Abstract
Main conclusion
The link HaWUS/ HaL1L , the opposite transcriptional behavior, and the decrease/increase in positive histone marks bond to both genes suggest an inhibitory effect of WUS on HaL1L in sunflower zygotic embryos.
In Arabidopsis, a group of transcription factors implicated in the earliest events of embryogenesis is the WUSCHEL-RELATED HOMEOBOX (WOX) protein family including WUSCHEL (WUS) and other 14 WOX protein, some of which contain a conserved WUS-box domain in addition to the homeodomain. WUS transcripts appear very early in embryogenesis, at the 16-cell embryo stage, but gradually become restricted to the center of the developing shoot apical meristem (SAM) primordium and continues to be expressed in cells of the niche/organizing center of SAM and floral meristems to maintain stem cell population. Moreover, WUS has decisive roles in the embryonic program presumably promoting the vegetative-to-embryonic transition and/or maintaining the identity of the embryonic stem cells. However, data on the direct interaction between WUS and key genes for seed development (as LEC1 and L1L) are not collected. The novelty of this report consists in the characterization of Helianthus annuus WUS (HaWUS) gene and in its analysis regarding the pattern of the methylated lysine 4 (K4) of the Histone H3 and of the acetylated histone H3 during the zygotic embryo development. Also, a parallel investigation was performed for HaL1L gene since two copies of the WUS-binding site (WUSATA), previously identified on HaL1L nucleotide sequence, were able to be bound by the HaWUS recombinant protein suggesting a not described effect of HaWUS on HaL1L transcription.
Similar content being viewed by others
Abbreviations
- ChIP:
-
Chromatin immunoprecipitation
- DAP:
-
Days after pollination
- EMSA:
-
Electrophoretic mobility shift assay
- ISH:
-
In situ hybridization
- qPCR:
-
Real-time RT-PCR
- RAM:
-
Root apical meristem
- SAM:
-
Shoot apical meristem
- WOX :
-
WUSCHEL-RELATED HOMEOBOX gene
References
Adkins NL, Hagerman TA, Georgel P (2006) GAGA protein: a multi-faceted transcription factor. Biochem Cell Biol 84:559–567
Aichinger E, Villar CBR, Farrona S, Reyes JC, Henning L, Köhler C (2009) CHAD3 proteins and polycomb group proteins antagonistically determine cell identity in Arabidopsis. PLoS Genet 5(8):e1000605
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
Atchison ML (2014) Function of YY1 in long-distance DNA interactions. Front Immunol 5:45
Bao X, Franks RG, Levin JZ, Liu Z (2004) Repression of AGAMOUS by BELLRINGER in floral and inflorescence meristems. Plant Cell 16:1478–1489
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2002) The pfam protein families database. Nucleic Acids Res 30:276–280
Bäurle I, Laux T (2005) Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17:2271–2280
Benhamed M, Martin-Magniette M-L, Taconnat L, Bitton F, Servet C, De Clercq R, De Meyer B, Buysschaert C, Rombauts S, Villarroel R, Aubourg S, Beynon J, Bhalerao RP, Coupland G, Gruissem W, Menke FLH, Weisshaar B, Renou J-P, Zhou D-X, Hilson P (2008) Genome-scale Arabidopsis promoter array identifies targets of the histone acetyltransferase GCN5. Plant J 56:493–504
Berger N, Dubreucq B (2012) Evolution goes GAGA: GAGA binding proteins across kingdoms. Biochim Biophys Acta 1819:863–868
Berr A, Shen WH (2010) Molecular mechanisms in epigenetic regulation of plant growth and development. Plant Dev Biol Biotech Perspect 2:325–344
Berr A, Shafiq S, Shen WH (2011) Histone modifications in transcriptional activation during plant development. Biochim Biophys Acta 1809:567–576
Berti F, Fambrini M, Turi M, Bertini D, Pugliesi C (2005) Mutations of corolla symmetry affect carpel and stamen development in Helianthus annuus. Can J Bot 83:1065–1072
Bertrand C, Bergounioux C, Domenichini S, Delarue M, Zhou D-X (2003) Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J Biol Chem 278:28246–28251
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619
Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13:624–630
Busch W, Miotk A, Ariel FD, Zhao Z, Forner J, Daum G, Suzaki T, Schuster C, Schultheiss SJ, Leibfried A, Haubeiss S, Ha N, Chan RL, Lohmann JU (2010) Transcriptional control of a plant stem cell niche. Dev Cell 18:849–861
Cartharius K, Frech K, Grote K, Klocke B, Haltmeier M, Klingenhoff A, Frisch M, Bayerlein M, Werner T (2005) MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21:2933–2942
Chiappetta A, Fambrini M, Petrarulo M, Rapparini F, Michelotti V, Bruno L, Greco M, Baraldi R, Salvini M, Pugliesi C, Bitonti MB (2009) Ectopic expression of LEAFY COTYLEDON-LIKE gene and localized auxin accumulation mark embryogenic competence in epiphyllous plants of Helianthus annuus × H. tuberosus. Ann Bot 103:735–747
Collings CK, Waddell PJ, Anderson JN (2013) Effects of DNA methylation on nucleosome stability. Nucleic Acids Res 41:2918–2931
Combet C, Jambon M, Deléage G, Geourjon C (2002) Geno3D: automatic comparative molecular modelling of protein. Bioinformatics 18:213–214
De Smet I, Lau S, Mayer U, Jürgens G (2010) Embryogenesis—the humble beginnings of plant life. Plant J 61:959–970
Deng W, Buzas DM, Ying H, Robertson M, Taylor J, Peacock WJ, Dennis ES, Helliwell C (2013) Arabidopsis Polycomb Repressive Complex 2 binding sites contain putative GAGA factor binding motifs within coding regions of genes. BMC Genom 14:593
Derkacheva M, Hennig L (2014) Variations on a theme: polycomb group proteins in plants. J Exp Bot 65:2769–2784
Doerner P (2001) Plant meristems: a ménage à trois to end it all. Curr Biol 11:R785–R787
Du Z, Li H, Wei Q, Zhao X, Wang C, Zhu Q, Yi X, Xu W, Liu XS, Jin W, Su Z (2013) Genome-wide analysis of histone modifications: H3K4me2, H3K4me3, H3K9ac, and H3K27ac in Oryza sativa L. Japonica. Mol Plant 6:1463–1472
Falquet L, Pagni M, Bucher P, Hulo N, Sigrist CJ, Hofmann K, Bairoch A (2002) The PROSITE database, its status in 2002. Nucleic Acids Res 30:235–238
Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V, Salvini M, Pugliesi C (2006) Characterization of LEAFY COTYLEDON1-LIKE gene in Helianthus annuus and its relationship with zygotic and somatic embryogenesis. Dev Genes Evol 216:253–264
Fambrini M, Salvini M, Pugliesi C (2011) A transposon-mediate inactivation of a CYCLOIDEA-like gene originates polysymmetric and androgynous ray flowers in Helianthus annuus. Genetica 139:1521–1529
Farré D, Roset R, Huerta M, Adsuara JE, Roselló L, Albà MM, Messeguer X (2003) Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res 31:3651–3653
Finley A, Copeland RA (2014) Small molecule control of chromatin remodeling. Chem Biol 18:1196–1210
Franco-Zorrilla JM, López-Vidriero I, Carrasco JL, Godoy M, Vera P, Solano R (2014) DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc Natl Acad Sci USA 111:2367–2372
Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M (2004) PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131:5021–5030
Gambino G, Minuto M, Boccacci P, Perrone I, Vallania R, Gribaudo I (2011) Characterization of expression dynamics of WOX homeodomain transcription factors during somatic embryogenesis in Vitis vinifera. J Exp Bot 62:1089–1101
Geertz M, Maerkl SJ (2010) Experimental strategies for studying transcription factor-DNA binding specificities. Brief Funct Genomics 5–6:362–373
González-Lamothe R, Boyle P, Dulude A, Roy V, Lezin-Doumbou C, Kaur GS, Bouarab K, Despres C, Brisson N (2008) The transcriptional activator pti4 is required for the recruitment of a repressosome nucleated by repressor SEBF at the potato PR-10a gene. Plant Cell 20:3136–3147
Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM (2009) Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci USA 106:16529–16534
Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723
Haecker A, Groß-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrman M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668
Hay A, Barkoulas M, Tsiantis M (2004) PINning down the connections: transcription factors and hormones in leaf morphogenesis. Curr Opin Plant Biol 7:575–581
Hay A, Barkoulas M, Tsiantis M (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133:3955–3961
He C, Huang H, Xu L (2013) Mechanisms guiding Polycomb activities during gene silencing in Arabidopsis thaliana. Front Plant Sci 4:454
Hennig L, Derkacheva M (2009) Diversity of Polycomb group complexes in plants: same rules, different players? Trends Genet 25:414–423
Hewezi T, Petitprez M, Gentzbittel L (2006) Primary metabolic pathways and signal transduction in sunflower (Helianthus annuus L.): comparison of transcriptional profiling in leaves and immature embryos using cDNA microarrays. Planta 223:948–964
Hilioti Z, Ganopoulos I, Bossis I, Tsaftaris A (2014) LEC1-LIKE paralog transcription factor: how to survive extinction and fit in NF-Y protein complex. Gene 543:220–233
Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21:3493–3505
Iwasaki M, Paszkowski J (2014) Epigenetic memory in plants. EMBO J 33:1987–1998
Jackson D (1991) In situ hybridisation in plants. In: Bowles DJ, Gurr GJ, McPherson M (eds) Molecular plant pathology: a practical approach. Oxford University Press, Oxford, pp 163–174
Keilwagen J, Grau J (2015) Varying levels of complexity in transcription factor binding motifs. Nucleic Acids Res. doi:10.1093/nar/gkv577
Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573
Kim DH, Su S (2014) Polycomb-mediated gene silencing in Arabidopsis thaliana. Mol Cells 37:841–850
Kwon CS, Chen C, Wagner D (2005) WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev 19:992–1003
Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18
Lai Z, Schluttenhofer CM, Bhide K, Shreve J, Thimmapuram J, Lee SY, Yun D-J, Mengiste T (2014) MED18 interaction with distinct transcription factors regulates multiple plant functions. Nat Commun 5:3064
Laux T, Mayer KF, Berger J, Jürgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122:87–96
Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609
Leibfried A, To JP, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:1172–1175
Lenhard M, Bohnert A, Jürgens G, Laux T (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105:805–814
Li C, Wu K, Fu G, Li Y, Zhong Y, Lin X, Zhou Y, Tian L, Huang S (2009) Regulation of oleosin expression in developing peanut (Arachis hypogaea L.) embryos through nucleosome loss and histone modifications. J Exp Bot 60:4371–4382
Lian G, Ding Z, Wang Q, Zhang D, Xu J (2014) Origins and evolution of WUSCHEL-related homeobox protein family in plant kingdom. Sci World J 2014:534140. doi:10.1155/2014/534140
Liu X, Kim YJ, Müller R, Yumul RE, Liu C, Pan Y, Cao X, Goodrich J, Chen X (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23:3654–3670
Liu X, Dinh TT, Li D, Shi B, Li Y, Cao X, Guo L, Pan Y, Jiao Y, Chen X (2014) AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. Plant J 80:629–641
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the \( 2^{-\Delta\Delta C_{\text{T}}} \) method. Methods 25:402–408
Lodha M, Marco CF, Timmermans MCP (2013) The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of Polycomb-repressive complex2. Genes Dev 27:596–601
Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803
Lotan T, Ohto M, Yee KM, West MAL, 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
Luo M, Yu CW, Chen FF, Zhao L, Tian G, Liu X, Cui Y, Yang JY, Wu K (2012) Histone deacetylase HDA6 is functionally associated with AS1 in repression of KNOX genes in Arabidopsis. PLoS Genet 8(12):e1003114
Mayer KFX, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815
Messeguer X, Escudero R, Farré D, Nuñez O, Martínez J, Albà MM (2002) PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18:333–334
Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55:853–867
Molitor AM, Bu Z, Yu Y, Shen WH (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10(1):e1004091
Mozgova I, Hennig L (2015) The Polycomb group protein regulatory network. Annu Rev Plant Biol 66:269–296
Nardmann J, Zimmermann R, Durantini D, Kranz E, Werr W (2007) WOX gene phylogeny in Poaceae: a comparative approach addressing leaf and embryo development. Mol Biol Evol 24:2474–2484
Palovaara J, Hallberg H, Stasolla C, Hakman I (2010) Comparative expression pattern analysis of WUSCHEL-related homeobox 2 (WOX2) and WOX8/9 in developing seeds and somatic embryos of the gymnosperm Picea abies. New Phytol 188:122–135
Perrella G, Lopez-Vernaza MA, Carr C, Sani E, Gosselé V, Verduyn C, Kellermeier F, Hannah MA, Amtmann A (2013) Histone Deacetylase Complex1 expression level titrates plant growth and abscisic acid sensitivity in Arabidopsis. Plant Cell 25:3491–3505
Ptashne M (2013a) Faddish stuff: epigenetics and the inheritance of acquired characteristics. FASEB J 27:1–2
Ptashne M (2013b) Epigenetics: core misconcept. Proc Natl Acad Sci USA 110:7101–7103
Rivera C, Gurard-Levin ZA, Almouzni G, Loyola A (2014) Histone lysine methylation and chromatin replication. Biochim Biophys Acta 1839:1433–1439
Rosinski JA, Atchley WR (1999) Molecular evolution of helix-turn-helix proteins. J Mol Evol 49:301–309
Salvini M, Sani E, Fambrini M, Pistelli L, Pucciariello C, Pugliesi C (2012) Molecular analysis of a sunflower gene encoding an homologous of the B subunit of a CAAT binding factor. Mol Biol Rep 39:6449–6465
Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L (2008) Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J 54:608–620
Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814
Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354
Schlög PS, dos Santos ALW, Viera LdoN, Floh EIS, Guerra MP (2012) Cloning and expression of embryogenesis-regulating genes in Araucaria angustifolia (Bert.) O. Kuntze (Brazilian Pine). Genet Mol Biol 35:172–181
Schoof H, Lenhard M, Haecker A, Mayer KF, Jürgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644
Shiraishi H, Okada K, Shimura Y (1993) Nucleotide sequences recognized by the AGAMOUS MADS domain of Arabidopsis thaliana in vitro. Plant J 4:385–398
Siebert PD, Chenchik A, Kellog DE, Lukyanov KA, Lukyanov SA (1995) An improved method for walking in uncloned genomic DNA. Nucleic Acids Res 23:1087–1088
Simonini S, Roig-Villanova I, Gregis V, Colombo B, Colombo L, Kater MM (2012) BASIC PENTACYSTEINE proteins mediate MADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 24:4163–4172
Sneath PHA, Sokal R (1973) Numerical taxonomy. WH Freeman and Company, San Francisco, pp 230–234
Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217
Srinivasan L, Atchison ML (2004) YY1 DNA binding and PcG recruitment requires CtBP. Genes Dev 18:2596–2601
Staller MV, Vincent BJ, Bragdon MDJ, Lydiard-Martin T, Wunderlich Z, Estrada J, DePace AH (2015) Shadow enhancers enable Hunchback bifunctionality in the Drosophila embryo. Proc Natl Acad Sci USA 112:785–790
Steffen PA, Ringrose L (2014) What are memories made of? How polycomb and trithorax proteins mediate epigenetic memory. Nat Rev Mol Cell Biol 15:340–356
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
Su Y, Zhao XY, Liu YB, Zhang C, 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
Sun B, Looi L-S, Guo S, He Z, Gan E-S, Huang J, Xu Y, Wee W-Y, Ito T (2014) Timing mechanism dependent on cell division is invoked by Polycomb eviction in plant stem cells. Science 343:6170. doi:10.1126/science.1248559
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
ten Hove CA, Lu K-J, Weijers D (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142:420–430
van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:248
Wilkinson FH, Park K, Atchison ML (2006) Polycomb recruitment to DNA in vivo by the YY1 REPO domain. Proc Natl Acad Sci USA 103:19296–19301
Wingender E, Chen X, Fricke E, Geffers R, Hehl R, Liebich I, Krull M, Matys V, Ohnhäuser R, Prüß M, Schacherer F, Thiele S, Urbach S (2001) The TRANSFAC system on gene expression regulation. Nucleic Acids Res 29:281–283
Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11:607–620
Yadav RK, Perales M, Gruel J, Girke T, Jönsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:2025–2030
Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10(6):R62
Zheng B, He H, Zheng Y, Wu W, McCormick S (2014) An ARID domain-containing protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana. PLoS Genet 10(7):e1004421
Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL, Tarr PT, Yan A, Kay SA, Meyerowitz EM (2014) Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:377–380
Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143–166
Zhu T, Moschou PN, Alvarez JM, Sohlberg JJ, von Arnold S (2014) WUSCHEL-RELATED HOMEOBOX 8/9 is important for proper embryo patterning in the gymnosperm Norway spruce. J Exp Bot 65:6543–6552
Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Salvini, M., Fambrini, M., Giorgetti, L. et al. Molecular aspects of zygotic embryogenesis in sunflower (Helianthus annuus L.): correlation of positive histone marks with HaWUS expression and putative link HaWUS/HaL1L . Planta 243, 199–215 (2016). https://doi.org/10.1007/s00425-015-2405-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-015-2405-2