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Genetic transformation and somaclonal variation in conifers

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Abstract

Production of biotic and abiotic resistant conifers is now primarily accomplished through production of embryo-derived transgenics. Furthermore, gene-drive systems like CRISPR/Cas9 are now providing optimistic outlooks for more precise manipulation of genes in the conifer genome. Nonetheless, experimental guidelines suggest that the careless mass production of propagates might result in severe commercial loss because infrequent mutations sometimes go unnoticed until much later stages in plant development or even in offspring. The micropropagation procedure, types of explants, subculture duration, and PGRs, mostly through hypermethylation, can all contribute to variations in mutation frequency. Furthermore, rapidly dividing cells may undergo mutation in genes essential for regeneration, causing genetic instability in offspring as a result. Monitoring the MET1, KYP, H3K4 JMJ14, HAC1, and sRNAs can potentially highlight epigenetic changes during micropropagation. Decrease in frequency of tissue culture-induced variation may be achieved by applying a cocktail of visual inspections, molecular markers, cytogenetic surveys through Mass/Flow cytometery, the consideration of hypo/hypermethylation, and acetylation percentages, assessing key genes involved in this process, and by further related monitoring strategies. Together, scrutinizing different aspects of conifer tissue culture and genetic transformation would contribute to a better understanding of pivotal elements that can boost higher quality and quantity of conifer production. Furthermore, this can prevent unwanted phenotypic plasticity which may sometimes go unnoticed until very late stages in offspring.

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Abbreviations

AC:

Activated charcoal

AMT:

Agrobacterium-mediated transformation

BA:

6-Benzyladenine

GDM:

Global DNA methylation

GE:

Germinated embryo

IAA:

Indole-3-acetic acid

MSG:

Modified Murashige and Skoog medium

NAA:

Naphthalene acetic acid

PGRs:

Plant growth regulators

SE:

Somatic embryogenesis

TF:

Transcription factor

2, 4-D:

2,4-dichloro-phenoxy-acetic acid

References

  • Ahn C, Tull R, Montello PM, Merkle SA (2015) A clonal propagation and cryopreservation system for Atlantic white cedar (Chamaecyparis thyoides) via somatic embryogenesis. In: Adams JP (ed), Proceedings of the 33rd Southern Forest Tree Improvement Conference. Hot Springs, p 113. http://www.sftic.org

  • Arnholdt-Schmitt B, Herterich S, Neumann K-H (1995) Physiological aspect of genome variability in tissue culture. І. Growth phase-dependent differential DNA methylation of the carrot genome (Dacaus carota L.) during primary culture. Theor Appl Genet 91:809–815

    CAS  PubMed  Google Scholar 

  • Aronen T, Hohtola A, Laukkanen H, Haggman H (1995) Seasonal changes in the transient expression of a 35S CaMV-GUS gene construct introduced into Scots pine buds. Tree Physiol 15:65–70

    Article  CAS  PubMed  Google Scholar 

  • Arya S, Kalia RK, Arya ID (2000) Induction of somatic embryogenesis in Pinus roxburghii Sarg. Plant Cell Rep 19:775–780

    Article  CAS  Google Scholar 

  • Bairu MW, Aremu AO, Staden JV (2011) Somaclonal variation in plants: causes and detection methods. Plant Grow Regul 63:147–173

    Article  CAS  Google Scholar 

  • Banks JA, Masson P, Federoff N (1988) Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev 2:1364–1380

    Article  CAS  PubMed  Google Scholar 

  • Becwar M, Nagmani R, Wann S (1990) Initiation of embryogenic cultures and somatic embryo development in loblolly pine (Pinus taeda). Can J For Res 20:810–817

    Article  Google Scholar 

  • Belmonte MF, Stasolla C (2009) Altered HBK3 expression affects glutathione and ascorbate metabolism during the early phases of Norway spruce (Picea abies) somatic embryogenesis. Plant Physiol Biochem 47:904–911

    Article  CAS  PubMed  Google Scholar 

  • Bishop-Hurley SL, Zabkiewicz RJ, Grace L, Gardner RC, Wagner A, Walter C (2001) Conifer genetic engineering: transgenic Pinus radiata (D. Don) and Picea abies (Karst) plants are resistant to the herbicide Buster. Plant Cell Rep 20:235–243

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Brettell RIS, Dennis ES, Scowcroft WR, Peacock WJ (1986) Molecular analysis of a somaclonal variant of alcohol dehydrogenase. Mol Gen Genet 202:335–344

    Article  Google Scholar 

  • Břiza J, Pavingerova D, Vlasak J, Niedermeierova H (2013) Norway spruce (Picea abies) genetic transformation with modified Cry3A gene of Bacillus thuringiensis. Acta Biochim Pol 60:395–400

    PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Chalupa W (1985) Somatic embryogenesis and plantlet regeneration from cultured immature and mature embryos of Picea abies (L.) Karst. Commun Inst For Cech 14:57–63

    Google Scholar 

  • Chandler VL, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. PNAS 83:1761–1771

    Article  Google Scholar 

  • Cyr DR, Klimaszewska K (2002) Conifer somatic embryogenesis: II. Applications. Dendrobiology 48:41–49

    Google Scholar 

  • D’Amato F (1985) Cytogenetics of plant cell and tissue culture and their regenerates. CRC Crit Rev Plant Sci 3:73–112

    Article  Google Scholar 

  • De Diego JG, David Rodríguez F, Rodríguez Lorenzo JL, Grappin P, Cervantes E (2006) cDNA-AFLP analysis of seed germination in Arabidopsis thaliana identifies transposons and new genomic sequences. J Plant Physiol 163:452–462

    Article  CAS  PubMed  Google Scholar 

  • de Vega-Bartol J, Simões M, Lorenz WW, Rodrigues AS, Alba R, Dean JFD, Miguel CM (2013) Transcriptomic analysis highlights epigenetic and transcriptional regulation during zygotic embryo development of Pinus pinaster. BMC Plant Biol 13:123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Verno LL, Park YS, Bongaand JM, Barrett JD (1990) Somaclonal variation in cryopreserved embryogenic clones of white spruce [Picea glauca (Monech Voss.)]. Plant Cell Rep 18:948–953

    Article  Google Scholar 

  • De Verno LL, Park YS, Bonga JM, Barrett JD (1999) Somaclonal variation in cryopreserved embryogenic clones of white spruce (Picea glauca (Moench)) Voss. Plant Cell Rep 18:948–953

    Article  CAS  Google Scholar 

  • Dennis ES, Brettell RIS, Peacock WJ (1987) A tissue culture induced Adhl null mutant of maize results from a single base change. Mol Gen Genet 210:181–183

    Article  CAS  Google Scholar 

  • Douhovnikoff V, Dodd RS (2015) Epigenetics: a potential mechanism for clonal plant success. Plant Ecol 216:227–233

    Article  Google Scholar 

  • FAO (2007) State of the World’s Forests (2007) Food and Agriculture Organization of the United Nations, Rome, p 44 ISBN 978-92-5-105586-1

  • Fourre JL (2000) Somaclonal variation and genetic molecular markers in woody plants. In: Jain SM, Minocha SC (eds) Molecular biology of woody plants. Kluwer Academic publisher, Netherlands, p 299

    Google Scholar 

  • Fourré JL, Berger P, Niquet L, André P (1997) Somatic embryogenesis and somaclonal variation in Norway spruce: morphogenetic, cytogenetic and molecular approaches. Theor Appl Genet 94:159–169

    Article  Google Scholar 

  • Fraga MF, Centeno ML, Valdés AE, Moncaleán P, Fernández B, Cañal MJ, Rodríguez R (2000) Genomic DNA methylation and polyamines titer as key processes in plant ageing: applications for clonal multiplication of mature Pinus radiata trees. In: Espinel S, Ritter E (eds) Applications of biotechnology to forest genetics. Neiker, Vitoria, pp 495–506

    Google Scholar 

  • Fraga MF, Rodriguez R, Can˜al MJ (2002) Genomic DNA methylation–demethylation during aging and reinvigoration of Pinus radiata. Tree Physiol 22:813–816

    Article  CAS  PubMed  Google Scholar 

  • Fraga HPF, Vieira LN, Heringer AS, Puttkammer CC, Silveira V, Guerra MP (2016) DNA methylation and proteome profiles of Araucaria angustifolia (Bertol.) Kuntze embryogenic cultures as affected by plant growth regulators supplementation. Plant Cell Tissue Organ Cult 125:353–374

    Article  CAS  Google Scholar 

  • Fu C, Li L, Wu W, Li M, Yu X, Yu L (2012) Assessment of genetic and epigenetic variation during long-term Taxus cell culture. Plant Cell Rep 31:1321–1331

    Article  CAS  PubMed  Google Scholar 

  • Gime´nez C, de Garcı´a E, de Enrech NX, Blanca I (2001) Somaclonal variation in banana: cytogenetic and molecular characterization of the somaclonal variant CIEN BTA-03. In Vitro Cell Dev Biol Plant 37:217–222

    Article  Google Scholar 

  • Gime´nez C, Palacios G, Colmenares M (2006) Musa methylated DNA sequences associated with tolerance to Mycosphaerella fijiensis toxins. Plant Mol Biol Rep 24:33–43

    Article  Google Scholar 

  • Giri CC, Shyamkumar B, Anjaneyulu C (2004) Progress in tissue culture, genetic transformation and application of biotechnology to trees: an overview. Trees 18:115–132

    Article  Google Scholar 

  • Godard K-A, Byun-McKay A, Levasseur C, Plant A, Se´guin A, Bohlmann J (2007) Testing of a heterologous, wound- and insect-inducible promoterfor functional genomics studies in conifer defense. Plant Cell Rep 26:2083–2090

    Article  CAS  PubMed  Google Scholar 

  • Grace LJ, Charity JA, Gresham B, Kay N, Walter C (2005) Insect-resistant transgenic Pinus radiata. Plant Cell Rep 24:103–111

    Article  CAS  PubMed  Google Scholar 

  • Grant JE, Cooper PA, Dale TM (2004) Transgenic Pinus radiata from Agrobacterium tumefaciens–mediated transformation of cotyledons. Plant Cell Rep 22:894–902

    Article  CAS  PubMed  Google Scholar 

  • Grant JE, Cooper PA, Dale TM (2015) Genetic transformation of micropropagated shoots of Pinus radiata D. Don. bioRxiv. doi:http://dx.doi.org/10.1101/030080

  • Haisel D, Hofman P, Va´gner M, Lipavska H, Ticha I, Scha¨fer C, Capkova V (2001) Ex vitro phenotype stability if affected by in vitro cultivation. Biol Plant 44:321–324

    Article  CAS  Google Scholar 

  • Hakman I, Fowke LC, von Arnold S, Eriksson T (1985) The development of somatic embryogenesis in tissue cultures initiated from immature embryos of Picea abies (Norway spruce). Plant Sci 38:53–59

    Article  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in post-transcriptional gene silencing in plants. Science 286:950–952

    Article  CAS  PubMed  Google Scholar 

  • Harvengt L, Trontin J-F, Reymond I, Canlet F, Pâques M (2001) Molecular evidence of true-to-type propagation of a 3-year-old Norway spruce through somatic embryogenesis. Planta 213:828–832

    Article  CAS  PubMed  Google Scholar 

  • Hazubska-Przybyl T, Chmielerz P, Michalak M, Dering M, Bojarczuk K (2013) Survival and genetic stability of Picea abies embryogenic cultures after cryopreservation using a pregrowth-dehydration method. Plant Cell Tissue Organ Cult 113:303–313

    Article  CAS  Google Scholar 

  • Hedman H, Zhu T, von Arnold S, Sohlberg JJ (2013) Analysis of the WUSCHELRELATED HOMEOBOX gene family in the conifer Picea abies reveals extensive conservation as well as dynamic patterns. BMC Plant Biol 13:89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helmersson A, von Arnold S, Burg K, Bozhkov PV (2004) High stability of nuclear microsatellite loci during the early stages of somatic embryogenesis in Norway spruce. Tree Physiol 24:1181–1186

    Article  CAS  PubMed  Google Scholar 

  • Helmersson A, Jansson G, Bozhkov PV, Von Arnold S (2008) Genetic variation in microsatellite stability of somatic embryo plants of Picea abies. A case study using six unrelated full-sib families. Scand J For Res 23:2–11

    Article  Google Scholar 

  • Hosoi Y, Maruyama TE (2016) Somatic Embryogenesis in Sawara Cypress (Chamaecyparis pisifera Sieb. et Zucc.). In: Mujib A (ed), Somatic embryogenesis in ornamentals and its applications. Springer, India, p 267. doi:10.1007/978-81-322-2683-3

  • Hosoi Y, Kuramoto N, Maruyama TE (2015) Screening RAPD primers to assess clonal fidelity in somatic embryos of Sawara cypress (Chamaecyparis pisifera Sieb. et Zucc.) and field performance of somatic embryo-derived trees. Plant Biotechnol 32:149–155

    Article  CAS  Google Scholar 

  • Huma´nez A, Blasco M, Brisa C, Segura J, Arrillaga I (2012) Somatic embryogenesis from different tissues of Spanish populations of maritime pine. Plant Cell Tissue Organ Cult 111:373–383

    Article  Google Scholar 

  • Kaeppler S, Phillips R (1993) DNA methylation and tissue culture induced variation in plants. In Vitro Cell Dev Biol Plant 29:125–130

    Article  Google Scholar 

  • Kaeppler SM, Phillips RL, Olhoft P (1998) Molecular basis of heritable tissue culture-induced variation in plants. In: Jain et al (eds) Somaclonal Variation and Induced Mutations in Crop Improvement. Current Plant Science and Biotechnology in Agriculture vol 32, Kluwer Academic Publishers, Dordrecht, Netherlands, pp 465–484

  • Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution in wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. PNAS 97:6603–6607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106

    Article  CAS  PubMed  Google Scholar 

  • Klimaszewska K, Cyr DR (2002) Conifer somatic embryogenesis: I. Development. Dendrobiology 48:31–39

    Google Scholar 

  • Klimaszewska K, Park Y-S, Overton C, Maceacheron I, Bonga JM (2001) Optimized somatic embryogenesis in Pinus strobus L. In Vitro Cell Dev Biol Plant 37:392–399

    Article  Google Scholar 

  • Klimaszewska K, Trontin J-F, Becwar MR, Devillard C, Park Y-S, Lelu-Walter MA (2007) Recent progress in somatic embryogenesis of four Pinus sp. Tree For Sci Biotechnol 1:11–25

    Google Scholar 

  • Klimaszewska K, Noceda C, Pelletier G, Label P, Rodriguez R, Lelu-Walter MA (2009) Biological characterization of young and aged embryogenic cultures of Pinus pinaster (Ait). In vitro Cell Dev Biol Plant 45:20–33

    Article  Google Scholar 

  • Klimaszewska K, Pelletier G, Overton C, Stewart D, Rutledge RG (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

    Article  CAS  PubMed  Google Scholar 

  • Klimaszewska K, Overton C, Stewart D, Rutledge RG (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

    Article  CAS  PubMed  Google Scholar 

  • 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, vol 1359, vol 7. Springer, New York. doi:10.1007/978-1-4939-3061-6_7

    Google Scholar 

  • Komari T, Ishida Y, Hiei Y (2005) Handbook of plant biotechnology. In: Christou P, Klee H (eds), Wiley, Chichester, pp 233–261

  • Konagaya K, Taniguchi T (2016) Somatic embryogenesis and genetic transformation in cupressaceae trees. In: Mujib A (ed), Somatic embryogenesis in ornamental plants and it’s applications. Springer, India, p 267. doi:10.1007/978-81-322-2683-3

  • Konagaya K, Kurita M, Taniguchi T (2013) High-efficiency Agrobacterium-mediated transformation of Cryptomeria japonica D. Don by co-cultivation on filter paper wicks followed by meropenem treatment to eliminate Agrobacterium. Plant Biotechnol 30:523–528

    Article  CAS  Google Scholar 

  • Krutovsky KV, Tretyakova IN, Oreshkova NV, Pak ME, Kvitko OV, Vaganov EA (2014) Somaclonal variation of haploid in vitro tissue culture obtained from Siberian larch (Larix sibirica Ledeb.) megagametophytes for whole genome de novo sequencing. In Vitro Cell Dev Biol Plant 50:655–664

    Article  CAS  Google Scholar 

  • Lachance D, Hamel LP, Pelletier F, Valéro J, Bernier-Cardou M, Chapman K, van Frankenhuyzen K, Séguin A (2007) Expression of a Bacillus thuringiensis cry1Ab gene in transgenic white spruce and its efficacy against the spruce budworm (Choristoneura fumiferana). Tree Genet Genom 3:153–167

    Article  Google Scholar 

  • Lakshmanan V, Venkataramareddy SR, Neelwarne B (2007) Molecular analysis of genetic stability in long-term micropropagated shoots of banana using RAPD and ISSR markers. Electron J Biotechnol 10:106–113

    Article  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation–a noval source of variability from cell culture for plant improvement. Theoretical Appl Genet 60:197–214

    Article  CAS  Google Scholar 

  • Lee H, Moon H-K, Park S-Y (2014) Agrobacterium-mediated Transformation via Somatic Embryogenesis System in Korean fir (Abies koreana Wil.), A Korean Native Conifer. Korean J Plant Res 27:242–248

    Article  Google Scholar 

  • Le-Feuvre R, Triviño C, Sabja AM, Bernier-Cardou M, Moynihan MR, Klimaszewska K (2013) Organic nitrogen composition of the tissue culture medium influences Agrobacterium tumefaciens growth and the recovery of transformed Pinus radiata embryonal masses after cocultivation. In Vitro Cell Dev Biol Plant 49:30–40

    Article  CAS  Google Scholar 

  • Leljak-Levanic D, Bauer N, Mihaljevic S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23:120–127

    Article  CAS  PubMed  Google Scholar 

  • Leljak-Levanić D, Mihaljević S, Jelaska S (2009) Variations in DNA methylation in Picea omorika embryogenic tissue and the ability for embryo maturation. Propag Ornam Plants 9:3–9

    Google Scholar 

  • Lelu MA, Bernier-Cardou M, Klimaszewska K (2006) Simplified and improved somatic embryogenesis for clonal propagation of Pinus pinaster (Ait.). Plant Cell Report 25:767–776

    Article  CAS  Google Scholar 

  • Lelu-Walter M-A, Klimaszewska K, Miguel C, Aronen T, Hargreaves C, Teyssier C, Trontin J-F (2016) Somatic Embryogenesis for More Effective Breeding and Deployment of Improved Varieties in Pinus spp.: Bottlenecks and Recent Advances. In: Loyola-Vargas VM, Ochoa-Alejo N (eds), Somatic Embryogenesis: Fundamental Aspects and Applications. doi:10.1007/978-3-319-33705-0_19

  • Lemmetinen J, Sopanen T (2004) Modification of flowering in forest trees. In: Kumar S, Fladung M (eds) Molecular genetics and breeding of forest trees. The Haworth Press Inc., New York, p 436

    Google Scholar 

  • Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, Zhang XS (2011) DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet 7(8):e1002243. doi:10.1371/journal.pgen.1002243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Zhang S, Wang J (2014) Transcriptome analysis of callus from Picea balfouriana. BMC Genom 15:553

    Article  CAS  Google Scholar 

  • Lida W, Yifan H, Jianjun H (2004) Transgenic forest trees for Insect Resistance. In: Kumar S, Fladung M (eds) Molecular genetics and breeding of forest trees. The Haworth Press Inc., New York, p 436

    Google Scholar 

  • Liu ZL, Han FP, Tan M, Shan XH, Dong YZ, Wang XZ, Fedak G, Hao S, Liu B (2004) Activation of a rice endogenous retrotransposon Tos17 in tissue culture is accompanied by cytosine demethylation and causes heritable alteration in methylation pattern of flanking genomic regions. Theor Appl Genet 109:200–209

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Xu X, Xu Q, Wang S, Xu J (2014) Transgenic tobacco plants expressing PicW gene from Picea wilsonii exhibit enhanced freezing tolerance. Plant Cell Tissue Organ Cult 118:391–400

    Article  CAS  Google Scholar 

  • Loopstra CA, Stomp A-M, Sederoff RR (1990) Agrobacterium-mediated DNA transfer in sugar pine. Plant Mol Biol 15:1–9

    Article  CAS  PubMed  Google Scholar 

  • Loureiro J, Capelo A, Brito G, Rodriguez E, Silva S, Pinto G, Santos C (2007) Micropropagation of Juniperus phoenicea from adult plant explants and analysis of ploidy stability using flow cytometry. Biol Plant 51:7–14

    Article  CAS  Google Scholar 

  • Lowe K, Wu E, Wang N, Hoerster G, Hasting C et al (2016) Morphogenic regulators baby boom and wuschel improve monocot transformation. Plant Cell 28:1998. doi:10.1105/tpc.16.00124

    Article  CAS  PubMed Central  Google Scholar 

  • Mackay J, Dean JFD, Plomion C, Peterson DG, Ca´novas FM, Pavy N, Ingvarsson PK, Savolainen U, Guevara MA, Fluch S, Vinceti B, Abarca D, Dı´az-Sala C, Cervera MT (2012) Towards decoding the conifer giga-genome. Plant Mol Biol 80:555–569

    Article  CAS  PubMed  Google Scholar 

  • Maekawa M, Hase Y, Shikazono N, Tanaka A (2003) Induction of somatic instability in stable yellow leaf mutant of rice by ion beam irradiation. Nucl Instrum Methods Phys Res B 206:579–585

    Article  CAS  Google Scholar 

  • Mageroy MH, Parent G, Germanos G, Gigu_ere I, Delvas N, Maaroufi H, Bauce E, Bohlmann J, Mackay JJ (2015) Expression of the b-glucosidase gene Pgbglu-1 underpins natural resistance of white spruce against spruce budworm. Plant J 81:68–80

    Article  CAS  PubMed  Google Scholar 

  • Mahdavi-Darvari F, Mohd Noor N, Ismanizan I (2015) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tissue Organ Cult 120:407–422

    Article  CAS  Google Scholar 

  • Malabadi RB, Van Staden J (2005) Somatic embryogenesis from vegetative shoot apices of mature trees of Pinus patula. Tree Physiol 25:11–16

    Article  PubMed  Google Scholar 

  • Marum L, Loureiro J, Rodriguez E, Santos C, Oliveira MM, Miguel C (2009a) Flow cytometric and morphological analyses of Pinus pinaster somatic embryogenesis. J Biotechnol 143:288–295

    Article  CAS  PubMed  Google Scholar 

  • Marum L, Rocheta M, Maroco J, Oliveira MM, Miguel C (2009b) Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Rep 28:673–682

    Article  CAS  PubMed  Google Scholar 

  • Maruyama TA, Hosoi Y (2016) Somatic Embryogenesis in Japanese Black Pine (Pinus thunbergii Parl.). In: Mujib A (ed), Somatic embryogenesis in ornamentals and its applications. Springer, India, p 267. doi:10.1007/978-81-322-2683-3

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

    Article  CAS  PubMed  Google Scholar 

  • McAfee BJ, White EE, Pelcher LE, Lapp MS (1993) Root induction in pine (Pinus) and larch (Larix) spp. using Agrobacterium rhizogenes. Plant Cell Tissue Organ Cult 34:53–62

    Article  Google Scholar 

  • Meyer P (2000) Transcriptional transgene silencing and chromatin component. Plant Mol Biol 43:221–234

    Article  CAS  PubMed  Google Scholar 

  • Miguel C, Goncalves S, Tereso S, Marum L, Oliveira MM (2004) Somatic embryogenesis from 20 open-pollinated seed families of Portuguese plus trees of maritime pine. Plant Cell Tissue Organ Cult 76:121–130

    Article  CAS  Google Scholar 

  • 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, pp 373–421

    Google Scholar 

  • Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214

    Article  CAS  PubMed  Google Scholar 

  • Nawrot-Chorabik K (2009) Somaclonal variation in embryogenic cultures of silver fir (Abies alba Mill.). Plant Biosyst 143:377–385

    Article  Google Scholar 

  • Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122

    Article  CAS  PubMed  Google Scholar 

  • Neale DB, Wegrzyn JL, Stevens KA, Zimin AV, Puiu D, Crepeau MW, Cardeno C, Koriabine M, Holtz-Morris AE, Liechty JD (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genom Biol 15:R59

    Article  CAS  Google Scholar 

  • Nic-Can GI, Lo´pez-Torres A, Barredo-Pool F, Wrobel K, Loyola- Vargas VM, Rojas-Herrera R, De-la-Pen˜a C (2013) New insights into somatic embryogenesis: LEAFY COTYLEDON1, BABY BOOM1 and WUSCHEL-RELATED HOMEOBOX4 are epigenetically regulated in Coffea canephora. PLoS One 8(8):e72160. doi:10.1371/journal.pone.0072160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niskanen A-M, Lu J, Seitz S, Keinonen K, von Weissenberg K, Pappinen A (2004) Effect of parent genotype on somatic embryogenesis in Scots pine (Pinus sylvestris). Tree Physiol 24:1259–1265

    Article  PubMed  Google Scholar 

  • No¨el A, Levasseur C, Le VQ, S´eguin A (2005) Enhanced resistance to fungal pathogens in forest trees. Physiol Mol Plant Pathol 67:92–99

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • O’Brien IEW, Smith DR, Gardner RC, Murray BG (1996) Flow cytometric determination of genome size in Pinus. Plant Sci 115:91–99

    Article  Google Scholar 

  • Oono K (1985) Putative homozygous mutations in regenerated plants of rice. Mol Gen Genet 198:377–384

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Parizot B, De Rybel B, Beeckman T (2010) VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome data sets. Plant Physiol 153:34–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pattanavibool R, von Aderkas P, Hanhijarvi A, Simola LK, Bonga JM (1995) Diploidization in megagametaphyte-derived cultures of the gymnosperm Larix decidua. Theor Appl Genet 90:671–674

    Article  CAS  PubMed  Google Scholar 

  • Pavokovic´ D, Krsnik-Rasol M (2012) Protein glycosylation in sugar beet cell line can be influenced by DNA hyper- and hypomethylating agents. Acta Botanica Croatica 71:1–12

    Article  CAS  Google Scholar 

  • Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C (2002) Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–612

    Article  CAS  PubMed  Google Scholar 

  • Piola F, Rohr R, Heizmann P (1999) Rapid detection of genetic variation within and among in vitro propagated cedar (Cedrus libani Loudon) clones. Plant Sci 141:159–163

    Article  CAS  Google Scholar 

  • Pischke MS, Huttlin EL, Hegeman AD, Sussman MR (2006) A transcriptome-based characterization of habituation in plant tissue culture. Plant Physiol 140:1255–1278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prunier J, Verta J-P, MacKay JJ (2016) Conifer genomics and adaptation: at the crossroads of genetic diversity and genome function. New Phytol 209:44–62

    Article  PubMed  CAS  Google Scholar 

  • Pullman GS, Chopra R, Chase K-M (2006) Loblolly pine (Pinus taeda L.) somatic embryogenesis: Improvements in embryogenic tissue initiation by supplementation of medium with organic acids, Vitamins B12 and E. Plant Sci 170:648–658

    Article  CAS  Google Scholar 

  • Pullman GS, Zeng X, Copeland-Kamp B, Crockett J, Lucrezi J, May SW, Bucalo K (2015) Conifer somatic embryogenesis: improvements by supplementation of medium with oxidation–reduction agents. Tree Physiol 35:209–224

    Article  PubMed  Google Scholar 

  • Rabinowicz PD, Palmer LE, May BP, Hemann MT, Lowe SW, McCombie WR, Martienssen RA (2003) Genes and transposons are differentially methylated in pants, but not in mammals. Genom Res 13:2658–2664

    Article  CAS  Google Scholar 

  • Ragonezi C, Klimaszewska K, Castro MR, Lima M, de Oliveira P, Zavattieri MA (2010) Adventitious rooting of conifers: influence of physical and chemical factors. Trees 24:975–992

    Article  CAS  Google Scholar 

  • Renau-Morata B, Nebauer SG, Arrillaga I, Segura J (2005a) Assessment of somaclonal variation in micropropagated shoots of Cedrus: consequences of axillary bud breaking. Tree Genet Genom 1:3–10

    Article  Google Scholar 

  • Renau-Morata B, Ollero J, Arrillagam I, Segura J (2005b) Factor influencing axillary proliferation and adventitious budding in cedar. Tree Physiol 25:477–486

    Article  PubMed  Google Scholar 

  • Reuveni O, Israeli Y, Golubowicz S (1993) Factors influencing the occurrence of somaclonal variations in micropropagated bananas. Acta Hortic 336:357–364

    Article  Google Scholar 

  • Robertson D, Weissinger AK, Ackley R, Glover S, Sederof RR (1992) Genetic transformation of Norway spruce (Picea abies (L.) Karst) using somatic embryo explants by microprojectile bombardment. Plant Mol Biol 19:925–935

    Article  CAS  PubMed  Google Scholar 

  • Rodrı´guez JL, Valledor L, Hasbu´n R, Sa´nchez P, Rodrı´guez R, Can˜ al MJ (2016) The Effects of Hormone Treatment on Epigenetic Marks During Organogenesis in Pinus radiata D. Don Embryos. J Plant Grow Regul 35:97–108

    Article  CAS  Google Scholar 

  • Rodrigues AS, de Vega-Bartol J, Chaves I, Simões M, Lorenz WW, Dean JFD, Bohn A, Miguel CM (2014) Regulators of gene expression in pine embryogenesis. The Third International Conference of the IUFRO unit 2.09.02: Somatic Embryogenesis and Other Vegetative Propagation Technologies. Vitoria-Gasteiz

  • Roth R, Ebert I, Schmidt J (1997) Trisomy associated with loss of maturation capacity in a long-term embryogenic culture of Abies alba. Theor Appl Genet 95:353–358

    Article  Google Scholar 

  • Rutledge RG, Stewart D, Caron S, Overton C, Boyle B, MacKay J, Klimaszewska K (2013) Potential link between biotic defense activation and recalcitrance to induction of somatic embryogenesis in shoot primordia from adult trees of white spruce (Picea glauca). BMC Plant Biol 13:116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salaj T, Matusikova I, Fraterova L, Pirselova B, Salaj J (2011) Regrowth of embryogenic tissues of Pinus nigra following cryopreservation. Plant Cell Tissue Organ Cult 106:55–61

    Article  Google Scholar 

  • Salajova T, Salaj J (1992) Somatic embryogenesis in European black pine (Pinus nigra Arn.). Biol Plant 4:213–218

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Sarmast MK, Salehi H, Khosh-Khui M (2011) Nano silver treatment is effective in reducing bacterial contamination of Araucaria excelsa R. Br. var. glauca explants. Acta Biol Hung 62:477–484

    Article  CAS  PubMed  Google Scholar 

  • Sarmast MK, Salehi H, Khosh-Khui M (2012a) In vitro rooting of Araucaria excelsa R. Br. var. glauca using Agrobacterium rhizogenes. J Cent Eur Agric 13:123–130

    Article  Google Scholar 

  • Sarmast MK, Salehi H, Ramzani Abolimoghadam AA, Niazi A, Khosh-Khui M (2012b) RAPD fingerprint to appraise the genetic fidelity of in vitro propagated Araucaria excelsa R. Br var. glauca plantlets. Mol Biotechnol 50:181–188

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Bryan G, Winfield M, Millam S (2007) Stability of potato (Solanum tuberosum L.) plants regenerated via somatic embryos, axillary bud proliferated shoots, microtubers and true potato seeds: a comparative phenotypic, cytogenetic and molecular assessment. Planta 226:1449–1458

    Article  CAS  PubMed  Google Scholar 

  • Shemer O, Landau U, Candela H, Zemach A, Williams LE (2015) Competency for shoot regeneration from Arabidopsis root explants is regulated by DNA methylation. Plant Sci 238:251–261

    Article  CAS  PubMed  Google Scholar 

  • Shin DI, Podila GK, Huang Y, Karnosky DF (1994) Transgenic larch expressing genes for herbicide and insect resistance. Can J For Res 24:2059–2067

    Article  Google Scholar 

  • Smith MK (1988) A review of factor influencing the genetic stability of micropropagated banana. Fruits 43:219–233

    Google Scholar 

  • Smith DR (1996) Growth medium. US Patent 5,565,355

  • Stasolla C, Yeung EC (1999) Ascorbic acid improves conversion of white spruce somatic embryos. In Vitro Cell Dev Biol Plant 35:316–319

    Article  CAS  Google Scholar 

  • Stasolla C, Kong L, Yeung DC, Thorpe TA (2002) Maturation of somatic embryos in conifers: morphogenesis, physiology, biochemistry, and molecular biology. In Vitro Cell Dev Biol Plant 38:93–105

    Article  CAS  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005a) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Peng X, Newton RJ (2005b) Enhanced tolerance to salt stress in transgenic loblolly pine simultaneously expressing two genes encoding mannitol-1-phosphate dehydrogenase and glucitol-6-phosphate dehydrogenase. Plant Physiol Biochem 43:139–146

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Newton RJ, Lin J, Charles TM (2006a) Expression of a transcription factor from Capsicum annuum in pine calli counteracts the inhibitory effects of salt stress on adventitious shoot formation. Mol Gen Genom 276:242–253

    Article  CAS  Google Scholar 

  • Tang W, Newton RJ, Charles TM (2006b) Plant regeneration through multiple adventitious shoot differentiation from callus cultures of slash pine (Pinus elliottii). J Plant Physiol 163:98–101

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Xiao B, Fei Y (2014) Slash pine genetic transformation through embryo cocultivation with A. tumefaciens and transgenic plant regeneration. In Vitro Cell Dev Biol Plant 50:199–209

    Article  CAS  Google Scholar 

  • Teyssier C, Maury S, Beaufour M, Grondin C, Delaunay A, Le Mette´ C et al (2014) In search of markers for somatic embryo maturation in hybrid larch (Larix × eurolepis): global DNA methylation and proteomic analyses. Physiol Plant 150:271–291

    Article  CAS  PubMed  Google Scholar 

  • Thorpe TA (1985) Application of tissue culture to forest tree improvement. For Chron 61:436–438

    Article  Google Scholar 

  • Tremblay L, Levasseur C, Tremblay FM (1999) Frequency of somaclonal variation in plants of black spruce (Picea mariana, Pinaceae) and white spruce (P. glauca, Pinaceae) derived from somatic embryogenesis and identification of some factors involved in genetic instability. Am J Bot 86:1373–1381

    Article  CAS  PubMed  Google Scholar 

  • Tretyakova IN, Voroshilova EV (2014) Somatic embryogenesis induction in Siberian pine megagametophytes. Russ For Sci 1:50–55

    Google Scholar 

  • Trontin J-F, Teyssier C, Avila C, Debille S, Le Metté C, Lesage-Descauses M-C, Boizot N, Canlet F, Le Provost G, Harvengt L, Plomion C, Label P, Cánovas F, Lelu-Walter M-A (2014) Molecular phenotyping of Maritime pine somatic plants transformed with an RNAi construct targeting cinnamyl alcohol dehydrogenase (CAD). The Third International Conference of the IUFRO unit 2.09.02: Somatic Embryogenesis and Other Vegetative Propagation Technologies. Vitoria-Gasteiz

  • Uddenberg D, Valladares S, Abrahamsson M, Sundstrıˆm J, Sundu¨s-Larsson A, Von Arnold S (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234(3):527–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Us-Camas R, Rivera-Solı´s G, Duarte-Ake´ F, De-la-Pen˜a C (2014) In vitro culture: an epigenetic challenge for plants. Plant Cell Tiss Organ Cult 118:187. doi:10.1007/s11240-014-0482-8

    Article  CAS  Google Scholar 

  • Valledor L, Hasbu´n R, Meijo´n M, Rodrı´guez JL, Santamarı´a E, Viejo M, Berdasco M, Feito I, Fraga MF, Can˜ al MJ, Rodrı´guez R (2007) Involvement of DNA methylation in tree development and micropropagation. Plant Cell Tissue Organ Cult 91:75–86

    Article  CAS  Google Scholar 

  • Vieira LN, Santa-Catarina C, de Freitas Fraga HP et al (2012) Glutathione improves early somatic embryogenesis in Araucaria angustifolia (Bert) O. Kuntze by alteration in nitric oxide emission. Plant Sci 195:80–87

    Article  CAS  Google Scholar 

  • Villalobos-Amador E, Rodríguez-Hernández G, Pérez-Molphe-Balch E (2002) Organogenesis and Agrobacterium rhizogenes-induced rooting in Pinus maximartinezii Rzedowsky and P. pinceana Gordon. Plant Cell Rep 20:779–785

    Article  CAS  Google Scholar 

  • von Aderkas P, Anderson P (1993) Aneuploidy and polyploidization in haploid tissue cultures of Larix decidua. Physiol Plant 88:73–77

    Article  Google Scholar 

  • von Aderkas P, Pattanavibool R, Hristoforoglu K, Ma Y (2003) Embryogenesis and genetic stability in long term megagametophyte-derived cultures of larch. Plant Cell Tissue Organ Cult 75:27–34

    Article  CAS  Google Scholar 

  • von Aderkasm P, Bonga J (2000) Influencing micropropagation and somatic embrygenesis in mature trees by manipulation of phase change, stress and culture environment. Tree Physiol 20:921–928

    Article  Google Scholar 

  • Wagner A, Lloyd Donaldson, Kim H, Phillips L, Flint H, Steward D, Torr K, Koch G, Schmitt U, Ralph J (2009) Suppression of 4-Coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol 149:370–383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner A, Tobimatsu Y, Phillips L, Flint H, Torr K, Donaldson L, Pears L, Ralph J (2011) CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant J 67:119–129

    Article  CAS  PubMed  Google Scholar 

  • Wagner A, Donaldson L, Ralph J (2012a) Lignification and lignin manipulations in conifers. Adv Bot Res 61:37–76

    Article  CAS  Google Scholar 

  • Wagner A, Tobimatsu Y, Goeminne G, Phillips L, Flint H, Steward D, Torr K, Donaldson L, Boerjan W, Ralph J (2012b) Suppression of CCR impacts metabolite profile and cell wall composition in Pinus radiata tracheary elements. Plant Mol Biol 81:105–117

    Article  PubMed  CAS  Google Scholar 

  • Walter C, Charity J, Grace L, Höfig K, Möller R, Wagner A (2002) Gene technologies in Pinus radiata and Picea abies: tools for conifer biotechnology in the 21st century. Plant Cell Tissue Organ Cult 70:3–12

    Article  CAS  Google Scholar 

  • Wang QM, Wang YZ, Sun LL, Gao FZ, Sun W, He J, Gao X, Wang L (2012) Direct and indirect organogenesis of Clivia miniata and assessment of DNA methylation changes in various regenerated plantlets. Plant Cell Rep 31:1283–1296

    Article  CAS  PubMed  Google Scholar 

  • Wei Tang, Tian Y (2003) Transgenic loblolly pine (Pinus taeda L.) plants expressing a modified δ-endotoxin gene of Bacillus thuringiensis with enhanced resistance to Dendrolimus punctatus Walker and Crypyothelea formosicola Staud. J Exp Bot 54:835–844

    Article  CAS  Google Scholar 

  • Wenck AR, Quinn M, Whetten RW, Pullman G, Sederoff RR (1999) High-efficiency Agrobacterium-mediated transformation of Norway spruce (Picea abies) and loblolly pine (Pinus taeda). Plant Mol Biol 39:407–416

    Article  CAS  PubMed  Google Scholar 

  • Whitelaw E, Martin DIK (2001) Retrotransposons as epigenetic mediators of phenotypic variation in mammals. Nat Genet 27:361–365

    Article  CAS  PubMed  Google Scholar 

  • Williams CG (2009) Conifer reproductive biology. Springer, Heidelberg, p 196

    Book  Google Scholar 

  • Williams GE, Maheswaran G (1986) Somatic embryogenesis: factors influencing coordinated behaviour of cells as an embryogenic group. Annu Bot 57:443–462

    Google Scholar 

  • Zavattieri MA, Ragonezi C, Klimaszewska K (2016) Adventitious rooting of conifers: influence of biological factors. Trees. doi:10.1007/s00468-016-1412-7

  • Zhang S, Zhou J, Han S, Yang W, Li W, Wei H, Li X, Oi L (2010) Four abiotic stress-induced miRNA families differentially regulated in the embryogenic and non-embryogenic callus tissues of Larix leptolepis. Biochem Bioph Res Commun 398:355–360

    Article  CAS  Google Scholar 

  • Zhang LF, Li WF, Xu HY, Qi LW, Han SY (2014) Cloning and characterization of four differentially expressed cDNAs encoding NFYA homologs involved in responses to ABA during somatic embryogenesis in Japanese larch (Larix leptolepis). Plant Cell Tissue Organ Cult 117:293–304

    Article  CAS  Google Scholar 

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Acknowledgements

We apologize to colleagues whose original work has not been cited due to the lack of space. Our special thanks to Jenna E. Gallegos (Department of Molecular and Cellular Biology, University of California, Davis) for critical reading the manuscript.

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Sarmast, M.K. Genetic transformation and somaclonal variation in conifers. Plant Biotechnol Rep 10, 309–325 (2016). https://doi.org/10.1007/s11816-016-0416-5

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