Skip to main content
Log in

Epigenetic regulation and gene markers as signals of early somatic embryogenesis

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

Abstract

Identification and characterization of gene markers for somatic embryogenesis offer the possibility of determining the embryogenic potential of somatic cells before any morphological changes appear and to provide information on molecular regulation of early somatic embryogenesis. In this review, based on evidence reported in the literature, we assess the reliability of the established SERK, LEC and WUS marker genes as well as the usefulness of mediating epigenetic regulation by DNA methylation, chromatin remodeling and microRNAs as markers of the induction of somatic embryogenesis. The evidence suggests that the SERK gene marker may be less reliable than has been thought while the germin-like protein-encoding genes may, like their protein products, be useful markers of early somatic embryogenesis.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

CMT:

Cytosine methyltransferase enzymes

DRM:

Domains rearranged methyltransferase

MTE:

Methyltransferase

miRNAs:

Micro RNAs

SERK:

Somatic embryogenesis receptor kinase

LEC:

Leafy cotyledon

WUS:

Wuschel

GLPs:

Germin-like protein encoding genes

References

  • Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana somatic embryogenesisreceptor-like kinases 1 and 2 control male sporogenesis. Plant Cell 17:3337–3349

    CAS  PubMed Central  PubMed  Google Scholar 

  • Arnold SV, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell, Tissue Organ Cult 69:233–249

    Google Scholar 

  • Arroyo-Herrera A, Gonzalez AK, Moo RC, Quiroz-Figueroa FR, Loyola-Vargas VM, Rodriguez-Zapata LC, Burgeff D′Hondt C, Suárez-Solís VM, Castaño E (2008) Expression of WUSCHEL in Coffea canephora causes ectopic morphogenesis and increases somatic embryogenesis. Plant Cell, Tissue Organ Cult 94:171–180

    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 230:12–22

    CAS  PubMed  Google Scholar 

  • Baudino S, Hansen S, Brettschneider R, Hecht V, Dresselhaus T, Lorz H, Dumas C, Rogowsky P (2001) Molecular characterization of two novel maize LRR receptor-likekinases, which belong to the SERK gene family. Planta 213:1–10

    CAS  PubMed  Google Scholar 

  • Berdasco M, Alcazar R, Garcıa-Ortiz MV, Ballestar E, Fernandez AF, Roldan-Arjona T, Tiburcio AF, Altabella T, Buisine N, Quesneville H, Baudry A, Lepiniec L, Alaminos M, Rodrıguez R, Lloyd A, Colot V, Bender J, Canal MJ, Esteller M, Fraga MF (2008) Promoter DNA hypermethylation and gene repression in undifferentiated Arabidopsis cells. PLoS ONE 3:e3306

    PubMed Central  PubMed  Google Scholar 

  • Bhalla PL, Singh MB (2006) Molecular control of stem cell maintenance in shoot apical meristem. Plant Cell Rep 25:249–256

    CAS  PubMed  Google Scholar 

  • Bhojwani SS, Dantu PK (2013) Plant tissue culture: an introductory text. Springer, New Delhi

    Google Scholar 

  • Bishop-Hurley SL, Gardner RC, Walter C (2003) Isolation and molecular characterization of genes expressed during somatic embryo development in Pinusradiate. Plant Cell, Tissue Organ Cult 74:267–281

    CAS  Google Scholar 

  • Bonga JM, Klimaszewska KK, von Aderkas P (2010) Recalcitrance in clonal propagation, in particular of conifers. Plant Cell Tissue Org Cult. 100:241–254

    Google Scholar 

  • Bouchabké-Coussa O, Obellianne M, Linderme D, Montes E, Maia-Grondard A, Vilaine F, Pannetier C (2013) Wuschel overexpression promotes somatic embryogenesis and induces organogenesis in cotton (Gossypium hirsutum L.) tissues cultured in vitro. Plant Cell Rep 32:675–686

    PubMed  Google Scholar 

  • Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loopregulated by CLV3 activity. Science 289(5479):617–619

    CAS  PubMed  Google Scholar 

  • Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13(12):624–630

    CAS  PubMed  Google Scholar 

  • Butler PJ (1983) The folding of chromatin. CRC Crit Rev Biochem 15:57–91

    CAS  PubMed  Google Scholar 

  • Caliskan M, Turet M, Cuming AC (2004) Formation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide generating germin-like oxalate oxidase. Planta 219:132–140

    CAS  PubMed  Google Scholar 

  • Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99:16491–16498

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cardon GH, Hohmann S, Nettesheim K, Saedler H, Huijser P (1997) Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J 12:367–377

    CAS  PubMed  Google Scholar 

  • Cedar H, Razin A (1990) DNA methylation and development. Biochim Biophys Acta 1049:1–8

    CAS  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 

  • Chen SK, Kurdyukov S, Kereszt A, Wang XD, Gressho PM, Rose RJ (2009) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230:827–840

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen CJ, Liu Q, Zhang YC, Qu LH, Chen YQ, Gautheret D (2011) Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus. RNA Biol 8:538–547

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Chugh A, Khurana P (2002) Gene expression during somatic embryogenesis—recent advances. Curr Sci 86:715–730

    Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89:575–585

    CAS  PubMed  Google Scholar 

  • Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis somatic Embryogenesisreceptor Kinases 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361

    CAS  PubMed Central  PubMed  Google Scholar 

  • Constabel CP, Yip L, Patton JJ, Christopher ME (2000) Polyphenol oxidase from hybrid poplar. Cloning and expression in response to wounding and herbivory. Plant Physiol 124:285–295

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cueva A, Conica L, Cella R (2012) Molecular characterization of a Cyrtochilum loxense Somatic Embryogenesis Receptor-like Kinase (SERK) gene expressed during somatic embryogenesis. Plant Cell Rep 31:1129–1139

    CAS  PubMed  Google Scholar 

  • De Oliveira Santos M, Romanoa E, Yotokoc KSC, Tinoco MLP, Diasa BBA, Aragao FJL (2005) Characterization of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Sci 168:723–729

    Google Scholar 

  • De Vries S, Shah K, Rienties I, Raz V, Hecht V, Russinova J (2003) The role of the Arabidopsis somatic embryogenesis receptor-like kinase 1 (AtSERK1) gene in embryogenic competence. In: Vasil IK (ed) Plant biotechnology 2002 and beyond. Proceeding of the 10th IAPTC&B Congress, Orlando, Florida, USA, 23–28 June 2002, pp 269–272

  • Domon JM, Meyer Y, Faye L, David A, David H (1994) Extracellular (g1yco)proteins in embryogenic and non-embryogenic cell lines of Caribbean pine. Comparison between phenotypes of stage one somatic embryos. Plant Physiol Biochem 32:1–11

    Google Scholar 

  • Domon JM, Dumas B, Laine E, Meyer Y, David A, David H (1995) Three glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 108:141–148

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dong J, Dunstan DI (2000) Expression of abundant mRNAs during somatic embryogenesis of white spruce. Planta 199:459–466

    Google Scholar 

  • Dudits D, Gyorgyey J, Bogre L, Bako L (1995) Molecular biology of somatic embryogenesis. In: Thorpe TA (ed) In vitro embryogenesis in plants. Kluwer, Dordrecht, pp 267–308

    Google Scholar 

  • Dunwell JM (1998) Cupins: a new superfamily of functionally diverse proteins that include germins and plant storage proteins. Biotechnol Genet Eng Rev 15:1–32

    CAS  PubMed  Google Scholar 

  • Dunwell JM, Culham A, Carter CE, Sosa-Aguirre CR, Goodenough PW (2001) Evolution of functional diversity in the cupin superfamily. Trends Biochem Sci 26:740–746

    CAS  PubMed  Google Scholar 

  • Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3(3):224–229

    CAS  PubMed Central  PubMed  Google Scholar 

  • Elhiti M, Stasolla C, Wang A (2013) Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol Plant. doi:10.1007/s11627-013-9547-3

  • Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The shoot meristemless gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J 10(6):967–979

    CAS  PubMed  Google Scholar 

  • Feher A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell, Tissue Organ Cult 74:201–228

    CAS  Google Scholar 

  • Fenga S, Cokusb SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SS, 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 107:8689–8694

    Google Scholar 

  • Figueroa FQ, Mendez-Zeel M, Teyer FS, Rojas-Herrera R, Loyola-Vargas VM (2002) Differential gene expression in embryogenic and non-embryogenic cell clusters from cell suspension cultures of Coffea arabica. J Plant Physiol 59:1267–1270

    Google Scholar 

  • Finer JJ (1995) Direct somatic embryogenesis. In: Gamborg OL, Philips GC (eds) Plant cell, tissue and organ culture-fundamental methods. Springer, Berlin, pp 91–102

  • Fisher K, Turner S (2007) PXY, a receptor-like kinase essential form aintaining polarity during plant vascular-tissue development. Curr Biol 17:1061–1066

    CAS  PubMed  Google Scholar 

  • Fraga HPF, Vieira LN, Caprestano CA, Steinmacher DA, Micke GA, Spudeit DA, Pescador R, Guerra MP (2012) 5-Azacytidine combined with 2,4-D improves somatic embryogenesis of Accase llowiana (O.Berg) Burret by means of changes in global DNA methylation levels. Plant Cell Rep 31:2165–2176

    CAS  PubMed  Google Scholar 

  • Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for inductionof somatic embryogenesis of Arabidopsis. Planta 222:977–988

    CAS  PubMed  Google Scholar 

  • Ge XX, Fan GE, Chai L, Guo WW (2010) Cloning, molecular characterization and expression analysis of a somatic embryogenesis receptor-like kinase gene (CitSERK1-like) in Valencia sweet orange. Acta Physiol Plant 32:1197–1207

    CAS  Google Scholar 

  • Ge XX, Chai LJ, Liu Z, Wu XM, Deng XX, Guo WW (2012) Transcriptional profiling of genes involved in embryogenic, non-embryogenic calluses and somatic embryogenesis of Valencia sweet orange by SSH-based microarray. Planta 236:1107–1124

    CAS  PubMed  Google Scholar 

  • Gonzalez AI, Saiz A, Acedo A, Ruiz ML, Polanco C (2013) Analysis of genomic DNA methylation patterns in regenerated and control plants of rye (Secale cereale L.). Plant Growth Regul 70:227–236

    CAS  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 306:838–846

    CAS  PubMed  Google Scholar 

  • Gruszczynska A, Rakoczy-Trojanowska M (2011) Expression analysis of somatic embryogenesis-related SERK, LEC1, VP1 and NiR ortologues in rye (Secale cereale L.). J Appl Genet 52:1–8

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guo F, Liu C, Xia H, Bi Y, Zhao C, Zhao S, Hou L, Li F, Wang X (2013) Induced expression of AtLEC1 and AtLEC2 differentially promotes somatic embryogenesis in transgenic tobacco plants. PLoS ONE 8(8):e71714

    CAS  PubMed Central  PubMed  Google Scholar 

  • Guzzo F, Baldan B, Mariani P, LoSchiavo F, Terzi M (1994) Studies on the origin of totipotent cells in explants of Daucus carota L. J Exp Bot 45:1427–1432

    CAS  Google Scholar 

  • Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409

    CAS  Google Scholar 

  • He K, Gou X, Yuan T, Lin H, Asami T, Yoshida S, Russell SD, Li J (2007) BAK1 and BKK1 regulate brassinosteroid-dependent growth and brassinosteroid-independent cell-death pathways. Curr Biol 17:1109–1115

    CAS  PubMed  Google Scholar 

  • He X, Chen T, Zhu J (2011) Regulation and function of DNA methylation in plants and animals. Cell Res 21:442–465

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, De Vries SC (2001) The Arabidopsis somatic embryogenesis receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

    CAS  PubMed Central  PubMed  Google Scholar 

  • Heck GR, Perry SE, Nichols KW, Fernandez DE (1995) AGL15, a MADS domain protein expressed in developing. Plant Cell 7(8):1271–1282

    CAS  PubMed Central  PubMed  Google Scholar 

  • Henderson JT, Li HC, Rider SD, Mordhorst AP, Romero-Severson J, Cheng JC, Robey J, Sung ZR, de Vries SC, Ogas J (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134:995–1005

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ho WK, Ooi SE, Mayes S, Namasivayam P, Ong-Abdullah M, Chin CF (2013) Methylation levels of a novel genetic element, EgNB3 as a candidate biomarker associated with the embryogenic competency of oil palm. Tree Genet Genomes 9:1099–1107

    Google Scholar 

  • Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulatessomatic embryogenesis of cultured cells and host defense responseagainst fungal infection. Planta 222:107–117

    CAS  PubMed  Google Scholar 

  • Huang X, Lu XY, Zhao JT, Chen JK, Dai XM, Xiao W, Chen YP, Chen YF, Huang XL (2010) MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Mol Biol Report 28:309–316

    CAS  Google Scholar 

  • Ikeda M, Umehara M, Kamada H (2006) Embryogenesis-related genes; its expression and roles during somatic and zygotic embryogenesis in carrot and Arabidopsis. Plant Biotechnol 23:153–161

    CAS  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 

  • Jarillo JA, Pineiro M, Cubas P, Martınez-Zapater JM (2009) Chromatin remodeling in plant development. Int J Dev Biol 53:1581–1596

    CAS  PubMed  Google Scholar 

  • Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karami O, Aghavaisi B, Pour AM (2009) Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol 2:177–190

    PubMed Central  PubMed  Google Scholar 

  • Keith K, Kraml M, Dengler NG, McCourt P (1994) fusca3: a heterochronic mutation affecting late embryo development in Arabidopsis. Plant Cell 6:589–600

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kim HJ, Triplett BA (2004) Cotton fiber germin-like protein. I. Molecular cloning and gene expression. Planta 218:516–524

    CAS  PubMed  Google Scholar 

  • Kiselev KV, Tchernoded GK (2009) Somatic embryogenesis in the Panax ginseng cell culture induced by the rolC oncogene is associated with increased expression of WUS and SERK genes. Russ J Genet 45:445–452

    CAS  Google Scholar 

  • Kiselev KV, Turlenko AV, Zhuravlev YN (2009) PgWUS expression during somatic embryo development in a Panax ginseng 2c3 cell culture expressing the rolC oncogene. Plant Growth Regul 59:237–243

    CAS  Google Scholar 

  • Kulinska-Lukaszek K, Tobojka M, Adamiok A, Kurczynska EU (2012) Expression of the BBM gene during somatic embryogenesis of Arabidopsis thaliana. Biol Plant 56(2):389–394

    CAS  Google Scholar 

  • Kurczynska EU, Gaj MD, Ujczak A, Mazur E (2007) Histological analysis of direct somatic embryogenesis in Arabidopsis thaliana (L.) Heynh. Planta 226:619–628

    CAS  PubMed  Google Scholar 

  • Kurdyukov S, Mathesius U, Nolan KE, Sheahan MB, Goffard N, Carroll BJ, Rose RJ (2014) The 2HA line of Medicago truncatula has characteristics of an epigenetic mutant that is weakly ethylene insensitive. BMC Plant Biol 14:174

    PubMed Central  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lane BG (2002) Oxalate, germins, and higher plant-pathogens. IUBMB Life 53(2):67–75

    CAS  PubMed  Google Scholar 

  • Lara-Chavez A, Egertsdotter U, Flinn BS (2012) Comparison of gene expression markers during zygotic and somatic embryogenesis in pine. In Vitro Cell Dev Biol Plant 48:341–354

    CAS  Google Scholar 

  • Ledwon A, Gaj MD (2009) LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep 28:1677–1688

    CAS  PubMed  Google Scholar 

  • Ledwon A, Gaj MD (2011) LEAFY COTYLEDON1, FUSCA3 expression and auxin treatment in relation to somatic embryogenesis induction in Arabidopsis. Plant Growth Regul 65:157–167

    CAS  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 23:120–127

    CAS  PubMed  Google Scholar 

  • Letarte J, Simion E, Miner M, Kasha KJ (2006) Arabinogalactans and arabinogalactan-proteins induce embryogenesis in wheat (Triticum aestivum L.) microspore culture. Plant Cell Rep 24:691–698

    CAS  PubMed  Google Scholar 

  • Li J (2010) Multi-tasking of somatic embryogenesis receptor-likeproteinkinases. Curr Opin Plant Biol 13(5):509–514

    CAS  PubMed  Google Scholar 

  • Li J, Chory J (1997) Aputativeleucine-rich repeat receptor kinaseinvolved in brassinosteroid signal transduction. Cell 90:929–938

    CAS  PubMed  Google Scholar 

  • Li G, Hall TC, Holmes-Davis R (2002) Plant chromatin: development and gene control. BioEssays 24:234–243

    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

    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

    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:e1002243

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li H, Zhao X, Dai H, Wu W, Mao W, Zhang Z (2012a) Tissue culture responsive microRNAs in strawberry. Plant Mol Biol Rep 30(4):1047–1054

    CAS  Google Scholar 

  • Li T, Chen J, Qiu S, Zhang Y, Wang P, Yang L, Lu Y, Shi J (2012b) Deep sequencing and microarray hybridization identify conserved and species-specific microRNAs during somatic embryogenesis in hybrid yellow poplar. PLoS ONE 7(8):e43451

    CAS  PubMed Central  PubMed  Google Scholar 

  • Linacero R, Rueda J, Esquivel E, Bellido A, Domingo A, Vazquez 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

    Google Scholar 

  • Lippert D, Zhuang J, Ralph S, Ellis DE, Gilbert M, Olafson R, Ritland K, Ellis B, Douglas CJ, Bohlmann J (2005) Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5:461–473

    CAS  PubMed  Google Scholar 

  • Liu Q, Zhang YC, Wang CY, Luo YC, Huang QJ, Chen SY, Zhou H, Qu LH, Chen YQ (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583(4):18723–18728

    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 embryonic carrot cell cultures and its variations as caused by mutation, differentiation, hormones, and hypomethylating drugs. Theor Appl Genet 77:325–331

    CAS  PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    CAS  PubMed  Google Scholar 

  • Luerssen H, Kirik V, Herrman P, Misera S (1998) FUSCA3encodesa protein with a conserved Vp1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15:755–764

    CAS  PubMed  Google Scholar 

  • Luo YC, Zhou H, Li Y, Chen JY, Yang JH, Chen YQ, Qu LH (2006) Rice embryogenic calli express a unique set of microRNAs, suggesting regulatory roles of microRNAs in plant post-embryogenic development. FEBS Lett 580:5111–5116

    CAS  PubMed  Google Scholar 

  • Malik M, Wang F, Dirpaul J, Zhou N, Polowick P, Ferrie A, Krochko J (2007) Transcript profiling and identification of molecular markersfor early microspore embryogenesis in Brassica napus. Plant Physiol 144:134–154

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mantiri FR, Kurdyukov S, Lohar DP, Sharopova N, Saeed NA, Wang XD, Vandenbosch KA, Rose RJ (2008) The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 146(4):1622–1636

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marsoni M, Bracale M, Espen L, Prinsi B, Negri AS, Vannini C (2008) Proteomic analysis of somatic embryogenesis in Vitis vinifera. Plant Cell Rep 27:347–356

    CAS  PubMed  Google Scholar 

  • Mathieu M, Lelu-Walter MA, Blervacq AS, David H, Hawkins S, Neutelings G (2006) Germin-like genes are expressed during somatic embryogenesis and early development of conifers. Plant Mol Biol 61:615–627

    CAS  PubMed  Google Scholar 

  • Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95(6):805–815

    CAS  PubMed  Google Scholar 

  • Meinke D (1992) A homeotic mutant of Arabidopsis thaliana with leafy cotyledons. Science 258:1647–1650

    CAS  PubMed  Google Scholar 

  • Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell. 6:1049–1064

    CAS  PubMed Central  PubMed  Google Scholar 

  • Membre N, Berna A, Neutelings G, David A, David H, Staiger D, Saez Vasquez J, Raynal M, Delseny M, Bernier F (1997) cDNA sequence, genomic organization and differential expression of three Arabidopsis genes for germin/oxalate oxidase-like proteins. Plant Mol Biol 35:459–469

    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 

  • 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

  • Munksgaard D, Mattsson O, Okkles FT (1995) Somatic embryo development in carrot is associated with an increase in levels of S-adenosylmethionine. S-adenosylhomocysteine and DNA methylation. Physiol Plant 93:5–10

    CAS  Google Scholar 

  • Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620

    CAS  PubMed  Google Scholar 

  • Neumann KH (2000) Some studies on somatic embryogenesis: a tool in plant biotechnology. http://geb.uni-giessen.de/geb/volltexte/2000/321/

  • Neutelings G, Domon JM, Membre N, Bernier F, Meyer Y, David A, David H (1998) Characterization of a germin-like protein gene expressed in somatic and zygotic embryos of pine (Pinus caribaea Morelet). Plant Mol Biol 38:1179–1190

    CAS  PubMed  Google Scholar 

  • Nic-Can GI, Lopez-Torres A, Barredo-Pool F, Wrobel K, Loyola- Vargas VM, Rojas-Herrera R, De-la-Pena 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Noceda C, Salaj T, Perez M, Viejo M, Canal AJ, Salaj J, Rodriguez R (2009) DNA demethylation and decrease on free polyamines is associated with the embryogenic capacity of Pinus nigra Arn. cell culture. Trees 23(6):1285–1293

  • 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 

  • Nodine MD, Yadegari R, Tax FE (2007) RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev Cell 12:943–956

    CAS  PubMed  Google Scholar 

  • Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94

    CAS  PubMed  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844

    CAS  PubMed Central  PubMed  Google Scholar 

  • Palovaara J, Hakman I (2008) Conifer WOX-related homeodomain transcription factors, developmental consideration and expression dynamic of WOX2 during Picea abies somatic embryogenesis. Plant Mol Biol 66:533–549

    CAS  PubMed  Google Scholar 

  • Parcy F, Valon C, Kohara A, Miséra S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE 3 (ABI3), FUSCA 3 (FUS3) and LEAFY COTYLEDON 1 (LEC1) loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    CAS  PubMed Central  PubMed  Google Scholar 

  • Perez-Nunez MT, Souza R, Saenz L, Chan JL, Zuniga-Aguilar JJ, Oropeza C (2009) Detection of a SERK-like gene in coconut and analysis of its expression during the formation of embryogenic callus and somatic embryos. Plant Cell Rep 28:11–19

    CAS  PubMed  Google Scholar 

  • Pogson BJ, Davies C (1995) Characterization of a cDNA encoding the protein moiety of a putative arabinogalactan protein from Lycopersiconesculentum. Plant Mol Biol 28:347–352

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Salaj J, Recklinghausen IR, Hecht V, de Vries SC, Schel JHN, van Lammeren AAM (2008) AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiology Biol 46:709–714

    CAS  Google Scholar 

  • Santa-Catarina C, Hanai LR, Dornelas MC, Viana AM, Floh EIS (2004) SERK gene homolog expression, polyamines and amino acids associated with somatic embryogenic competence of Ocotea catharinensis Mez. (Lauraceae). Plant Cell, Tissue Organ Cult 79:53–61

    CAS  Google Scholar 

  • Santa-Catarina C, de Oliveira RR, Cutri L, Floh EIS, Dornelas MC (2012) WUSCHEL-related genes are expressed during somatic embryogenesis of the basal angiosperm Ocotea catharinensis Mez. (Lauraceae). Trees 26:493–501

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Santos MDO, Romano E, Yotoko KSC, Tinoco MLP, Dias BBA, Aragao FJL (2005) Characterization of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Sci 168:723–729

    CAS  Google Scholar 

  • Savona M, Mattioli R, Nigro S, Falasca G, Della Rovere F, Costantino P, De Vries S, Ruffoni B, Trovato M, Altamura MM (2012) Two SERK genes are markers of pluripotency in Cyclamen persicum Mill. J Exp Bot 63(1):471–488

    CAS  PubMed  Google Scholar 

  • Schellenbaum P, Jacques A, Maillot P, Bertsch C, Mazet F, Farine S, Walter B (2008) Characterization of VvSERK1, VvSERK2, VvSERK3, and VvL1L genes and their expression during somatic embryogenesis of grapevine (Vitis vinifera L). Plant Cell Rep 27:1799–1809

    CAS  PubMed  Google Scholar 

  • Schmidt EDL, De Jong AJ, de Vries SC (1994) Signal molecules involved in plant embryogenesis. Plant Mol Biol 26:1305–1313

    CAS  PubMed  Google Scholar 

  • Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) Aleucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development. 124:2049–2062

    CAS  PubMed  Google Scholar 

  • Schrader S, Kaldenhoff R, Richter G (1997) Expression of novel genes during somatic embryogenesis of suspension-cultured carrot cells (Daucus carota). J Plant Physiol 50:63–68

    Google Scholar 

  • Sharma SK, Millam S, Hein I, Bryan GJ (2008) Cloning and molecular characterization of a potato SERK gene transcriptionally induced during initiation of somatic embryogenesis. Planta 228:319–330

    CAS  PubMed  Google Scholar 

  • Shibukawa T, Yazawa K, Kikuchi A, Kamada H (2009) Possible involvement of DNA methylation on expression regulation of carrot LEC1 gene in its 50-upstream region. Gene 437:22–31

    CAS  PubMed  Google Scholar 

  • Shimada T, Hirabayashi T, Endo T, Fujii H, Kita M, Omura M (2005) Isolation and characterization of the somatic embryogenesis receptor-like kinase gene homologue (CitSERK1) from Citrus unshiu Marc. Sci Hortic 103(2):233–238

    CAS  Google Scholar 

  • Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768

    CAS  PubMed Central  PubMed  Google Scholar 

  • Singla B, Tyagi AK, Khurana JP, Khurana P (2007) Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions. Plant Mol Biol 65:677–692

    CAS  PubMed  Google Scholar 

  • Somleva MN, Schmidt EDL, de Vries SC (2000) Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Rep 19:718–726

    CAS  Google Scholar 

  • Steiner N, Santa-Catarina C, Guerra MP, Cutri L, Dornelasm C, Floh EIS (2011) A gymnosperm homolog of somatic embryogenesis receptor-like kinase-1 (SERK1) is expressed during somatic embryogenesis. Plant Cell, Tissue Organ Cult 109:41–50

    Google Scholar 

  • Steward FC, Mapes MO, Mears K (1958) Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. Am J Bot 45:693–703

    Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98:11806–11811

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh TF, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci USA 105(8):3151–3156

    CAS  PubMed Central  PubMed  Google Scholar 

  • Struhl K (1998) Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12:599–606

    CAS  PubMed  Google Scholar 

  • Su YH, Zhao XY, Liu YB, Zhang CL, O’Neill SD, Zhang XS (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59:448–460

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tchorbadjieva MI (2005) Protein markers for somatic embryogenesis. In: Mujib A, Samaj J (eds) Somatic embryogenesis. Plant Cell Monogr 2:215–233

  • Tchorbadjieva M, Pantchev I, Harizanova N (2004) Two-dimensional protein pattern analysis of extracellular proteins secreted by embryogenic and nonembryogenic suspension cultures of Dactylis glomerata L. Biotechnol Biotechnol Equip 18(2):20–27

    CAS  Google Scholar 

  • Thomas C, Jiménez VM (2005) Mode of action of plant hormones and plant growth regulators during induction of somatic embryogenesis: molecular aspects. Plant Cell Monogr 2:157–175

    Google Scholar 

  • Thomas C, Meyer D, Himber C, Steinmetz A (2004) Spatial expression of a sunflower SERK gene during induction of somatic embryogenesis and shoot organogenesis. Plant Physiol Biochem 42:35–42

    CAS  PubMed  Google Scholar 

  • Thompson EW, Lane BG (1980) Relation of protein synthesis in imbibing wheat embryos to the cell-free translational capacities of bulk mRNA from dry and imbibing embryos. J Biol Chem 255:5965–5970

    CAS  PubMed  Google Scholar 

  • Tokuji Y, Takano S, Tonomura M, Tanaka S, Igari T, Watanabe T (2011) Influence of 50-azacytidine on promoting recovery of cell competence for shoot organogenesis in Arabidopsis. Plant Cell Tissue Org Cult 106:289–297

    CAS  Google Scholar 

  • Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y (1996) The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine rich repeats. Plant Cell 8:735–746

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tse C, Sera T, Wolffe AP, Hansen JC (1998) Disruption of higher-order folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol Cell Biol 18:4629–4638

    CAS  PubMed Central  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vanyushin BF, Ashapkin VV (2011) DNA methylation in higher plants: past, present and future. Biochim Biophys Acta 1809:360–368

    CAS  PubMed  Google Scholar 

  • Wagner D (2003) Chromatin regulation of plant development. Curr Opin Plant Biol 6:20–28

    CAS  PubMed  Google Scholar 

  • Wang X, Niu QW, Teng C, Li C, Mu J, Chua NH, Zuo J (2009) Overexpression of PGA37/MYB118 and MYB115 promotes vegetative-to-embryonic transition in Arabidopsis. Cell Res 19:224–235

    CAS  PubMed  Google Scholar 

  • Weigel D, Jurgens G (2002) Stem cells that make stems. Nature 415:751–754

    CAS  PubMed  Google Scholar 

  • West MAL, Yee KM, Danao J, Zimmerman JL, Fischer RL, Goldberg RB, Harada JJ (1994) LEAFY COTYLEDON1is an essential regulator of late embryogenesis and cotyledon identity in Arabidopsis. Plant Cell 6:1731–1745

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wilde HD, Seffens WS, Thomas TL (1995) Gene expression in somatic embryos. In: Bajaj YPS (ed) Somatic embryogenesis and synthetic seed I Biotechnology in agriculture and forestry, vol 30. Springer, Berlin, pp 41–52

    Google Scholar 

  • Willemsen V, Scheres B (2004) Mechanisms of pattern formation in plant embryogenesis. Annu Rev Genet 38:587–614

    CAS  PubMed  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 128:113–120

    Google Scholar 

  • Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155:1871–1884

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wojcikowska B, Jaskoła K, Gasiorek P, Meus M, Nowak K, Gaj MD (2013) LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta 238:425–440

    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 

  • Xiao W, Custard KD, Brown RC, Lemmon BE, Harada JJ, Goldberg RB, Fischer RL (2006) DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18:805–814

    CAS  PubMed Central  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding Carrot leafy cotyledon1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42(3):215–223

    CAS  PubMed  Google Scholar 

  • Zhang S, Wong L, Meng L, Lemaux PG (2002) Similarity of expression patterns of knotted1 and ZmLEC1 during somatic and zygotic embryogenesis in maize (Zea mays L.). Planta 215:191–194

    CAS  PubMed  Google Scholar 

  • Zhang H, Rider SD Jr, Henderson JT, Fountain M, Chuang K, Kandachar V, Simons A, Edenberg HJ, Romero-Severson J, Muir WM, Ogas J (2008) The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J Biol Chem 283:22637–22648

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Liu X, Lin Y, Xie G, Fu F, Liu H, Wang J, Gao S, Lan H, Rong T (2011) Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell, Tissue Organ Cult 105:29–37

    CAS  Google Scholar 

  • Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J (2012) The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 159:418–432

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhao DZ, Wang GF, Speal B, Ma H (2002) The EXCESSMICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev 16:2021–2031

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng Q, Zheng Y, Perry SE (2013) AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and Soybean in part by the control of ethylene biosynthesis and response. Plant Physiol 161(4):2113–2127

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zheng W, Zhang X, Yang Z, Wu J, Li F, Duan L, Liu C, Lu L, Zhang C, Li F (2014) AtWuschel promotes formation of the embryogenic callus in gossypium hirsutum. PLoS ONE 9(1):e87502

    PubMed Central  PubMed  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    CAS  PubMed  Google Scholar 

  • Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30(3):349–359

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by Science Fund 02-01-02-SF0847 under the Ministry of Science, Technology and Innovation (MOSTI), Malaysia. The authors thank Alena Sanusi for her editorial comments on this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fatemeh Mahdavi-Darvari.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mahdavi-Darvari, F., Noor, N.M. & Ismanizan, I. Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tiss Organ Cult 120, 407–422 (2015). https://doi.org/10.1007/s11240-014-0615-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0615-0

Keywords

Navigation