Tree Genetics & Genomes

, 15:52 | Cite as

Transcriptome dynamics of cork oak (Quercus suber) somatic embryogenesis reveals active gene players in transcription regulation and phytohormone homeostasis of embryo development

  • Tiago Capote
  • Anabel Usié
  • Pedro Barbosa
  • Marcos Ramos
  • Leonor Morais-Cecílio
  • Sónia GonçalvesEmail author
Original Article
Part of the following topical collections:
  1. Gene Expression


Cork oak (Quercus suber L.) is one of the most important Mediterranean forest tree species. The last decades have been marked by a decline in this species. Implementation of breeding programs is fundamental to revert this trend. Somatic embryogenesis is the system of choice for clonal propagation, constituting a valuable tool for embryo production and improved genotype testing. In this study, the cork oak transcriptome during somatic embryogenesis was characterized in four stages of development to identify relevant genes in the process and to understand the molecular and biochemical events occurring in each specific stage. A total 66,693 candidate coding regions were predicted from the generated de novo transcriptome assembly. Differential gene expression analysis identified 11,507 genes distributed in 30 clusters with distinct gene expression patterns and enriched in various biological process GO terms. Results show 1159 differentially expressed genes coding for transcription regulators, namely transcription factors (76%) with important roles in embryogenesis, like orthologous of AINTEGUMENTA-like, PLETHORA, CYTOKININ RESPONSE FACTOR, GATA transcription factors, and AUXIN RESPONSE FACTORs genes. Results also show 250 differentially expressed phytohormone-related genes involved in important aspects of embryogenesis as tissue specification, differentiation, and embryogenesis competence. Finally, we identified a group of genes with functions in cellular protection and abiotic stress tolerance coding for LATE EMBRYOGENESIS ABUNDANT proteins. Cork oak embryogenesis transcriptome characterization represents a tool for future biotechnological applications. Our results provide a molecular insight into embryo development, establishing a basis for further research towards improvement of somatic embryogenesis in cork oak.


Quercus suber Somatic embryogenesis Transcriptomics Transcription factor Hormone Plant biotechnology 



The authors acknowledge Fundação para a Ciência e a Tecnologia (FCT) for awarding a PhD grant to Tiago Capote (SFRH/BD/69785/2010) and for funding António Marcos Ramos, Anabel Usié, and Pedro Barbosa through the Project Investigador FCT IF/01015/2013/CP1209/CT0001 - Genomics and bioinformatics applied to Portuguese plant and animal genetic resources, the project PTDC/AGR-FOR/3356/2014, and the research unit LEAF Unit UID/AGR/04129/2013. We also thank the Program Alentejo 2020 funded through the European Fund for Regional Development under the scope of LENTIDEV – A molecular approach to cork porosity (REF: ALT20-03-0145-FEDER-000020).


Fundação para a Ciência e a Tecnologia (FCT) funded the PhD grant for Tiago Capote (SFRH/BD/69785/2010). António Marcos Ramos, Anabel Usié, and Pedro Barbosa were funded by the Project Investigador FCT IF/01015/2013/CP1209/CT0001 - Genomics and bioinformatics applied to Portuguese plant and animal genetic resources. This work was funded by Program Alentejo 2020, through the European Fund for Regional Development under the scope of LENTIDEV – A molecular approach to cork porosity (REF: ALT20-03-0145-FEDER-000020).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11295_2019_1353_MOESM1_ESM.xlsx (33 kb)
Online Resource 1 Primers list and details (XLSX 32 kb)
11295_2019_1353_MOESM2_ESM.pdf (3.6 mb)
Online Resource 2 Smear plots and volcano plots (PDF 3663 kb)
11295_2019_1353_MOESM3_ESM.pdf (68 kb)
Online Resource 3 Cluster analysis of differentially expressed genes by the K-means method from the gene expression profile. Vertical axes represent relative expression values. Horizontal axes represent the 4 embryos developmental stages: ST1, ST2, ST3 and ST4. (PDF 67 kb)
11295_2019_1353_MOESM4_ESM.pdf (382 kb)
Online Resource 4 GO functional classification of differentially expressed genes on biological process at level 2, molecular function at level 3 and cellular localization at level 4 (PDF 382 kb)
11295_2019_1353_MOESM5_ESM.xlsx (1.4 mb)
Online Resource 5 GO slim annotations of all differentially expressed genes (XLSX 1413 kb)
11295_2019_1353_MOESM6_ESM.xlsx (193 kb)
Online Resource 6 Differential expression of transcription factors, transcription regulators and chromatin regulators (XLSX 192 kb)
11295_2019_1353_MOESM7_ESM.xlsx (35 kb)
Online Resource 7 Hormone related genes, blastx annotation, gene description, and expression data (XLSX 34 kb)
11295_2019_1353_MOESM8_ESM.xlsx (20 kb)
Online Resource 8 Embryogenesis related genes, blastx annotation, gene description, and expression data (XLSX 32 kb) (XLSX 19 kb)


  1. Abid G, Jacquemin J, Sassi K, Muhovski Y (2010) Gene expression and genetic analysis during higher plants embryogenesis. Biotechnol Agron Soc Environ 14:667–680Google Scholar
  2. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:119–120. CrossRefGoogle Scholar
  3. Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg EH(T), Gonzalez P, Fensham R, Zhang Z, Castro J, Demidova N, Lim JH, Allard G, Running SW, Semerci A, Cobb N (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684. CrossRefGoogle Scholar
  4. Álvarez R, Alonso P, Cortizo M et al (2004) Genetic transformation of selected mature cork oak (Quercus suber L.) trees. Plant Cell Rep 23:218–223. CrossRefPubMedGoogle Scholar
  5. Álvarez R, Álvarez JM, Humara JM, Revilla Á, Ordás RJ (2009) Genetic transformation of cork oak (Quercus suber L.) for herbicide resistance. Biotechnol Lett 31:1477–1483. CrossRefPubMedGoogle Scholar
  6. Baima S, Forte V, Possenti M, Peñalosa A, Leoni G, Salvi S, Felici B, Ruberti I, Morelli G (2014) Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol Plant 7:1006–1025. CrossRefPubMedGoogle Scholar
  7. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465. CrossRefPubMedGoogle Scholar
  8. Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, Martinoia E, Farmer EE (2007) A gain-of-function allele of TPC1 activates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J 49:889–898. CrossRefPubMedGoogle Scholar
  9. Boutilier K, Offringa R, Sharma VK et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Braisier CM (1996) Phytophthora cinnamomi and oak decline in southern Europe. Environmental constraints including climate change. Ann Sci For 53:347–358. CrossRefGoogle Scholar
  11. Brasier CM (1992) Oak tree mortality in Iberia. Nature 360:539. CrossRefGoogle Scholar
  12. Brioudes F, Thierry A-M, Chambrier P, Mollereau B, Bendahmane M (2010) Translationally controlled tumor protein is a conserved mitotic growth integrator in animals and plants. Proc Natl Acad Sci U S A 107:16384–16389. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Bueno MA, Gómez A, Manzanera JA (2000) Somatic and Gamatic Embryogenesis in Quercus Suber L. In: Jain SM, Gupta PK, Newton RJ (eds) Somatic embryogenesis in woody plants: volume 6. Springer Netherlands, Dordrecht, pp 479–508CrossRefGoogle Scholar
  14. Cao D, Hussain A, Cheng H, Peng J (2005) Loss of function of four DELLA genes leads to light- and gibberellin-independent seed germination in Arabidopsis. Planta 223:105–113. CrossRefPubMedGoogle Scholar
  15. Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Conesa A, Gotz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832:1–12. CrossRefGoogle Scholar
  17. Cushing DA, Forsthoefel NR, Gestaut DR, Vernon DM (2005) Arabidopsis emb175 and other ppr knockout mutants reveal essential roles for pentatricopeptide repeat (PPR) proteins in plant embryogenesis. Planta 221:424–436. CrossRefPubMedGoogle Scholar
  18. Dai X, Sinharoy S, Udvardi M, Zhao PX (2013) PlantTFcat: an online plant transcription factor and transcriptional regulator categorization and analysis tool. BMC Bioinformatics 14:321. CrossRefPubMedPubMedCentralGoogle Scholar
  19. De Smet I, Vassileva V, De Rybel B et al (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597. CrossRefPubMedGoogle Scholar
  20. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330(6004):622–627. CrossRefGoogle Scholar
  22. Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Müller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20:1875–1887. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057. CrossRefPubMedGoogle Scholar
  24. Gao M, Gropp G, Wei S (2012) Combinatorial networks regulating seed development and seed filling. In: Ken-Ichi Sato (ed) Embryogenesis. InTech, pp 189–228Google Scholar
  25. García-Martín G, González-Benito ME, Manzanera JA (2001) Quercus suber L. somatic embryo germination and plant conversion: pretreatments and germination conditions. In Vitro Cellular & Developmental Biology-Plant 37(2):190–198. CrossRefGoogle Scholar
  26. Ge C, Cui X, Wang Y, Hu Y, Fu Z, Zhang D, Cheng Z, Li J (2006) BUD2, encoding an S-adenosylmethionine decarboxylase, is required for Arabidopsis growth and development. Cell Res 16:446–456. CrossRefPubMedGoogle Scholar
  27. Gomez-Garay A, Lopez JA, Camafeita E, Bueno MA, Pintos B (2013) Proteomic perspective of Quercus suber somatic embryogenesis. J Proteome 93:314–325. CrossRefGoogle Scholar
  28. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Graeber K, Nakabayashi K, Miatton E et al (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35:1769–1786. CrossRefPubMedGoogle Scholar
  30. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Gutierrez L, Van Wuytswinkel O, Castelain M, Bellini C (2007) Combined networks regulating seed maturation. Trends Plant Sci 12:294–300. CrossRefPubMedGoogle Scholar
  32. Hanzawa Y, Takahashi T, Michael AJ, Burtin D, Long D, Pineiro M, Coupland G, Komeda Y (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J 19:4248–4256. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Harmon F, Imaizumi T, Gray WM (2008) CUL1 regulates TOC1 protein stability in the Arabidopsis circadian clock. Plant J 55:568–579. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Hellemans J, Mortier G, De Paepe A et al (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hellmann H, Hobbie L, Chapman A, Dharmasiri S, Dharmasiri N, del Pozo C, Reinhardt D, Estelle M (2003) Arabidopsis AXR6 encodes CUL1 implicating SCF E3 ligases in auxin regulation of embryogenesis. EMBO J 22:3314–3325. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Hernández I, Celestino C, Alegre J, Toribio M (2003) Vegetative propagation of Quercus suber L. by somatic embryogenesis. II. Plant regeneration from selected cork oak trees. Plant Cell Rep 21:765–770. CrossRefPubMedGoogle Scholar
  39. Hincha DK, Thalhammer A (2012) LEA proteins: IDPs with versatile functions in cellular dehydration tolerance. Biochem Soc Trans 40:1000–1003. CrossRefPubMedGoogle Scholar
  40. Hu H, Xiong L, Yang Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222:107–117. CrossRefPubMedGoogle Scholar
  41. Jiang Z, Liu X, Peng Z, Wan Y, Ji Y, He W, Wan W, Luo J, Guo H (2011) AHD2.0: an update version of arabidopsis hormone database for plant systematic studies. Nucleic Acids Res 39:1–7. CrossRefGoogle Scholar
  42. Jing D, Zhang J, Xia Y, Kong L, OuYang F, Zhang S, Zhang H, Wang J (2017) Proteomic analysis of stress-related proteins and metabolic pathways in Picea asperata somatic embryos during partial desiccation. Plant Biotechnol J 15:27–38. CrossRefPubMedGoogle Scholar
  43. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240. CrossRefPubMedPubMedCentralGoogle Scholar
  44. Joshi N, Fass J (2011) Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files (version 1.33) [software]. Available at
  45. Kakehi JI, Kuwashiro Y, Niitsu M, Takahashi T (2008) Thermospermine is required for stem elongation in Arabidopsis thaliana. Plant Cell Physiol 49:1342–1349. CrossRefPubMedGoogle Scholar
  46. Kim S, Choi H, Ryu H-J, Park JH, Kim MD, Kim SY (2004) ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiol 136:3639–3648. CrossRefPubMedPubMedCentralGoogle Scholar
  47. Klein M, Perfus-Barbeoch L, Frelet A, Gaedeke N, Reinhardt D, Mueller-Roeber B, Martinoia E, Forestier C (2003) The plant multidrug resistance ABC transporter AtMRP5 is involved in guard cell hormonal signalling and water use. Plant J 33:119–129CrossRefGoogle Scholar
  48. Lee EK, Kwon M, Ko J-H, Yi H, Hwang MG, Chang S, Cho MH (2004) Binding of sulfonylurea by AtMRP5, an Arabidopsis multidrug resistance-related protein that functions in salt tolerance. Plant Physiol 134:528–538. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Li H, Durbin R (2010) Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26:589–595. CrossRefPubMedPubMedCentralGoogle Scholar
  50. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J 44:960–971. CrossRefPubMedGoogle Scholar
  52. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lu Y, Li C, Wang H, Chen H, Berg H, Xia Y (2011) AtPPR2, an Arabidopsis pentatricopeptide repeat protein, binds to plastid 23S rRNA and plays an important role in the first mitotic division during gametogenesis and in cell proliferation during embryogenesis. Plant J 67:13–25. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21:3448–3449. CrossRefPubMedGoogle Scholar
  55. Mahonen AP, ten TK, Siligato R et al (2014) PLETHORA gradient formation mechanism separates auxin responses. Nature 515:125–129. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Mallón R, Valladares S, Corredoira E, Vieitez AM, Vidal N (2014) Overexpression of the chestnut CsTL1 gene coding for a thaumatin-like protein in somatic embryos of Quercus robur. Plant Cell Tissue Organ Cult 116:141–151. CrossRefGoogle Scholar
  57. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu Ü, Müller-Röber B, Schulz B (2002) Multifunctionality of plant ABC transporters--more than just detoxifiers. Planta 214:345–355. CrossRefPubMedGoogle Scholar
  58. McCarthy DJ, Chen Y, Smyth GK (2012) Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation. Nucleic Acids Res 40:4288–4297. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Miguel A, de Vega-Bartol J, Marum L, Chaves I, Santo T, Leitão J, Varela MC, Miguel CM (2015) Characterization of the cork oak transcriptome dynamics during acorn development. BMC Plant Biol 15:158. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Milhinhos A, Prestele J, Bollhöner B, Matos A, Vera-Sirera F, Rambla JL, Ljung K, Carbonell J, Blázquez MA, Tuominen H, Miguel CM (2013) Thermospermine levels are controlled by an auxin-dependent feedback loop mechanism in Populus xylem. Plant J 75:685–698. CrossRefPubMedGoogle Scholar
  61. Miransari M, Smith DL (2014) Plant hormones and seed germination. Environ Exp Bot 99:110–121. CrossRefGoogle Scholar
  62. Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80. CrossRefPubMedGoogle Scholar
  63. Moon J, Zhao Y, Dai X, Zhang W, Gray WM, Huq E, Estelle M (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol 143:684–696. CrossRefPubMedPubMedCentralGoogle Scholar
  64. Muñiz L, Minguet EG, Singh SK et al (2008) ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–2582. CrossRefPubMedGoogle Scholar
  65. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. CrossRefGoogle Scholar
  66. El Ouakfaoui S, Schnell J, Abdeen A et al (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74:313–326. CrossRefPubMedPubMedCentralGoogle Scholar
  67. Pagnussat GC, Yu H-J, Ngo QA et al (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603–614. CrossRefPubMedGoogle Scholar
  68. Peiter E, Maathuis FJM, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+−activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Pérez M, Viejo M, LaCuesta M, Toorop P, Cañal MJ (2015) Epigenetic and hormonal profile during maturation of Quercus Suber L. somatic embryos. J Plant Physiol 173:51–61. CrossRefPubMedGoogle Scholar
  70. Pinto G, Valentim H, Costa A, Castro S, Santos C (2002) Somatic embryogenesis in leaf callus from a mature Quercus suber L. tree. In Vitro Cellular & Developmental Biology-Plant 38(6):569–572. CrossRefGoogle Scholar
  71. Pintos B, Bueno MA, Cuenca B, Manzanera JA (2008) Synthetic seed production from encapsulated somatic embryos of cork oak (Quercus suber L.) and automated growth monitoring. Plant Cell Tissue Organ Cult 95:217–225. CrossRefGoogle Scholar
  72. Prasad K, Grigg SP, Barkoulas M, Yadav RK, Sanchez-Perez GF, Pinon V, Blilou I, Hofhuis H, Dhonukshe P, Galinha C, Mähönen AP, Muller WH, Raman S, Verkleij AJ, Snel B, Reddy GV, Tsiantis M, Scheres B (2011) Arabidopsis PLETHORA transcription factors control phyllotaxis. Curr Biol 21:1123–1128. CrossRefPubMedGoogle Scholar
  73. Radoeva T, Weijers D (2014) A roadmap to embryo identity in plants. Trends Plant Sci 19:709–716. CrossRefPubMedGoogle Scholar
  74. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc Natl Acad Sci U S A 103:11081–11085. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Riefler M, Novak O, Strnad M, Schmu T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth , leaf senescence , seed size , germination , root development , and cytokinin. Metabolism. 18:40–54. CrossRefGoogle Scholar
  76. Robinson MD, McCarthy DJ, Smyth GK (2009) edgeR: a bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Rodríguez-Sanz H, Manzanera JA, Solís MT, Gómez-Garay A, Pintos B, Risueño MC, Testillano PS (2014) Early markers are present in both embryogenesis pathways from microspores and immature zygotic embryos in cork oak, Quercus suber L. BMC Plant Biol 14:1–18. CrossRefGoogle Scholar
  78. Saeed AI, Bhagabati NK, Braisted JC et al (2006) TM4 microarray software suite. Methods Enzymol 411:134–193. CrossRefPubMedGoogle Scholar
  79. Saracco S a, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145:119–134. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction and growth of monocotyledonous and dicotyledonous plant cell cultures. Can J Bot 50:199–204. CrossRefGoogle Scholar
  81. Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jürgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916. CrossRefPubMedGoogle Scholar
  82. Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472. CrossRefPubMedGoogle Scholar
  83. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. CrossRefPubMedPubMedCentralGoogle Scholar
  84. Shen W-H, Parmentier Y, Hellmann H, Lechner E, Dong A, Masson J, Granier F, Lepiniec L̈, Estelle M, Genschik P (2002) Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol Biol Cell 13:1916–1928. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Spitzer C, Reyes FC, Buono R, Sliwinski MK, Haas TJ, Otegui MS (2009) The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell 21:749–766. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914. CrossRefPubMedGoogle Scholar
  87. Tanaka H, Watanabe M, Watanabe D, Tanaka T, Machida C, Machida Y (2002) ACR4, a putative receptor kinase gene of Arabidopsis thaliana, that is expressed in the outer cell layers of embryos and plants, is involved in proper embryogenesis. Plant Cell Physiol 43:419–428. CrossRefPubMedGoogle Scholar
  88. Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492. CrossRefPubMedGoogle Scholar
  89. Tzafrir I, Pena-muralla R, Dickerman A et al (2004) Identification of genes required for embryo development in Arabidopsis. Plant Physiol 135:1206–1220. published CrossRefPubMedPubMedCentralGoogle Scholar
  90. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM (2007) Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 35:W71–W74. CrossRefPubMedPubMedCentralGoogle Scholar
  91. Valladares S, Toribio M, Celestino C, Vieitez AM (2004) Cryopreservation of embryogenic cultures from mature Quercus suber trees using vitrification. Cryo-Letters 25:177–186PubMedGoogle Scholar
  92. Vieitez AM, Corredoira E, Martínez MT, San-José MC, Sánchez C, Valladares S, Vidal N, Ballester A (2012) Application of biotechnological tools to Quercus improvement. Eur J For Res 131:519–539. CrossRefGoogle Scholar
  93. Von Arnold S, Sabala I, Bozhkov P et al (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249. CrossRefGoogle Scholar
  94. Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004) The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:298–308. CrossRefPubMedGoogle Scholar
  95. Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Willems AR, Schwab M, Tyers M (2004) A hitchhiker’s guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta, Mol Cell Res 1695:133–170. CrossRefPubMedGoogle Scholar
  97. Wu XM, Kou SJ, Liu YL, Fang YN, Xu Q, Guo WW (2015) Genomewide analysis of small RNAs in nonembryogenic and embryogenic tissues of citrus: microRNA- and siRNA-mediated transcript cleavage involved in somatic embryogenesis. Plant Biotechnol J 13:383–394. CrossRefPubMedGoogle Scholar
  98. Xu XM, Møller SG (2004) AtNAP7 is a plastidic SufC-like ATP-binding cassette/ATPase essential for Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 101:9143–9148. CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zdobnov EM, Apweiler R (2001) InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848. CrossRefPubMedPubMedCentralGoogle Scholar
  100. Zhang Y, Wang Y, Wang C (2012) Gene overexpression and gene silencing in birch using an agrobacterium-mediated transient expression system. Mol Biol Rep 39:5537–5541. CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Centro de Biotecnologia Agrícola e Agro-Alimentar do Alentejo (CEBAL)Instituto Politécnico de Beja (IPBeja)BejaPortugal
  2. 2.Linking Landscape, Environment, Agriculture and Food, Instituto Superior de AgronomiaUniversity of LisbonLisbonPortugal
  3. 3.Instituto de Ciências Agrárias e Ambientais Mediterrânicas (ICAAM)Universidade de ÉvoraÉvoraPortugal
  4. 4.Wellcome Sanger Institute, Wellcome Genome CampusCambridgeUK

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