KNOX1 is expressed and epigenetically regulated during in vitro conditions in Agave spp
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BACKGROUND: The micropropagation is a powerful tool to scale up plants of economical and agronomical importance, enhancing crop productivity. However, a small but growing body of evidence suggests that epigenetic mechanisms, such as DNA methylation and histone modifications, can be affected under the in vitro conditions characteristic of micropropagation. Here, we tested whether the adaptation to different in vitro systems (Magenta boxes and Bioreactors) modified epigenetically different clones of Agave fourcroydes and A. angustifolia. Furthermore, we assessed whether these epigenetic changes affect the regulatory expression of KNOTTED1-like HOMEOBOX (KNOX) transcription factors. RESULTS: To gain a better understanding of epigenetic changes during in vitro and ex vitro conditions in Agave fourcroydes and A. angustifolia, we analyzed global DNA methylation, as well as different histone modification marks, in two different systems: semisolid in Magenta boxes (M) and temporary immersion in modular Bioreactors (B). No significant difference was found in DNA methylation in A. fourcroydes grown in either M or B. However, when A. fourcroydes was compared with A. angustifolia, there was a two-fold difference in DNA methylation between the species, independent of the in vitro system used. Furthermore, we detected an absence or a low amount of the repressive mark H3K9me2 in ex vitro conditions in plants that were cultured earlier either in M or B. Moreover, the expression of AtqKNOX1 and AtqKNOX2, on A. fourcroydes and A. angustifolia clones, is affected during in vitro conditions. Therefore, we used Chromatin ImmunoPrecipitation (ChIP) to know whether these genes were epigenetically regulated. In the case of AtqKNOX1, the H3K4me3 and H3K9me2 were affected during in vitro conditions in comparison with AtqKNOX2. CONCLUSIONS: Agave clones plants with higher DNA methylation during in vitro conditions were better adapted to ex vitro conditions. In addition, A. fourcroydes and A. angustifolia clones displayed differential expression of the KNOX1 gene during in vitro conditions, which is epigenetically regulated by the H3K4me3 and H3K9me2 marks. The finding of an epigenetic regulation in key developmental genes will make it important in future studies to identify factors that help to find climate-resistant micropropagated plants.
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In Agave fourcroydes and A. angustifolia, no significant differences in global DNA methylation were found between clones grown in Magenta boxes and bioreactors, but a two-fold difference was found between the two species independent of the in vitro system used.
“A global DNA methylation level analysis revealed no significant differences between the A. fourcroydes clones grown in either M or B in vitro systems, but, when the two agave species were compared, there was a two-fold difference between them, independent of the in vitro system used.”
From Somaclonal Variation—Advantage or Disadvantage in Micropropagation of the Medicinal Plants (2023) · cites this paper as de-la-Pena et al. (2012) [126]
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Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
Altschul, S. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.17.3389 · Cited by 73,302 · see citing works
A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures
Murashige, T., & Skoog, F. K. (1962) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1962.tb08052.x · Cited by 67,420 · see citing works
Chromatin modifications and their function
Kouzarides, T. (2007) · Cell · doi:10.1016/j.cell.2007.02.005 · Cited by 10,883 · see citing works
Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
The language of covalent histone modifications
Strahl, B. D., & Allis, C. D. (2000) · Nature · doi:10.1038/47412 · Cited by 8,679 · see citing works
Chen, X., Xiu, M., Xing, J., Yu, S., Min, D., & Guo, F. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479439 · Cited by 5,759 · see citing works
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Epigenetic regulation of stress responses in plants
Chinnusamy, V., & Zhu, J. (2009) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2008.12.006 · Cited by 1,164 · see citing works
Shilatifard, A. (2006) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.75.103004.142422 · Cited by 1,099 · see citing works
Histone methylation in transcriptional control
Kouzarides, T. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(02)00287-3 · Cited by 908 · see citing works
Jasinski, S., Piazza, P., Craft, J., Hay, A., Woolley, L., Rieu, I., Phillips, A., Hedden, P., & Tsiantis, M. (2005) · Current Biology · doi:10.1016/j.cub.2005.07.023 · Cited by 749 · see citing works
Histone Methylation in Higher Plants
Liu, C., Lu, F., Cui, X., & Cao, X. (2010) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.043008.091939 · Cited by 735 · see citing works
KNOX genes: versatile regulators of plant development and diversity
Hay, A., & Tsiantis, M. (2010) · Development · doi:10.1242/dev.030049 · Cited by 591 · see citing works
Genomic 5-methyldeoxycytidine decreases with age.
Wilson, V. L., Smith, R. A., Ma, S., & Cutler, R. G. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61057-9 · Cited by 521 · see citing works
THE ROLE OF KNOX GENES IN PLANT DEVELOPMENT
Hake, S., Smith, H. M. S., Holtan, H., Magnani, E., Mele, G., & Ramirez, J. C. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.031803.093824 · Cited by 456 · see citing works
Mechanisms that control knox gene expression in the Arabidopsis shoot
Ori, N., Eshed, Y., Chuck, G. S., Bowman, J. L., & Hake, S. (2000) · Development · doi:10.1242/dev.127.24.5523 · Cited by 455 · see citing works
Progress in Plant Cellular and Molecular Biology
Nijkamp, H. J. J., van der Plas, L. H. W., & Aartrijk, J. V. (1990) · Current plant science and biotechnology in agriculture · doi:10.1007/978-94-009-2103-0 · Cited by 411 · see citing works
An epigenetic view of plant cells cultured in vitro: Somaclonal variation and beyond
Miguel, C., & Marum, L. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err155 · Cited by 395 · see citing works
Epigenetic Variation in Mangrove Plants Occurring in Contrasting Natural Environment
Lira, C. F., Parisod, C., Fernandes, R. A., da Mata, C. S., Cardoso, M. A., & Ferreira, P. C. G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010326 · Cited by 361 · see citing works
A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta
Barkoulas, M., Hay, A., Kougioumoutzi, E., & Tsiantis, M. (2008) · Nature Genetics · doi:10.1038/ng.189 · Cited by 329 · see citing works
Jackson, J. P., Johnson, L. M., Jasencakova, Z., Zhang, X., Perez-Burgos, L., Singh, P. B., Cheng, X., Schubert, I. A., Jenuwein, T., & Jacobsen, S. E. (2004) · Chromosoma · doi:10.1007/s00412-004-0275-7 · Cited by 326 · see citing works
LoSchiavo, F., Pitto, L., Giuliano, G., Torti, G., Nuti-Ronchi, V., Marazziti, D., Vergara, R., Orselli, S., & Terzi, M. (1989) · Theoretical and Applied Genetics · doi:10.1007/bf00305823 · Cited by 309 · see citing works
Hay, A., Barkoulas, M., & Tsiantis, M. (2006) · Development · doi:10.1242/dev.02545 · Cited by 308 · see citing works
Rupp, H., Frank, M., Werner, T., Strnad, M., & Schmülling, T. (1999) · The Plant Journal · doi:10.1046/j.1365-313x.1999.00472.x · Cited by 292 · see citing works
Embryo production through somatic embryogenesis can be used to study cell differentiation in plants
Quiroz‐Figueroa, F. R., Rojas-Herrera, R. A., Galaz-Ávalos, R. M., & Loyola-Vargas, V. M. (2006) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-006-9139-6 · Cited by 273 · see citing works
Johnson, L. M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh992 · Cited by 252 · see citing works
Epigenetic alterations in aging
Gonzalo, S. (2010) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00238.2010 · Cited by 249 · see citing works
Epigenetics in plant tissue culture
Smulders, M. J. M., & de Klerk, G. J. (2011) · Plant Growth Regulation · doi:10.1007/s10725-010-9531-4 · Cited by 249 · see citing works
Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis
Mathieu, O., Probst, A. V., & Paszkowski, J. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600743 · Cited by 243 · see citing works
Regulation of transcription in plants: mechanisms controlling developmental switches
Kaufmann, K., Pajoro, A., & Angenent, G. C. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2885 · Cited by 237 · see citing works
Chromatin regulation functions in plant abiotic stress responses
Kim, J.-M., To, T. K., NISHIOKA, T., & Seki, M. (2009) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2009.02076.x · Cited by 230 · see citing works
Tissue Culture-Induced DNA Methylation Variation in Maize
Kaeppler, S. M., & Phillips, R. L. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.19.8773 · Cited by 225 · see citing works
Somaclonal variation in oil palm (Elaeis guineensis Jacq.): The DNA methylation hypothesis
Jaligot, E., Rival, A., Beulé, T., Dussert, S., & Verdeil, J.-L. (2000) · Plant Cell Reports · doi:10.1007/s002999900177 · Cited by 220 · see citing works
Epigenomic consequences of immortalized plant cell suspension culture
Tanurdzic, M., Vaughn, M. W., Jiang, H., Lee, T.-J., Slotkin, R. K., Sosinski, B., Thompson, W. F., Doerge, R. W., & Martienssen, R. A. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060302 · Cited by 218 · see citing works
Recalcitrance in clonal propagation, in particular of conifers
Bonga, J. M., Klimaszewska, K., & von Aderkas, P. (2009) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-009-9647-2 · Cited by 217 · see citing works
Development and application of photoautotrophic micropropagation plant system
Xiao, Y., Niu, G., & Kozai, T. (2010) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-010-9863-9 · Cited by 208 · see citing works
Phelps-Durr, T., Thomas, J., Vahab, P., & Timmermans, M. C. P. (2005) · The Plant Cell · doi:10.1105/tpc.105.035477 · Cited by 206 · see citing works
Role of histone and DNA methylation in gene regulation
Vaillant, I., & Paszkowski, J. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.06.008 · Cited by 185 · see citing works
Epigenetic regulation of flowering
Dennis, E. S., & Peacock, W. J. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.06.009 · Cited by 181 · see citing works
Ay, N., Irmler, K., Fischer, A., Uhlemann, R., Reuter, G., & Humbeck, K. (2009) · The Plant Journal · doi:10.1111/j.0960-7412.2009.03782.x · Cited by 173 · see citing works
Clathrin‐ and Dynamin‐Dependent Coated Vesicle Formation from Isolated Plasma Membranes
Miwako, I., Schröter, T., & Schmid, S. L. (2003) · Traffic · doi:10.1111/j.1365-313x.2008.03782.x · Cited by 159 · see citing works
Genomic DNA methylation-demethylation during aging and reinvigoration of Pinus radiata
Fraga, M. F., Rodriguez, R., & Cañal, M. J. (2002) · Tree Physiology · doi:10.1093/treephys/22.11.813 · Cited by 146 · see citing works
Involvement of DNA methylation in tree development and micropropagation
Valledor, L., Hasbún, R., Meijón, M., Rodriguez, J. L., Santamaria, M. E., Viejo, M. D., Berdasco, M., Feito, I., Fraga, M. F., Cañal, M. J., et al. (2007) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-007-9262-z · Cited by 145 · see citing works
Greene, B., Walko, R. M., & Hake, S. (1994) · Genetics · doi:10.1093/genetics/138.4.1275 · Cited by 137 · see citing works
Peraza-Echeverría, S., Herrera-Valencia, V. A., & Kay, A.-J. (2001) · Plant Science · doi:10.1016/s0168-9452(01)00421-6 · Cited by 136 · see citing works
Alteration of Hormone Levels in Transgenic Tobacco Plants Overexpressing the Rice Homeobox Gene OSH1
Kusaba, S., Kano‐Murakami, Y., Matsuoka, M., Tamaoki, M., Sakamoto, T., Yamaguchi, I., & Fukumoto, M. (1998) · PLANT PHYSIOLOGY · doi:10.1104/pp.116.2.471 · Cited by 131 · see citing works
Smýkal, P., Valledor, L., Rodríguez, R., & Griga, M. (2007) · Plant Cell Reports · doi:10.1007/s00299-007-0413-9 · Cited by 128 · see citing works
Epigenetic responses to stress: triple defense?
Gutzat, R., & Scheid, O. M. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.08.007 · Cited by 126 · see citing works
Promoter DNA Hypermethylation and Gene Repression in Undifferentiated Arabidopsis Cells
Berdasco, M., Alcázar, R., García‐Ortiz, M. V., Ballestar, E., Fernández, A. F., Roldán‐Arjona, T., Tiburcio, A. F., Altabella, T., Buisine, N., Quesneville, H., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003306 · Cited by 120 · see citing works
Loyola-Vargas, V. M. (2012) · Methods in molecular biology · doi:10.1007/978-1-61779-818-4 · Cited by 120 · see citing works
DNA methylation increases throughout Arabidopsis development
Ruiz‐García, L., Cervera, M., & Martínez-Zapater, J. M. (2005) · Planta · doi:10.1007/s00425-005-1524-6 · Cited by 116 · see citing works
Plant hormones and homeoboxes: bridging the gap?
Hay, A., Craft, J., & Tsiantis, M. (2004) · BioEssays · doi:10.1002/bies.20016 · Cited by 106 · see citing works
Williams, L. E., Zhao, J., Morozova, N., Li, Y., Avivi, Y., & Grafi, G. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10348 · Cited by 101 · see citing works
KNAT6 gene of Arabidopsis is expressed in roots and is required for correct lateral root formation
Dean, G. H., Casson, S. A., & Lindsey, K. (2004) · Plant Molecular Biology · doi:10.1023/b:plan.0000028772.22892.2d · Cited by 94 · see citing works
DNA-methylation changes in grapevine somaclones following in vitro culture and thermotherapy
Baránek, M., Krizan, B., Ondrušíková, E., & Pidra, M. (2009) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-009-9656-1 · Cited by 85 · see citing works
Human Histone Deacetylase SIRT2 Interacts with the Homeobox Transcription Factor HOXA10
Bae, N. S. (2004) · The Journal of Biochemistry · doi:10.1093/jb/mvh084 · Cited by 84 · see citing works
Do We Understand Somaclonal Variation?
Phillips, R. L., Kaeppler, S. M., & Peschke, V. M. (1990) · Current plant science and biotechnology in agriculture · doi:10.1007/978-94-009-2103-0_19 · Cited by 82 · see citing works
Morcillo, F., Gagneur, C., Adam, H., Richaud, F., Singh, R., Cheah, S. C., Rival, A., Duval, Y., & Tregear, J. W. (2006) · Tree Physiology · doi:10.1093/treephys/26.5.585 · Cited by 78 · see citing works
De‐la‐Peña, C., RANGEL‐CANO, A., & Álvarez-Venegas, R. (2011) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2011.00757.x · Cited by 77 · see citing works
Self-citationLópez-Torres, A., Barrientos, E. Y., Wróbel, K., & Wróbel, K. (2011) · Analytical Chemistry · doi:10.1021/ac2020799 · Cited by 77 · see citing works
Self-citationIn vitro propagation of Agave fourcroydes Lem. (Henequen)
Robert, M. L., Herrera, J. L., Contreras, F., & Scorer, K. N. (1987) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/bf00040731 · Cited by 77 · see citing works
Li, H., He, Z., Lu, G., Lee, S. C., Alonso, J. M., Ecker, J. R., & Luan, S. (2007) · The Plant Cell · doi:10.1105/tpc.107.053579 · Cited by 76 · see citing works
SMULDERS, M. J. M., Rus-Kortekaas, W., & Vosman, B. (1995) · Theoretical and Applied Genetics · doi:10.1007/bf00220938 · Cited by 73 · see citing works
Valledor, L., Meijón, M., Hasbún, R., Cañal, M. J., & Madrera, R. R. (2009) · Journal of Plant Physiology · doi:10.1016/j.jplph.2009.09.018 · Cited by 72 · see citing works
A Simple and Efficient Method for Isolation of DNA in High Mucilaginous Plant Tissues
Echevarría‐Machado, I., Sánchez-Cach, L. A., Hernández‐Zepeda, C., Madrid, R. R., & Moreno-Valenzuela, O. A. (2005) · Molecular Biotechnology · doi:10.1385/mb:31:2:129 · Cited by 58 · see citing works
Genetic and epigenetic stability of cryopreserved and cold-stored hops (Humulus lupulus L.)
Peredo, E. L., Arroyo-García, R. A., Reed, B. M., & Revilla, M. A. (2008) · Cryobiology · doi:10.1016/j.cryobiol.2008.09.002 · Cited by 58 · see citing works
Variation in potato microplant morphology in vitro and DNA methylation
Joyce, S. M., & Cassells, A. C. (2002) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1023/a:1016312303320 · Cited by 57 · see citing works
Epigenetic changes detected in micropropagated hop plants
Peredo, E. L., Arroyo-García, R., & Revilla, M. Á. (2009) · Journal of Plant Physiology · doi:10.1016/j.jplph.2008.12.015 · Cited by 56 · see citing works
DNA methylation profiles differ between field- andin vitro-grown leaves of apple
Li, X., Xu, M., & Korban, S. S. (2002) · Journal of Plant Physiology · doi:10.1078/0176-1617-00899 · Cited by 53 · see citing works
Methylation of DNA — One of the Major Epigenetic Markers
Salozhin, S. V., Prokhortchouk, E., & Georgiev, G. P. (2005) · Biochemistry (Moscow) · doi:10.1007/s10541-005-0146-8 · Cited by 52 · see citing works
Maldonado-Santoyo, M., Flores, C. R., López-Torres, A., Wróbel, K., & Wrobel, K. (2011) · Environmental Pollution · doi:10.1016/j.envpol.2011.06.041 · Cited by 51 · see citing works
Self-citationClass I KNOX genes are associated with organogenesis during bulbil formation in Agave tequilana
Abraham‐Juárez, M. J., Martı́nez-Hernández, A., Leyva‐González, M. A., Herrera‐Estrella, L., & Simpson, J. K. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq215 · Cited by 49 · see citing works
Law, R. D., & Suttle, J. C. (2005) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2005.03.014 · Cited by 48 · see citing works
Montero-Cortés, M., Sáenz-Carbonell, L., Córdova, I., Quiroz, Á. O., Verdeil, J., & Oropeza, C. (2010) · Plant Cell Reports · doi:10.1007/s00299-010-0890-0 · Cited by 48 · see citing works
Arnholdt‐Schmitt, B., Herterich, S., & Neumann, K. ‐. (1995) · Theoretical and Applied Genetics · doi:10.1007/bf00220964 · Cited by 46 · see citing works
Trap-Gentil, M.-V., Hébrard, C., Placette, C. L., Delaunay, A., Hagège, D., Joseph, C., Brignolas, F., Lefèbvre, M., Barnes, S., & Maury, S. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/erq433 · Cited by 43 · see citing works
Are Homeobox Knotted-Like Genes and Cytokinins the Leaf Architects?
Frugis, G., Giannino, D., Mele, G., Nicolodi, C., Innocenti, A. M., Chiappetta, A. A. C., Bitonti, M. B., Dewitte, W., Onckelen, H. A. V., & Mariotti, D. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.119.2.371 · Cited by 43 · see citing works
Varga, A., Thoma, L. H., & Bruinsma, J. (1988) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/bf00033646 · Cited by 40 · see citing works
[DNA methylation and epigenetics].
Bf, V. (2006) · PubMed · Cited by 40 · see citing works
Park, S. Y., Murthy, H. N., Chakrabarthy, D., & Paek, K. (2008) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/s11627-008-9166-6 · Cited by 39 · see citing works
Reversible variations in the methylation pattern of carrot DNA during somatic embryogenesis
Vergara, R., Verde, F., Pitto, L., Schiavo, F. L., & Terzi, M. (1990) · Plant Cell Reports · doi:10.1007/bf00272097 · Cited by 39 · see citing works
DNA methylation and epigenetics
Vanyushin, B. F. (2006) · Russian Journal of Genetics · doi:10.1134/s1022795406090055 · Cited by 39 · see citing works
Díaz-Martínez, M., Nava-Cedillo, A., Guzmán-López, J. A., Escobar-Guzmán, R., & Simpson, J. K. (2012) · Plant Science · doi:10.1016/j.plantsci.2012.01.004 · Cited by 37 · see citing works
Chromatin dynamics and Arabidopsis development
Berger, F., & Gaudin, V. (2003) · Chromosome Research · doi:10.1023/a:1022844127716 · Cited by 35 · see citing works
Micropropagation of Agave spp.
Robert, M. L., Herrera, J. L., Chan, J. L., & Contreras, F. (1992) · Biotechnology in agriculture and forestry · doi:10.1007/978-3-662-07770-2_19 · Cited by 32 · see citing works
A New Temporary Immersion Bioreactor System for Micropropagation
Robert, M. L., Herrera-Herrera, J. L., Herrera-Herrera, G., Herrera-Alamillo, M. Á., & Fuentes-Carrillo, P. (2005) · Humana Press eBooks · doi:10.1385/1-59259-959-1:121 · Cited by 29 · see citing works
Self-citationAlatzas, A., & FOUNDOULI, A. (2006) · Plant Science · doi:10.1016/j.plantsci.2006.05.008 · Cited by 22 · see citing works
Writers and readers: deconvoluting the harmonic complexity of the histone code
Cosgrove, M. S. (2012) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2350 · Cited by 13 · see citing works
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Nic-Can, G. I., López-Torres, A., Barredo-Pool, F., Wrobel, K., Loyola-Vargas, V. M., Rojas-Herrera, R., & De-la-Peña, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072160 · Cited by 164 · see citing works
Self-citationAbnormalities in somatic embryogenesis caused by 2,4-D: an overview
Garcia, C., de Almeida, A.-A. F., Costa, M. G. C., Britto, D. S., Valle, R. R., Royaert, S., & Marelli, J. (2019) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-019-01569-8 · Cited by 142 · see citing works
Plant tissue culture environment as a switch-key of (epi)genetic changes
Bednarek, P. T., & Orłowska, R. (2019) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-019-01724-1 · Cited by 140 · see citing works
In vitro culture: an epigenetic challenge for plants
Us-Camas, R. Y., Rivera-Solís, G., Duarte-Aké, F., & De‐la‐Peña, C. (2014) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-014-0482-8 · Cited by 138 · see citing works
Self-citationThe role of chromatin modifications in somatic embryogenesis in plants
De‐la‐Peña, C., Nic-Can, G. I., Galaz-Ávalos, R. M., Avilez-Montalvo, R. N., & Loyola-Vargas, V. M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00635 · Cited by 117 · see citing works
Self-citationBiotic Interactions in the Rhizosphere: A Diverse Cooperative Enterprise for Plant Productivity
De-la-Pena, C., & Loyola-Vargas, V. M. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.241810 · Cited by 117 · see citing works
Somaclonal Variation—Advantage or Disadvantage in Micropropagation of the Medicinal Plants
Duta-Cornescu, G., Constantin, N., Pojoga, D.-M., Nicuta, D., & Simon-Gruita, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24010838 · Cited by 108 · see citing works
“(2012) [126] analyzed whether the adaptation to different in vitro culture systems (Magenta boxes—M and Bioreactors—B) epigenetically modifies different clones of Agave fourcroydes and A.”
BackgroundAgavebiotechnology: an overview
Nava-Cruz, N. Y., Medina-Morales, M. Á., Martinez, J. L., Rodriguez, R., & Aguilar, C. N. (2014) · Critical Reviews in Biotechnology · doi:10.3109/07388551.2014.923813 · Cited by 85 · see citing works
Tissue culture-induced DNA methylation in crop plants: a review
Ghosh, A., Igamberdiev, A. U., & Debnath, S. C. (2021) · Molecular Biology Reports · doi:10.1007/s11033-020-06062-6 · Cited by 81 · see citing works
Nic-Can, G. I., Galaz-Ávalos, R., De-la-Peña, C., Alcázar-Magaña, A., Wrobel, K., & Loyola-Vargas, V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126414 · Cited by 80 · see citing works
Self-citationGuo, H., Wu, T., ShuXing, L., He, Q., Yang, Z.-L., Zhang, W., Gan, Y., Sun, P., Xiang, G.-L., Zhang, H., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205089 · Cited by 72 · see citing works
Adjustments to In Vitro Culture Conditions and Associated Anomalies in Plants
Isah, T. (2015) · Acta Biologica Cracoviensia s Botanica · doi:10.1515/abcsb-2015-0026 · Cited by 67 · see citing works
Genomic analyses of the CAM plant pineapple
Zhang, J., Liu, J., & Ming, R. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru101 · Cited by 60 · see citing works
Epi-fingerprinting and epi-interventions for improved crop production and food quality
Lopez, C. M. R., & Wilkinson, M. J. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00397 · Cited by 50 · see citing works
Gimenez, M. D., Yañez-Santos, A. M., Paz, R. C., Quiroga, M. P., Marfil, C. F., Conci, V. C., & García-Lampasona, S. C. (2016) · Plant Cell Reports · doi:10.1007/s00299-015-1874-x · Cited by 47 · see citing works
Azizi, P., Hanafi, M. M., Sahebi, M., Harikrishna, J. A., Taheri, S., Yassoralipour, A., & Nasehi, A. (2020) · Functional Plant Biology · doi:10.1071/fp19077 · Cited by 46 · see citing works
Tamayo‐Ordoñez, M. C., Rodríguez‐Zapata, L. C., Narváez-Zapata, J. A., Tamayo-Ordóñez, Y. D. J., Ayil‐Gutiérrez, B. A., Barredo-Pool, F., & Sánchez‐Teyer, L. F. (2016) · Journal of Plant Physiology · doi:10.1016/j.jplph.2016.03.009 · Cited by 33 · see citing works
Plant gene expression control using genome- and epigenome-editing technologies
Miglani, G. S., Kaur, A., & Kaur, L. (2019) · Journal of Crop Improvement · doi:10.1080/15427528.2019.1678541 · Cited by 32 · see citing works
Osorio-Montalvo, P. M., De‐la‐Peña, C., Oropeza, C., Nic-Can, G. I., Córdova‐Lara, I., Castillo-Castro, E., & Sáenz-Carbonell, L. (2020) · Plant Cell Reports · doi:10.1007/s00299-020-02568-2 · Cited by 31 · see citing works
Self-citationAssessment of molecular and epigenetic changes in the albinism of Agave angustifolia Haw
Us-Camas, R. Y., Castillo-Castro, E., Aguilar‐Espinosa, M., Limones-Briones, V., Madrid, R. R., Robert, M. L., & De‐la‐Peña, C. (2017) · Plant Science · doi:10.1016/j.plantsci.2017.07.010 · Cited by 27 · see citing works
Self-citationTowards the Understanding of Important Coconut Endosperm Phenotypes: Is there an Epigenetic Control?
Angeles, J. G. C., Lado, J. P., Pascual, E. D., Cueto, C. A., Laurena, A. C., & Laude, R. P. (2018) · Agronomy · doi:10.3390/agronomy8100225 · Cited by 25 · see citing works
An efficient immunodetection method for histone modifications in plants
Nic-Can, G. I., Castellano, S., Ku, A. F., Loyola-Vargas, V. M., & De‐la‐Peña, C. (2013) · Plant Methods · doi:10.1186/1746-4811-9-47 · Cited by 21 · see citing works
Self-citationEpigenetic changes and photosynthetic plasticity in response to environment
Duarte-Aké, F., Us-Camas, R. Y., Cancino-García, V. J., & De‐la‐Peña, C. (2018) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2018.12.010 · Cited by 19 · see citing works
Self-citationAuxin perception in Agave is dependent on the species’ Auxin Response Factors
Cancino-García, V. J., Ramírez-Prado, J. H., & De‐la‐Peña, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-60865-y · Cited by 16 · see citing works
Self-citationValledor, L., Pascual, J., Meijón, M., Escandón, M., & Cañal, M. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126405 · Cited by 15 · see citing works
Somatic Embryogenesis: Polycomb Complexes Control Cell-to-Embryo Transition
Duarte-Aké, F., Nic-Can, G. I., & De‐la‐Peña, C. (2019) · Springer eBooks · doi:10.1007/978-3-030-14760-0_13 · Cited by 15 · see citing works
Self-citationBiotechnological Advances in Rubber Tree (Hevea brasiliensis Muell. Arg.) Breeding
Sobha, S., Rekha, K., & Uthup, T. K. (2019) · Springer eBooks · doi:10.1007/978-3-030-23265-8_7 · Cited by 13 · see citing works
Developmental regulatory genes: Key switches in the developmental events of plant tissue culture
Mehraj, H., Maruyama, T. E., Tsuruta, M., & Ueno, S. (2025) · Current Plant Biology · doi:10.1016/j.cpb.2025.100550 · Cited by 8 · see citing works
Geneva, M., Kirova, E. B., Sichanova, M., Stancheva, I., & Zayova, E. G. (2022) · Biologia · doi:10.1007/s11756-022-01231-3 · Cited by 8 · see citing works
Retroelements and DNA Methylation Could Contribute to Diversity of 5S rDNA in Agave L.
Tamayo-Ordóñez, Y. D. J., Narváez-Zapata, J. A., Tamayo‐Ordoñez, M. C., & Sánchez‐Teyer, L. F. (2018) · Journal of Molecular Evolution · doi:10.1007/s00239-018-9856-6 · Cited by 6 · see citing works
Rodriguez, J. L., Valledor, L., Hasbún, R., Sánchez, P., Madrera, R. R., & Cañal, M. J. (2015) · Journal of Plant Growth Regulation · doi:10.1007/s00344-015-9510-0 · Cited by 6 · see citing works
Effects of TDZ and IBA on DNA methylation during callus induction in pear (Pyrus ussuriensis Maxim)
Zhou, F., Zhou, S., Cui, S., Liu, J., Yang, Y., & Wang, R. (2023) · Fruit Research · doi:10.48130/frures-2023-0007 · Cited by 5 · see citing works
Rubio-Piña, J. A., Quiroz-Moreno, A., & Sánchez‐Teyer, L. F. (2016) · Electronic Journal of Biotechnology · doi:10.1016/j.ejbt.2016.05.002 · Cited by 5 · see citing works
Molecular mechanism of plant-microbe interactions
Parray, J. A., & Shameem, N. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817109-7.00003-1 · Cited by 5 · see citing works
Us-Camas, R. Y., & De‐la‐Peña, C. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8594-4_26 · Cited by 3 · see citing works
Self-citationDuarte-Aké, F., & De‐la‐Peña, C. (2023) · Journal of the Mexican Chemical Society · doi:10.29356/jmcs.v67i3.1943 · Cited by 2 · see citing works
Self-citationRESPUESTA MORFOGENÉTICA DE DOS ESPECIES DE AGAVE REGENERADAS IN VITRO
Arzate-Fernandez, A. M., Martínez-Velasco, I., Aragón, C. A., Martínez-Martínez, S. Y., & Norman-Mondragon, T. H. (2020) · Tropical and Subtropical Agroecosystems · doi:10.56369/tsaes.3201 · Cited by 2 · see citing works
Maguey Cenizo (Agave durangensis Gentry) Breeding
Almaráz-Abarca, N., & Ávila-Reyes, J. A. (2025) · Advances in plant breeding strategies · doi:10.1007/978-3-032-00407-9_8 · Cited by 1 · see citing works
Mehraj, H., Raisa, R. I., & Islam, T. (2026) · Next Bioengineering · doi:10.1016/j.nxbio.2026.100013 · Cited by 1 · see citing works
Epigenetic Considerations on Altered Phenotypes of the Coconut Endosperm
Angeles, J. G. C., Lado, J. P., Pascual, E. D., Laurena, A. C., & Laude, R. P. (2021) · Compendium of plant genomes · doi:10.1007/978-3-030-76649-8_13 · Cited by 1 · see citing works
Balzon, T. A., Monteiro, T. R., Lopes, R., da Cunha, R. N. V., Gomes, H. T., Silva-Cardoso, I. M. D. A., de Souza, A. L. X., Inglis, P. W., & Scherwinski-Pereira, J. E. (2026) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-026-03498-9
Epigenetic Gatekeepers of the Totipotent State
Kumar, P. (2026) · SpringerBriefs in plant science · doi:10.1007/978-981-92-1631-4_4
- Authors
- De-la-Peña, C., Nic-Can, G., Ojeda, G., Herrera-Herrera, J. L., López-Torres, A., Wrobel, K., & Robert-Díaz, M. L.
- Affiliations
- Autonomous University of Yucatán (MX)
- Centro de Investigación Científica de Yucatán, A.C (MX)
- Universidad de Guanajuato (MX)
- Venue
- BMC Plant Biology
- Published
- 2012
- Volume
- 12
- Issue
- 1
- Pages
- 203
- ISSN
- 1471-2229 (ISSN-L)
- PMC
- PMC3541254
- OpenAlex
- W1967932067
- Cited by
- 43
- References
- 89
- Citations by year
- 2026: 3 · 2025: 2 · 2023: 3 · 2022: 1 · 2021: 2 · 2020: 6 · 2019: 6 · 2018: 4 · 2017: 1 · 2016: 2 · 2015: 7 · 2014: 4 · 2013: 2
- FWCI
- 1.67
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Plant Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Consejo Nacional de Ciencia y Tecnología (CB2012)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant tissue culture and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- Agave fourcroydes, Agave angustifolia, KNOX transcription factors, DNA methylation, histone modifications, H3K4me3, H3K9me2, epigenetic regulation, in vitro adaptation, ex vitro acclimatization, bioreactors
- MeSH terms
- Histones, Lysine, Plant Proteins, Immunoblotting, Homeodomain Proteins, Gene Expression Regulation, Plant, DNA, Plant, Genome, Plant, DNA Methylation, Agave, Epigenesis, Genetic, Chromatin Immunoprecipitation, Real-Time Polymerase Chain Reaction
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