Skip to main content
Log in

In vitro culture: an epigenetic challenge for plants

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

Abstract

In vitro plant cell and tissue culture techniques are the basis of many micropropagation and breeding programs for scientific research. Plant tissue culture (PTC) involves organogenesis and embryogenesis, and the outcome depends on the different conditions to which the tissue is exposed. PTC is a stressful environment—high relative humidity, low ventilation rate, high concentrations of plant growth regulators, and low light availability—for plants that need to rapidly change their molecular regulation in order to respond fast and efficiently during cell division and growth. For instance, somatic embryogenesis (SE), which plays an important role in plant multiplication, requires complex cellular, biochemical and molecular processes for embryo formation and development. New data has come out about a connection between plant morphogenesis and epigenetics. Epigenetics is a very sensitive regulatory mechanism, which in most of cases is affected by the environment. Although it is known that, under plant morphogenesis, the genome has little or no change, DNA methylation and histone modifications are very susceptible to those in vitro environmental conditions. In the present review, we highlight the most used in vitro systems such as organogenesis and SE in plants and discuss how epigenetics plays a pivotal role in the phenotype outcome. Furthermore, we discuss the big role that the small RNAs have during cell division and propagation and propose different challenges and opportunities to study epigenetics in plant cell tissue and organ cultures.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ABP1:

Auxin binding protein1

ARF:

Auxin response factors

DCL1:

Dicer-like1

IAA:

Indolacetic acid

ISSR:

Inter-simple sequence repeat

MSAP:

Methylation-sensitive amplification polymorphism

MET1:

Methyltransferase 1

SE:

Somatic embryogenesis

miRNAs:

micro RNAs

sRNAs:

Small non-coding RNAs

TE:

Transposable elements

TSA:

Trichostatin A

References

  • Agrawal N, Dasaradhi PVN, Mohmmed A, Malhotra P, Bhatnagar RK, Mukherjee SK (2003) RNA interference: biology, mechanism, and applications. Microbiol Mol Biol Rev 67(4):657–685. doi:10.1128/mmbr.67.4.657-685.2003

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allis CD, Jenuwein T, Reinberg D, Caparros ML (2007) Epigenetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Arnholdt-Schmitt B (1993) Rapid changes in amplification and methylation pattern of genomic DNA in cultured carrot root explants (Daucus carota L.). Theor. Appl. Gen. 85(6):793-800

    Google Scholar 

  • Avivi Y, Morad V, Ben-Meir H, Zhao J, Kashkush K, Tzfira T, Citovsky V, Grafi G (2004) Reorganization of specific chromosomal domains and activation of silent genes in plant cells acquiring pluripotentiality. Dev Dyn 230(1):12–22

    CAS  PubMed  Google Scholar 

  • Baurens FC, Nicolleau J, Legavre T, Verdeil JL, Monteuuis O (2004) Genomic DNA methylation of juvenile and mature Acacia mangium micropropagated in vitro with reference to leaf morphology as a phase change marker. Tree Physiol 24(4):401–407

    CAS  PubMed  Google Scholar 

  • Becker C, Weigel D (2012) Epigenetic variation: origin and transgenerational inheritance. Curr Opin Plant Biol 15(5):562–567. doi:10.1016/j.pbi.2012.08.004

    CAS  PubMed  Google Scholar 

  • Bird A (2007) Perceptions of epigenetics. Nature 447(7143):396–398

    CAS  PubMed  Google Scholar 

  • Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou J-P, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7(3):e1002014. doi:10.1371/journal.pgen.1002014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bräutigam K, Vining KJ, Lafon-Placette C, Fossdal CG, Mirouze M, Marcos JG, Fluch S, Fraga MF, Guevara MÁ, Abarca D, Johnsen Ø, Maury S, Strauss SH, Campbell MM, Rohde A, Díaz-Sala C, Cervera M-T (2013) Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol Evol 3(2):399–415. doi:10.1002/ece3.461

    PubMed Central  PubMed  Google Scholar 

  • Brettell RS, Dennis E (1991) Reactivation of a silent Ac following tissue culture is associated with heritable alterations in its methylation pattern. Mol Gen Genet 229(3):365–372. doi:10.1007/bf00267457

    CAS  PubMed  Google Scholar 

  • Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, VatÇn A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465(7296):316–321

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cassells AC, Curry RF (2001) Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. Plant Cell Tiss Org 64(2–3):145–157

    CAS  Google Scholar 

  • Causevic A, Gentil MV, Delaunay A, El-Soud W, Garcia Z, Pannetier C, Brignolas F, Hagége D, Maury S (2006) Relationship between DNA methylation and histone acetylation levels, cell redox and cell differentiation states in sugarbeet lines. Planta 224(4):812–827

    CAS  PubMed  Google Scholar 

  • Cazzonelli CI, Vanstraelen M, Simon S, Yin K, Carron-Arthur A, Nisar N, Tarle G, Cuttriss AJ, Searle IR, Benkova E, Mathesius U, Masle J, Friml J, Pogson BJ (2013) Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development. PLoS ONE 8(7):e70069. doi:10.1371/journal.pone.0070069

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chakrabarty D, Yu KW, Paek KY (2003) Detection of DNA methylation changes during somatic embryogenesis of siberian ginseng (Eleuterococcus senticosus). Plant Sci 165(1):61–68

    CAS  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, Goodrich J (2004) Interaction of polycomb-group proteins controlling flowering in Arabidopsis. Development 131(21):5263–5276

    CAS  PubMed  Google Scholar 

  • Charron JBF, He H, Elling AA, Deng XW (2009) Dynamic landscapes of four histone modifications during deetiolation in Arabidopsis. Plant Cell 21:3732–3748

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen M, Lv S, Meng Y (2010) Epigenetic performers in plants. Develop Growth Differ 52:555–566

    CAS  Google Scholar 

  • Chen YT, Shen CH, Lin WD, Chu HA, Huang BL, Kuo CI, Yeh KW, Huang LC, Chang IF (2013) Small RNAs of Sequoia sempervirens during rejuvenation and phase change. Plant Biol 15(1):27–36. doi:10.1111/j.1438-8677.2012.00622.x

    CAS  PubMed  Google Scholar 

  • Cheung P, Lau P (2005) Epigenetic regulation by histone methylation and histone variants. Mol Endocrin 19(3):563–573

    CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452(7184):215–219

    CAS  PubMed Central  PubMed  Google Scholar 

  • De-la-Pena C, Nic-Can G, Ojeda G, Herrera-Herrera J, Lopez-Torres A, Wrobel K, Robert-Diaz M (2012) KNOX1 is expressed and epigenetically regulated during in vitro conditions in Agave spp. BMC Plant Biol 12(1):203

    CAS  PubMed Central  PubMed  Google Scholar 

  • Diaz-Sala C, Rey M, Boronat A, Besford R, Rodriguez R (1995) Variations in the DNA methylation and polypeptide patterns of adult hazel (Corylus avellana L.) associated with sequential in vitro subcultures. Plant Cell Rep 15(3):218–221

    CAS  PubMed  Google Scholar 

  • Ding Y, Wang X, Su L, Zhai J, Cao SY, Zhang DF, Liu C, Bi YP, Qian Q, Cheng Z, Chu C, Cao X (2007) SDG714, a histone H3K9 methyltransferase, is involved in Tos17 DNA methylation and transposition in rice. Plant Cell 19(1):9–22

    CAS  PubMed Central  PubMed  Google Scholar 

  • Duncan RR (1996) Tissue culture-induced variation and crop improvement. In: Donald LS (ed) Advances in agronomy, vol 58. Academic Press, Waltham, pp 201–240

    Google Scholar 

  • Elmeer KES (2013) Factors regulating somatic embryogenesis in plants. In: Aslam Junaid, Srivastava PS, Sharma MP (eds) Somatic embryogenesis and gene expression. Narosa Publishing House, New Delhi, pp 56–81

    Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of auxin response factor3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16(9):939–944. doi:10.1016/j.cub.2006.03.065

    CAS  PubMed  Google Scholar 

  • Feil R (2009) Epigenetics: ready for the marks. Nature 461:359–360

    CAS  PubMed  Google Scholar 

  • Feng SH, Cokus SJ, Zhang XY, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, Ukomadu C, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107(19):8689–8694

    CAS  PubMed Central  PubMed  Google Scholar 

  • Finnegan EJ, Genger RK, Peacock WJ, Dennis ES (1998) DNA Methylation in plants. Annu Rev Plant Physiol Plant Mol Biol 49(1):223–247. doi:10.1146/annurev.arplant.49.1.223

    CAS  PubMed  Google Scholar 

  • Fiuk A, Bednarek PT, Rybczynski JJ (2010) Flow cytometry, HPLC-RP, and metAFLP analyses to assess genetic variability in somatic embryo-derived plantlets of Gentiana pannonica scop. Plant Mol Biol Rep 28(3):413–420

    CAS  Google Scholar 

  • Ford D (2013) Honeybees and cell lines as models of DNA methylation and aging in response to diet. Exp Ger 48(7):614–619. doi:10.1016/j.exger.2012.07.010

    CAS  Google Scholar 

  • Fraga M, Cañal M, Rodríguez R (2002) Phase-change related epigenetic and physiological changes in Pinus radiata D. Don Planta 215(4):672–678

    CAS  Google Scholar 

  • Fu Y, Kawabe A, Etcheverry M, Ito T, Toyoda A, Fujiyama A, Colot V, Tarutani Y, Kakutani T (2013) Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J 32(17):2407–2417. doi:10.1038/emboj.2013.169

    CAS  PubMed  Google Scholar 

  • Gamborg OL, Phillips GC (1995) Plant cell, tissue and organ culture: fundamental methods. Springer, Berlin

    Google Scholar 

  • Gao X, Yang D, Cao D, Ao M, Sui X, Wang Q, Kimatu J, Wang L (2010) In vitro micropropagation of Freesia hybrida and the assessment of genetic and epigenetic stability in regenerated plantlets. J Plant Growth Regul 29(3):257–267

    CAS  Google Scholar 

  • Gaspar T, Kevers C, Penel C, Greppin H, Reid D, Thorpe T (1996) Plant hormones and plant growth regulators in plant tissue culture. Vitro Cell Dev Biol Plant 32(4):272–289. doi:10.1007/bf02822700

    CAS  Google Scholar 

  • George EF, Hall MA, De Klerk G-J (2008) Plant propagation by tissue culture: 1 volume. The background, vol 1. Springer, Berlin

    Google Scholar 

  • Giménez C, Palacios G, Colmenares M (2006) Musa methylated DNA sequences associated with tolerance to Mycosphaerella fijiensis toxins. Plant Mol Biol Rep 24(1):33–43. doi:10.1007/bf02914044

    Google Scholar 

  • Grafi G, Ben-Meir H, Avivi Y, Moshe M, Dahan Y, Zemach A (2007) Histone methylation controls telomerase-independent telomere lengthening in cells undergoing dedifferentiation. Dev Biol 306(2):838–846

    CAS  PubMed  Google Scholar 

  • Greenwood MS (1987) Rejuvenation of forest trees. Plant Growth Regul 6(1–2):1–12. doi:10.1007/BF00043947

    CAS  Google Scholar 

  • Guo HS, Xie Q, Fei JF, Chua NH (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(5):1376–1386

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hadi MZ, Bridgen MP (1996) Somaclonal variation as a tool to develop pest resistant plants of Torenia fournieri, “Compacta Blue”. Plant Cell Tiss Organ Cult 46(1):43–50. doi:10.1007/bf00039695

    CAS  Google Scholar 

  • Hao Y-J, Deng X–X (2003) Genetically stable regeneration of apple plants from slow growth. Plant Cell Tiss Org 72(3):253–260. doi:10.1023/a:1022388728497

    CAS  Google Scholar 

  • Hasbún R, Valledor L, Berdasco M, Santamaría E, Cañal M, Rodríguez R, Rios D, Sánchez M (2005) In vitro proliferation and genome DNA methylation in adult chestnuts. Acta Hort 693(1):333–340

    Google Scholar 

  • Hasbún R, Valledor L, Santamaria E, Canal M, Rodriguez R, Berdasco M (2007) Dynamics of DNA methylation in chestnut trees development. Acta Hort. 760(2):563

    Google Scholar 

  • He C, Chen X, Huang H, Xu L (2012) Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet 8(8):e1002911. doi:10.1371/journal.pgen.1002911

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hirsch S, Baumberger R & Grossniklaus U (2013) Epigenetic variation, inheritance, and selection in plant populations. Cold Spring Harbor Symposia on Quantitative Biology doi:10.1101/sqb.2013.77.014605

  • Holec S, Berger F (2012) Polycomb group complexes mediate developmental transitions in plants. Plant Physiol 158(1):35–43. doi:10.1104/pp.111.186445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. doi:10.1105/tpc.113.116053

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ivey KN, Srivastava D (2010) MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7(1):36–41

    CAS  PubMed  Google Scholar 

  • Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(3s):245–254

    CAS  PubMed  Google Scholar 

  • Jain SM (1997) Micropropagation of selected somaclones of Begonia and Saintpaulia. J Biosci 22(5):585–592. doi:10.1007/bf02703396

    Google Scholar 

  • Jain SM, Brar DS, Ahloowalia B (1998) Somaclonal variation and induced mutations in crop improvement, vol 32. Springer, Berlin

    Google Scholar 

  • Jaligot E, Rival A, Beulé T, Dussert S, Verdeil JL (2000) Somaclonal variation in oil palm (Elaeis guineensis Jacq.): the DNA methylation hypothesis. Plant Cell Rep 19:684–690

    CAS  Google Scholar 

  • Johnson L, Mollah S, Garcia BA, Muratore TL, Shabanowitz J, Hunt DF, Jacobsen SE (2004) Mass spectrometry analysis of Arabidopsis histone H3 reveals distinct combinations of post-translational modifications. Nucleic Acids Res 32(22):6511–6518

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jonard R (1986) Micrografting and its applications to tree improvement. In: Bajaj YPS (ed) Trees I. Biotechnology in agriculture and forestry, vol 1. Springer, Berlin, pp 31–48

    Google Scholar 

  • Joshi R, Joshi PR, Aramod Kumar PK (2013) Regulation of somatic embryogenesis in crops: a review. Agri Rev 34(1):1–20

    Google Scholar 

  • Joyce SM, Cassells AC, Jain SM (2003) Stress and aberrant phenotypes in vitro culture. Plant Cell Tiss Org 74(2):103–121

    CAS  Google Scholar 

  • Kaeppler S, Phillips R (1993a) DNA methylation and tissue culture-induced variation in plants. Vitro Cell Dev Biol Plant 29(3):125–130

    Google Scholar 

  • Kaeppler SM, Phillips RL (1993b) Tissue culture-induced DNA methylation variation in maize. Proc Natl Acad Sci USA 90:8773–8776

    CAS  PubMed Central  PubMed  Google Scholar 

  • Katz A, Oliva M, Mosquna A, Hakim O, Ohad N (2004) FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development. Plant J 37(5):707–719. doi:10.1111/j.1365-313X.2003.01996.x

    CAS  PubMed  Google Scholar 

  • Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11(12):830–842

    CAS  PubMed  Google Scholar 

  • Kinoshita T, Harada JJ, Goldberg RB, Fischer RL (2001) Polycomb repression of flowering during early plant development. Proc Natl Acad Sci USA 98(24):14156–14161. doi:10.1073/pnas.241507798

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kornberg RD (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184(4139):868–871

    CAS  PubMed  Google Scholar 

  • Lafos M, Kroll P, Hohenstatt ML, Thorpe FL, Clarenz O, Schubert D (2011) Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet 7(4):e1002040. doi:10.1371/journal.pgen.1002040

    CAS  PubMed Central  PubMed  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation: a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    CAS  PubMed  Google Scholar 

  • Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23(3):120–127

    CAS  PubMed  Google Scholar 

  • Li Y, Butenko Y, Grafi G (2005) Histone deacetylation is required for progression through mitosis in tobacco cells. Plant J 41(3):346–352. doi:10.1111/j.1365-313X.2004.02301.x

    CAS  PubMed  Google Scholar 

  • Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128(4):707–719

    CAS  PubMed  Google Scholar 

  • Li H, Zhang Z, Huang F, Chang L, Ma Y (2009) MicroRNA expression profiles in conventional and micropropagated strawberry (Fragaria × ananassa Duch.) plants. Plant Cell Rep 28(6):891–902. doi:10.1007/s00299-009-0693-3

    CAS  PubMed  Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7(8):e1002243. doi:10.1371/journal.pgen.1002243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li H, Zhao X, Dai H, Wu W, Mao W, Zhang Z (2012) Tissue culture responsive microRNAs in strawberry. Plant Mol Biol Rep 30(4):1047–1054. doi:10.1007/s11105-011-0406-2

    CAS  Google Scholar 

  • Liang D, White RG, Waterhouse PM (2012) Gene Silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol 159(3):984–1000. doi:10.1104/pp.112.197129

    CAS  PubMed Central  PubMed  Google Scholar 

  • Linacero R, Rueda J, Esquivel E, Bellido A, Domingo A, Vázquez AM (2011) Genetic and epigenetic relationship in rye, Secale cereale L., somaclonal variation within somatic embryo-derived plants. In Vitro Cell Dev Biol Plant 47(5):618–628. doi:10.1007/s11627-011-9407-y

    Google Scholar 

  • Lindroth AM, Shultis D, Jasencakova Z, Fuchs J, Johnson L, Schubert D, Patnaik D, Pradhan S, Goodrich J, Schubert I, Jenuwein T, Khorasanizadeh S, Jacobsen SE (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23(21):4146–4155

    PubMed Central  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, Ecker JR (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133(3):523–536

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu P–P, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of auxin response factor10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52(1):133–146. doi:10.1111/j.1365-313X.2007.03218.x

    CAS  PubMed  Google Scholar 

  • Liu C, Lu F, Cui X, Cao X (2010) Histone methylation in higher plants. Annu Rev Plant Biol 61(1):395–420. doi:10.1146/annurev.arplant.043008.091939

    CAS  PubMed  Google Scholar 

  • LoSchiavo F, Pitto L, Giuliano G, Torti G, Nuti-Ronchi V, Marazziti D, Vergara R, Orselli S, Terzi M (1989) DNA methylation of embryogenic carrot cell cultures and its variations as caused by mutation, differentiation, hormones and hypomethylating drugs. Theor Appl Genet 77(3):325–331

    CAS  PubMed  Google Scholar 

  • Loyola-Vargas VM, Ochoa-Alejo N (2012) An introduction to plant cell culture: the future ahead. In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Plant cell culture protocols. Springer, Berlin, pp 1–8

    Google Scholar 

  • Loyola-Vargas VM, Vázquez-Flota F (2006) Plant cell culture protocols. Springer, Berlin

    Google Scholar 

  • Luo Y-C, Zhou H, Li Y, Chen J-Y, Yang J-H, Chen Y-Q, Qu L-H (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS Lett 580(21):5111–5116

    CAS  PubMed  Google Scholar 

  • Makarevitch I, Eichten SR, Briskine R, Waters AJ, Danilevskaya ON, Meeley RB, Myers CL, Vaughn MW, Springer NM (2013) Genomic distribution of maize facultative heterochromatin marked by trimethylation of H3K27. Plant Cell. doi:10.1105/tpc.112.106427

    PubMed Central  PubMed  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14(12):1035–1046

    CAS  PubMed  Google Scholar 

  • Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their auxin response factor targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22(4):1104–1117. doi:10.1105/tpc.109.072553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martins M, Sarmento D, Oliveira MM (2004) Genetic stability of micropropagated almond plantlets, as assessed by RAPD and ISSR markers. Plant Cell Rep 23(7):492–496. doi:10.1007/s00299-004-0870-3

    CAS  PubMed  Google Scholar 

  • Maury S, Trap-Gentil MV, Hebrard C, Weyens G, Delaunay A, Barnes S, Lefebvre M, Joseph C (2012) Genic DNA methylation changes during in vitro organogenesis: organ specificity and conservation between parental lines of epialleles. Physiol Plant 146(3):321–335. doi:10.1111/j.1399-3054.2012.01634.x

    CAS  PubMed  Google Scholar 

  • McGarry RC, Kragler F (2013) Phloem-mobile signals affecting flowers: applications for crop breeding. Trends Plant Sci 18(4):198–206

    CAS  PubMed  Google Scholar 

  • Meijon M, Feito I, Valledor L, Rodriguez R, Canal MJ (2010) Dynamics of DNA methylation and Histone H4 acetylation during floral bud differentiation in azalea. BMC Plant Biol 10:10

    PubMed Central  PubMed  Google Scholar 

  • Meijón M, Valledor L, Santamaría E, Testillano PS, Risueño MC, Rodríguez R, Feito I, Cañal MJ (2009) Epigenetic characterization of the vegetative and floral stages of azalea buds: dynamics of DNA methylation and histone H4 acetylation. J Plant Physiol 166(15):1624–1636

    PubMed  Google Scholar 

  • Meins F Jr (1989) Habituation: heritable variation in the requirement of cultured plant cells for hormones. Annu Rev Genet 23(1):395–408

    CAS  PubMed  Google Scholar 

  • Meins F, Foster R (1985) Reversible, cell-heritable changes during the development of tobacco pith tissues. Dev Biol 108(1):1–5

    CAS  PubMed  Google Scholar 

  • Meins F Jr, Thomas M (2003) Meiotic transmission of epigenetic changes in the cell-division factor requirement of plant cells. Development 130(25):6201–6208

    CAS  PubMed  Google Scholar 

  • Mendoza M, Kaeppler H (2002) Auxin and sugar effects on callus induction and plant regeneration frequencies from mature embryos of wheat (Triticum aestivum L.). In Vitro Cell Dev Biol Plant 38(1):39–45. doi:10.1079/IVP2001250

    CAS  Google Scholar 

  • Merkle SA, Dean JFD (2000) Forest tree biotechnology. Curr Opin Biotech 11(3):298–302

    CAS  PubMed  Google Scholar 

  • Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62(11):3713–3725

    CAS  PubMed  Google Scholar 

  • Millner PA (1995) The auxin signal. Curr Opin Cell Biol 7(2):224–231

    CAS  PubMed  Google Scholar 

  • Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC (2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328(5980):872–875

    CAS  PubMed  Google Scholar 

  • Monteuuis O, Doulbeau S, Verdeil JL (2008) DNA methylation in different origin clonal offspring from a mature Sequoiadendron giganteum genotype. Trees Struct Funct 22(6):779–784

    CAS  Google Scholar 

  • Nic-Can GI, López-Torres A, Barredo-Pool F, Wrobel K, Loyola-Vargas VM, Rojas-Herrera R, De-la-Peña C (2013) New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS ONE 8(8):e72160. doi:10.1371/journal.pone.0072160

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Gene Dev 24(23):2678–2692

    CAS  PubMed Central  PubMed  Google Scholar 

  • Novak FJ, Júvova Z (1983) Clonal propagation of grapevine through in vitro axillary bud culture. Sci Hortic 18(3):231–240

    Google Scholar 

  • Parra R, Pastor MT, Pérez-Payá E, Amo-Marco JB (2001) Effect of in vitro shoot multiplication and somatic embryogenesis on 5-methylcytosine content in DNA of Myrtus communis L. Plant Growth Regul 33(2):131–136

    CAS  Google Scholar 

  • Paszkowski J, Whitham SA (2001) Gene silencing and DNA methylation processes. Curr Opin Plant Biol 4(2):123–129

    CAS  PubMed  Google Scholar 

  • Pavokovic D, Krsnik-Rasol M (2012) Protein glycosylation in sugar beet cell line can be influenced by DNA hyper- and hypomethylating agents. Acta Bot Croat 71(1):1–12

    CAS  Google Scholar 

  • Peña-Ramírez Y, Juárez-Gómez J, González-Rodríguez JA, Robert ML (2012) Tissue culture methods for the clonal propagation and genetic improvement of Spanish red cedar (Cedrela odorata). In: Loyola-Vargas VM, Ochoa-Alejo N (eds) Plant cell culture protocols. Methods in molecular biology. Humana Press, New York City, pp 129–141

    Google Scholar 

  • Peredo EL, Revilla MA, Arroyo-García R (2006) Assessment of genetic and epigenetic variation in hop plants regenerated from sequential subcultures of organogenic calli. J Plant Physiol 163(10):1071–1079

    CAS  PubMed  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10(6):645–652

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips DMP (1963) The presence of acetyl groups in histones. Biochem J 87(2):258

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci USA 91(12):5222–5226

    CAS  PubMed Central  PubMed  Google Scholar 

  • Piccolo FM, Fisher AG (2014) Getting rid of DNA methylation. Trends Cell Biol 24(2):136–143

    CAS  PubMed  Google Scholar 

  • Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140(4):1255–1278

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pontvianne F, Blevins T & Pikaard CS (2010) Arabidopsis histone lysine methyltransferases. In: Jean-Claude K & Michel D (eds) Adv Bot Res, vol Volume 53. Academic Press, pp 1–22

  • Pooggin M (2013) How can plant DNA viruses evade siRNA-directed DNA methylation and silencing? Int J Mol Sci 14(8):15233–15259

    PubMed Central  PubMed  Google Scholar 

  • Quiroz-Figueroa F, Rojas-Herrera R, Galaz-Avalos R, Loyola-Vargas V (2006) Embryo production through somatic embryogenesis can be used to study cell differentiation in plants. Plant Cell Tiss Org 86(3):285–301

    Google Scholar 

  • Revilla MA, Pacheco J, Casares A, Rodríguez R (1996) In vitro reinvigoration of mature olive trees (Olea europaea L.) through micrografting. In Vitro Cell Dev Biol Plant 32(4):257–261. doi:10.1007/bf02822697

    Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520

    CAS  PubMed  Google Scholar 

  • Robert ML, Herrera JL, Contreras F, Scorer KN (1987) In vitro propagation of Agave fourcroydes Lem. (Henequen). Plant Cell Tiss. Org. 8:37–48

    CAS  Google Scholar 

  • Robert ML, Herrera JL, Chan JL, Contreras F (1992) Micropropagation of agave spp. In: Bajaj JPY (ed) Biotechnology in agriculture and forestry. Springer, Berlin, pp 306–329

    Google Scholar 

  • Rottach A, Leonhardt H, Spada F (2009) DNA methylation-mediated epigenetic control. J Cell Biochem 108(1):43–51

    CAS  PubMed  Google Scholar 

  • Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25(11):511–517

    CAS  PubMed  Google Scholar 

  • Sanan-Mishra N, Varanasi SRM, Mukherjee S (2013) Micro-regulators of auxin action. Plant Cell Rep 32(6):733–740. doi:10.1007/s00299-013-1425-2

    CAS  PubMed  Google Scholar 

  • Santana-Buzzy N, Canto-Flick A, Barahona-Pérez F, Montalvo-Peniche MADC, Zapata-Castillo PY, Solís-Ruiz A, Zaldívar-Collí A, Gutiérrez-Alonso O, Miranda-Ham MDL (2005) Regeneration of habanero pepper (Capsicum chinense Jacq.) via organogenesis. HortScience 40(6):1829–1831

    Google Scholar 

  • Santos D, Fevereiro P (2002) Loss of DNA methylation affects somatic embryogenesis in Medicago truncatula. Plant Cell Tiss Org 70:155–161

    CAS  Google Scholar 

  • Schellenbaum P, Mohler V, Wenzel G, Walter B (2008) Variation in DNA methylation patterns of grapevine somaclones (Vitis vinifera L.). BMC Plant Biol 8:78

    PubMed Central  PubMed  Google Scholar 

  • Schubert D, Clarenz O, Goodrich J (2005) Epigenetic control of plant development by polycomb-group proteins. Curr Opin Plant Biol 8(5):553–561

    CAS  PubMed  Google Scholar 

  • Shilatifard A (2006) Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. Annu Rev Biochem 75(1):243–269. doi:10.1146/annurev.biochem.75.103004.142422

    CAS  PubMed  Google Scholar 

  • Skoog F, Miller C (1957) Chemical regulation of growth and organ formation in plant tissue cultured. In vitro Symp Soc Exp Biol 11:118–131

    CAS  Google Scholar 

  • Smith ZD, Meissner A (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14:204–220

    CAS  PubMed  Google Scholar 

  • Smulders M, de Klerk G (2011) Epigenetics in plant tissue culture. Plant Growth Regul 63(2):137–146

    CAS  Google Scholar 

  • Smulders MJM, Kortekass WR, Vosman B (1995) Tissue culture-induced DNA methylation polymorphism in repetitive DNA of tomato calli and regenerated plants. Theor Appl Genet 91:1257–1264

    CAS  PubMed  Google Scholar 

  • Smykal P, Valledor L, Rodriguez R, Griga M (2007) Assessment of genetic and epigenetic stability in long-term in vitro shoot culture of pea (Pisum sativum L.). Plant Cell Rep 26(11):1985–1998

    CAS  PubMed  Google Scholar 

  • Springer NM (2013) Epigenetics and crop improvement. Trends Genet 29(4):241–247

    CAS  PubMed  Google Scholar 

  • Sripaoraya S, Marchant R, Power JB, Davey M (2003) Plant regeneration by somatic embryogenesis and organogenesis in commercial pineapple (Ananas comosus L.). In Vitro Cell Dev Biol Plant 39(5):450–454. doi:10.1079/ivp2003445

    Google Scholar 

  • Sun Q, Zhou D-X (2008) Rice jmjC domain-containing gene JMJ706 encodes H3K9 demethylase required for floral organ development. Proc Natl Acad Sci USA 105(36):13679–13684. doi:10.1073/pnas.0805901105

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sunkar R, Li Y-F, Jagadeeswaran G (2012) Functions of microRNAs in plant stress responses. Trends Plant Sci 17(4):196–203

    CAS  PubMed  Google Scholar 

  • Swartz HJ, Galletta GJ, Zimmerman RH (1981) Field performance and phenotypic stability of tissue culture-propagated strawberries. J Am Soc Hort Sci 106:667–673

    Google Scholar 

  • Tanurdzic M, Vaughn MW, Jiang H, Lee TJ, Slotkin RK, Sosinski B, Thompson WF, Doerge RW, Martienssen RA (2008) Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6(12):2880–2895

    CAS  PubMed  Google Scholar 

  • Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20(6):244–251

    CAS  PubMed  Google Scholar 

  • Tian C-E, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT (2004) Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant J 40(3):333–343. doi:10.1111/j.1365-313X.2004.02220.x

    CAS  PubMed  Google Scholar 

  • Uddenberg D, Valladares S, Abrahamsson M, Sundstrîm J, Sundüs-Larsson A & Von Arnold S (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234(3):527–539

    Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle TJ (1999) Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci USA 96(10):5844–5849. doi:10.1073/pnas.96.10.5844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Valenzuela-Sánchez K, Juárez-Hernández R, Cruz-Hernández A, Olalde-Portugal V, Valverde ME, Paredes-Lopez O (2006) Plant regeneration of Agave tequilana by indirect organogenesis. Vitro Cell Dev Biol Plant 42(4):336–340. doi:10.1079/ivp2006788

    Google Scholar 

  • Valledor L, Hasbún R, Meijón M, Rodríguez J, Santamaría E, Viejo M, Berdasco M, Feito I, Fraga M, Cañal MJ, Rodríguez R (2007a) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tiss Org 91:75–86

    CAS  Google Scholar 

  • Valledor L, Rodríguez R, Sánchez P, Fraga M, Berdasco M, Hasbún R, Rodríguez JL, Pacheco JC, García I, Uribe MM, Ríos D, Materán ME, Walter C, Cañal M (2007b) Propagation of pinus genotypes regarless of age. In: Jain M, Häggman H (eds) Protocols of micropropagation for woody trees and fruits. Springer, Netherlands, pp 137–146

    Google Scholar 

  • Valledor L, Meijón M, Hasbún R, Cañal MJ, Rodríguez R (2010) Variations in DNA methylation, acetylated histone H4, and methylated histone H3 during Pinus radiata needle maturation in relation to the loss of in vitro organogenic capability. J Plant Physiol 167(5):351–357

    CAS  PubMed  Google Scholar 

  • Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28(1):463–487. doi:10.1146/annurev-cellbio-101011-155741

    CAS  PubMed  Google Scholar 

  • Viejo M, Rodríguez R, Valledor L, Pérez M, Cañal M, Hasbún R (2010) DNA methylation during sexual embryogenesis and implications on the induction of somatic embryogenesis in Castanea sativa miller. Sex Plant Reprod 23(4):315–323

    CAS  PubMed  Google Scholar 

  • Vining K, Pomraning K, Wilhelm L, Ma C, Pellegrini M, Di Y, Mockler T, Freitag M, Strauss S (2013) Methylome reorganization during in vitro dedifferentiation and regeneration of Populus trichocarpa. BMC Plant Biol 13(1):92

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang K, Zhang S, Weber J, Baxter D, Galas DJ (2010) Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res 38(20):7248–7259. doi:10.1093/nar/gkq601

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang QM, Wang YZ, Sun LL, Gao FZ, Sun W, He J, Gao X, Wang L (2012) Direct and indirect organogenesis of Clivia miniata and assessment of DNA methylation changes in various regenerated plantlets. Plant Cell Rep 31(7):1283–1296. doi:10.1007/s00299-012-1248-6

    CAS  PubMed  Google Scholar 

  • Williams EG, Maheswaran G (1986) Somatic embryogenesis: factors influencing coordinated behaviour of cells as an embryogenic group. Ann Bot 57(4):443–462

    Google Scholar 

  • Williams L, Zhao J, Morozova N, Li Y, Avivi Y, Grafi G (2003) Chromatin reorganization accompanying cellular dedifferentiation is associated with modifications of histone H3, redistribution of HP1, and activation of E2F-target genes. Dev Dyn 228(1):113–120

    CAS  PubMed  Google Scholar 

  • Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286(5439):481–486

    CAS  PubMed  Google Scholar 

  • Wu G, Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu XM, Liu MY, Ge XX, Xu Q, Guo WW (2011) Stage and tissue-specific modulation of ten conserved miRNAs and their targets during somatic embryogenesis of valencia sweet orange. Planta 233(3):495–505

    CAS  PubMed  Google Scholar 

  • Yakovlev IA, Asante DKA, Fossdal CG, Junttila O, Johnsen O (2011) Differential gene expression related to an epigenetic memory affecting climatic adaptation in Norway spruce. Plant Sci 180(1):132–139

    CAS  PubMed  Google Scholar 

  • Yang X, Wang L, Yuan D, Lindsey K, Zhang X (2013) Small RNA and degradome sequencing reveal complex miRNA regulation during cotton somatic embryogenesis. J Exp Bot 64(6):1521–1536. doi:10.1093/jxb/ert013

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38(4):1382–1391. doi:10.1093/nar/gkp1128

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng H, Wang G, Hu X, Wang H, Du L, Zhu Y (2014) Role of microRNAs in plant responses to nutrient stress. Plant Soil 374(1–2):1005–1021. doi:10.1007/s11104-013-1907-6

    CAS  Google Scholar 

  • Zhang H, Ogas J (2009) An epigenetic perspective on developmental regulation of seed genes. Mol Plant 2(4):610–627. doi:10.1093/mp/ssp027

    CAS  PubMed  Google Scholar 

  • Zhang K, Sridhar VV, Zhu J, Kapoor A, Zhu JK (2007) Distinctive core histone post-translational modification patterns in Arabidopsis thaliana. PLoS ONE 2(11):e1210

    PubMed Central  PubMed  Google Scholar 

  • Zhao J, Morozova N, Williams L, Libs L, Avivi Y, Grafi G (2001a) Two phases of chromatin decondensation during dedifferentiation of plant cells. J Biol Chem 276(25):22772–22778

    CAS  PubMed  Google Scholar 

  • Zhao J, Morozova N, Williams L, Libs L, Avivi Y, Grafi G (2001b) Two phases of chromatin decondensation during dedifferentiation of plant cells: distinction between competence for cell fate switch and a commitment for S phase. J Biol Chem 276(25):22772–22778. doi:10.1074/jbc.M101756200

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by CONSEJO NACIONAL DE CIENCIA Y TECNOLOGÍA (CONACYT), scholarships 242997 to RUC, 242979 to GRS and 255368 to FDA; and Grant CB2012-178149 to CD.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Clelia De-la-Peña.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Us-Camas, R., Rivera-Solís, G., Duarte-Aké, F. et al. In vitro culture: an epigenetic challenge for plants. Plant Cell Tiss Organ Cult 118, 187–201 (2014). https://doi.org/10.1007/s11240-014-0482-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0482-8

Keywords

Navigation