Advertisement

Somatic Embryogenesis for More Effective Breeding and Deployment of Improved Varieties in Pinus spp.: Bottlenecks and Recent Advances

Chapter

Abstract

Global transition towards a bioeconomy sets new demands for wood supply (bioenergy, biomaterials, biochemicals, etc.), and the forestry sector is also expected to help mitigate climate change by increasing carbon fixation. For increased biomass production, the use of improved, genetically superior materials becomes a necessity, and vegetative propagation of elite genotypes provides a potential delivery mechanism for this. Vegetative propagation through somatic embryogenesis alone or in combination with rooted cuttings obtained from somatic young trees can facilitate both tree breeding (greater selection accuracy and gains, breeding archives of donor material for making crosses after selection) and the implementation of deployment strategies for improved reforestation materials. To achieve these goals, progress in the efficiency of pine somatic embryogenesis biotechnology has been made for a few commercial pine species, and a better understanding has been gained of the molecular mechanisms underpinning somatic and zygotic embryo development.

Keywords

Somatic Embryogenesis Genetic Gain Seed Orchard Embryo Maturation Somatic Embryogenesis Induction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The “Genetics and Biotechnology” team of the FCBA is gratefully acknowledged for its contribution to the technical and scientific developments presented throughout this chapter for maritime pine somatic embryogenesis. We especially thank Isabelle Reymond, Francis Canlet, Sandrine Debille, Karine Durandeau, Pierre Alazard and Luc Harvengt. We also thank Alain Bouvet for statistical support.

In France, the maritime pine multiyear project was supported by grants from the “Conseil Régional de la Région Centre” (EMBRYOME project, contract 33639; IMTEMPERIES, contract 2014-00094511), the “Conseil Régional de la Région Aquitaine” (Embryo2011, contract 09012579-045), the French Ministry of Foreign Affairs and the French Ministry of Higher Education and Research through the France/Czech Republic Science Cooperation BARRANDE Program. Data analysis and experiments were made possible through the involvement of INRA’s GenoToul bioinformatics platform in Toulouse (France) and the XYLOFOREST platform (ANR-10-EQPX-16), especially the XYLOBIOTECH technical facility located at INRA Orléans and FCBA Pierroton (France). In Portugal, the preparation of this chapter was supported through projects funded by (1) the European Community’s Seventh Framework Programme (FP7/2007-2013, Grant Agreement N°289841-PROCOGEN), and (2) Fundação para a Ciência e Tecnologia (FCT), through grants GREEN-it (UID/Multi/04551/2013) and IF/01168/2013. In Canada, KK was supported by Natural Resources Canada, Canadian Forest Service. Ms Isabelle Lamarra (NRCan-CFS) is thanked for English editing.

References

  1. Aidun CK, Egertsdotter EMU (2012) Fluidics-based automation of clonal propagation via somatic embryogenesis: SE-fluidics system. In: Second International conference of the IUFRO working party 2.09.02, June 25–28, Brno, Czech Republic, pp. S3–3Google Scholar
  2. Alvarez JM, Cortizo M, Bueno N et al (2013) CLAVATA1-LIKE, a leucine-rich-repeat protein receptor kinase gene differentially expressed during adventitious caulogenesis in Pinus pinaster and Pinus pinea. Plant Cell Tiss Org 112:331–342. doi: 10.1007/s11240-012-0240-8 CrossRefGoogle Scholar
  3. Anonymous (2014) Close to the application of somatic embryogenesis. Scand J For Res News Views 6:615–616Google Scholar
  4. Anonymous (2015) Are hybrid pines the super trees of the future? New Zeal Logger, Sept 2015:46–49Google Scholar
  5. Antony F, Schimleck LR, Jordan L et al (2014) Growth and wood properties of genetically improved loblolly pine: propagation type comparison and genetic parameters. Can J For Res 44:263–272. doi: 10.1139/cjfr-2013-0163 CrossRefGoogle Scholar
  6. Aquea F, Arce-Johnson P (2008) Identification of genes expressed during early somatic embryogenesis in Pinus radiata. Plant Physiol Biochem 46:559–568. doi: 10.1016/j.plaphy.2008.02.012 CrossRefPubMedGoogle Scholar
  7. Aquea F, Gutierrez F, Medina C, Arce-Johnson P (2008) A novel Otubain-like cysteine protease gene is preferentially expressed during somatic embryogenesis in Pinus radiata. Mol Biol Rep 35:567–573. doi: 10.1007/s11033-007-9124-0 CrossRefPubMedGoogle Scholar
  8. Aronen T (2016) From lab to field-current state of somatic embryogenesis in Scots pine. In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 515–527Google Scholar
  9. Aronen T, Pehkonen T, Ryynänen L (2009) Enhancement of somatic embryogenesis from immature zygotic embryos of Pinus sylvestris. Scand J For Res 24:372–383. doi: 10.1080/02827580903228862 CrossRefGoogle Scholar
  10. Baltunis BS, Brawner JT (2010) Clonal stability in Pinus radiat a across New Zealand and Australia. I. Growth and from traits. New Forest 40:305–322. doi: 10.1007/s11056-010-9201-4 CrossRefGoogle Scholar
  11. Baltunis BS, Wu HX, Dungey HS et al (2009) Comparisons of genetic parameters and clonal value predictions from clonal trials and seedling base population trials of radiate pine. Tree Genet Genomes 5:269–278. doi: 10.1007/s11295-008-0172-y CrossRefGoogle Scholar
  12. Bettinger P, Clutter M, Siry J et al (2009) Broad implications of Southern United States pine clonal forestry on planning and management of forests. Int For Rev 11(3):331–345. doi: 10.1505/ifor.11.3.331 Google Scholar
  13. Bishop-Hurley SL, Gardner RC, Walter C (2003) Isolation and molecular characterization of genes expressed during somatic embryo development in Pinus radiata. Plant Cell Tiss Org 74:267–281. doi: 10.1023/A:1024067703550 CrossRefGoogle Scholar
  14. Breton D, Harvengt L, Trontin J-F et al (2005) High subculture frequency, maltose-based and hormone-free medium sustained early development of somatic embryos in maritime pine. In Vitro Cell Dev-Pl 41:494–504. doi: 10.1079/IVP200567 CrossRefGoogle Scholar
  15. Breton D, Harvengt, L, Trontin et al (2006) Long-term subculture randomly affects morphology and subsequent maturation of early somatic embryos in maritime pine. Plant Cell Tiss Org 87:95–108. doi: 10.1007/s11240-006-9144-9 Google Scholar
  16. Brownfield DL, Todd CD, Stone SL et al (2007) Patterns of storage protein and triacylglycerol accumulation during loblolly pine somatic embryo maturation. Plant Cell Tiss Org 88:217–223. doi: 10.1007/s11240-006-9193-0 CrossRefGoogle Scholar
  17. Burg K, Helmersson A, Bozhkov P, von Arnold S (2007) Developmental and genetic variation in nuclear microsatellite stability during somatic embryogenesis in pine. J Exp Bot 58:687–698. doi: 10.1093/jxb/erl241 CrossRefPubMedGoogle Scholar
  18. Cairney J, Pullman J (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176:511–536. doi: 10.1111/j.1469-8137.2007.02239.x CrossRefPubMedGoogle Scholar
  19. Cairney J, Xu N, MacKay J, Pullman J (2000) Transcript profiling: a tool to assess the development of conifer embryos. In Vitro Cell Dev-Pl 36:155–162. doi: 10.1007/s11627-000-0031-5 Google Scholar
  20. Carneros E, Celestino C, Klimaszewska K et al (2009) Plant regeneration in Stone pine (Pinus pinea L.) by somatic embryogenesis. Plant Cell Tiss Org 98:165–178. doi: 10.1007/s11240-009-9549-3 CrossRefGoogle Scholar
  21. Carson M, Carson S, Te Riini C (2015) Successful varietal forestry with radiate pine in New Zealand. New Zeal J Forestry 60:8–11Google Scholar
  22. Ciavatta VT, Morillon R, Pullman GS et al (2001) An aquaglyceroporin is abundantly expressed early in the development of the suspensor and the embryo proper of loblolly pine. Plant Physiol 127:1556–1567. doi: 10.1104/pp.010793 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ciavatta VT, Egertsdotter U, Clapham D et al (2002) A promoter from the loblolly pine PtNIP1;1 gene directs expression in an early-embryogenesis and suspensor-specific fashion. Planta 215:694–698. doi: 10.1007/s00425-002-0822-5 CrossRefPubMedGoogle Scholar
  24. Cown D, Sorensson CT (2008) Can use of clones improve wood quality? New Zeal J Forestry 52:14–19Google Scholar
  25. Cyr DR, Klimaszewska K (2002) Conifer somatic embryogenesis: II. Applications. Dendrobiology 48:41–49Google Scholar
  26. Daoust G, Klimaszewska K, Plourde D (2009) Somatic embryogenesis, a tool for accelerating the selection and deployment of hybrids of eastern white pine (Pinus strobus) and Himalayan white pine (P. wallichiana) resistant to white pine blister rust (Cronartium ribicola). In: Noshad D, Noh Eun Woon, King J, Sniezko RA (eds) Breeding and Genetic Resources of Five-Needle Pines. Proceedings of the IUFRO Conference 2008, Yangyang, Korea. Korea Forest Research Institute, Seoul 104 p. ISBN 978-89-8176-605-4 (93520)Google Scholar
  27. De-la-Peña C, Nic-Can GI, Galaz-Ávalos RM et al (2015) The role of chromatin modifications in somatic embryogenesis in plants. Frontiers Plant Sci 6:635. doi: 10.3389/fpls.2015.00635 CrossRefGoogle Scholar
  28. de Vega-Bartol JJ, Simões M, Lorenz WW et al (2013) Transcriptomic analysis highlights epigenetic and transcriptional regulation during zygotic embryo development of Pinus pinaster. BMC Plant Biol 13:123. doi: 10.1186/1471-2229-13-123 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Dungey HS, Brawner JT, Burger F et al (2009) A new breeding strategy for Pinus radiata in New Zealand and New South Wales. Silvae Genetica 58:28–38Google Scholar
  30. Elhiti M, Stasolla C, Wang A (2013) Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev-Pl 49:631–642. doi: 10.1007/s11627-013-9547-3 CrossRefGoogle Scholar
  31. El-Kassaby YA, Klápště J (2015) Genomic selection and clonal forestry revival. In: Park YS, Bonga JM (eds) Proceedings of the IUFRO unit 2.09.02 on “Woody plant production integrating genetic and vegetative propagation technologies”, pp 98-100. Sept 8–12, 2014, Vitoria-Gasteiz, Spain. http://www.iufro20902.org. doi: 10.1007/s11056-016-9525-9 Google Scholar
  32. Find JI, Hargreaves CL, Reeves CB (2014) Progress towards initiation of somatic embryogenesis from differentiated tissues of radiata pine (Pinus radiata D. Don) using cotyledonary embryos. In Vitro Cell Dev-Pl 50:190–198. doi: 10.1007/s11627-013-9581-1 CrossRefGoogle Scholar
  33. Fourré J-L (2000) Somaclonal variation and genetic molecular markers in woody plants. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. Kluwer, The Netherlands, pp 425–449. doi: 10.1007/978-94-017-2311-4_18 Google Scholar
  34. Garcia-Mendiguren O, Montalbán IA, Stewart D et al (2015) Gene expression profiling of shoot-derived calli from adult radiata pine and zygotic embryo-derived embryonal masses. PLoS ONE 10:e0128679. doi: 10.1371/journal.pone.0128679 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Gonçalves S, Cairney J, Rodríguez MP et al (2007) PpRab1, a Rab GTPase gene from maritime pine is differentially expressed during embryogenesis. Mol Genet Genomics 278:273–282. doi: 10.1007/s00438-007-0247-8 CrossRefPubMedGoogle Scholar
  36. Gupta PK, Durzan DJ (1985) Shoot multiplication from mature trees of Douglas-fir (Pseudotsuga menziesii) and sugar pine (Pinus lambertiana). Plant Cell Rep 4:177–179. doi: 10.1007/BF00269282 CrossRefPubMedGoogle Scholar
  37. Gupta PK, Durzan DJ (1986) Somatic polyembryogenesis from callus of mature sugar pine embryos. Bio/Technol 4:643–645CrossRefGoogle Scholar
  38. Gupta PK, Durzan DJ (1987) Biotechnology of somatic polyembryogenesis and plantlet regeneration in loblolly pine. Bio/Technol 5:147–151CrossRefGoogle Scholar
  39. Gupta P, Hartle J, Jamruszka A (2014). Advancement of somatic embryogenesis of conifers at Weyerhaeuser. In: 3rd international conference of the IUFRO Working Party 2.09.02, Woody plant production integrating genetic and vegetative propagation technologies, Sept 8–12, Vitoria-Gasteiz, Spain, p 105Google Scholar
  40. Hargreaves C, Menzies M (2007) Organogenesis and cryopreservation of juvenile radiate pine. In: Jain SM, Häggman H (eds) Protocols for Micropropagation of Woody Trees and Fruits. Springer, The Netherlands, p 51–65. doi: 10.1007/978-1-4020-6352-7_6 Google Scholar
  41. Hargreaves CL, Grace LJ, van der Maas SA et al (2005) Comparative in vitro and early nursery performance of adventitious shoots from cryopreserved cotyledons and axillary shoots from epicotyls of the same zygotic embryo of control-pollinated Pinus radiata. Can J For Res 35:2629–2641. doi: 10.1139/x05-178 CrossRefGoogle Scholar
  42. Hargreaves CL, Reeves CB, Find JI et al (2009) Improving initiation, genotype capture, and family representation in somatic embryogenesis of Pinus radiata by a combination of zygotic embryo maturity, media, and explant preparation. Can J For Res 39:1566–1574. doi: 10.1139/X09-082 CrossRefGoogle Scholar
  43. Hargreaves CL, Reeves CB, Find JI et al (2011) Overcoming the challenges of family and genotype representation and early cell line proliferation in somatic embryogenesis from control-pollinated seeds of Pinus radiata. New Zeal J For Sci 41:97–114Google Scholar
  44. Harvengt L, Trontin J-F, Reymond I et al (2001) Molecular evidence of true-to-type propagation of a 3-year-old Norway spruce through somatic embryogenesis. Planta 213:828–832. doi: 10.1007/s004250100628 CrossRefPubMedGoogle Scholar
  45. Hernández I, Carneros E, Pizatrro A et al (2011) Expression pattern of the GRAS gene family during somatic embryogenesis in pine. BMC Proc 5:P136. doi: 10.1186/1753-6561-5-S7-P136 CrossRefPubMedCentralGoogle Scholar
  46. Hosoi Y, Maruyama TE (2012) Plant regeneration from embryogenic tissue of Pinus luchuensis Mayr, an endemic species in Ryukyu Island, Japan. Plant Biotech 29:401–406. doi: 10.5511/plantbiotechnology.12.0530a CrossRefGoogle Scholar
  47. Humánez A, Blasco M, Brisa C et al (2012) Somatic embryogenesis from different tissues of Spanish populations of maritime pine. Plant Cell Tiss Org 111:373–383. doi: 10.1007/s11240-012-0203-0 CrossRefGoogle Scholar
  48. Jones B (2011) Identification, isolation, expression analysis and molecular characterization of nine genes key to late embryogenesis in loblolly pine. Ph.D. Dissertation, School of Biology, Georgia Institute of Technology, 173 pGoogle Scholar
  49. Kim YW, Moon HK (2014) Enhancement of somatic embryogenesis and plant regeneration in Japanese red pine (Pinus densiflora). Plant Biotechnol Rep 8:259–266. doi: 10.1007/s11816-014-0319-2 CrossRefGoogle Scholar
  50. Klimaszewska K, Smith DR (1997) Maturation of somatic embryos of Pinus strobus is promoted by a high concentration of gellan gum. Physiol Plant 100:949–957. doi: 10.1111/j.1399-3054.1997.tb00022.x CrossRefGoogle Scholar
  51. Klimaszewska K, Rutledge RG (2016) Is there potential for propagation of adult spruce trees through somatic embryogenesis? In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 195–210Google Scholar
  52. Klimaszewska K, Bernier-Cardou M, Cyr DR, Sutton BCS (2000) Influence of gelling agents on culture medium gel strength, water availability, tissue water potential, and maturation response in embryogenic cultures of Pinus strobus L. In Vitro Cell Dev-Pl 36:279–286. doi: 10.1007/s11627-000-0051-1 CrossRefGoogle Scholar
  53. Klimaszewska K, Park Y-S, Overton C et al (2001) Optimized somatic embryogenesis in Pinus strobus L. In Vitro Cell Dev-Pl 37:392–399. doi: 10.1079/IVP2001175 CrossRefGoogle Scholar
  54. Klimaszewska K, Morency F, Jones-Overton C, Cooke J (2004) Accumulation pattern and identification of seed storage proteins in zygotic embryos of Pinus strobus and in somatic embryos from different maturation treatments. Physiol Plant 121:682–690. doi: 10.1111/j.1399-3054.2004.00370.x CrossRefGoogle Scholar
  55. Klimaszewska K, Trontin J-F, Becwar MR et al (2007) Recent progress in somatic embryogenesis of four Pinus spp. Tree For Sci Biotechnol 1:11–25. doi: 10.1007/s11627-000-0051-1 Google Scholar
  56. Klimaszewska K, Noceda C, Pelletier G et al (2009) Biological characterization of young and aged embryogenic cultures of Pinus pinaster (Ait.). In Vitro Cell Dev-Pl 45:20–33. doi: 10.1007/s11627-008-9158-6 CrossRefGoogle Scholar
  57. Klimaszewska K, Pelletier G, Overton C et al (2010) Hormonally regulated overexpression of Arabidopsis WUS and conifer LEC1 (CHAP3A) in transgenic white spruce: implications for somatic embryo development and somatic seedling growth. Plant Cell Rep 29:723–734. doi: 10.1007/s00299-010-0859-z CrossRefPubMedGoogle Scholar
  58. Klimaszewska K, Overton C, Stewart D, Rutledge RC (2011) Initiation of somatic embryos and regeneration of plants from primordial shoots of 10-year-old somatic white spruce and expression profiles of 11 genes followed during the tissue culture process. Planta 233:635–647. doi: 10.1007/s00425-010-1325-4 CrossRefPubMedGoogle Scholar
  59. Klimaszewska K, Hargreaves C, Lelu-Walter M-A, Trontin J-F (2016) Advances in conifer somatic embryogenesis since year 2000. In: Germanà MA, Lambardi M (eds) In vitro Embryogenesis in Higher Plants, Methods in Molecular Biology, Chapter 7, vol 1359, Springer Science+Business Media, New York. doi: 10.1007/978-1-4939-3061-6_7 pp 131–162
  60. Krakau UK, Liesebach M, Aronen T et al (2013) Scots pine (Pinus sylvestris L.). In: Pâques LE (ed) Forest tree breeding in europe: current state-of-the-art and perspectives. Managing forest ecosystems 25. Springer Science+Business Media, Dordrecht, pp 267–323. doi: 10.1007/978-94-007-6146-9_6 Google Scholar
  61. Lara-Chavez A, Flinn BS, Egertsdotter U (2011) Initiation of somatic embryogenesis from immature zygotic embryos of Oocarpa pine (Pinus oocarpa Schiede ex Schlectendal). Tree Physiol 31:539–554. doi: 10.1093/treephys/tpr040 CrossRefPubMedGoogle Scholar
  62. Lara-Chavez A, Egertsdotter U, Flinn BS (2012) Comparison of gene expression markers during zygotic and somatic embryogenesis in pine. In Vitro Cell Dev-Pl 48:341–354. doi: 10.1007/s11627-012-9440-5 CrossRefGoogle Scholar
  63. Latutrie M, Aronen T (2013) Long-term cryopreservation of embryogenic Pinus sylvestris cultures. Scand J For Res 28:103–109. doi: 10.1080/02827581.2012.701325 CrossRefGoogle Scholar
  64. Lelu M-A, Bastien C, Drugeault A et al (1999) Somatic embryogenesis and plantlet development in Pinus sylvestris and Pinus pinaster on medium with and without growth regulators. Physiol Plant 105:719–728. doi: 10.1034/j.1399-3054.1999.105417.x CrossRefGoogle Scholar
  65. Lelu-Walter M-A, Bernier-Cardou M, Klimaszewska K (2006) Simplified and improved somatic embryogenesis for clonal propagation of Pinus pinaster (Ait.). Plant Cell Rep 25:767–776. doi: 10.1007/s00299-006-0115-8 CrossRefPubMedGoogle Scholar
  66. Lelu-Walter M-A, Bernier-Cardou M, Klimaszewska K (2008) Clonal plant production from self- and cross-pollinated seed families of Pinus sylvestris (L.) through somatic embryogenesis. Plant Cell Tiss Org 92:31–45. doi: 10.1007/s11240-007-9300-x CrossRefGoogle Scholar
  67. Lelu-Walter M-A, Thompson D, Harvengt L et al (2013) Somatic embryogenesis in forestry with a focus on Europe: state-of-the-art, benefits, challenges and future direction. Tree Genet Genomes 9:883–899. doi: 10.1007/s11295-013-0620-1 CrossRefGoogle Scholar
  68. Lindgren D (2009) A way to utilise the advantages of clonal forestry for Norway spruce? In: Aronen T, Nikkanen T, Tynkkynen T (eds) Vegetative propagation of conifers for enhancing landscaping and tree breeding. Proceedings of the Nordic meeting held in September 10th–11th 2008 at Punkaharju, Finland. Working Papers of the Finnish Forest Research Institutem, vol 114, pp 8–15Google Scholar
  69. Lipavská H, Konrádová H (2004) Somatic embryogenesis in conifers: the role of carbohydrate metabolism. In Vitro Cell Dev-Pl 40:23–30. doi: 10.1079/IVP2003482. doi:  10.1079/IVP2003482 Google Scholar
  70. Lippert D, Zhuang J, Ralph S et al (2005) Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5:461–473. doi: 10.1002/pmic.200400986 CrossRefPubMedGoogle Scholar
  71. Litvay JD, Verma DC, Johnson MA (1985) Influence of loblolly pine (Pinus taeda L.) culture medium and its components on growth and somatic embryogenesis of the wild carrot (Daucus carota L.). Plant Cell Rep 4:325–328. doi: 10.1007/BF00269890 CrossRefPubMedGoogle Scholar
  72. Lstibůrek M, Mullin TJ, El-Kassaby YA (2006) The impact of differential success of somatic embryogenesis on the outcome of clonal forestry programs. I. Initial comparison under multitrait selection. Can J For Res 36:1376–1384. doi: 10.1139/x06-036 CrossRefGoogle Scholar
  73. Lu J, Vahala J, Pappinen A (2011) Involvement of ethylene in somatic embryogenesis in Scots pine (Pinus sylvestris L.). Plant Cell Tiss Org. 107:25–33. doi: 10.1007/s11240-011-9952-4 Google Scholar
  74. Mahdavi-Darvari F, Mohd Noor N, Ismanizan I (2015) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tiss Org 120:407–422. doi: 10.1007/s11240-014-0615-0 CrossRefGoogle Scholar
  75. Marum L (2009) Evaluation of the stability of embryogenic cultures and of emblings of maritime pine (Pinus pinaster Ait.) using molecular markers. Ph.D. Thesis, Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, Portugal, 181 pGoogle Scholar
  76. Marum L, Loureiro J, Rodriguez E et al (2009a) Flow cytometric and morphological analyses of Pinus pinaster somatic embryogenesis. J Biotechnol 143:288–295. doi: 10.1016/j.jbiotec.2009.08.001 CrossRefPubMedGoogle Scholar
  77. Marum L, Rocheta M, Maroco J et al (2009b) Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Rep 28:673–682. doi: 10.1007/s00299-008-0668-9 CrossRefPubMedGoogle Scholar
  78. Maruyama TE, Hosoi Y (2012) Post-maturation treatment improves and synchronizes somatic embryo germination of three species of Japanese pines. Plant Cell Tiss Org 110:45–52. doi: 10.1007/s11240-012-0128-7 CrossRefGoogle Scholar
  79. Miguel C, Marum L (2011) An epigenetic view of plant cells cultured in vitro: somaclonal variation and beyond. J Exp Bot 62:3713–3725. doi: 10.1093/jxb/err155 CrossRefPubMedGoogle Scholar
  80. Miguel CM, Rupps A, Raschke J et al (2016) Impact of molecular studies on somatic embryogenesis development for implementation in conifer multi-varietal forestry. In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 373–421Google Scholar
  81. Montalbán IA, De Diego N, Moncaleán P (2010) Bottlenecks in Pinus radiata somatic embryogenesis: improving maturation and germination. Trees Struct Funct 24:1061–1071. doi: 10.1007/s00468-010-0477-y CrossRefGoogle Scholar
  82. Montalbán IA, De Diego N, Aguirre-Igartua E et al (2011) A combined pathway of somatic embryogenesis and organogenesis to regenerate radiata pine plants. Plant Biotech Rep 5:177–186. doi: 10.1007/s11816-011-0171-6 CrossRefGoogle Scholar
  83. Montalbán IA, Setién-Olarra A, Hargreaves CL, Moncaleán P (2013) Somatic embryogenesis in Pinus halepensis Mill.: an important ecological species from the Mediterranean forest. Trees 27:1339–1351. doi: 10.1007/s00468-013-0882-0 CrossRefGoogle Scholar
  84. Montalbán IA, García-Mendiguren O, Goicoa T et al (2015) Cold storage of initial plant material affects positively somatic embryogenesis in Pinus radiata. New Forest 46:309–317. doi: 10.1007/s11056-014-9457-1 CrossRefGoogle Scholar
  85. Morel A (2014) Molecular physiology of somatic embryo development in maritime pine (Pinus pinaster Ait.): transcriptomic and proteomic approaches. Ph.D. Thesis, University of Orléans, France, 317 pGoogle Scholar
  86. Morel A, Teyssier C, Trontin J-F et al (2014a) Early molecular events involved in Pinus pinaster Ait somatic embryo development under reduced water availability: transcriptomic and proteomic analysis. Physiol Plant 152:184–201. doi: 10.1111/ppl.12158 CrossRefPubMedGoogle Scholar
  87. Morel A, Trontin J-F, Corbineau F et al (2014b) Cotyledonary somatic embryos of Pinus pinaster Ait most closely resemble fresh, maturing cotyledonary zygotic embryos: biological, carbohydrate and proteomic analyses. Planta 240:1075–1095. doi: 10.1007/s00425-014-2125-z CrossRefPubMedGoogle Scholar
  88. Noceda C, Salaj T, Pérez M et al (2009) DNA demethylation and decrease on free polyamines is associated with the embryogenic capacity of Pinus nigra Arn cell culture. Trees 23:1285–1293. doi: 10.1007/s00468-009-0370-8 CrossRefGoogle Scholar
  89. Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Develop 24:2678–2692. doi: 10.1101/gad.1986710 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Oh TJ, Wartell RM, Cairney J, Pullman GS (2008) Evidence for stages-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytol 179:67–80. doi: 10.1111/j.1469-8137.2008.02448.x CrossRefPubMedGoogle Scholar
  91. 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. doi: 10.1007/s11103-008-9289-5 CrossRefPubMedGoogle Scholar
  92. Park Y-S (2002) Implementation of conifer somatic embryogenesis in clonal forestry: technical requirements and deployment considerations. Ann For Sci 59:651–656. doi: 10.1051/forest:2002051 CrossRefGoogle Scholar
  93. Park Y-S, Barrett JD, Bonga JM (1998) Application of somatic embryogenesis in high-value clonal forestry: deployment, genetic control, and stability of cryopreserved clones. In Vitro Cell Dev-Pl 34:231–239. doi: 10.1007/BF02822713 CrossRefGoogle Scholar
  94. Park Y-S, Lelu-Walter M-A, Harvengt L et al (2006) Initiation of somatic embryogenesis in Pinus banksiana, P. strobus, P. pinaster, and P. sylvestris at three laboratories in Canada and France. Plant Cell Tiss Org 86:87–101. doi: 10.1007/s11240-006-9101-7 CrossRefGoogle Scholar
  95. Park S-Y, Klimaszewska K, Park J-Y, Mansfield S (2010) Lodgepole pine: the first evidence of seed-based somatic embryogenesis and the expression of embryogenesis marker genes in shoot bud cultures of adult trees. Tree Physiol 30:1469–1478. doi: 10.1093/treephys/tpq081 CrossRefPubMedGoogle Scholar
  96. Pérez Rodríguez MJ, Suárez MF, Heredia R et al (2006) Expression patterns of two glutamine synthetase genes in zygotic and somatic pine embryos support specific roles in nitrogen metabolism during embryogenesis. New Phytol 169:35–44. doi: 10.1111/j.1469-8137.2005.01551.x CrossRefGoogle Scholar
  97. Plomion C, Bastien C, Bogeat-Triboulot M-B et al (2016) Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci 73: 77–103. doi: 10.1007/s13595-015-0488-3 Google Scholar
  98. Pullman G, Bucalo K (2014) Pine somatic embryogenesis: analyses of seed tissue and medium to improve protocol development. New Forest 45:353–377. doi: 10.1007/s11056-014-9407-y CrossRefGoogle Scholar
  99. Pullman GS, Buchanan M (2008) Identification and quantitative analysis of stage-specific carbohydrates in loblolly pine (Pinus taeda) zygotic embryo and female gametophyte tissues. Tree Physiol 28:985–996. doi: 10.1093/treephys/28.7.985 CrossRefPubMedGoogle Scholar
  100. Pullman GS, Johnson S (2009) Loblolly pine (Pinus taeda) female gametophyte and embryo pH changes during seed development. Tree Physiol 29:829–836. doi: 10.1093/treephys/tpp020 CrossRefPubMedGoogle Scholar
  101. Pullman GS, Johnson S, Peter G et al (2003) Improving loblolly pine somatic embryo maturation: comparison of somatic and zygotic embryo morphology, germination, and gene expression. Plant Cell Rep 21:747–758. doi: 10.1007/s00299-003-0586-9 PubMedGoogle Scholar
  102. Pullman GS, Zeng X, Copeland-Kamp B et al (2015) Conifer somatic embryogenesis: improvements by supplementation of medium with oxidation-reduction agents. Tree Physiol 35:209–224. doi: 10.1093/treephys/tpu117 CrossRefPubMedGoogle Scholar
  103. Ramarosandratana A, Harvengt L, Bouvet A et al (2001) Influence of the embryonal-suspensor mass (ESM) sampling on development and proliferation of maritime pine somatic embryos. Plant Sci 160:473–479. doi: 10.1016/S0168-9452(00)00410-6 CrossRefPubMedGoogle Scholar
  104. Resende MFR, Munoz P, Acosta JJ et al (2012) Accelerating the domestication of trees using genomic selection: accuracy of prediction models across ages and environments. New Phytol 193:617–624. doi: 10.1111/j.1469-8137.2011.03895.x CrossRefPubMedGoogle Scholar
  105. Robinson AR, Dauwe R, Ukrainetz NK et al (2009) Predicting the regenerative capacity of conifer somatic embryogenic cultures by metabolomics. Plant Biotech J 7:952–963. doi: 10.1111/j.1467-7652.2009.00456.x CrossRefGoogle Scholar
  106. Rosvall O, Mullin TJ (2013) Introduction to breeding strategies and evaluation of alternatives. In: Mullin TJ, Lee SJ (eds) Best practice for tree breeding in Europe, Skogforsk, pp. 7–27. ISBN: 978-91-977649-6-4Google Scholar
  107. Salaj T, Fráterová L, Cárach M, Salaj J (2014) The effect of culture medium formulation on Pinus nigra somatic embryogenesis. Dendrobiology 71:119–128. doi: 10.12657/denbio.071.012 Google Scholar
  108. Simões M, Rodrigues A, de Vega-Bartol J et al (2011) Molecular characterization of pine embryogenesis: pursuing the role of a putative non-specific lipid-transfer protein. BMC Proc 5:P71. doi: 10.1186/1753-6561-5-S7-P71 CrossRefPubMedCentralGoogle Scholar
  109. Soresson (2006) Varietal pines boom in the US South. New Zeal J Forestry, August 2006:34-40Google Scholar
  110. Tang W, Newton RJ (2008) Pines. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants. Transgenic forest tree species, vol 9, pp 109–150. Wiley-Blackwell, John Wiley & Sons Ltd. Oxford, UKGoogle Scholar
  111. Tereso S, Zoglauer K, Milhinhos A et al (2007) Zygotic and somatic embryo morphogenesis in Pinus pinaster: comparative histological and histochemical study. Trees Physiol 27:661–669. doi: 10.1093/treephys/27.5.661 CrossRefGoogle Scholar
  112. Trontin J-F, Reymond I, Quoniou S et al (2011) An overview of current achievements and shortcomings in developing Maritime pine somatic embryogenesis and enabling technologies in France. In: Park Y-S, Bonga JM, Park S-Y, Moon H-K (eds) Advances in Somatic Embryogenesis of Trees and Its Application for the Future Forests and Plantations. IUFRO Working Party 2.09.02: Somatic embryogenesis and other clonal propagation methods of forest trees, August 19–21 2010 (Suwon, South Korea), p 100–102Google Scholar
  113. Trontin J-F, Teyssier C, Morel A et al (2016a) Prospects for new variety deployment through somatic embryogenesis in maritime pine. In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 572–606Google Scholar
  114. Trontin J-F, Klimaszewska K, Morel A et al (2016b) Molecular aspects of conifer zygotic and somatic embryo development: a review of genome-wide approaches and recent insights. In: Germana MA, Lambardi M (eds) In vitro Embryogenesis in Higher Plants, Methods in Molecular Biology, Chapter 8, vol. 1359, pp 167–207. Springer Science+Business Media, New York. doi: 10.1007/978-1-4939-3061-6_8 Google Scholar
  115. Trontin J-F, Aronen T, Hargreaves C et al (2016c). International effort to induce somatic embryogenesis in adult pine trees. In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 211–260Google Scholar
  116. Uddenberg D, Valladares S, Abrahamsson M et al (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234:527–539. doi: 10.1186/1753-6561-5-S7-P151 CrossRefPubMedPubMedCentralGoogle Scholar
  117. Valdés AE, Fernández B, Centeno ML (2003) Alterations in endogenous levels of cytokinins following grafting of Pinus radiata support ratio of cytokinins as an index of ageing and vigour. J Plant Physiol 160:1407–1410. doi: 10.1078/0176-1617-00992 CrossRefPubMedGoogle Scholar
  118. Vales T, Feng X, Ge L et al (2007) Improved somatic embryo maturation in loblolly pine by monitoring ABA-responsive gene expression. Plant Cell Rep 26:133–143. doi: 10.1007/s00299-006-0221-7 CrossRefPubMedGoogle Scholar
  119. von Aderkas P, Bonga J, Klimaszewska K, Owens J (1991) Comparison of larch embryogeny in vivo and in vitro. In: Ahuja MR (ed) Woody plant biotechnology, New York Plenum Press, pp. 139–155. doi: 10.1007/978-1-4684-7932-4_15 Google Scholar
  120. von Arnold S, Larsson E, Moschou PN et al (2016) Norway spruce as a model for studying regulation of somatic embryo development in conifers. In: Park Y-S, Bonga JM, Moon H-K (eds) Vegetative Propagation of Forest Trees. National Institute of Forest Science (NIFoS). Seoul, Korea, pp. 351–372Google Scholar
  121. Vuosku J (2011) A matter of life and death—polyamine metabolism during zygotic embryogenesis of pine. Ph.D. Thesis, University of Oulu, Finland, 68 pGoogle Scholar
  122. Vuosku J, Jokela A, Läärä E et al (2006) Consistency of polyamine profiles and expression of arginine decarboxylase in mitosis during zygotic embryogenesis of Scots pine. Plant Physiol 142:1027–1038. doi: 10.1104/pp.106.083030 CrossRefPubMedPubMedCentralGoogle Scholar
  123. Vuosku J, Sutela S, Kestilä J et al (2015) Expression of catalase and retinoblastoma-related protein genes associates with cell death processes in Scots pine zygotic embryogenesis. BMC Plant Biol 15:88. doi: 10.1186/s12870-015-0462-0 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Weng Y, Park YS, Krasowski MJ, Mullin TJ (2011) Allocation of varietal testing efforts for implementing conifer multi-varietal forestry using white spruce as a model species. Ann For Sci 68:129–138. doi: 10.1007/s13595-011-0014-1 CrossRefGoogle Scholar
  125. Wood ER, Bullock BP, Isik F, McKeand SE (2015) Variation in stem taper and growth traits in a clonal trial of loblolly pine. For Sci 61:76–78. doi: 10.5849/forsci.12-068 Google Scholar
  126. Yan G, Menli X, Guifeng W et al (2010) Molecular characterization and expression analysis of PmSERK1 during somatic embryogenesis in masson pine. Mol Plant Breeding 8:53–58Google Scholar
  127. Zhen Y, Zhao Z-Z, Zheng R-H, Shi J (2012) Proteomic analysis of early seed development in Pinus massoniana L. Plant Physiol Biochem 54:97–104. doi: 10.1016/j.plaphy.2012.02.009 CrossRefPubMedGoogle Scholar
  128. Zhu C (2008) Serine palmitoyltransferase and ceramide kinase in embryo development of Loblolly pine. Ph.D. Thesis, School of Biology, Georgia Institute of Technology, 160 pGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.INRA, UR 0588 Unité AméliorationGénétique et Physiologie ForestièresOrléans Cedex 2France
  2. 2.Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S.QuebecCanada
  3. 3.Instituto de Biologia Experimental e Tecnológica (iBET)OeirasPortugal
  4. 4.Instituto de Tecnologia Química e Biológica António XavierUniversidade Nova de Lisboa (ITQB-UNL)OeirasPortugal
  5. 5.Natural Resources Institute Finland (Luke)Bio-based Business and Industry/Forest BiotechnologyPunkaharjuFinland
  6. 6.ScionTe Papa Tipu Innovation ParkRotoruaNew Zealand
  7. 7.FCBAPôle Biotechnologie et Sylviculture Avancée, Campus Forêt-Bois de PierrotonCestasFrance

Personalised recommendations