callus during somatic embryogenesis. Plant Cell Tissue Org Cult 113(1):103–119. https://doi.org/10.1007/s11240-012-0255-1

    Article  CAS  Google Scholar 

  • Taber RP, Zhang C, Hu W-S (1998) Kinetics of Douglas-fir (Pseudotsuga menziesii) somatic embryo development. Can J Bot 76(5):863–871

    CAS  Google Scholar 

  • Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240(1):1–18

    Article  CAS  PubMed  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GFE (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47(3):346–354. https://doi.org/10.1093/pcp/pci252

    Article  CAS  PubMed  Google Scholar 

  • Vale EM, Heringer AS, Barroso T, Ferreira AT, da Costa MN, Perales JEA, Santa-Catarina C, Silveira V (2014) Comparative proteomic analysis of somatic embryo maturation in Carica papaya L. Proetome Sci 12(1):37

    Article  Google Scholar 

  • Vale EM, Reis RS, Passamani LZ, Santa-Catarina C, Silveira V (2018) Morphological analyses and variation in carbohydrate content during the maturation of somatic embryos of Carica papaya. Physiol Mol Biol Plants. https://doi.org/10.1007/s12298-017-0501-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira LdN, Santa-Catarina C, de Freitas Fraga HP, Wendt dos Santos AL, Steinmacher DA, Schlogl PS, Silveira V, Steinera N, Segal Floh EL, Guerra MP (2012) Glutathione improves early somatic embryogenesis in Araucaria angustifolia (Bert) O. Kuntze by alteration in nitric oxide emission. Plant Sci 195:80–87. https://doi.org/10.1016/j.plantsci.2012.06.011

    Article  CAS  Google Scholar 

  • Weiger TM, Hermann A (2014) Cell proliferation, potassium channels, polyamines and their interactions: a mini review. Amino Acids 46(3):681–688

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Zhang G, Zhang J, Ju L, Zhu Q, Song Y, Wang J, Niu N, Ma S (2015) Molecular cloning and characterization of a proliferating cell nuclear antigen gene by chemically induced male sterility in wheat (Triticum aestivum L.). Genet Mol Res 14(4):12030–12042

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Funding for this work was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (444453/2014-8) and the Fundação Carlos Chagas Filho de Amparo a Pesquisa no Estado do Rio de Janeiro (FAPERJ) (E26/010.001507/2014; E26/202.969/2016). This study was financed also by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. VPMA and RSR acknowledge the scholarship funded by FAPERJ. JCDP thanks the CAPES – Finance Code 001 for the scholarship.

Author information

Authors and Affiliations

  1. Laboratório de Biologia Celular e Tecidual, Centro de Biociências e Biotecnologia (CBB), Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Av. Alberto Lamego 2000, Campos Dos Goytacazes, RJ, 28013-602, Brazil

    Jackellinne Caetano Douétts-Peres, Victor Paulo Mesquita Aragão & Claudete Santa-Catarina

  2. Laboratório de Biotecnologia Vegetal, Núcleo em Ecologia e Desenvolvimento Sócio-Ambiental de Macaé, Universidade Federal do Rio de Janeiro, Macaé, RJ, Brazil

    Marco Antônio Lopes Cruz

  3. Laboratório de Biotecnologia, CBB, UENF, Campos Dos Goytacazes, RJ, Brazil

    Ricardo Souza Reis & Vanildo Silveira

  4. Unidade de Biologia Integrativa, Setor de Genômica e Proteômica, UENF, Campos Dos Goytacazes, RJ, Brazil

    Ricardo Souza Reis & Vanildo Silveira

  5. Laboratório de Biologia Celular de Plantas, Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil

    Paula Elbl, André Luis Wendt dos Santos & Eny Iochevet Segal Floh

Authors
  1. Jackellinne Caetano Douétts-Peres
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Victor Paulo Mesquita Aragão
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marco Antônio Lopes Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo Souza Reis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paula Elbl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. André Luis Wendt dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eny Iochevet Segal Floh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vanildo Silveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudete Santa-Catarina
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JCDP conducted the experiments, analyzed the data, and wrote the manuscript. JCDP, MALC, VS, EISF, and CSC conceived and designed the experiments and revised the manuscript. RSR, ALWS, PE and VPAM participated in the experiments and data analysis. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Claudete Santa-Catarina.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Communicated by Ali R. Alan.

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.

Figure S1

Settled cell volume (SCV) of A. angustifolia embryogenic suspension cultures during 30 days of incubation with and without 10 μM Mps1 inhibitor SP600125. (Mean ± SD; n = 5) (TIFF 366 kb)

Figure S2

Venn diagram of identified proteins (a) and total protein contents (µg.g−1 FM) (b) in embryogenic suspension cultures of A. angustifolia at 15 days of incubation in the presence of different concentrations (0 or 10 µM) of Mps1 inhibitor (mean ± standard deviation; n = 3). Differentially abundant proteins in (a) were classified as up- or down-regulated by comparing the differential abundance comparing the 10 µM Mps1 inhibitor treatment with the control treatment (without Mps1 inhibitor) (TIFF 204 kb)

Figure S3

Kyoto Encyclopedia of Genes and Genomes (KEGG) map of differentially regulated proteins that are related to carbohydrate metabolism and were identified in the embryogenic suspension cultures of A. angustifolia between the 10 µM Mps1 inhibitor treatment and the control treatment (without Mps1 inhibitor) (TIFF 165 kb)

Supplementary material 4 (PDF 552 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Douétts-Peres, J.C., Aragão, V.P.M., Cruz, M.A.L. et al. AaMps1 protein inhibition regulates the protein profile, nitric oxide, carbohydrate and polyamine contents in embryogenic suspension cultures of Araucaria angustifolia (Bertol.) Kuntze (Araucariaceae). Plant Cell Tiss Organ Cult 138, 273–286 (2019). https://doi.org/10.1007/s11240-019-01623-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-019-01623-5

Keywords

Search

Navigation