Meristem micropropagation of cassava (Manihot esculenta) evokes genome-wide changes in DNA methylation

Kitimu, Shedrack R.; Taylor, Julian; March, Timothy J.; Tairo, Fred; Wilkinson, Mike J.; Rodríguez López, Carlos M.

doi:10.3389/fpls.2015.00590

Cited by 50Plant tissue culture and regenerationEpigenetics and DNA MethylationCassava research and cyanide

Meristem micropropagation of cassava (Manihot esculenta) evokes genome-wide changes in DNA methylation

Open access

Kitimu, Shedrack R., Taylor, Julian, March, Timothy J., Tairo, Fred, Wilkinson, Mike J., Rodríguez López, Carlos M.·2015·Frontiers in Plant Science

DOI 10.3389/fpls.2015.00590PMC PMC4534864

Open this paper in CoChat — free account Open PDF

Abstract

There is great interest in the phenotypic, genetic and epigenetic changes associated with plant in vitro culture known as somaclonal variation. In vitro propagation systems that are based on the use of microcuttings or meristem cultures are considered analogous to clonal cuttings and so widely viewed to be largely free from such somaclonal effects. In this study, we surveyed for epigenetic changes during propagation by meristem culture and by field cuttings in five cassava (Manihot esculenta) cultivars. Principal Co-ordinate Analysis of profiles generated by methylation-sensitive amplified polymorphism revealed clear divergence between samples taken from field-grown cuttings and those recovered from meristem culture. There was also good separation between the tissues of field samples but this effect was less distinct among the meristem culture materials. Application of methylation-sensitive Genotype by sequencing identified 105 candidate epimarks that distinguish between field cutting and meristem culture samples. Cross referencing the sequences of these epimarks to the draft cassava genome revealed 102 sites associated with genes whose homologs have been implicated in a range of fundamental biological processes including cell differentiation, development, sugar metabolism, DNA methylation, stress response, photosynthesis, and transposon activation. We explore the relevance of these findings for the selection of micropropagation systems for use on this and other crops.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.3389/fpls.2015.00590

Cites

82 of 82 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Favoring direct organogenesis over indirect methods minimizes variation and preserves genetic fidelity, as indirect organogenesis typically consists of a callus phase associated with prolonged cell proliferation and extended culture exposure, increasing the risk of genetic instability.
“Another crucial approach involves favoring direct organogenesis over indirect methods, as indirect organogenesis typically consists of a callus phase associated with prolonged cell proliferation and extended culture exposure, increasing the risk of genetic instability [158].”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [158]
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
In Manihot esculenta meristem micropropagation, variation was observed.
“Variation observed”
From Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives (2025) · cites this paper as [158]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
<tt>edgeR</tt> : a Bioconductor package for differential expression analysis of digital gene expression data
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
genalex 6: genetic analysis in Excel. Population genetic software for teaching and research
Peakall, R., & Smouse, P. E. (2005) · Molecular Ecology Notes · doi:10.1111/j.1471-8286.2005.01155.x · Cited by 16,596 · see citing works
GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update
Peakall, R., & Smouse, P. E. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts460 · Cited by 13,165 · see citing works
A scaling normalization method for differential expression analysis of RNA-seq data
Robinson, M. D., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-3-r25 · Cited by 7,876 · see citing works
A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species
Elshire, R. J., Glaubitz, J. C., Sun, Q., Poland, J., Kawamoto, K., Buckler, E. S., & Mitchell, S. E. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019379 · Cited by 6,461 · see citing works
Development of High-Density Genetic Maps for Barley and Wheat Using a Novel Two-Enzyme Genotyping-by-Sequencing Approach
Poland, J., Brown, P. J., Sorrells, M. E., & Jannink, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032253 · Cited by 1,802 · see citing works
Epigenetic reprogramming in mammals
Morgan, H. D., Santos, F., Green, K., Dean, W., & Reik, W. (2005) · Human Molecular Genetics · doi:10.1093/hmg/ddi114 · Cited by 1,344 · 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
Small-sample estimation of negative binomial dispersion, with applications to SAGE data
Robinson, M. D., & Smyth, G. K. (2007) · Biostatistics · doi:10.1093/biostatistics/kxm030 · Cited by 1,073 · see citing works
A Generic Estimation of Population Subdivision Using Distances Between Alleles With Special Reference for Microsatellite Loci
Michalakis, Y., & Excoffier, L. (1996) · Genetics · doi:10.1093/genetics/142.3.1061 · Cited by 957 · see citing works
The UCSC Genome Browser database: extensions and updates 2013
Meyer, L. R., Zweig, A. S., Hinrichs, A. S., Karolchik, D., Kuhn, R. M., Wong, M., Sloan, C. A., Rosenbloom, K. R., Roe, G. R., Rhead, B. L., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1048 · Cited by 901 · see citing works
Moderated statistical tests for assessing differences in tag abundance
Robinson, M. D., & Smyth, G. K. (2007) · Bioinformatics · doi:10.1093/bioinformatics/btm453 · Cited by 856 · see citing works
Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development.
Finnegan, E. J., Peacock, W. J., & Dennis, E. S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8449 · Cited by 720 · see citing works
Somaclonal Variation in Plants: Causes and Detection Methods
Bairu, M. W., Aremu, A. O., & Van Staden, J. (2011) · Plant Growth Regulation · doi:10.1007/s10725-010-9554-x · Cited by 674 · see citing works
DNA methylation in Arabidopsis has a genetic basis and shows evidence of local adaptation
Dubin, M., Zhang, P.-Y., Meng, D.-Z., Remigereau, M.-S., Osborne, E. J., Casale, F. P., Drewe, P., Kahles, A., Jean, G., Vilhjálmsson, B., et al. (2015) · eLife · doi:10.7554/elife.05255 · Cited by 497 · see citing works
Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense
Yu, A., Lepère, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Abraham, A., Penterman, J. N., Fischer, R. L., Voinnet, O., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211757110 · Cited by 463 · see citing works
Epigenetic Memory for Stress Response and Adaptation in Plants
Kinoshita, T., & Seki, M. (2014) · Plant and Cell Physiology · doi:10.1093/pcp/pcu125 · Cited by 433 · see citing works
Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms
Reyna-López, G. E., Simpson, J. K., & Ruíz-Herrera, J. (1997) · Molecular and General Genetics MGG · doi:10.1007/s004380050374 · Cited by 433 · 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 control
Delcuve, G. P., Rastegar, M., & Davie, J. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21678 · Cited by 392 · see citing works
Primed plants do not forget
Pastor, V., Luna, E., Mauch‐Mani, B., Ton, J., & Flors, V. (2012) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2012.02.013 · Cited by 388 · see citing works
DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs
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
Control of FWA gene silencing in Arabidopsis thaliana by SINE‐related direct repeats
Kinoshita, Y., Saze, H., Kinoshita, T., Miura, A., Soppe, W. J. J., Koornneef, M., & Kakutani, T. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02936.x · Cited by 282 · see citing works
DNA Methylation Is Critical for Arabidopsis Embryogenesis and Seed Viability
Xiao, W., Custard, K. D., Brown, R. C., Lemmon, B. E., Harada, J. J., Goldberg, R. B., & Fischer, R. L. (2006) · The Plant Cell · doi:10.1105/tpc.105.038836 · Cited by 278 · 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
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
Targets of RNA-directed DNA methylation
Matzke, M. A., Kanno, T., Hüettel, B., Daxinger, L., & Matzke, A. J. M. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.06.007 · Cited by 228 · see citing works
Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA
Messeguer, R., Ganal, M. W., Steffens, J. C., & Tanksley, S. D. (1991) · Plant Molecular Biology · doi:10.1007/bf00015069 · Cited by 223 · 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
Specificity ofHpaII andHaeII DNA methylases
Mann, M. B., & Smith, H. O. (1977) · Nucleic Acids Research · doi:10.1093/nar/4.12.4211 · Cited by 216 · see citing works
ARGONAUTE4 Is Required for Resistance toPseudomonas syringaeinArabidopsis
Agorio, A., & Vera, P. (2007) · The Plant Cell · doi:10.1105/tpc.107.054494 · Cited by 206 · see citing works
DNA cytosine methylation in plant development
Zhang, M., Kimatu, J. N., Xu, K., & Liu, B. (2010) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/s1673-8527(09)60020-5 · Cited by 205 · see citing works
Mutational Analysis of the Arabidopsis Nucleotide Binding Site–Leucine-Rich Repeat Resistance Gene RPS2
Tao, Y., Yuan, F., Leister, R. T., Ausubel, F. M., & Katagiri, F. (2000) · The Plant Cell · doi:10.1105/tpc.12.12.2541 · Cited by 189 · see citing works
Epigenetic control of plant immunity
Álvarez, M. E., Nota, F., & Cambiagno, D. A. (2010) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2010.00621.x · Cited by 181 · see citing works
How to interpret Methylation Sensitive Amplified Polymorphism (MSAP) profiles?
Fulneček, J., & Kovařı́k, A. (2014) · BMC Genetics · doi:10.1186/1471-2156-15-2 · Cited by 175 · see citing works
New Insights into Somatic Embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 Are Epigenetically Regulated in Coffea canephora
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
Impact of Amplified Fragment Length Polymorphism Size Homoplasy on the Estimation of Population Genetic Diversity and the Detection of Selective Loci
Caballero, A., Quesada, H., & Rolán‐Alvarez, E. (2008) · Genetics · doi:10.1534/genetics.107.083246 · Cited by 151 · see citing works
Ecological Epigenetics: Beyond MS-AFLP
Schrey, A. W., Álvarez, M., Foust, C. M., Kilvitis, H. J., Lee, J. D., Liebl, A. L., Martin, L. B., Richards, C. L., & Robertson, M. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict012 · Cited by 148 · 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
Variation in oil palm (Elaeis guineensis Jacq.) tissue culture-derived regenerants revealed by AFLPs with methylation-sensitive enzymes
Matthes, M. C., Singh, R., Cheah, S. C., & Karp, A. (2001) · Theoretical and Applied Genetics · doi:10.1007/s001220000491 · Cited by 144 · see citing works
msap : a tool for the statistical analysis of methylation‐sensitive amplified polymorphism data
Pérez‐Figueroa, A. (2013) · Molecular Ecology Resources · doi:10.1111/1755-0998.12064 · Cited by 141 · 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
Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP)
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
Common themes in siRNA-mediated epigenetic silencing pathways
Verdel, A., Vavasseur, A., Le Gorrec, M., & Touat-Todeschini, L. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082691av · Cited by 135 · see citing works
Low relative humidity triggers RNA-directed de novo DNA methylation and suppression of genes controlling stomatal development
Tricker, P. J., Gibbings, J. G., Lopez, C. M. R., Hadley, P., & Wilkinson, M. J. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers076 · Cited by 128 · see citing works
Self-citation
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
DNA methylation: a source of random variation in natural populations
Massicotte, R., Whitelaw, E., & Angers, B. (2011) · Epigenetics · doi:10.4161/epi.6.4.14532 · Cited by 111 · see citing works
Arabidopsis thaliana calcium-dependent lipid-binding protein (AtCLB): a novel repressor of abiotic stress response
de Silva, K., Laska, B., Brown, C. S., Sederoff, H. W., & Khodakovskaya, M. V. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/erq468 · Cited by 107 · see citing works
Field performance of transgenic potato plants compared with controls regenerated from tuber discs and shoot cuttings
Dale, P. J., & McPartlan, H. C. (1992) · Theoretical and Applied Genetics · doi:10.1007/bf00224156 · Cited by 105 · see citing works
Progressive erosion of genetic and epigenetic variation in callus‐derived cocoa (Theobroma cacao) plants
Lopez, C. M. R., Wetten, A. C., & Wilkinson, M. J. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03242.x · Cited by 104 · see citing works
Self-citation
Somatic Embryogenesis in Leguminous Plants
Lakshmanan, P., & Taji, A. (2000) · Plant Biology · doi:10.1055/s-2000-9159 · Cited by 93 · see citing works
Cloning of the MspI modification enzyme. The site of modification and its effects on cleavage by MspI and HpaII.
Walder, R. Y., Langtimm, C. J., Chatterjee, R., & Walder, J. A. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)33184-3 · Cited by 86 · 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
Mutational Analysis of the Arabidopsis Nucleotide Binding Site: Leucine-Rich Repeat Resistance Gene RPS2
Yi, T., Yuan, F., Leister, R. T., Ausubel, F. M., & Katagiri, F. (2000) · The Plant Cell · doi:10.2307/3871247 · Cited by 81 · see citing works
Somaclonal variation in micropropagated oil palm. Characterization of two novel genes with enhanced expression in epigenetically abnormal cell lines and in response to auxin
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
Regulation of disease‐responsive genes mediated by epigenetic factors: interaction of Arabidopsis–Pseudomonas
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
Conservation and divergence of DNA methylation in eukaryotes
Su, Z., Han, L., & Zhao, Z. (2011) · Epigenetics · doi:10.4161/epi.6.2.13875 · Cited by 72 · see citing works
Potato cytosine methylation and gene expression changes induced by a beneficial bacterial endophyte, Burkholderia phytofirmans strain PsJN
Da, K., Nowak, J., & Flinn, B. S. (2011) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2011.09.013 · Cited by 69 · see citing works
Transgenerational, Dynamic Methylation of Stomata Genes in Response to Low Relative Humidity
Tricker, P. J., Lopez, C. M. R., Gibbings, G., Hadley, P., & Wilkinson, M. J. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14046674 · Cited by 60 · see citing works
Self-citation
Assessment of the Genetic Stability of Micropropagated Plants ofCannabis sativaby ISSR Markers
Lata, H., Chandra, S., Techen, N., Khan, I. A., & ElSohly, M. A. (2009) · Planta Medica · doi:10.1055/s-0029-1185945 · Cited by 60 · see citing works
Field performance of transgenic potatoes
Conner, A. J., Williams, M., Abernethy, D. J., Fletcher, P. J., & Genet, R. A. (1994) · New Zealand Journal of Crop and Horticultural Science · doi:10.1080/01140671.1994.9513847 · Cited by 58 · see citing works
Rapid changes in amplification and methylation pattern of genomic DNA in cultured carrot root explants (Daucus carota L.)
Arnholdt‐Schmitt, B. (1993) · Theoretical and Applied Genetics · doi:10.1007/bf00225021 · Cited by 51 · 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
Self-citation
An efficient mass propagation system for cassava (Manihot esculenta Crantz) based on nodal explants and axillary bud-derived meristems
Konan, N. K., Schöpke, C. R., Cárcamo, R., Beachy, R. N., & Fauquet, C. (1997) · Plant Cell Reports · doi:10.1007/bf01092763 · Cited by 48 · see citing works
Small sample estimation of ρ1
Wallis, J. R., & O'Connell, P. E. (1972) · Water Resources Research · doi:10.1029/wr008i003p00707 · Cited by 44 · see citing works
Genetic Variation among Sweetpotatoes Propagated through Nodal and Adventitious Sprouts
Villordon, A. Q., & LaBonte, D. R. (1996) · Journal of the American Society for Horticultural Science · doi:10.21273/jashs.121.2.170 · Cited by 42 · see citing works
Effects of auxins and cytokinins on epigenetic instability of callus-propagated Kalanchoe blossfeldiana Poelln.
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
A simple and low-cost strategy for micropropagation of cassava (Manihot esculenta Crantz).
Santana, M. A., Romay, G., Matehus, J., Villardón, J. L. V., & Demey, J. R. (2009) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb2009.000-9375 · Cited by 37 · see citing works
Relationship between DNA methylation and histone acetylation levels, cell redox and cell differentiation states in sugarbeet lines
Causevic, A., Gentil, M.-V., Delaunay, A., Abuelsoud, W., Garcia, Z., Pannetier, C., Brignolas, F., Hagège, D., & Maury, S. (2006) · Planta · doi:10.1007/s00425-006-0267-3 · Cited by 36 · see citing works
Direct and indirect organogenesis of Clivia miniata and assessment of DNA methylation changes in various regenerated plantlets
Wang, Q.-M., Wang, Y.-Z., Sun, L.-L., Gao, F., Sun, W. D., He, J., Gao, X., & Wang, L. (2012) · Plant Cell Reports · doi:10.1007/s00299-012-1248-6 · Cited by 36 · see citing works
AFSM sequencing approach: a simple and rapid method for genome-wide SNP and methylation site discovery and genetic mapping
Xia, Z., Zou, M., Zhang, S., Feng, B., & Wang, W. (2014) · Scientific Reports · doi:10.1038/srep07300 · Cited by 33 · 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
Detection and quantification of tissue of origin in salmon and veal products using methylation sensitive AFLPs
Lopez, C. M. R., Morán, P., Lago, F. C., Espiñeira, M., Beckmann, M., & Consuegra, S. (2011) · Food Chemistry · doi:10.1016/j.foodchem.2011.09.120 · Cited by 30 · see citing works
Variations in the DNA methylation and polypeptide patterns of adult hazel (Corylus avellana L.) associated with sequential in vitro subcultures
Díaz‐Sala, C., Rey, M., Boronat, A., Besford, R. T., & Rodriguez, R. (1995) · Plant Cell Reports · doi:10.1007/bf00193723 · Cited by 28 · see citing works
Detection of somaclonal variation during cocoa somatic embryogenesis characterised using cleaved amplified polymorphic sequence and the new freeware Artbio
Lopez, C. M. R., Bravo, H. S., Wetten, A. C., & Wilkinson, M. J. (2009) · Molecular Breeding · doi:10.1007/s11032-009-9348-x · Cited by 26 · see citing works
Self-citation
Morphological Development of Lingonberry as Affected by In Vitro and Ex Vitro Propagation Methods and Source Propagule
Debnath, S. C. (2005) · HortScience · doi:10.21273/hortsci.40.3.760 · Cited by 24 · see citing works
Biotechnology of the Banana: A Review of Recent Progress
Rout, G. R., Samantaray, S., & Das, P. S. (2000) · Plant Biology · doi:10.1055/s-2000-7470 · Cited by 24 · see citing works
Use of secondary somatic embryos promotes genetic fidelity in cryopreservation of cocoa (Theobroma cacao L.)
FANG, J.-Y., Wetten, A. C., & Adu‐Gyamfi, R. (2008) · Agricultural and Food Science · doi:10.2137/145960609789267579 · Cited by 24 · see citing works
Regeneration from chrysanthemum flowers: a review
da Silva, J. A. T., Lema-Rumińska, J., Tymoszuk, A., & Kulpa, D. (2015) · Acta Physiologiae Plantarum · doi:10.1007/s11738-015-1773-3 · Cited by 19 · see citing works
DNA methylation variation in Arabidopsis has a genetic basis and shows evidence of local adaptationPreprint
Dubin, M., Zhang, P., Meng, D., Remigereau, M., Osborne, E. J., Casale, F. P., Drewe, P., Kahles, A., Vilhjálmsson, B. J., Jagoda, J., et al. (2014) · arXiv (Cornell University) · doi:10.48550/arxiv.1410.5723 · Cited by 11 · see citing works
Tissue Culture Applications for Plant Quarantine
Kahn, R. P. (1979) · Elsevier eBooks · doi:10.1016/b978-0-12-470285-1.50019-1 · Cited by 6 · see citing works

Flagged first, then by citations

2 of the 84 references couldn’t be matched to a known paper.

Sorted by citations

Widespread natural variation of DNA methylation within angiosperms
Niederhuth, C. E., Bewick, A. J., Ji, L., Alabady, M., Kim, K. D., Li, Q., Rohr, N. A., Rambani, A., Burke, J. M., Udall, J. A., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1059-0 · Cited by 557 · see citing works
Abnormalities 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
Cassava Mosaic and Brown Streak Diseases: Current Perspectives and Beyond
Rey, M. E. C., & Vanderschuren, H. (2017) · Annual Review of Virology · doi:10.1146/annurev-virology-101416-041913 · Cited by 113 · see citing works
Plant Stress Responses and Phenotypic Plasticity in the Epigenomics Era: Perspectives on the Grapevine Scenario, a Model for Perennial Crop Plants
Fortes, A. M., & Gallusci, P. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00082 · Cited by 96 · see citing works
The potential of using biotechnology to improve cassava: a review
Chavarriaga‐Aguirre, P., Brand, A., Medina, A., Prías, M., Escobar, R., Martinez, J., Tatis, P. A. D., López, C. E., Roca, W. M., & Tohme, J. M. (2016) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/s11627-016-9776-3 · Cited by 84 · see citing works
A Concise Review on Multi-Omics Data Integration for Terroir Analysis in Vitis vinifera
Jullian, P., Collins, C., Cavagnaro, T. R., & Lopez, C. M. R. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01065 · Cited by 82 · see citing works
Global DNA Methylation Patterns Can Play a Role in Defining Terroir in Grapevine (Vitis vinifera cv. Shiraz)
Xie, H., Konaté, M., Sai, N., Tesfamicael, K., Cavagnaro, T. R., Gilliham, M., Breen, J., Metcalfe, A. V., Stephen, J. R., Bei, R. D., et al. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01860 · Cited by 73 · see citing works
Somaclonal Variation and Clonal Fidelity in Commercial Micropropagation: Challenges and Perspectives
Majumder, S., Igamberdiev, A. U., & Debnath, S. C. (2025) · Agronomy · doi:10.3390/agronomy15061489 · Cited by 46 · see citing works
Salt Stress Induces Non-CG Methylation in Coding Regions of Barley Seedlings (Hordeum vulgare)
Konaté, M., Wilkinson, M. J., Mayne, B. T., Pederson, S., Scott, E. S., Berger, B., & Lopez, C. M. R. (2018) · Epigenomes · doi:10.3390/epigenomes2020012 · Cited by 43 · see citing works
Self-citation
Effect of Cryopreservation and Post-Cryopreservation Somatic Embryogenesis on the Epigenetic Fidelity of Cocoa (Theobroma cacao L.)
Adu‐Gyamfi, R., Wetten, A., Lopez, C. M. R., & López, R. (2016) · PLoS ONE · doi:10.1371/journal.pone.0158857 · Cited by 34 · see citing works
Somaclonal Variation and Methods Used for Its Detection
Ranghoo‐Sanmukhiya, V. M. (2020) · Springer eBooks · doi:10.1007/978-981-15-7736-9_1 · Cited by 29 · see citing works
Whole-Genome Bisulfite Sequencing Reveals a Role for DNA Methylation in Variants from Callus Culture of Pineapple (Ananas comosus L.)
Lin, W., Xiao, X., Zhang, H., Li, Y., Liu, S., Sun, W., Zhang, X., & Wu, Q. (2019) · Genes · doi:10.3390/genes10110877 · Cited by 27 · see citing works
Use of Combined MSAP and NGS Techniques to Identify Differentially Methylated Regions in Somaclones: A Case Study of Two Stable Somatic Wheat Mutants
Baránek, M., Čechová, J., Kovács, T., Eichmeier, A., Wang, S., Raddová, J., Nečas, T., & Ye, X. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165749 · Cited by 23 · see citing works
Multiple morphogenic culture systems cause loss of resistance to cassava mosaic disease
Chauhan, R. D., Beyene, G., & Taylor, N. J. (2018) · BMC Plant Biology · doi:10.1186/s12870-018-1354-x · Cited by 22 · see citing works
Dynamics of the Methylome and Transcriptome during the Regeneration of Rice
Hsu, F., Gohain, M., Allishe, A., Huang, Y., Liao, J., Kuang, L., & Chen, P. (2018) · Epigenomes · doi:10.3390/epigenomes2030014 · Cited by 21 · see citing works
Common garden experiment reveals altered nutritional values and DNA methylation profiles in micropropagated three elite Ghanaian sweet potato genotypes
Akomeah, B., Quain, M. D., Ramesh, S. A., Anand, L., & Lopez, C. M. R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0208214 · Cited by 17 · see citing works
A novel micropropagation of Lycium ruthenicum and epigenetic fidelity assessment of three types of micropropagated plants in vitro and ex vitro
Gao, Y., Wang, Q.-M., An, Q., Cui, J., Zhou, Y., Qi, X., Zhang, L., & Li, L. (2021) · PLOS ONE · doi:10.1371/journal.pone.0247666 · Cited by 15 · see citing works
Additive and non-additive epigenetic signatures of natural hybridization between fish species with different mating systems
Berbel‐Filho, W. M., Pacheco, G., Lira, M. G. S., de Leániz, C. G., Lima, S. M. Q., Lopez, C. M. R., Zhou, J., & Consuegra, S. (2022) · Epigenetics · doi:10.1080/15592294.2022.2123014 · Cited by 13 · see citing works
Agromorphologic, genetic and methylation profiling of Dioscorea and Musa species multiplied under three micropropagation systems
Jekayinoluwa, T., Guèye, B., Bhattacharjee, R., Osibanjo, O., Shah, T. M., & Abberton, M. T. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216717 · Cited by 13 · see citing works
Phylogenomics reveals extensive introgression and a case of mito-nuclear discordance in the killifish genus Kryptolebias
Berbel‐Filho, W. M., Pacheco, G., Tatarenkov, A., Lira, M. G. S., de Leániz, C. G., Lopez, C. M. R., Lima, S. M. Q., & Consuegra, S. (2022) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2022.107617 · Cited by 13 · see citing works
Against the Odds: Hybrid Zones between Mangrove Killifish Species with Different Mating Systems
Berbel‐Filho, W. M., Tatarenkov, A., Pacheco, G., Espírito‐Santo, H. M. V., Lira, M. G. S., de Leániz, C. G., Avise, J. C., Lima, S. M. Q., Lopez, C. M. R., & Consuegra, S. (2021) · Genes · doi:10.3390/genes12101486 · Cited by 11 · see citing works
Changes in DNA methylation pattern of apple long-term in vitro shoot culture and acclimatized plants
Gulyás, A., Dobránszki, J., Kiss, E., da Silva, J. A. T., Posta, K., & Hidvégi, N. (2019) · Journal of Plant Physiology · doi:10.1016/j.jplph.2019.05.007 · Cited by 10 · see citing works
DNA Methylation Mechanism
Budak, M., & Yıldız, M. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.78125 · Cited by 8 · see citing works
Analysis of DNA Methylation Patterns Associated with In Vitro Propagated Globe Artichoke Plants Using an EpiRADseq-Based Approach
Cerruti, E., Comino, C., Acquadro, A., Marconi, G., Repetto, A. M., Pisanu, A. B., Pilia, R., Albertini, E., & Portis, E. (2019) · Genes · doi:10.3390/genes10040263 · Cited by 7 · see citing works
Organogénesis in-vitro using three tissues types of tree tomato [ Solanum betaceum (Cav.)]
Murillo-Gómez, P. A., Rodrigo Hoyos, S., & Chavarriaga, P. (2017) · Agronomía Colombiana · doi:10.15446/agron.colomb.v35n1.61330 · Cited by 7 · see citing works
Greenhouse Spatial Effects Detected in the Barley (Hordeum vulgare L.) Epigenome Underlie Stochasticity of DNA Methylation
Konaté, M., Wilkinson, M. J., Taylor, J., Scott, E. S., Berger, B., & Lopez, C. M. R. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.553907 · Cited by 8 · see citing works
Self-citation
Effect of sterilants and plant growth regulators in regenerating commonly used cassava cultivars at the Kenyan coast
Kidasi, P. C., Kilalo, D. C., & Mwang’ombe, A. W. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e17263 · Cited by 5 · see citing works
Environmental conditions and agronomic practices induce consistent global changes in DNA methylation patterns in grapevine ( Vitis vinifera cv Shiraz)Preprint
Xie, H., Konaté, M., Sai, N., Tesfamicael, K., Cavagnaro, T. R., Gilliham, M., Breen, J., Metcalfe, A. V., DeBei, R., Collins, C., et al. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/127977 · Cited by 5 · see citing works
Molecular Markers for the Detection and Analysis of Somaclonal Variation
Martín, C., & González-Benito, M. E. (2024) · Somaclonal Variation: Basic and Practical Aspects · doi:10.1007/978-3-031-51626-9_4 · Cited by 4 · see citing works
Atlas of Age- and Tissue-Specific DNA Methylation during Early Development of Barley (Hordeum vulgare)
Konaté, M., Wilkinson, M. J., Mayne, B. T., Scott, E. S., Berger, B., & Lopez, C. M. R. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.90886 · Cited by 4 · see citing works
Self-citation
Systematic exploration of Ziziphus species collection and gene identification influencing physiological traits using genotype‐by‐sequencing technology
Uddin, N., Shinde, H., Ali, N., Zhang, Q., Ullah, R., Iqbal, Z., & Zhu, D. (2024) · Physiologia Plantarum · doi:10.1111/ppl.14426 · Cited by 4 · see citing works
Differential DNA methylation and gene expression during development of reproductive and vegetative organs in Ilex species
Cascales, J., Acevedo, R. M., Paiva, D. I., & Gottlieb, A. M. (2021) · Journal of Plant Research · doi:10.1007/s10265-021-01279-3 · Cited by 4 · see citing works
Phytoplasma Diseases Affecting Cassava
Álvarez, E. (2019) · Sustainability in plant and crop protection · doi:10.1007/978-3-030-29650-6_7 · Cited by 3 · see citing works
Temporary Immersion Bioreactors: Establishment of Cassava
Golle, D. P., Koefender, J., Horn, R. C., Piuco, N., Kaiper, C., & Câmera, J. N. (2019) · Journal of Agricultural Science · doi:10.5539/jas.v11n4p176 · Cited by 2 · see citing works
Genetic similarity enhances the strength of the relationship between gut bacteria and host DNA methylationPreprint
Zhou, J., Tesfamicael, K., Zhou, S. J., Rollins, L. A., & Lopez, C. M. R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.10.451923 · Cited by 2 · see citing works
Cassava for the future: embryogenic liquid cultures suitable for new biotech techniques
Dedičová, B., & López‐Lavalle, L. A. B. (2024) · BioTechniques · doi:10.1080/07366205.2024.2393546 · Cited by 1 · see citing works
Micropropagation of Cannabis sativa: genetic and epigenetic stability assessment over multiple generations
Lefebvre, V., Torkamaneh, D., Deslauriers, S., Devèze, T., de Ronne, M., Plourde, M. B., Lamara, M., & Germain, H. (2026) · Journal of Cannabis Research · doi:10.1186/s42238-026-00406-y · Cited by 1 · see citing works
Understanding and modifying starch metabolism to limit yield losses in field-grown cassava
David, L. C., Deslandes‐Hérold, G., Hostettler, C., Bischof, S., Fischer‐Stettler, M., Carluccio, A. V., Pfister, B., George, G. M., Wang, W., Stavolone, L., et al. (2026) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiag341 · Cited by 1 · see citing works
Library Preparation for Whole Genome Bisulfite Sequencing of Plant Genomes
Corbin, K. R., & Lopez, C. M. R. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.90716 · Cited by 1 · see citing works
NGHIÊN CỨU PHƯƠNG PHÁP NHÂN GIỐNG IN VITRO CÂY SẮN (Manihot esculenta) ĐỂ SẢN XUẤT CÂY GIỐNG SẠCH BỆNH
Thanh, T. D. T., Phương, N. P. T., Triêu, H. T. T., Thu, H. L. T., Hoàng, Đ. T. T., & Phúc, L. K. (2023) · Tạp chí Khoa học và công nghệ nông nghiệp Trường Đại học Nông Lâm Huế · doi:10.46826/huaf-jasat.v7n2y2023.1059 · Cited by 1 · see citing works
Common garden experiment reveals altered nutritional values and DNA methylation profiles in micropropagated three elite Ghanaian sweet potato genotypesPreprint
Akomeah, B., Quain, M. D., Ramesh, S. A., & Lopez, C. M. R. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/471623 · Cited by 1 · see citing works
Effect of Cryopreservation and Post-Cryopreservation Somatic Embryogenesis on
Adu‐Gyamfi, R., Wetten, A., Marcelino, C. H. D. S., López, M. D. C. R., & Osmond, G. (2016)
Additive and non-additive epigenetic signatures of hybridisation between fish species with different mating systemsPreprint
Berbel‐Filho, W. M., Tatarenkov, A., Pacheco, G., Espírito‐Santo, H. M. V., Lira, M. G. S., de Leániz, C. G., Avise, J. C., Lima, S. M. Q., Lopez, C. M. R., & Consuegra, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.07.01.182022
Relative roles of genetic and epigenetic variation on the ecology and evolution of mangrove killifishes (Kryptolebias spp.)
Berbel‐Filho, W. M. (2019) · doi:10.23889/suthesis.55248
Identification of marker-trait associated SNPs for fruit weight and plant height in a wild and domesticated jujube fruit tree ( Ziziphus spp.) collection using genotyping-by-sequencingPreprint
Uddin, N., Shinde, H., Tesfamicael, K., Ali, N., Tricker, P. J., & Lopez, C. M. R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.30.466592
El principio de laicidad como límite a determinadas manifestaciones de pertenencia religiosa dentro de los centros docentes públicos de Francia
Zabala, M. L. L. (2008) · La justicia uruguaya: revista jurìdica
Detection of differential DNA methylation in date palm (Phoenix dactylifera L.) vitroplants using whole genome bisulfite sequencing analysis
Mattat, I., Ahmed, A. A., Younuskunju, S., Pawar, K., Mohamoud, Y. A., Al-Malki, A., Malek, J. A., & Hamada, W. (2026) · BMC Plant Biology · doi:10.1186/s12870-026-09190-6
Epigenetic regulation of plant regeneration and its implications for somaclonal variation and genetic stability
Bharti, M., Shrishti, & Mukherjee, P. (2026) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1007/s11627-026-10697-8
Linking ex situ propagation and conservation of Rhizophora mangle through donor plant management and indole−3-butyric acid application
de Souza, M. R., Souza, C. D. S., de Melo, A. M. C., & Dias, P. C. (2026) · Wetlands Ecology and Management · doi:10.1007/s11273-026-10197-x

In vitro mutagenesis creates distinct morphological variants in cassava (Manihot esculenta Crantz.): A characterisation study
Antony, R., Joseph, J., Bastian, D., & Menon, M. V. (2018) · Electronic Journal of Plant Breeding · doi:10.5958/0975-928x.2018.00054.6 · Cited by 3 · see citing works
Evaluation of cassava plants generated by somatic embryogenesis in different stages of development using molecular markers
Infante, D., Osorio, M., Gámez, E., & Molina, S. (2012) · Electronic Journal of Biotechnology · doi:10.2225/vol15-issue4-fulltext-3 · Cited by 12 · see citing works
Direct and indirect organogenesis of Clivia miniata and assessment of DNA methylation changes in various regenerated plantlets
Wang, Q.-M., Wang, Y.-Z., Sun, L.-L., Gao, F., Sun, W. D., He, J., Gao, X., & Wang, L. (2012) · Plant Cell Reports · doi:10.1007/s00299-012-1248-6 · Cited by 36 · see citing works
Morphoagronomic characterization of (Manihot esculenta Crantz) clones obtained by in vitro culture
Beovides, Y., Medero, V., González, C., Xiqués, X., Román, M. I., Milián, M., García, S. M., Toledo, H., & Guerra, D. (2002) · DOAJ (DOAJ: Directory of Open Access Journals)
Genetic fidelity and variability of micropropagated cassava plants (Manihot esculenta Crantz) evaluated using ISSR markers
Vidal, Á. M., Vieira, L. J. D., Ferreira, C. F., Souza, F. V. D., Souza, A. S., & Lédo, C. A. D. S. (2015) · Genetics and Molecular Research · doi:10.4238/2015.july.14.2 · Cited by 13 · see citing works

Authors: Kitimu, S. R., Taylor, J., March, T. J., Tairo, F., Wilkinson, M. J., & Rodríguez López, C. M.
Affiliations: The University of Adelaide (AU)
Mikocheni Agricultural Research Institute (TZ)
ORCID: Taylor, Julian
March, Timothy J.
Tairo, Fred
Wilkinson, Mike J.
Venue: Frontiers in Plant Science
Publisher: Frontiers Media SA
Published: 2015-08-13
Volume: 6
Pages: 590-590
ISSN: 1664-462X (ISSN-L)
DOI: 10.3389/fpls.2015.00590
PMC: PMC4534864
OpenAlex: W1683146644
Cited by: 50
References: 84
Citations by year: 2026: 5 · 2025: 1 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 5 · 2020: 5 · 2019: 11 · 2018: 4 · 2017: 6 · 2016: 5
FWCI: 2.17
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Plant Science (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: Bill and Melinda Gates Foundation
Agence Nationale de la Recherche (ANR-11-BTBR-0005)
Institut National de la Recherche Agronomique
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 › Cassava research and cyanide
Keywords: cassava, meristem culture, micropropagation, DNA methylation, epigenetic variation, somaclonal variation, methylation-sensitive amplified polymorphism, transposon activation, cell differentiation, photosynthesis, stress response, sugar metabolism

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Meristem micropropagation of cassava (Manihot esculenta) evokes genome-wide changes in DNA methylation

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks