European Journal of Forest Research

, Volume 131, Issue 3, pp 519–539 | Cite as

Application of biotechnological tools to Quercus improvement

  • Ana M. Vieitez
  • Elena Corredoira
  • M. Teresa Martínez
  • M. Carmen San-José
  • Conchi Sánchez
  • Silvia Valladares
  • Nieves Vidal
  • Antonio Ballester


The genus Quercus, which belongs to the family Fagaceae, is native to the northern hemisphere and includes deciduous and evergreen species. The trees of the different species are very important from both economic and ecological perspectives. Application of new technological approaches (which span the fields of plant developmental biology, genetic transformation, conservation of elite germplasm and discovery of genes associated with complex multigenic traits) to these long-rotation hardwoods may be of interest for accelerating tree improvement programs. This review provides a summary of the advances made in the application of biotechnological tools to specific oak species. Significant progress has been made in the area of clonal propagation via organogenesis and somatic embryogenesis (SE). Standardized procedures have been developed for micropropagating the most important European (Q. robur, Q. petarea, Q. suber) and American (Q. alba, Q. bicolor, Q. rubra) oaks by axillary shoot growth. Although regenerated plantlets are grown in experimental trials, large-scale propagation of oak species has not been carried out. The induction of SE in oaks from juvenile explants is generally not problematic, although the use of explants other than zygotic embryos is much less efficient. During the last decade, enormous advances have been made in inducing SE from selected adult trees, mainly specimens of pedunculate oak (Q. robur) and cork oak (Q. suber). Advances in the understanding of the maturation and germination steps are required for better use of embryogenic process in clonal forestry. Quercus species are late-maturing and late-flowering, exhibit irregular seed set, and produce seeds that are recalcitrant to storage by conventional procedures. Vitrification-based cryopreservation techniques were used successfully in somatic embryos of pedunculate oak and cork oak, and an applied genbank of cork oak selected genotypes is now under development. The feasibility of genetic transformation of pedunculate oak and cork oak somatic embryos by means of co-culture techniques with several strains of Agrobacterium tumefaciens has also been demonstrated. To date, most research on the genomics of Quercus species has concerned population genetics. Approaches using functional genomics to examine the molecular and cellular mechanisms that control organogenesis and or somatic embryogenesis are still scarce, and efforts on the isolation and characterization of genes related to other specific traits should be intensified in the near future, as this would help improve the practical application of clonal forestry in recalcitrant species such as oaks.


Cryopreservation Genetic transformation Genomics In vitro tissue culture Micropropagation Oak Somatic embryogenesis Tree improvement 



This research was partly funded by the Xunta de Galicia (Spain) through project 09MRU002400PR.


  1. Aldrich PR, Michler C, Sun W, Romero-Severson J (2002) Microsatellite markers for northern red oak (Fagaceae: Quercus rubra). Mol Ecol Notes 2:472–475CrossRefGoogle Scholar
  2. Alvarez R, Ordás RJ (2007) Improved genetic transformation protocol for cork oak (Quercus suber L.). Plant Cell Tissue Organ Cult 91:45–52CrossRefGoogle Scholar
  3. Alvarez R, Alonso P, Cortizo M, Celestino C, Hernández I, Toribio T, Ordás RJ (2004) Genetic transformation of selected mature cork oak (Quercus suber L.). Plant Cell Rep 23:218–223PubMedCrossRefGoogle Scholar
  4. Alvarez R, Alvarez JM, Humara JM, Revilla A, Ordás RJ (2009) Genetic transformation of cork oak (Quercus suber L.) for herbicide resistance. Biotechnol Lett 31:1477–1483PubMedCrossRefGoogle Scholar
  5. Andrade GM, Merkle SA (2005) Enhancement of American chestnut somatic seedling production. Plant Cell Rep 24:326–334PubMedCrossRefGoogle Scholar
  6. Anten NPR, Casado-García R, Pierik R, Ponds TL (2006) Ethylene sensitivity affects changes in growth patterns, but not stem properties, in response to mechanical stress in tobacco. Physiol Plant 128:274–282CrossRefGoogle Scholar
  7. Aronen T, Krajnakova J, Häggman H, Ryynanen L (1999) Genetic fidelity of cryopreserved embryogenic cultures of open-pollinated Abies cephalonica. Plant Sci 142:163–172CrossRefGoogle Scholar
  8. Ballester A, Sánchez MC, San-José MC, Vieitez FJ, Vieitez AM (1990) Development of rejuvenation methods for in vitro establishment, multiplication and rooting of mature trees. In: Rodríguez R, Tamés RS, Durzan DJ (eds) Plant aging: basic and applied approaches. Plenum Press, New York, pp 43–49Google Scholar
  9. Ballester A, Vidal N, Vieitez AM (2009) Developmental stages during in vitro rooting of hardwood trees from material with juvenile and mature characteristics. In: Niemii K, Scagel C (eds) Adventitious root formation of forest trees and horticultural plants—from genes to applications. Research Singpost, Kerala, pp 277–299Google Scholar
  10. Barreneche T, Casasoli M, Russell K, Akkak A, Meddour H, Plomion C, Villani F, Kremer A (2004) Comparative mapping between Quercus and Castanea using simple-sequence repeats (SSRs). Theor Appl Genet 108:558–566PubMedCrossRefGoogle Scholar
  11. Ben Amar A, Cobanov P, Boonrod K, Krezal G, Bouzid S, Ghorbel A, Reustle GM (2007) Efficient procedure for grapevine embryogenic suspension establishment and plant regeneration: role of conditioned medium for cell proliferation. Plant Cell Rep 26:1439–1447PubMedCrossRefGoogle Scholar
  12. Bergot M, Cloppet E, Pérarnaud V, Déqué M, Marçais B, Desprez-Loustau ML (2004) Simulation of potential range expansion of oak disease caused by Phytophthora cinnamomi under climate change. Global Change Biol 10:1539–1552CrossRefGoogle Scholar
  13. Berjak P, Walker M, Mycock DJ, Wesley-Smith J, Watt P, Pammenter NW (2000) Cryopreservation of recalcitrant zygotic embryos. In: Engelman F, Tajagi H (eds) Cryopreservation of tropical plant germplasm. Current research progress and application. IPGRI, Rome, pp 140–155Google Scholar
  14. Bonga JM, MacDonald JE, von Aderkas P (2008) Cloning conifers, with emphasis on mature trees. In: Rao GP, Zhao Y, Radchuck VV, Batnagar SK (eds) Advances in plant biotechnology. Studium Press LLC, Houston, pp 475–490Google Scholar
  15. Bonga JM, Klimaszewska KK, von Aderkas P (2010) Recalcitrance in clonal propagation, in particular in conifers. Plant Cell Tissue Organ Cult 100:241–254CrossRefGoogle Scholar
  16. Bradford KJ, Van Deynze N, Parrott W, Strauss SH (2005) Regulating transgenic crops sensibly: lessons from plant breeding, biotechnology and genomics. Nat Biotechnol 23:439–444PubMedCrossRefGoogle Scholar
  17. Brendel O, Le Thiec D, Scotti-Saintagne C, Bodénès C, Kremer A, Guehl JM (2008) Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L. Tree Genet Genome 4:263–278CrossRefGoogle Scholar
  18. Brown LB, Allen-Diaz B (2009) Forest stand dynamics and sudden oak death: Mortality in mixed-evergreen forests dominated by coast live oak. For Ecol Manag 257:1271–1280CrossRefGoogle Scholar
  19. Brunner AM, Li J, DiFazio S, Shevchenko O, Montgomery BE, Mohamed R, Wei H, Ma C, Elias AA, VanWormer K, Strauss SH (2007) Genetic containment of forest plantations. Tree Genet Genome 3:75–100CrossRefGoogle Scholar
  20. Bueno MA, Gómez A, Boscaiu M, Manzanera JA, Vicente O (1997) Stress-induced formation of haploid plants through anther culture in cork oak (Quercus suber). Physiol Plant 99:335–341CrossRefGoogle Scholar
  21. Bueno MA, Gómez A, Sepúlveda F, Segui JM, Testillano PS, Manzanera JA, Risueño MC (2003) Microspore-derived embryos from Quercus suber anthers mimic zygotic embryos and maintain haploidy in long-term anther culture. J Plant Physiol 160:953–960PubMedCrossRefGoogle Scholar
  22. Burley J, Kanowski PJ (2005) Breeding strategies for temperate hardwoods. Forestry 78:199–208CrossRefGoogle Scholar
  23. Canhoto JM, Lopes ML, Cruz GS (1999) Somatic embryogenesis and plant regeneration in myrtle (Myrtaceae). Plant Cell Tissue Organ Cult 57:13–21CrossRefGoogle Scholar
  24. Carraway DT, Merkle SA (1997) Plantlet regeneration from somatic embryos of American chestnut. Can J For Res 27:1805–1812CrossRefGoogle Scholar
  25. Casasoli M, Derory J, Morera-Dutrey C, Brendel O, Porth I, Guehl JM, Villani F, Kremer A (2006) Comparison of quantitative trait loci for adaptive traits between oak and chestnut based on expressed sequence tag consensus map. Genetics 172:533–546PubMedCrossRefGoogle Scholar
  26. Catry FX, Moreira F, Duarte I, Acácio V (2009) Factors affecting post-fire crown regeneration in cork oak (Quercus suber L.) trees. Eur J Forest Res 128:231–240CrossRefGoogle Scholar
  27. Celestino C, Hernández I, López-Vela D, Carneros E, Alegre J, Toribio M, Fernández-Guijarro B, Cardo L (2007) First data from a field trial of Quercus suber plants regenerated from mature selected trees and from their half-sib progenies by somatic embryogenesis. Acta Hortic 748:215–218Google Scholar
  28. Chalupa V (1988) Large scale micropropagation of Quercus robur L. using adenine-type cytokinins and thidiazuron to stimulate shoot proliferation. Biol Plant 30:414–421CrossRefGoogle Scholar
  29. Chalupa V (1993) Vegetative propagation of oak (Quercus robur and Q. petraea) by cutting and tissue culture. Ann Sci For 50(Suppl 1):295–307CrossRefGoogle Scholar
  30. Chalupa V (1995) Somatic embryogenesis in oak (Quercus spp.). In: Jain S, Gupta P, Newton R (eds) Somatic embryogenesis in woody plants, vol 2, angiosperms. Kluwer, Dordrecht, pp 67–87CrossRefGoogle Scholar
  31. Chalupa V (2000) In vitro propagation of mature trees of pedunculate oak (Quercus robur L.). J For Sci 46:537–542Google Scholar
  32. Coggeshall MV (1996) Oak grafting techniques. Comb Proc Int Plant Prop Soc 46:481–486Google Scholar
  33. Compton ME, Gray DJ (1996) Effects of sucrose and methylglyoxal bis-(guanylhydrazone) on controlling grape somatic embryogenesis. Vitis 35:1–6Google Scholar
  34. Conte L, Cotti C, Cristofolini G (2007) Molecular evidence for hybrid origin of Quercus crenata Lam. (Fagaceae) from Q. cerris L. and Q. suber L. Plant Biosyst 141:181–193Google Scholar
  35. Corredoira E, Ballester A, Vieitez AM (2003) Proliferation, maturation and germination of Castanea sativa Mill. somatic embryos originated from leaf explants. Ann Bot 92:1129–1136CrossRefGoogle Scholar
  36. Corredoira E, Ballester A, Vieitez AM (2006a) Somatic embryogenesis in chestnut. In: Mujib S, Samaj J (eds) Somatic embryogenesis, plant cell monographs, vol 2. Springer, Heidelberg, pp 177–199Google Scholar
  37. Corredoira E, Valladares S, Vieitez AM (2006b) Morphohistological analysis of the origin and development of somatic embryos from leaves of mature Quercus robur. In Vitro Cell Dev Biol Plant 42:525–533CrossRefGoogle Scholar
  38. Covelo G, Ferro E, Vielba J, Sánchez C (2009) Molecular analysis of adventitious rooting in Fagaceae species. In: Niemi K, Scagel C (eds) Adeventitious root formation of forest trees and horticultural plants—from genes to applications. Research Signpost, Kerala, pp 105–122Google Scholar
  39. Cuenca B, San-José MC, Martínez MT, Ballester A, Vieitez AM (1999) Somatic embryogenesis from stem and leaf explant of Quercus robur L. Plant Cell Rep 18:538–543CrossRefGoogle Scholar
  40. Deng MD, Cornu D (1992) Maturation and germination of walnut somatic embryos. Plant Cell Tissue Organ Cult 28:195–202CrossRefGoogle Scholar
  41. Deroy J, Léger P, Garcia V, Schaeffer J, Hauser MT, Salin F, Lusching C, Plomion C, Glössl J, Kremer A (2006) Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytol 170:723–738CrossRefGoogle Scholar
  42. DeVerno LL, Charest PJ, Bonen L (1994) Somaclonal variation in somatic embryogenic cultures of Larix. Theor Appl Genet 88:727–732CrossRefGoogle Scholar
  43. Dodeman VL, Ducreux G, Kreis M (1997) Zygotic embryogenesis versus somatic embryogenesis. J Exp Bot 48:1493–1509Google Scholar
  44. Ducousso A, Bordacs S (2004) EUFORGEN technical guidelines for genetic conservation and use for pedunculate and sessile oaks (Quercus robur and Q. petraea). International Plant Genetic Resources Institute, RomeGoogle Scholar
  45. El Maâtaoui M, Espagnac H, Michaux-Ferrière N (1990) Histology of callogenesis and somatic embryogenesis induced in stem fragments of cork oak (Quercus suber) cultured in vitro. Ann Bot 66:183–190Google Scholar
  46. Endemann M, Hristoforoglu K, Stauber T, Wilhelm E (2001) Assessment of age-related polyploidy in Quercus robur L. somatic embryos and regenerated plants using DNA flow cytometry. Biol Plant 44:339–345CrossRefGoogle Scholar
  47. Evers P, Vermeer E, van Eeden S (1993) Rejuvenation of Quercus robur. Ann Sci For 50(Suppl 1):330–335CrossRefGoogle Scholar
  48. Favre JM, Juncker B (1987) In vitro growth of buds taken from seedlings and adult-plant material in Quercus robur L. Plant Cell Tissue Organ Cult 8:49–60CrossRefGoogle Scholar
  49. Fenning TM (2006) The use of genetic transformation procedures to study defence and disease resistance traits of trees. In: Fladung M, Ewald D (eds) Tree transgenesis. Springer, Heidelberg, pp 201–234CrossRefGoogle Scholar
  50. Fenning TM, Gershenzon J (2002) Where will the wood come from? Plantation forests and the role of biotechnology. Trends Biotechnol 20:291–296PubMedCrossRefGoogle Scholar
  51. Féraud-Keller C, Espagnac H (1989) Conditions d’apparition d’une embryogénèse somatique sur des cals issus de la culture de tissus foliaires du chêne vert (Quercus ilex). Can J Bot 67:1066–1070Google Scholar
  52. Fernández-Guijarro B, Celestino C, Toribio M (1995) Influence of external factors on secondary embryogenesis and germination in somatic embryos from leaves of Quercus suber L. Plant Cell Tissue Organ Cult 41:99–106CrossRefGoogle Scholar
  53. Flachowsky H, Hanke M-V, Peil A, Strauss SH, Fladung M (2009) A review on transgenic approaches to accelerate breeding of woody plants. Plant Breed 128:217–226CrossRefGoogle Scholar
  54. Forestry Commission (2009) Pyhtophthora ramorum. (
  55. Gallego FJ, Martínez I, Celestino C, Toribio M (1997) Testing somaclonal variation using RAPDs in Quercus suber L. somatic embryos. Int J Plant Sci 158:563–567CrossRefGoogle Scholar
  56. García-Martín G, González-Benito ME, Manzanera JA (2001) Quercus suber L. somatic embryo germination and plant conversion: Pretreatments and germination conditions. In Vitro Cell Dev Biol Plant 37:190–198CrossRefGoogle Scholar
  57. García-Martín G, Manzanera JA, González-Benito ME (2005) Effect of exogenous ABA on embryo maturation and quantification of endogenous levels of ABA and IAA in Quercus suber somatic embryos. Plant Cell Tissue Organ Cult 80:171–177CrossRefGoogle Scholar
  58. Gartland KMA, Oliver CD (2007) Growing trees: risks and rewards for society. Tree Genet Genome 3:169–172CrossRefGoogle Scholar
  59. Gil B, Pastoriza E, Ballester A, Sánchez C (2003) Isolation and characterization of a cDNA from Quercus robur differentially expressed in juvenile-like and mature shoots. Tree Physiol 23:633–640PubMedCrossRefGoogle Scholar
  60. Gómez A, López JA, Pintos B, Camafeita E, Bueno MA (2009) Proteomic analysis from haploid and diploid embryos of Quercus suber L. identifies qualitative and quantitative differential expression. Proteomics 9:4355–4367PubMedCrossRefGoogle Scholar
  61. Gömöry D, Schmidtova J (2007) Extent of nuclear genome sharing among white oak species (Quercus L. subgen, Lepidobalanus (Endl.) Oerst) in Slowakia estimated by allozymes. Plant Syst Evol 266:253–264CrossRefGoogle Scholar
  62. González-Benito ME, Pérez-Ruiz C (1992) Cryopreservation of Quercus faginea embryonic axes. Cryobiology 29:685–690CrossRefGoogle Scholar
  63. González-Benito ME, García-Martín G, Manzanera JA (2002a) Shoot development in Quercus suber L. somatic embryos. In Vitro Cell Dev Biol Plant 38:477–480CrossRefGoogle Scholar
  64. González-Benito ME, Prieto RM, Herradon E, Martin C (2002b) Cryopreservation of Quercus suber and Quercus ilex embryonic axes: In vitro culture, desiccation and cooling factors. CryoLetters 23:283–290PubMedGoogle Scholar
  65. Grattapaglia D, Plomion C, Kirst M, Sederoff RR (2009) Genomics of growth traits in forest trees. Curr Opin Plant Biol 12:148–156PubMedCrossRefGoogle Scholar
  66. Gresshoff PM, Doy CH (1972) Development and differentiation of haploid Lycopersicon esculentum. Planta 107:161–170CrossRefGoogle Scholar
  67. Häggman H, Niemi K, Timonen H, Ylioja T, Chiang V (2006) Environmental aspects of lignin modified trees. In: Fladung M, Ewald D (eds) Tree transgenesis. Springer, Heidelberg, pp 105–117CrossRefGoogle Scholar
  68. Häggman H, Rusanen M, Jokipii S (2008) Cryopreservation of in vitro tissues of deciduous trees. In: Reed B (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 365–386CrossRefGoogle Scholar
  69. Hajji M, Dreyer E, Maçais B (2009) Impact of Erysiphe alphitoides on transpiration and photosynthesis in Quercus robur leaves. Eur J Plant Pathol 125:63–72CrossRefGoogle Scholar
  70. Harvengt L, Meier-Dinkel A, Dumas E, Collin E (2004) Establishment of a cryopreserved gene bank of European elms. Can J For Res 34:43–55CrossRefGoogle Scholar
  71. Heinze B, Schmit J (1994) Clonal fidelity of Norway spruce somatic embryos by RAPD. In: Pardos A, Ahuja MR, Rosello RE (eds) Biotechnology of Trees. J Investigación Agraria Sistema y Recursos Forestales, INIA, Spain, pp 143–148Google Scholar
  72. Hernández I, Celestino C, Martínez I, Manjón JL, Díez J, Fernández-Guijarro B, Toribio M (2001) Cloning mature cork oak (Quercus suber L.) trees by somatic embryogenesis. Melhoramento 37:50–57Google Scholar
  73. Hernández I, Celestino C, Toribio M (2003a) Vegetative propagation of Quercus suber L. by somatic embryogenesis. I. Factors affecting the induction in leaves from mature cork oak trees. Plant Cell Rep 21:759–764PubMedGoogle Scholar
  74. Hernández I, Celestino C, Alegre J, Toribio M (2003b) Vegetative propagation of Quercus suber L. by somatic embryogenesis: II. Plant regeneration from selected cork oak trees. Plant Cell Rep 21:765–770PubMedGoogle Scholar
  75. Hornero J, Martínez I, Celestino C, Gallego FJ, Torres V, Toribio M (2001) Early checking of genetic stability of cork oak somatic embryos by AFLP analysis. Int J Plant Sci 162:827–833CrossRefGoogle Scholar
  76. Juncker B, Favre JM (1989) Clonal effects in propagating oak trees via in vitro culture. Plant Cell Tissue Organ Cult 19:267–276CrossRefGoogle Scholar
  77. Jung T, Blaschke H, Osswald W (2000) Involvement of soilborne Phytophthora species in Central European oak decline and the effect of site factors on the disease. Plant Pathol 49:706–718CrossRefGoogle Scholar
  78. Kernode AR (1995) Regulatory mechanisms in the transition from seed development to germination: interaction between and the see environment. In: Kigel J, Galili G (eds) Seed development and germination. Marcel Dekker, Inc., New York, pp 273–332Google Scholar
  79. Kim YW (2000) Somatic embryogenesis in Quercus acutissima. In: Jain SM, Gupta PK, Newton RJ (eds) Somatic embryogenesis in woody plants, vol 6. Kluwer, Dordrecht, pp 671–685Google Scholar
  80. Kleinschmit J (1993) Interspecific variation of growth and adaptive traits in European oak species. Ann Sci For 50(Suppl 1):166–185CrossRefGoogle Scholar
  81. Knapic S, Louzada JL, Leal S, Pereira H (2008) Within-tree and between-tree variation of wood density components in cork oak trees in two sites in Portugal. Forestry 81:465–473CrossRefGoogle Scholar
  82. Krahl-Urban J (1959) Die Eichen. Paul Parey Verlag, Hamburg, p 288Google Scholar
  83. Kremer A, Casasoli M, Barreneche T et al (2007) Fagaceae trees. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 7, forest trees. Springer, Berlin, pp 161–187Google Scholar
  84. Krüssmann G (1978) Hanbuch der Laubgehölze. Paul Parey Verlag, Berlin, pp 79–115Google Scholar
  85. Letarte J, Simion E, Miner M, Kasha KJ (2006) Arabinogalatans and arabinogalactan-proteins induce embryogenesis in wheat (Triticum aestivum L.) microspore culture. Plant Cell Rep 24:691–698PubMedCrossRefGoogle Scholar
  86. Lloyd G, McCown B (1980) Comercially-feasible micropropagation of mountain laurel, Kalmia latifolia, by use of shoot-tip culture. Comb Proc Int Plant Prop Soc 30:421–427Google Scholar
  87. Lopes T, Pinto G, Loureiro J, Costa A, Santos C (2006) Determination of genetic stability in long-term somatic embryogenic cultures and derived plantlets of cork oak using microsatellite markers. Tree Physiol 26:1145–1152PubMedCrossRefGoogle Scholar
  88. Loureiro J, Pinto G, Lopes T, Dolezel J, Santos C (2005) Assessment of ploidy stability of the somatic embryogenesis process in Quercus suber L. using flow cytometry. Planta 221:815–822PubMedCrossRefGoogle Scholar
  89. Manion PD, Lachance D (1992) Forest decline concepts. In: Manion PD, Lachance D (eds) Forest decline concepts. American Phytopathological Society, St. Paul, pp 181–190Google Scholar
  90. Manzanera JA, Bueno MA, Pardos JA (1996) Quercus robur L. (pedunculate oak). In: Bajaj YPS (ed) Biotechnology in agriculture and forestry, vol 35, Trees IV. Springer, Berlin, pp 321–341Google Scholar
  91. Marçais B, Bréda N (2006) Role of an opportunistic pathogen in the decline of stressed oak trees. J Ecol 94:1214–1223CrossRefGoogle Scholar
  92. Martínez MT, Ballester A, Vieitez AM (2003) Cryopreservation of embryogenic cultures of Quercus robur using desiccation and vitrification procedures. Cryobiology 46:182–189PubMedCrossRefGoogle Scholar
  93. Martínez MT, Corredoira E, Valladares S, Jorquera L, Vieitez AM (2008) Germination and conversion of somatic embryos derived from mature Quercus robur trees: the effects of cold storage and thidiazuron. Plant Cell Tissue Organ Cult 95:341–351CrossRefGoogle Scholar
  94. Mauri PV, Manzanera JA (2003) Induction, maturation and germination of holm oak (Quercus ilex L.) somatic embryos. Plant Cell Tissue Organ Cult 74:229–235CrossRefGoogle Scholar
  95. Mauri PV, Manzanera JA (2004) Effect of abscisic acid and stratification on somatic embryo maturation and germination of holm oak (Quercus ilex L.). In Vitro Cell Dev Biol Plant 40:495–498CrossRefGoogle Scholar
  96. Maynard CA, Powell WA, Polin-McGuigan LD, Vieitez AM, Ballester A, Corredoira E, Merkle SA, Andrade GM (2008) Chestnut. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants: transgenic forest tree species. Blackwell Publishing, Chichester, pp 169–192Google Scholar
  97. McCown BH (2000) Recalcitrance of woody and herbaceous perennials plants: dealing with genetic predeterminism. In Vitro Cell Dev Biol Plant 36:149–154CrossRefGoogle Scholar
  98. Meentemeyer RK, Rank NE, Shoemaker DA, Oneal CB, Wickland AC, Frangioso KM, Rizzo DM (2008) Impact of sudden oak death on tree mortality in the Big Sur ecoregion of California. Biol Invasions 10:1243–1255CrossRefGoogle Scholar
  99. Meier-Dinkel A, Becker B, Duckstein D (1993) Micropropagation and ex vitro rooting of several clones of late-flushing Quercus robur L. Ann Sci For 50(Suppl 1):319–322CrossRefGoogle Scholar
  100. Merkle SA, Nairn CJ (2005) Hardwood tree biotechnology. In Vitro Cell Dev Biol Plant 41:602–619CrossRefGoogle Scholar
  101. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497CrossRefGoogle Scholar
  102. Neger FT, Münch E (1950) Die Laubhölzer. Sammlung Göschen de Gruyter, Berlin Bd 718, p 160Google Scholar
  103. Nehra NS, Becwar MR, Rottmann WH et al (2005) Forest biotechnology: innovative methods, emerging opportunities. In Vitro Cell Dev Biol Plant 41:701–717CrossRefGoogle Scholar
  104. Parelle J, Zapater M, Scotti-Saintagne C, Kremer A, Jolivet Y, Dreyer E, Brendel O (2007) Quantitative trait loci of tolerance to waterlogging in a European oak (Quercus robur L.): physiological relevance and temporal effects patterns. Plant Cell Environ 30:422–434PubMedCrossRefGoogle Scholar
  105. Percy REL, Livingston NJ, Moran JA, von Aderkas P (2001) Desiccation, cryopreservation and water relations parameters of white spruce (Picea glauca) and interior spruce (Picea glauca × engelmannii complex) somatic embryos. Tree Physiol 21:1303–1310PubMedCrossRefGoogle Scholar
  106. Petit RJ, Bodénès C, Ducousso A, Roussel G, Kremer A (2004) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164CrossRefGoogle Scholar
  107. Pijut PM, Woeste KE, Vengadesan G, Michler CH (2007) Technological advances in temperate hardwood tree improvement including breeding and molecular marker applications. In Vitro Cell Dev Biol Plant 43:283–303Google Scholar
  108. 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 Cell Dev Biol Plant 38:569–572CrossRefGoogle Scholar
  109. Pinto G, Silva S, Park YS, Neves L, Araújo C, Santos C (2008) Factors influencing somatic embryogenesis induction in Eucalyptus globulus Labill.: basal medium and anti-browning agents. Plant Cell Tissue Organ Cult 95:79–88CrossRefGoogle Scholar
  110. 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 95:217–225CrossRefGoogle Scholar
  111. Pintos B, Manzanera JA, Bueno MA (2010) Oak somatic and gametic embryos maturation is affected by charcoal and specific aminoacids mixture. Ann For Sci 67. doi: 10.1051/forest/2009098
  112. Porth I, Scotti-Saintagne C, Barreneche T, Kremer A, Burg K (2005) Linkage mapping of osmotic stress genes of oak. Tree Genet Genome 1:31–40CrossRefGoogle Scholar
  113. Prewein P, Wilhelm E (2003) Plant regeneration from encapsulated somatic embryos of pedunculate oak (Quercus robur L.). In Vitro Cell Dev Biol Plant 39:613–617CrossRefGoogle Scholar
  114. Prewein C, Vagner M, Wilhelm E (2004) Changes in water status and proline and abscisic acid concentrations in developing somatic embryos on pedunculate oak (Quercus robur) during maturation and germination. Tree Physiol 24:1251–1257PubMedCrossRefGoogle Scholar
  115. Puddephat IJ, Alderson PG, Wright NA (1999) In vitro root induction in axillary microshoots of Quercus robur L. Ann Appl Biol 134:233–239CrossRefGoogle Scholar
  116. Puigdejarrols P, Fernández-Guijarro B, Toribio M, Molinas M (1996) Origin and early development of secondary embryos in Quercus suber L. Int J Plant Sci 157:674–684CrossRefGoogle Scholar
  117. Puigdejarrols P, Mir G, Molinas M (2001) Ultrastructure of early secondary embryogenesis by multicellular and unicellular pathways in cork oak (Quercus suber L.). Ann Bot 87:179–189CrossRefGoogle Scholar
  118. Reed BM (2008) Cryopreservation-practical considerations. In: Reed B (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 3–13CrossRefGoogle Scholar
  119. Repo T, Mononen K, Alvila L, Pakkanen TT, Hänninen H (2008) Cold acclimation of pedunculate oak (Quercus robur L.) at its northernmost distribution range. Environ Exp Bot 63:59–70CrossRefGoogle Scholar
  120. Robin C, Desprez-Loustau ML, Delatour C (1992) Factors influencing the enlargement of trunk cankers of Phytophthora cinnamomi in red oak. Can J For Res 22:367–374CrossRefGoogle Scholar
  121. Roest S, Brueren HGMJ, Evers PW, Vermeer E (1991) Agrobacterium-mediated transformation of oak (Quercus robur L.). Acta Hortic 289:259–260Google Scholar
  122. Romano A, Noronha C, Martins-Louçao MA (1992) Influence of growth regulators on shoot proliferation in Quercus suber L. Ann Bot 70:531–536Google Scholar
  123. Saintagne C, Bodénès C, Barreneche T, Pot D, Plomion C, Kremer A (2004) Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 12:20–30CrossRefGoogle Scholar
  124. Sánchez MC (1991) Propagación in vitro de material adulto de castaño y roble. Desarrollo de métodos de rejuvenecimiento. Doctoral thesis, University of Santiago de Compostela, SpainGoogle Scholar
  125. Sánchez MC, San-José MC, Ballester A, Vieitez AM (1996) Requirements for in vitro rooting of Quercus robur and Q. rubra shoots derived from mature trees. Tree Physiol 16:673–680PubMedCrossRefGoogle Scholar
  126. Sánchez MC, Martínez MT, Valladares S, Ferro E, Vieitez AM (2003) Maturation and germination of oak somatic embryos originated from leaf and stem explants: RAPD markers for genetic analysis of regenerants. J Plant Physiol 160:699–707PubMedCrossRefGoogle Scholar
  127. Sánchez N, Manzanera JA, Pintos B, Bueno MA (2005) Agrobacterium-mediated transformation of cork oak (Quercus suber L.) somatic embryos. New For 29:169–176CrossRefGoogle Scholar
  128. Sánchez MC, Martínez MT, Vidal N, San-José MC, Valladares S, Vieitez AM (2008) Preservation of Quercus robur germplasm by cryostorage of embryogenic cultures derived from mature trees and RAPD analysis of genetic stability. CryoLetters 29:493–504PubMedGoogle Scholar
  129. San-José MC, Ballester A, Vieitez AM (1988) Factors affecting in vitro propagation of Quercus robur L. Tree Physiol 4:281–290PubMedGoogle Scholar
  130. San-José MC, Vieitez AM, Ballester A (1990) Clonal propagation of juvenile and adult trees of sessile oak by tissue culture. Silvae Genet 39:50–55Google Scholar
  131. San-José MC, Corredoira E, Martínez MT, Vidal N, Valladares S, Mallón R, Vieitez AM (2010) Shoot apex explants for induction of somatic embryogenesis in mature Quercus robur trees. Plant Cell Rep 29:661–671PubMedCrossRefGoogle Scholar
  132. Savill PS, Kanowski PJ (1993) Tree improvement programs for European oaks: goals and strategies. Ann Sci For 50(Suppl 1):368–383CrossRefGoogle Scholar
  133. Savill PS, Fennessy J, Samuel CJA (2005) Approaches in Great Britain and Ireland to the genetic improvement of broadleaved trees. Forestry 78:163–173CrossRefGoogle Scholar
  134. Schenk RU, Hildebrandt AC (1972) Medium and techniques for induction of growth of monocotyledonous and dicotyledonous plant cell culture. Can J Bot 50:199–204CrossRefGoogle Scholar
  135. Schroeder H, Degen B (2008) Spatial genetic structure in populations of the green oak leaf roller, Tortrix viridiana L. (Lepidoptera, Tortricidae). Eur J For Res 127:447–453CrossRefGoogle Scholar
  136. Schwarz OJ, Schlarbaum SE (1993) Axillary bud proliferation of 2 North American oak species: Quercus alba and Quercus rubra. Ann Sci For 50(Suppl 1):425–429Google Scholar
  137. Scotti-Saintagne C, Meriette S, Porth I, Goicoechea T, Bodénès C, Burg K, Kremer A (2004a) Genome scanning for interspecific differentiation between two closely related species [Quercus robur L. and Q. petraea (Matt.) Liebl.]. Genetics 168:1615–1626PubMedCrossRefGoogle Scholar
  138. Scotti-Saintagne C, Bodénès C, Barreneche T, Bertocchi E, Plomion C, Kremer A (2004b) Detection of quantitative trait loci controlling bud burst and height growth in Quercus robur L. Theor Appl Genet 109:1648–1659PubMedCrossRefGoogle Scholar
  139. Scotti-Saintagne C, Bertocchi E, Barreneche T, Kremer A, Plomion C (2005) Quantitative trait loci mapping for vegetative propagation in pedunculate oak. Ann For Sci 62:369–374CrossRefGoogle Scholar
  140. Sederoff R (2007) Regulatory science in forest biotechnology. Tree Genet Genome 3:71–74CrossRefGoogle Scholar
  141. Steiner KC (1993) Genetic improvement of oaks in North America. Ann Sci For 50(Suppl 1):359–367CrossRefGoogle Scholar
  142. Strauss SH, Tan H, Boerjan W, Sedjo R (2009) Strangle at birth? Forest biotech and the convention on biology diversity. Nat Biotechnol 27:519–527PubMedCrossRefGoogle Scholar
  143. Sunderlikova V, Wilhelm E (2002) High accumulation of legumin and Lea-like mRNAs during maturation is associated with increased conversion frequency of somatic embryos from pedunculate oak (Quercus robur L.). Protoplasma 220:97–103PubMedCrossRefGoogle Scholar
  144. Sunderlikova V, Salaj J, Matusikova I, Wilhelm E (2009a) Isolation and characterization of an embryo-specific Em-like gene of pedunculate oak (Quercus robur L.) and its temporal and spatial expression patterns during somatic and zygotic embryo development. Tree Struct Funct 23:135–144CrossRefGoogle Scholar
  145. Sunderlikova V, Salaj J, Kopecky D, Salaj T, Wilhelm E (2009b) Dehydrin genes and their expression in recalcitrant oak (Quercus robur) embryos. Plant Cell Rep 28:1011–1021PubMedCrossRefGoogle Scholar
  146. Sutton B (2002) Commercial delivery of genetic improvement to conifer plantations using somatic embryogenesis. Ann Forest Sci 59:657–661CrossRefGoogle Scholar
  147. Thomas FM, Blank R, Hartmann G (2002) Abiotic and biotic factors and their interactions as causes of oak decline in central Europe. For Pathol 32:277–307CrossRefGoogle Scholar
  148. Toribio M, Fernández C, Celestino C, Martínez MT, San-José MC, Vieitez AM (2004) Somatic embryogenesis in mature Quercus robur trees. Plant Cell Tissue Organ Cult 76:283–287CrossRefGoogle Scholar
  149. Toribio M, Celestino C, Molinas M (2005) Cork oak, Quercus suber L. In: Jain SM, Gupta PK (eds) Protocol for somatic embryogenesis in woody plants. Springer, Dordrecht, pp 445–457CrossRefGoogle Scholar
  150. Tsvetkov I, Hausman J-F (2005) In vitro regeneration from alginate-encapsulated microcuttings of Quercus sp. Sci Hortic 103:503–507CrossRefGoogle Scholar
  151. Valladares S, Toribio M, Celestino C, Vieitez AM (2004) Cryopreservation of embryogenic cultures from mature Quercus suber trees using vitrification. CryoLetters 25:177–186PubMedGoogle Scholar
  152. Valladares S, Sánchez C, Martínez MT, Ballester A, Vieitez AM (2006) Plant regeneration through somatic embryogenesis from tissues of mature oak trees: true-to-type conformity of plantlets by RAPD analysis. Plant Cell Rep 25:879–886PubMedCrossRefGoogle Scholar
  153. Vengadesan G, Pijut PM (2007) In vitro propagation of northern red oak (Quercus rubra L.). In Vitro Cell Dev Biol Plant 45:474–482Google Scholar
  154. Vengadesan G, Pijut PM (2009) Somatic embryogenesis and plant regeneration of northern red oak (Quercus rubra L.). Plant Cell Tissue Organ Cult 97:141–149CrossRefGoogle Scholar
  155. Vettraino AM, Barzanti GP, Bianco MC, Ragazzi A, Capretti P, Paoletti E, Luisi N, Anselmi A, Vannini A (2002) Occurrence of Phytophthora species in oak stands in Italy and their association with declining oak trees. For Pathol 32:19–28CrossRefGoogle Scholar
  156. Vidal N, Vieitez AM, Fernández MR, Cuenca B, Ballester A (2010a) Establishment of cryopreserved gene banks of European chestnut and cork oak. Eur J For Res 129:635–643CrossRefGoogle Scholar
  157. Vidal N, Mallón R, Valladares S, Meijomín AM, Vieitez AM (2010b) Regeneration of transgenic plants by Agrobacterium-mediated transformation of somatic embryos of juvenile and mature Quercus robur. Plant Cell Rep 29:1411–1422PubMedCrossRefGoogle Scholar
  158. Vieitez AM, San-José MC, Vieitez E (1985) In vitro plantlet regeneration from juvenile and mature Quercus robur L. J Hort Sci 60:99–106Google Scholar
  159. Vieitez AM, Pintos F, San-José MC, Ballester A (1993) In vitro shoot proliferation determined by explant orientation of juvenile and mature Quercus rubra L. Tree Physiol 12:107–117PubMedGoogle Scholar
  160. Vieitez AM, Sánchez MC, Amo-Marco JB, Ballester A (1994) Forced flushing of branch segments as a method for obtaining reactive explants of mature Quercus robur trees for micropropagation. Plant Cell Tissue Organ Cult 37:287–295Google Scholar
  161. Vieitez AM, Sánchez C, García-Nimo ML, Ballester A (2007) Protocol for micropropagation of Castanea sativa. In: Jain SM, Häggman H (eds) Protocols for micropropagation of woody trees and fruits. Springer, Heidelberg, pp 299–312CrossRefGoogle Scholar
  162. Vieitez AM, Corredoira E, Ballester A, Muñoz F, Durán J, Ibarra M (2009) In vitro regeneration of important North American oak species Quercus alba, Quercus bicolor and Quercus rubra. Plant Cell Tissue Organ Cult 98:135–145CrossRefGoogle Scholar
  163. von Arnold S, Sabala I, Bozhkov P, Dyachock J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249CrossRefGoogle Scholar
  164. Wargo PM, Houston DR, LaMadeleine LA (1983) Oak decline. Forest insect and disease leaflet 165. U.S. Department of Agriculture ServiceGoogle Scholar
  165. Wilhelm E (2000) Somatic embryogenesis in oak (Quecus spp.). In Vitro Cell Dev Biol Plant 36:349–357CrossRefGoogle Scholar
  166. Wilhelm E, Burg A, Berenyi M, Endemann M, Rodler R (1996) Plantlet regeneration via somatic embryogenesis and investigations on Agrobacterium tumefaciens mediated transformation of oak (Quercus robur). In: Ahuja MR, Boerjan W, Neale DB (eds) Somatic cell genetics and molecular genetics of trees. Kluwer, Dordrecht, pp 119–124CrossRefGoogle Scholar
  167. Wilhelm E, Hristoforoglu K, Fluch S, Burg K (2005) Detection of microsatellite instability during somatic embryogenesis of oak (Quercus robur L.). Plant Cell Rep 23:790–795PubMedCrossRefGoogle Scholar
  168. Zegzouti R, Arnould M-F, Favre J-M (2001) Histological investigation of the multiplication step in secondary somatic embryogenesis of Quercus robur L. Ann For Sci 58:681–690CrossRefGoogle Scholar
  169. Zhao XY, Su YH, Cheng ZJ, Zhang XS (2008) Cell fate switch during in vitro plant organogenesis. J Int Plant Biol 50:816–824CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Ana M. Vieitez
    • 1
  • Elena Corredoira
    • 1
  • M. Teresa Martínez
    • 1
  • M. Carmen San-José
    • 1
  • Conchi Sánchez
    • 1
  • Silvia Valladares
    • 1
  • Nieves Vidal
    • 1
  • Antonio Ballester
    • 1
  1. 1.Instituto de Investigaciones Agrobiológicas de GaliciaCSICSantiago de CompostelaSpain

Personalised recommendations