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

Mendel Centre for Genomics and Proteomics of Plants Systems CEITEC MU Central European Institute of Technology Masaryk University Brno Czechia

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 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. 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. 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. 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. 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 DOI

Birnbaum K. D., Roudier F. (2017). Epigenetic memory and cell fate reprogramming in plants. 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. 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. PubMed DOI PMC

Boycheva I., Vassileva V., Iantcheva A. (2014). Histone acetyltransferases in plant development and plasticity. 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. 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. 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. 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. PubMed DOI

Chang S., Pikaard C. S. (2005). Transcript profiling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation. 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. 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. DOI

Chen J. T., Chang W. C. (2004). TIBA affects the induction of direct somatic embryogenesis from leaf explants of Oncidium. 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 ( 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. 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. PubMed DOI PMC

Chinnusamy V., Zhu J. K. (2009). Epigenetic regulation of stress responses in plants. 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. PubMed DOI PMC

Choudhury F. K., Rivero R. M., Blumwald E., Mittler R. (2017). Reactive oxygen species, abiotic stress and stress combination. 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 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. PubMed DOI

Deng W., Luo K., Li Z., Yang Y. (2009). A novel method for induction of plant regeneration via somatic embryogenesis. 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. PubMed DOI PMC

Eberharter A., Becker P. B. (2002). Histone acetylation: a switch between repressive and permissive chromatin. 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. PubMed DOI

Elhiti M., Stasolla C. (2015). “ROS Signalling in plant embryogenesis,” iIn

Fehér A. (2015). Somatic embryogenesis - Stress-induced remodeling of plant cell fate. PubMed DOI

Feng S., Jacobsen S. E., Reik W. (2010). Epigenetic reprogramming in plant and animal development. PubMed DOI PMC

Feng W., Michaels S. D. (2015). Accessing the inaccessible: the organization, transcription, replication, and repair of heterochromatin in plants. 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. PubMed DOI

Gaj M. D. (2001). Direct somatic embryogenesis as a rapid and efficient system for in vitro regeneration of DOI

Gaj M. D. (2011). Somatic embryogenesis and plant regeneration in the culture of PubMed

Gaj M. D., Zhang S., Harada J. J., Lemaux P. G. (2005). LEAFY COTYLEDON genes are essential for induction of somatic embryogenesis of PubMed DOI

Gamborg O. L., Miller R. A., Ojima K. (1968). Nutrient requirement of suspension culture of soybean root cells. 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. PubMed DOI

Gendrel A. V., Lippman Z., Martienssen R., Colot V. (2005). Profiling histone modification patterns in plants using genomic tiling microarrays. 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 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. 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. PubMed DOI PMC

Görisch S. M., Wachsmuth M., Toth K. F., Lichter P., Rippe K. (2005). Histone acetylation increases chromatin accessibility. 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. 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 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. 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. 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.

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. 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. 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. PubMed DOI

He X. J., Chen T., Zhu J. K. (2011). Regulation and function of DNA methylation in plants and animals. 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. PubMed DOI PMC

Horstman A., Bemer M., Boutilier K. (2017a). A transcriptional view on somatic embryogenesis. 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. 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. 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. 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. 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. 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. PubMed DOI

Jung M., Hoffmann K., Brosch G., Loidl P. (1997). Analogues of trichosòatin a and trapoxin B as histone deacetylase inhibitors. 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 PubMed DOI

Kairong C., Gengsheng X., Xinmin L., Gengmei X., Yafu W. (1999). Effect of hydrogen peroxide on somatic embryogenesis of DOI

Kasahara H. (2016). Current aspects of auxin biosynthesis in plants. PubMed DOI

Kidner C. A., Martienssen R. A. (2004). Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. 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. 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. DOI

Kurczyńska E. U., Gaj M. D., Ujczak A., Mazur E. (2007). Histological analysis of direct somatic embryogenesis in PubMed DOI

Lauria M., Rossi V. (2011). Epigenetic control of gene regulation in plants. PubMed DOI

Lee K., Park O. S., Jung S. J., Seo P. J. (2016). Histone deacetylation-mediated cellular dedifferentiation in Arabidopsis. PubMed DOI

Leljak-Levanić D., Bauer N., Mihaljević S., Jelaska S. (2004). Changes in DNA methylation during somatic embryogenesis in 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. 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. 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. 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. 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. 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. PubMed DOI PMC

Luo M., Cheng K., Xu Y., Yang S., Wu K. (2017). Plant responses to abiotic stress regulated by histone deacetylases. 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. 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. 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. 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. 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. PubMed DOI PMC

Mittler R. (2017). ROS are good. 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. PubMed DOI PMC

Mozgová I., Muñoz-Viana R., Hennig L. (2017). PRC2 represses hormone-induced somatic embryogenesis in vegetative tissue of PubMed DOI PMC

Murashige T., Skoog F. A. (1962). A revised medium for rapid growth and bioassays with tobacco tissue cultures. 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. 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 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. 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. 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 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. PubMed DOI PMC

Peserico A., Simone C. (2011). Physical and functional HAT/HDAC interplay regulates protein acetylation balance. PubMed DOI PMC

Pfluger J., Wagner D. (2007). Histone modifications and dynamic regulation of genome accessibility in plants. 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. 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. 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 PubMed DOI

Rossetti S., Bonatti P. M. (2001). In situ histochemical monitoring of ozone-and TMV-induced reactive oxygen species in tobacco leaves. DOI

Santos D., Fevereiro P. (2002). Loss of DNA methylation affects somatic embryogenesis in 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. DOI

Spange S., Wagner T., Heinzel T., Krämer O. H. (2009). Acetylation of non-histone proteins modulates cellular signalling at multiple levels. PubMed DOI

Speth C., Laubinger S. (2014). “Rapid and parallel quantification of small and large RNA species,” in PubMed

Steunou A. L., Rossetto D., Côté J. (2013). “Regulating chromatin by histone acetylation,” in

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. 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. PubMed DOI PMC

Stricker S. H., Köferle A., Beck S. (2017). From profiles to function in epigenomics. 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. PubMed DOI PMC

Tai H. H., Tai G. C., Beardmore T. (2005). Dynamic histone acetylation of late embryonic genes during seed germination. 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. 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. PubMed DOI

Tognetti V. B., Bielach A., Hrtyan M. (2017). Redox regulation at the site of primary growth: Auxin, cytokinin and ROS crosstalk. PubMed DOI

Tsuji N., Kobayashi M., Nagashima K., Wakisaka Y., Koizumi K. (1976). A new antifungal antibiotic, trichostatin. 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. PubMed DOI

Turner B. M. (2000). Histone acetylation and an epigenetic code. 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. 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. 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. 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. 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. 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. PubMed DOI

Wang Z., Cao H., Chen F., Liu Y. (2014). The roles of histone acetylation in seed performance and plant development. PubMed DOI

Weijers D., Wagner D. (2016). Transcriptional responses to the auxin hormone. PubMed DOI

Weiste C., Dröge-Laser W. (2014). The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery. PubMed DOI

Wickramasuriya A. M., Dunwell J. M. (2015). Global scale transcriptome analysis of Arabidopsis embryogenesis in vitro. 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. 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. PubMed DOI PMC

Wójcikowska B., Gaj M.D. (2016). “Somatic embryogenesis in Arabidopsis,” in DOI

Wójcikowska B., Gaj M. D. (2017). Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. 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. PubMed DOI PMC

Xu W. S., Parmigiani R. B., Marks P. A. (2007). Histone deacetylase inhibitors: molecular mechanisms of action. PubMed DOI

Yaacob J. S., Loh H. S., Mat Taha R. (2013). Protein profiling and histone deacetylation activities in somaclonal variants of oil palm ( 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 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. 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. 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. 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. 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 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. PubMed DOI PMC

Zilberman D., Gehring M., Tran R. K., Ballinger T., Henikoff S. (2007). Genome-wide analysis of PubMed DOI

Zuo J., Niu Q. W., Frugis G., Chua N. H. (2002). The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. PubMed DOI

MONOPTEROS isoform MP11ir plays a role during somatic embryogenesis in Arabidopsis thaliana

Epigenetics for Crop Improvement in Times of Global Change