Trichostatin A Triggers an Embryogenic Transition in Arabidopsis Explants via an Auxin-Related Pathway
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
30271420
PubMed Central
PMC6146766
DOI
10.3389/fpls.2018.01353
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis thaliana, auxin, epigenetics, histone acetylation, in vitro culture, somatic embryogenesis, transcription factors, trichostatin A,
- Publikační typ
- časopisecké články MeSH
Auxin is an important regulator of plant ontogenies including embryo development and the exogenous application of this phytohormone has been found to be necessary for the induction of the embryogenic response in plant explants that have been cultured in vitro. However, in the present study, we show that treatment of Arabidopsis explants with trichostatin A (TSA), which is a chemical inhibitor of histone deacetylases, induces somatic embryogenesis (SE) without the exogenous application of auxin. We found that the TSA-treated explants generated somatic embryos that developed efficiently on the adaxial side of the cotyledons, which are the parts of an explant that are involved in auxin-induced SE. A substantial reduction in the activity of histone deacetylase (HDAC) was observed in the TSA-treated explants, thus confirming a histone acetylation-related mechanism of the TSA-promoted embryogenic response. Unexpectedly, the embryogenic effect of TSA was lower on the auxin-supplemented media and this finding further suggests an auxin-related mechanism of TSA-induced SE. Congruently, we found a significantly increased content of indolic compounds, which is indicative of IAA and an enhanced DR5::GUS signal in the TSA-treated explants. In line with these results, two of the YUCCA genes (YUC1 and YUC10), which are involved in auxin biosynthesis, were found to be distinctly up-regulated during TSA-induced SE and their expression was colocalised with the explant sites that are involved in SE. Beside auxin, ROS were extensively accumulated in response to TSA, thereby indicating that a stress-response is involved in TSA-triggered SE. Relevantly, we showed that the genes encoding the transcription factors (TFs) that have a regulatory function in auxin biosynthesis including LEC1, LEC2, BBM, and stress responses (MYB118) were highly up-regulated in the TSA-treated explants. Collectively, the results provide several pieces of evidence about the similarities between the molecular pathways of SE induction that are triggered by TSA and 2,4-D that involve the activation of the auxin-responsive TF genes that have a regulatory function in auxin biosynthesis and stress responses. The study suggests the involvement of histone acetylation in the auxin-mediated release of the embryogenic program of development in the somatic cells of Arabidopsis.
Department of Genetics University of Silesia in Katowice Katowice Poland
Department of Molecular Biology and Genetics Medical University of Silesia Katowice Poland
Scanning Electron Microscopy Laboratory University of Silesia in Katowice Katowice Poland
Zobrazit více v PubMed
Abrahamsson M., Valladares S., Merino I., Larsson E., von Arnold S. (2017). Degeneration pattern in somatic embryos of Pinus sylvestris L. In Vitro Cell Dev. Plant 53 86–96. 10.1007/s11627-016-9797-y PubMed DOI PMC
Alinsug M. V., Yu C. W., Wu K. (2009). Phylogenetic analysis, subcellular localization, and expression patterns of RPD3/HDA1 family histone deacetylases in plants. BMC Plant Biol. 9:37. 10.1186/1471-2229-9-37 PubMed DOI PMC
Bai B., Su Y. H., Yuan J., Zhang X. S. (2013). Induction of somatic embryos in Arabidopsis requires local YUCCA expression mediated by the down-regulation of ethylene biosynthesis. Mol. Plant 6 1247–1260. 10.1093/mp/sss154 PubMed DOI
Barthole G., To A., Marchive C., Brunaud V., Soubigou-Taconnat L., Berger N., et al. (2014). MYB118 represses endosperm maturation in seeds of Arabidopsis. Plant Cell 26 3519–3537. 10.1105/tpc.114.130021 PubMed DOI PMC
Beigh S. A., Ahad W. A., Bhat R. A., Nabi N., Ahmed T., Reshi M., et al. (2017). Role of trichostatin A as reprogramming enhancer on in vitro development of cloned embryos: a review. Int. J. Curr. Microbiol. Appl. Sci. 6 1055–1058. 10.20546/ijcmas.2017.611.123 DOI
Belide S., Zhou X. R., Kennedy Y., Lester G., Shrestha P., Petrie J. R., et al. (2013). Rapid expression and validation of seed-specific constructs in transgenic LEC2 induced somatic embryos of Brassica napus. Plant Cell Tissue Organ. Cult. 113 543–553. 10.1007/s11240-013-0295-1 DOI
Birnbaum K. D., Roudier F. (2017). Epigenetic memory and cell fate reprogramming in plants. Regeneration 4 15–20. 10.1002/reg2.73 PubMed DOI PMC
Boulard C., Fatihi A., Lepiniec L., Dubreucq B. (2017). Regulation and evolution of the interaction of the seed B3 transcription factors with NF-Y subunits. Biochim. Biophys. Acta 1860 1069–1078. 10.1016/j.bbagrm.2017.08.008 PubMed DOI
Boutilier K., Offringa R., Sharma V. K., Kieft H., Ouellet T., Zhang L., et al. (2002). Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14 1737–1749. 10.1105/tpc.001941 PubMed DOI PMC
Boycheva I., Vassileva V., Iantcheva A. (2014). Histone acetyltransferases in plant development and plasticity. Curr. Genomics 15 28–37. 10.2174/138920291501140306112742 PubMed DOI PMC
Bric J. M., Bostock R. M., Silverstonet S. E. (1991). Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl. Environ. Microbiol. 57 535–538. PubMed PMC
Brosch G., Lusser A., Goralik-Schramel M., Loidl P. (1996). Purification and characterization of a high molecular weight histone deacetylase complex (HD2) of maize embryos. Biochemistry 35 15907–15914. 10.1021/bi961294x PubMed DOI
Brundrett M. C., Kendrick B., Peterson C. A. (1991). Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol-glycerol. Biotech. Histochem. 66 111–116. 10.3109/10520299109110562 PubMed DOI
Buszewicz D., Archacki R., Palusiński A., Kotliński M., Fogtman A., Iwanicka-Nowicka R., et al. (2016). HD2C histone deacetylase and a SWI/SNF chromatin remodelling complex interact and both are involved in mediating the heat stress response in Arabidopsis. Plant Cell Environ. 39 2108–2122. 10.1111/pce.12756 PubMed DOI
Chang S., Pikaard C. S. (2005). Transcript profiling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation. J. Biol. Chem. 280 796–804. 10.1074/jbc.M409053200 PubMed DOI
Chanvivattana Y., Bishopp A., Schubert D., Stock C., Moon Y., Sung Z. R., et al. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131 5263–5276. 10.1242/dev.01400 PubMed DOI
Charrière F., Sotta B., Miginiac E., Hahne G. (1999). Induction of adventitious shoots or somatic embryos on in vitro cultured zygotic embryos of Helianthus annuus: variation of endogenous hormone levels. Plant Physiol Biochem. 37 751–757. 10.1016/S0981-9428(00)86688-7 DOI
Chen J. T., Chang W. C. (2004). TIBA affects the induction of direct somatic embryogenesis from leaf explants of Oncidium. Plant Cell Tissue Organ Cult. 79 315–320. 10.1007/s11240-004-4613-5 DOI
Cheng W. H., Wang F. L., Cheng X. Q., Zhu Q. H., Sun Y. Q., Zhu H. G., et al. (2015). Polyamine and its metabolite H2O2 play a key role in the conversion of embryogenic callus into somatic embryos in upland cotton (Gossypium hirsutum L.). Front. Plant Sci. 6:1063. 10.3389/fpls.2015.01063 PubMed DOI PMC
Cheng W. H., Zhu H. G., Tian W. G., Zhu S. H., Xiong X. P., Sun Y. Q., et al. (2016). De novo transcriptome analysis reveals insights into dynamic homeostasis regulation of somatic embryogenesis in upland cotton (G. hirsutum L.). Plant Mol. Biol. 92 279–292. 10.1007/s11103-016-0511-6 PubMed DOI PMC
Cheng Y., Dai X., Zhao Y. (2007). Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19 2430–2439. 10.1105/tpc.107.053009 PubMed DOI PMC
Chinnusamy V., Zhu J. K. (2009). Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12 133–139. 10.1016/j.pbi.2008.12.006 PubMed DOI PMC
Chitwood D. H., Nogueira F. T., Howell M. D., Montgomery T. A., Carrington J. C., Timmermans M. C. (2009). Pattern formation via small RNA mobility. Genes Dev. 23 549–554. 10.1101/gad.1770009 PubMed DOI PMC
Choudhury F. K., Rivero R. M., Blumwald E., Mittler R. (2017). Reactive oxygen species, abiotic stress and stress combination. Plant J. 90 856–867. 10.1111/tpj.13299 PubMed DOI
Cueva-Agila A. Y., Medina J., Concia L., Cella R. (2016). “Effects of plant growth regulator, auxin polar transport inhibitors on somatic embryogenesis and CmSERK gene expression in Cattleya maxima (Lindl.),” in Somatic Embryogenesis in Ornamentals and Its Applications, ed. Mujib A. (New Delhi: Springer; ), 255–267. 10.1007/978-81-322-2683-3_16 DOI
Damaskos C., Valsami S., Kontos M., Spartalis E., Kalampokas T., Kalampokas E., et al. (2017). Histone deacetylase inhibitors: an attractive therapeutic strategy against breast cancer. Anticancer. Res. 37 35–46. 10.21873/anticanres.11286 PubMed DOI
Deng W., Luo K., Li Z., Yang Y. (2009). A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci. 177 43–48. 10.1016/j.plantsci.2009.03.009 DOI
Duffy S. K., Friesen H., Baryshnikova A., Lambert J. P., Chong Y. T., Figeys D., et al. (2012). Exploring the yeast acetylome using functional genomics. Cell 149 936–948. 10.1016/j.cell.2012.02.064 PubMed DOI PMC
Eberharter A., Becker P. B. (2002). Histone acetylation: a switch between repressive and permissive chromatin. EMBO Rep. 3 224–229. 10.1093/embo-reports/kvf053 PubMed DOI PMC
Elhiti M., Hebelstrup K. H., Wang A., Li C., Cui Y., Hill R. D., et al. (2013). Function of type–2 Arabidopsis hemoglobin in the auxin-mediated formation of embryogenic cells during morphogenesis. Plant J. 74 946–958. 10.1111/tpj.12181 PubMed DOI
Elhiti M., Stasolla C. (2015). “ROS Signalling in plant embryogenesis,” iIn Reactive Oxygen and Nitrogen Species Signaling and Communication in Plants, eds Gupta K., Igamberdiev A. (Heidelberg: Springer International Publishing; ), 197–214.
Fehér A. (2015). Somatic embryogenesis - Stress-induced remodeling of plant cell fate. Biochim. Biophys. Acta 1849 385–402. 10.1016/j.bbagrm.2014.07.005 PubMed DOI
Feng S., Jacobsen S. E., Reik W. (2010). Epigenetic reprogramming in plant and animal development. Science 330 622–627. 10.1126/science.1190614 PubMed DOI PMC
Feng W., Michaels S. D. (2015). Accessing the inaccessible: the organization, transcription, replication, and repair of heterochromatin in plants. Annu. Rev. Genet. 49 439–459. 10.1146/annurev-genet-112414-055048 PubMed DOI
Finnin M. S., Donigian J. R., Cohen A., Richon V. M., Rifkind R. A., Marks P. A., et al. (1999). Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401 188–193. 10.1038/43710 PubMed DOI
Gaj M. D. (2001). Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of Arabidopsis thaliana. Plant Cell Tissue Organ. Cult. 64 39–46. 10.1007/978-1-61737-988-8_18 DOI
Gaj M. D. (2011). Somatic embryogenesis and plant regeneration in the culture of Arabidopsis thaliana (L.) Heynh. immature zygotic embryos. Methods Mol. Biol InPlantEmbryoCultureHumanaPress. 710 257–265. PubMed
Gaj M. D., Zhang S., Harada J. J., Lemaux P. G. (2005). LEAFY COTYLEDON genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222 977–988. 10.1007/s00425-005-0041-y PubMed DOI
Gamborg O. L., Miller R. A., Ojima K. (1968). Nutrient requirement of suspension culture of soybean root cells. Exp. Cell Res. 50 151–158. 10.1016/0014-4827(68)90403-5 PubMed DOI
Garcia D., Collier S. A., Byrne M. E., Martienssen R. A. (2006). Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr. Biol. 16 933–938. 10.1016/j.cub.2006.03.064 PubMed DOI
Gendrel A. V., Lippman Z., Martienssen R., Colot V. (2005). Profiling histone modification patterns in plants using genomic tiling microarrays. Nat. Methods 2 213–218. 10.1038/nmeth0305-213 PubMed DOI
Gliwicka M., Nowak K., Balazadeh S., Mueller-Roeber B., Gaj M. D. (2013). Extensive modulation of the transcription factor transcriptome during somatic embryogenesis in Arabidopsis thaliana. PLoS One 8:e69261. 10.1371/journal.pone.0069261 PubMed DOI PMC
Gliwicka M., Nowak K., Cieśla E., Gaj M. D. (2012). Expression of seed storage product genes (CRA1 and OLEO4) in embryogenic cultures of somatic tissues of Arabidopsis. Plant Cell Tissue Organ. Cult. 109 235–245. 10.1007/s11240-011-0089-2 DOI
Godee C., Mira M. M., Wally O., Hill R. D., Stasolla C. (2017). Cellular localization of the Arabidopsis class 2 phytoglobin influences somatic embryogenesis. J. Exp. Bot. 68 1013–1023. 10.1093/jxb/erx003 PubMed DOI PMC
Görisch S. M., Wachsmuth M., Toth K. F., Lichter P., Rippe K. (2005). Histone acetylation increases chromatin accessibility. J. Cell Sci. 118 5825–5834. 10.1242/jcs.02689 PubMed DOI
Grigg S. P., Galinha C., Kornet N., Canales C., Scheres B., Tsiantis M. (2009). Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr. Biol. 19 1485–1490. 10.1016/j.cub.2009.06.070 PubMed DOI
Grzyb M., Kalandyk A., Waligórski P., Mikuła A. (2017). The content of endogenous hormones and sugars in the process of early somatic embryogenesis in the tree fern Cyathea delgadii Sternb. Plant Cell Tissue Organ. Cult. 129 387–397. 10.1007/s11240-017-1185-8 DOI
Grzybkowska D., Morończyk J., Wójcikowska B., Gaj M. D. (2018). Azacitidine (5-AzaC)-treatment and mutations in DNA methylase genes affect embryogenic response and expression of the genes that are involved in somatic embryogenesis in Arabidopsis. Plant Growth Regul. 85 243–256. 10.1007/s10725-018-0389-1 DOI
Guan C., Wu B., Yu T., Wang Q., Krogan N. T., Liu X., et al. (2017). Spatial auxin signaling controls leaf flattening in Arabidopsis. Curr. Biol. 27 2940–2950. 10.1016/j.cub.2017.08.042 PubMed DOI PMC
Halim N. A. A., Tan B. C., Midin M. R., Madon M., Khalid N., Yaacob J. S. (2017). Abscisic acid and salinity stress induced somaclonal variation and increased histone deacetylase (HDAC) activity in Ananas comosus var. MD2. Plant Cell Tissue Organ Cult. 133 1–13.
Harding E. W., Tang W., Nichols K. W., Fernandez D. E., Perry S. E. (2003). Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-LIKE15. Plant Physiol. 133 653–663. 10.1104/pp.103.023499 PubMed DOI PMC
Hartl M., Füßl M., Boersema P. J., Jost J., Kramer K., Bakirbas A., et al. (2017). Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis. Mol. Syst. Biol. 13:949. 10.15252/msb.20177819 PubMed DOI PMC
Hattori N., Nishino K., Ko Y. G., Hattori N., Ohgane J., Tanaka S., et al. (2004). Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J. Biol. Chem. 279 17063–17069. 10.1074/jbc.M309002200 PubMed DOI
He X. J., Chen T., Zhu J. K. (2011). Regulation and function of DNA methylation in plants and animals. Cell Res. 54 442–465. 10.1038/cr.2011.23 PubMed DOI PMC
Heidmann I., de Lange B., Lambalk J., Angenent G. C., Boutilier K. (2011). Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep. 30 1107–1115. 10.1007/s00299-011-1018-x PubMed DOI PMC
Horstman A., Bemer M., Boutilier K. (2017a). A transcriptional view on somatic embryogenesis. Regeneration 4 201–216. 10.1002/reg2.91 PubMed DOI PMC
Horstman A., Li M., Heidmann I., Weemen M., Chen B., Muino J. M., et al. (2017b). The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-LEC2 network to induce somatic embryogenesis. Plant Physiol. 175 848–857. 10.1104/pp.17.00232 PubMed DOI PMC
Ikeuchi M., Iwase A., Rymen B., Harashima H., Shibata M., Ohnuma M., et al. (2015). PRC2 represses dedifferentiation of mature somatic cells in Arabidopsis. Nat. Plants 1:15089. 10.1038/nplants.2015.89 PubMed DOI
Inoue K., Oikawa M., Kamimura S., Ogonuki N., Nakamura T., Nakano T., et al. (2015). Trichostatin A specifically improves the aberrant expression of transcription factor genes in embryos produced by somatic cell nuclear transfer. Sci. Rep. 5:10127. 10.1038/srep10127 PubMed DOI PMC
Jefferson R. A., Kavanagh T. A., Bevan M. W. (1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6 3901–3907. PubMed PMC
Jia H., Suzuki M., McCarty D. R. (2014). Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks. Wires Dev. Biol. 3 135–145. 10.1002/wdev.126 PubMed DOI PMC
Jiang F., Ryabova D., Diedhiou J., Hucl P., Randhawa H., Marillia E. F., et al. (2017). Trichostatin A increases embryo and green plant regeneration in wheat. Plant Cell Rep. 36 1701–1706. 10.1007/s00299-017-2183-3 PubMed DOI
Jung M., Hoffmann K., Brosch G., Loidl P. (1997). Analogues of trichosòatin a and trapoxin B as histone deacetylase inhibitors. Bioorg. Med. Chem. Lett. 7 1655–1658. 10.1016/S0960-894X(97)00284-9 DOI
Junker A., Mönke G., Rutten T., Keilwagen J., Seifert M., Thi T. M. N., et al. (2012). Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. Plant J. 71 427–442. 10.1111/j.1365-313X.2012.04999.x PubMed DOI
Kairong C., Gengsheng X., Xinmin L., Gengmei X., Yafu W. (1999). Effect of hydrogen peroxide on somatic embryogenesis of Lycium barbarum L. Plant Sci. 146 9–16. 10.1016/S0168-9452(99)00087-4 DOI
Kasahara H. (2016). Current aspects of auxin biosynthesis in plants. Biosci Biotech. Biochem. 80 34–42. 10.1080/09168451.2015.1086259 PubMed DOI
Kidner C. A., Martienssen R. A. (2004). Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81. 10.1038/nature02366 PubMed DOI
Kishigami S., Van Thuan N., Hikichi T., Ohta H., Wakayama S., Mizutani E., et al. (2006). Epigenetic abnormalities of the mouse paternal zygotic genome associated with microinsemination of round spermatids. Dev. Biol. 289 195–205. 10.1016/j.ydbio.2005.10.026 PubMed DOI
Kraut M., Wójcikowska B., Ledwoń A., Gaj M. D. (2011). Immature zygotic embryo cultures of Arabidopsis - a model system for molecular studies on morphogenic pathways induced in vitro. Acta Biol. Cracov. Bot. 53 59–67. 10.2478/v10182-011-0028-x DOI
Kurczyńska E. U., Gaj M. D., Ujczak A., Mazur E. (2007). Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh. Planta 226 619–628. 10.1007/s00425-007-0510-6 PubMed DOI
Lauria M., Rossi V. (2011). Epigenetic control of gene regulation in plants. Biochim. Biophys. Acta 1809 369–378. 10.1016/j.bbagrm.2011.03.002 PubMed DOI
Lee K., Park O. S., Jung S. J., Seo P. J. (2016). Histone deacetylation-mediated cellular dedifferentiation in Arabidopsis. J. Plant Physiol. 191 95–100. 10.1016/j.jplph.2015.12.006 PubMed DOI
Leljak-Levanić D., Bauer N., Mihaljević S., Jelaska S. (2004). Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep. 23 120–127. 10.1007/s00299-004-0819-6 PubMed DOI
Li H., Soriano M., Cordewener J., Muiño J. M., Riksen T., Fukuoka H., et al. (2014). The histone deacetylase inhibitor trichostatin a promotes totipotency in the male gametophyte. Plant Cell 26 195–209. 10.1105/tpc.113.116491 PubMed DOI PMC
Li W., Liu H., Cheng Z. J., Su Y. H., Han H. N., Zhang Y., et al. (2011). DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet. 7:e1002243. 10.1371/journal.pgen.1002243 PubMed DOI PMC
Liu X., Yang S., Zhao M., Luo M., Yu C. W., Chen C. Y., et al. (2014). Transcriptional repression by histone deacetylases in plants. Mol. Plant 7 764–772. 10.1093/mp/ssu033 PubMed DOI
LoSchiavo F., Pitto L., Giuliano G., Torti G., Nuti-Ronchi V., Marazziti D., et al. (1989). DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs. Theor. Appl. Genet. 77 325–331. 10.1007/BF00305823 PubMed DOI
Lotan T., Ohto M. A., Yee K. M., West M. A., Lo R., Kwong R. W., et al. (1998). Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93 1195–1205. 10.1016/S0092-8674(00)81463-4 PubMed DOI
Lowe K., Wu E., Wang N., Hoerster G., Hastings C., Cho M. J., et al. (2016). Morphogenic regulators BABY BOOM and WUSCHEL improve monocot transformation. Plant Cell 28 1998–2015. 10.1105/tpc.16.00124 PubMed DOI PMC
Luo M., Cheng K., Xu Y., Yang S., Wu K. (2017). Plant responses to abiotic stress regulated by histone deacetylases. Front. Plant Sci. 8:2147. 10.3389/fpls.2017.02147 PubMed DOI PMC
Ma X., Zhang C., Zhang B., Yang C., Li S. (2016). Identification of genes regulated by histone acetylation during root development in Populus trichocarpa. BMC Genomics 17:96. 10.1186/s12864-016-2407-x PubMed DOI PMC
Machida C., Nakagawa A., Kojima S., Takahashi H., Machida Y. (2015). The complex of ASYMMETRIC LEAVES (AS) proteins plays a central role in antagonistic interactions of genes for leaf polarity specification in Arabidopsis. Wires Dev. Biol. 4 655–671. 10.1002/wdev.196 PubMed DOI PMC
Magnani E., Jiménez-Gómez J. M., Soubigou-Taconnat L., Lepiniec L., Fiume E. (2017). Profiling the onset of somatic embryogenesis in Arabidopsis. BMC Genomics 18:998. 10.1186/s12864-017-4391-1 PubMed DOI PMC
Mengel A., Ageeva A., Georgii E., Bernhardt J., Wu K., Durner J., et al. (2017). Nitric oxide modulates histone acetylation at stress genes by inhibition of histone deacetylases. Plant Physiol. 173 1434–1452. 10.1104/pp.16.01734 PubMed DOI PMC
Michalczuk L., Ribnicky D. M., Cooke T. J., Cohen J. D. (1992). Regulation of indole-3-acetic acid biosynthetic pathways in carrot cell cultures. Plant Physiol. 100 1346–1353. 10.1104/pp.100.3.1346 PubMed DOI PMC
Mittler R. (2017). ROS are good. Trends Plant Sci. 22 11–19. 10.1016/j.tplants.2016.08.002 PubMed DOI
Miyamoto K., Tajima Y., Yoshida K., Oikawa M., Azuma R., Allen G. E., et al. (2017). Reprogramming towards totipotency is greatly facilitated by synergistic effects of small molecules. Biol. Open 6 415–424. 10.1242/bio.023473 PubMed DOI PMC
Mozgová I., Muñoz-Viana R., Hennig L. (2017). PRC2 represses hormone-induced somatic embryogenesis in vegetative tissue of Arabidopsis thaliana. PLoS Genet 13:e1006562. 10.1371/journal.pgen.1006562 PubMed DOI PMC
Murashige T., Skoog F. A. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol. Plant. 15 473–497. 10.1111/j.1399-3054.1962.tb08052.x DOI
Nguyen H. N., Kim J. H., Jeong C. Y., Hong S. W., Lee H. (2013). Inhibition of histone deacetylation alters Arabidopsis root growth in response to auxin via PIN1 degradation. Plant Cell Rep. 32 1625–1636. 10.1007/s00299-013-1474-6 PubMed DOI
Nic-Can G. I., López-Torres A., Barredo-Pool F., Wrobel K., Loyola-Vargas V. M., Rojas-Herrera R., et al. (2013). New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS One 8:e72160. 10.1371/journal.pone.0072160 PubMed DOI PMC
Nowak K., Gaj M. D. (2016). “Transcription factors in the regulation of somatic embryogenesis,” in Loyola-Vargas V., Ochoa-Alejo N. eds Somatic Embryogenesis, Aspects Fundamental, and Applications (Cham: Springer; ), 53–79. 10.1007/978-3-319-33705-0_5 DOI
Nowak K., Wojcikowska B., Szyrajew K., Gaj M. D. (2012). Evaluation of different embryogenic systems for production of true somatic embryos in Arabidopsis. Biol. Plantarum 56 401–408. 10.1007/s10535-012-0063-9 DOI
Ou J. N., Torrisani J., Unterberger A., Provençal N., Shikimi K., Karimi M., et al. (2007). Histone deacetylase inhibitor Trichostatin A induces global and gene-specific DNA demethylation in human cancer cell lines. Biochem. Pharmacol. 73 1297–1307. 10.1016/j.bcp.2006.12.032 PubMed DOI
Pandey R., Muller A., Napoli C. A., Selinger D. A., Pikaard C. S., Richards E. J., et al. (2002). Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Res. 30 5036–5055. 10.1093/nar/gkf660 PubMed DOI PMC
Pasternak T., Prinsen E., Ayaydin F., Miskolczi P., Potters G., Asard H., et al. (2002). The role of auxin, pH and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol. 129 1807–1819. 10.1104/pp.000810 PubMed DOI PMC
Peserico A., Simone C. (2011). Physical and functional HAT/HDAC interplay regulates protein acetylation balance. Biomed. Res. Int. 2011:371832. 10.1155/2011/371832 PubMed DOI PMC
Pfluger J., Wagner D. (2007). Histone modifications and dynamic regulation of genome accessibility in plants. Curr. Opin. Plant Biol. 10 645–652. 10.1016/j.pbi.2007.07.013 PubMed DOI PMC
Raghavan V. (2004). Role of 2, 4-dichlorophenoxyacetic acid (2, 4-D) in somatic embryogenesis on cultured zygotic embryos of Arabidopsis: cell expansion, cell cycling, and morphogenesis during continuous exposure of embryos to 2,4-D. Am. J. Bot. 91 1743–1756. 10.3732/ajb.91.11.1743 PubMed DOI
Robert H. S., Crhak Khaitova L., Mroue S., Benková E. (2015). The importance of localized auxin production for morphogenesis of reproductive organs and embryos in Arabidopsis. J. Exp. Bot. 66 5029–5042. 10.1093/jxb/erv256 PubMed DOI
Rodríguez-Sanz H., Moreno-Romero J., Solís M. T., Köhler C., Risueño M. C., Testillano P. S. (2014). Changes in histone methylation and acetylation during microspore reprogramming to embryogenesis occur concomitantly with BnHKMT and BnHAT expression and are associated with cell totipotency, proliferation, and differentiation in Brassica napus. Cytogenet. Genome. Res. 143 209–218. 10.1159/000365261 PubMed DOI
Rossetti S., Bonatti P. M. (2001). In situ histochemical monitoring of ozone-and TMV-induced reactive oxygen species in tobacco leaves. Plant Physiol. Biochem. 39 433–442. 10.1016/S0981-9428(01)01250-5 DOI
Santos D., Fevereiro P. (2002). Loss of DNA methylation affects somatic embryogenesis in Medicago truncatula. Plant Cell Tissue Organ. Cult. 70 155–161. 10.1023/A:1016369921067 DOI
Solís-Ramos L. Y., González-Estrada T., Nahuath-Dzib S., Zapata-Rodriguez L. C., Castaño E. (2009). Overexpression of WUSCHEL in C. chinense causes ectopic morphogenesis. Plant Cell Tissue Organ. Cult. 96 279–287. 10.1007/s11240-008-9485-7 DOI
Spange S., Wagner T., Heinzel T., Krämer O. H. (2009). Acetylation of non-histone proteins modulates cellular signalling at multiple levels. Int. J. Biochem. Cell Biol. 41 185–198. 10.1016/j.biocel.2008.08.027 PubMed DOI
Speth C., Laubinger S. (2014). “Rapid and parallel quantification of small and large RNA species,” in Plant Circadian Networks Methods and Protocols, ed. Staiger D. (New York, NY: Springer; ), 93–106. PubMed
Steunou A. L., Rossetto D., Côté J. (2013). “Regulating chromatin by histone acetylation,” in Fundamentals of Chromatin, eds Workman J. L., Abmayr S. L. (New York, NY: Springer; ), 147–212.
Stone S. L., Braybrook S. A., Paula S. L., Kwong L. W., Meuser J., Pelletier J., et al. (2008). Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. PNAS 105 3151–3156. 10.1073/pnas.0712364105 PubMed DOI PMC
Stone S. L., Kwong L. W., Yee K. M., Pelletier J., Lepiniec L., Fischer R. L., et al. (2001). LEAFY COTYLEDON2 encodes B3 domain transcription factor that induces embryo development. Proc. Natl. Acad. Sci. U.S.A. 98 11806–11811. 10.1073/pnas.201413498 PubMed DOI PMC
Stricker S. H., Köferle A., Beck S. (2017). From profiles to function in epigenomics. Nat. Rev. Genet. 18:51. 10.1038/nrg.2016.138 PubMed DOI
Su Y. H., Zhao X. Y., Liu Y. B., Zhang C. L., O’Neill S. D., Zhang X. S. (2009). Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J. 59 448–460. 10.1111/j.1365-313X.2009.03880.x PubMed DOI PMC
Tai H. H., Tai G. C., Beardmore T. (2005). Dynamic histone acetylation of late embryonic genes during seed germination. Plant Mol. Biol. 59 909–925. 10.1007/s11103-005-2081-x PubMed DOI
Tanaka M., Kikuchi A., Kamada H. (2008). The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol. 146 149–161. 10.1104/pp.107.111674 PubMed DOI PMC
Thellin O., Zorzi W., Lakaye B., de Borman B., Coumans B., Hennen G., et al. (1999). Housekeeping genes as internal standards: use and limits. J. Biotechnol. 75 291–295. 10.1016/S0168-1656(99)00163-7 PubMed DOI
Tognetti V. B., Bielach A., Hrtyan M. (2017). Redox regulation at the site of primary growth: Auxin, cytokinin and ROS crosstalk. Plan Cell Environ. 40 2586–2605. 10.1111/pce.13021 PubMed DOI
Tsuji N., Kobayashi M., Nagashima K., Wakisaka Y., Koizumi K. (1976). A new antifungal antibiotic, trichostatin. J. Antibiot. 29 l–6 10.7164/antibiotics.29.1 PubMed DOI
Tsuwamoto R., Yokoi S., Takahata Y. (2010). Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol. Biol. 73 481–492. 10.1007/s11103-010-9634-3 PubMed DOI
Turner B. M. (2000). Histone acetylation and an epigenetic code. Bioessays 22 836–845. 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X PubMed DOI
Uddenberg D., Valladares S., Abrahamsson M., Sundström J., Sundås-Larsson A., von Arnold S. (2011). Embryogenic potential and expression of embryogenesis- related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234 527–539. 10.1007/s00425-011-1418-8 PubMed DOI PMC
Us-Camas R., Rivera-Solís G., Duarte-Aké F., De-la-Pena C. (2014). In vitro culture: an epigenetic challenge for plants. Plant Cell Tissue Organ Cult. 118 187–201. 10.1007/s11240-014-0482-8 DOI
Valledor L., Meijón M., Hasbún R., Cañal M. J., Rodríguez R. (2010). Variations in DNA methylation, acetylated histone H4, and methylated histone H3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability. J. Plant Physiol. 167 351–357. 10.1016/j.jplph.2009.09.018 PubMed DOI
Venturelli S., Belz R. G., Kämper A., Berger A., von Horn K., Wegner A., et al. (2015). Plants release precursors of histone deacetylase inhibitors to suppress growth of competitors. Plant Cell 27 3175–3189. 10.1105/tpc.15.00585 PubMed DOI PMC
Wang W., Xu B., Wang H., Li J., Huang H., Xu L. (2011). YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol. 157 1805–1819. 10.1104/pp.111.186395 PubMed DOI PMC
Wang X., Niu Q. W., Teng C., Li C., Mu J., Chua N. H., et al. (2009). Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res. 19 224–235. 10.1038/cr.2008.276 PubMed DOI
Wang Z., Cao H., Chen F., Liu Y. (2014). The roles of histone acetylation in seed performance and plant development. Plant Physiol Bioch 84 125–133. 10.1016/j.plaphy.2014.09.010 PubMed DOI
Weijers D., Wagner D. (2016). Transcriptional responses to the auxin hormone. Annu. Rev. Plant Biol. 67 539–574. 10.1146/annurev-arplant-043015-112122 PubMed DOI
Weiste C., Dröge-Laser W. (2014). The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. Nat. Commun. 5:3883. 10.1038/ncomms4883 PubMed DOI
Wickramasuriya A. M., Dunwell J. M. (2015). Global scale transcriptome analysis of Arabidopsis embryogenesis in vitro. BMC Genomics 16:301–323. 10.1186/s12864-015-1504-6 PubMed DOI PMC
Williams L., Zhao J., Morozova N., Li Y., Avivi Y., Grafi G. (2003). Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev. Dyn. 228 113–120. 10.1002/dvdy.10348 PubMed DOI
Wójcik A. M., Nodine M. D., Gaj M. D. (2017). miR160 and miR166/165 Contribute to the LEC2-mediated auxin response involved in the somatic embryogenesis Induction in Arabidopsis. Front. Plant Sci. 8:2024. 10.3389/fpls.2017.02024 PubMed DOI PMC
Wójcikowska B., Gaj M.D. (2016). “Somatic embryogenesis in Arabidopsis,” in Somatic Embryogenesis: Fundamental Aspects and Applications, eds Loyola-Vargas V., Ochoa-Alejo N. (Cham: Springer; ), 185–199. 10.1007/978-3-319-33705-0_11 DOI
Wójcikowska B., Gaj M. D. (2017). Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. Plant Cell Rep. 36 843–858. 10.1007/s00299-017-2114-3 PubMed DOI PMC
Wójcikowska B., Jaskóła K., Gąsiorek P., Meus M., Nowak K., Gaj M. D. (2013). LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta 238 425–440. 10.1007/s00425-013-1892-2 PubMed DOI PMC
Xu W. S., Parmigiani R. B., Marks P. A. (2007). Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 26 5541–5552. 10.1038/sj.onc.1210620 PubMed DOI
Yaacob J. S., Loh H. S., Mat Taha R. (2013). Protein profiling and histone deacetylation activities in somaclonal variants of oil palm (Elaeis guineensis Jacq.). Sci. World J. 2013 1–8. 10.1155/2013/613635 PubMed DOI PMC
Yamagishi K., Tatematsu K., Yano R., Preston J., Kitamura S., Takahashi H., et al. (2008). CHOTTO1, a double AP2 domain protein of Arabidopsis thaliana, regulates germination and seedling growth under excess supply of glucose and nitrate. Plant Cell Physiol. 50 330–340. 10.1093/pcp/pcn201 PubMed DOI
Yang F., Zhang L., Li J., Huang J., Wen R., Ma L., et al. (2010). Trichostatin A and 5-azacytidine both cause an increase in global histone H4 acetylation and a decrease in global DNA and H3K9 methylation during mitosis in maize. BMC Plant Biol. 10:178. 10.1186/1471-2229-10-178 PubMed DOI PMC
Yano R., Kanno Y., Jikumaru Y., Nakabayashi K., Kamiya Y., Nambara E. (2009). CHOTTO1, a putative double APETALA2 repeat transcription factor, is involved in abscisic acid-mediated repression of gibberellin biosynthesis during seed germination in Arabidopsis. Plant Physiol. 151 641–654. 10.1104/pp.109.142018 PubMed DOI PMC
Yoshida M., Horinouchi S., Beppu T. (1995). Trichostatin A and trapoxin: novel chemical probes for the role of histone acetylation in chromatin structure and function. Bioessays 17 423–430. 10.1002/bies.950170510 PubMed DOI
Zhang Y., Cao G., Qu L. J., Gu H. (2009). Involvement of an R2R3-MYB transcription factor gene AtMYB118 in embryogenesis in Arabidopsis. Plant Cell Rep. 28 337–346. 10.1007/s00299-008-0644-4 PubMed DOI
Zhang Y., Li B., Huai D., Zhou Y., Kliebenstein D. J. (2015). The conserved transcription factors, MYB115 and MYB118, control expression of the newly evolved benzoyloxy glucosinolate pathway in Arabidopsis thaliana. Front. Plant Sci. 6:343. 10.3389/fpls.2015.00343 PubMed DOI PMC
Zheng Q., Zheng Y., Ji H., Burnie W., Perry S. E. (2016). Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiol. 172 2374–2387. 10.1104/pp.16.00564 PubMed DOI PMC
Zilberman D., Gehring M., Tran R. K., Ballinger T., Henikoff S. (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat. Genet. 39 61. 10.1038/ng1929 PubMed DOI
Zuo J., Niu Q. W., Frugis G., Chua N. H. (2002). The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J. 30 349–359. 10.1046/j.1365-313X.2002.01289.x PubMed DOI