Plant Molecular Biology

, Volume 70, Issue 1–2, pp 173–192 | Cite as

Transcriptome analysis during somatic embryogenesis of the tropical monocot Elaeis guineensis: evidence for conserved gene functions in early development

  • Hsiang-Chun Lin
  • Fabienne Morcillo
  • Stéphane Dussert
  • Christine Tranchant-Dubreuil
  • James W. Tregear
  • Timothy John Tranbarger
Article

Abstract

With the aim of understanding the molecular mechanisms underlying somatic embryogenesis (SE) in oil palm, we examined transcriptome changes that occur when embryogenic suspension cells are initiated to develop somatic embryos. Two reciprocal suppression subtractive hybridization (SSH) libraries were constructed from oil palm embryogenic cell suspensions: one in which embryo development was blocked by the presence of the synthetic auxin analogue 2,4-dichlorophenoxyacetic acid (2,4-d) in the medium (proliferation library); and another in which cells were stimulated to form embryos by the removal of 2,4-d from the medium (initiation library). A total of 1867 Expressed Sequence Tags (ESTs) consisting of 1567 potential unigenes were assembled from the two libraries. Functional annotation indicated that 928 of the ESTs correspond to proteins that have either no similarity to sequences in public databases or are of unknown function. Gene Ontology (GO) terms assigned to the two EST populations give clues to the underlying molecular functions, biological processes and cellular components involved in the initiation of embryo development. Macroarrays were used for transcript profiling the ESTs during SE. Hierarchical cluster analysis of differential transcript accumulation revealed 4 distinct profiles containing a total of 192 statistically significant developmentally regulated transcripts. Similarities and differences between the global results obtained with in vitro systems from dicots, monocots and gymnosperms will be discussed.

Keywords

Somatic embryogenesis Oil palm Auxin Transcript profiling 

Abbreviations

2,4-d

2,4-Dichlorophenoxyacetic acid

ARF

ADP-ribosylation factor

EST

Expressed sequence tag

GO

Gene Ontology

GST

Glutathione S-transferases

HCA

Hierarchical cluster analysis

PR

Pathogenesis-related

STM-like

Shootmeristemless-like

SEm

Somatic embryo

SE

Somatic embryogenesis

SSH

Suppression subtractive hybridization

Notes

Acknowledgments

We would like to thank Xavier Sabau for the expertise in cDNA arraying at the Robotics and DNA Sequencing Platform CIRAD, Montpellier Languedoc-Roussillon Genopole (http://www.genopole-montpellier-lr.org), Thierry Beule for helpful technical advice on macroarray methodology, and Ivanna Fuentes for excellent technical assistance with handling the PCR amplification of the EST plasmid inserts. This work was financed by institutional funds from IRD and CIRAD.

Supplementary material

11103_2009_9464_MOESM10_ESM.ppt (1 mb)
Supplementary material 10 (PPT 1034 kb)
11103_2009_9464_MOESM1_ESM.xls (354 kb)
Supplementary material 1 (XLS 353 kb)
11103_2009_9464_MOESM2_ESM.xls (49 kb)
Supplementary material 2 (XLS 49 kb)
11103_2009_9464_MOESM3_ESM.xls (82 kb)
Supplementary material 3 (XLS 82 kb)
11103_2009_9464_MOESM4_ESM.xls (72 kb)
Supplementary material 4 (XLS 72 kb)
11103_2009_9464_MOESM5_ESM.xls (52 kb)
Supplementary material 5 (XLS 52 kb)
11103_2009_9464_MOESM6_ESM.doc (332 kb)
Supplementary material 6 (DOC 332 kb)
11103_2009_9464_MOESM7_ESM.ppt (99 kb)
Supplementary material 7 (PPT 99 kb)
11103_2009_9464_MOESM8_ESM.ppt (106 kb)
Supplementary material 8 (PPT 106 kb)
11103_2009_9464_MOESM9_ESM.ppt (135 kb)
Supplementary material 9 (PPT 135 kb)

References

  1. Abel S, Oeller PW, Theologis A (1994) Early auxin-induced genes encode short-lived nuclear proteins. Proc Natl Acad Sci USA 91:326–330. doi: 10.1073/pnas.91.1.326 PubMedCrossRefGoogle Scholar
  2. Aberlenc-Bertossi F, Noirot M, Duval Y (1999) BA enhances the germination of oil palm somatic embryos derived from embryogenic suspension cultures. Plant Cell Tissue Organ Cult 56:53–57. doi: 10.1023/A:1006241215717 CrossRefGoogle Scholar
  3. Alba R, Fei Z, Payton P, Liu Y, Moore SL, Debbie P, Cohn J, D’Ascenzo M, Gordon JS, Rose JK, Martin G, Tanksley SD, Bouzayen M, Jahn MM, Giovannoni J (2004) ESTs, cDNA microarrays, and gene expression profiling: tools for dissecting plant physiology and development. Plant J 39:697–714. doi: 10.1111/j.1365-313X.2004.02178.x PubMedCrossRefGoogle Scholar
  4. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402. doi: 10.1093/nar/25.17.3389 PubMedCrossRefGoogle Scholar
  5. Bevan M, Bancroft I, Bent E, Love K, Goodman H, Dean C, Bergkamp R, Dirkse W, Van Staveren M, Stiekema W, Drost L, Ridley P, Hudson SA, Patel K, Murphy G, Piffanelli P, Wedler H, Wedler E, Wambutt R, Weitzenegger T, Pohl TM, Terryn N, Gielen J, Villarroel R, De Clerck R, Van Montagu M, Lecharny A, Auborg S, Gy I, Kreis M, Lao N, Kavanagh T, Hempel S, Kotter P, Entian KD, Rieger M, Schaeffer M, Funk B, Mueller-Auer S, Silvey M, James R, Montfort A, Pons A, Puigdomenech P, Douka A, Voukelatou E, Milioni D, Hatzopoulos P, Piravandi E, Obermaier B, Hilbert H, Dusterhoft A, Moores T, Jones JD, Eneva T, Palme K, Benes V, Rechman S, Ansorge W, Cooke R, Berger C, Delseny M, Voet M, Volckaert G, Mewes HW, Klosterman S, Schueller C, Chalwatzis N (1998) Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391:485–488. doi: 10.1038/35140 PubMedCrossRefGoogle Scholar
  6. Buffard-Morel J, Verdeil JL, Pannetier C (1992) Embryogenèse somatique du cocotier (Cocos nucifera L.) à partir de tissus foliaires: étude histologique. Can J Bot 70:735–741Google Scholar
  7. Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 176:511–536. doi: 10.1111/j.1469-8137.2007.02239.x PubMedCrossRefGoogle Scholar
  8. Cairney J, Zheng L, Cowels A, Hsiao J, Zismann V, Liu J, Ouyang S, Thibaud-Nissen F, Hamilton J, Childs K, Pullman GS, Zhang Y, Oh T, Buell CR (2006) Expressed sequence tags from loblolly pine embryos reveal similarities with angiosperm embryogenesis. Plant Mol Biol 62:485–501. doi: 10.1007/s11103-006-9035-9 PubMedCrossRefGoogle Scholar
  9. Chatthai M, Kaukinen KH, Tranbarger TJ, Gupta PK, Misra S (1997) The isolation of a novel metallothionein-related cDNA expressed in somatic and zygotic embryos of Douglas-fir: regulation by ABA, osmoticum, and metal ions. Plant Mol Biol 34:243–254. doi: 10.1023/A:1005839832096 PubMedCrossRefGoogle Scholar
  10. Che P, Love TM, Frame BR, Wang K, Carriquiry AL, Howell SH (2006) Gene expression patterns during somatic embryo development and germination in maize Hi II callus cultures. Plant Mol Biol 62:1–14. doi: 10.1007/s11103-006-9013-2 PubMedCrossRefGoogle Scholar
  11. Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK, Wu HM, Cheung AY (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14:2175–2190. doi: 10.1105/tpc.003038 PubMedCrossRefGoogle Scholar
  12. Clay NK, Nelson T (2005) Arabidopsis thickvein mutation affects vein thickness and organ vascularization, and resides in a provascular cell-specific spermine synthase involved in vein definition and in polar auxin transport. Plant Physiol 138:767–777. doi: 10.1104/pp.104.055756 PubMedCrossRefGoogle Scholar
  13. Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182. doi: 10.1146/annurev.arplant.53.100301.135154 PubMedCrossRefGoogle Scholar
  14. Consortium GO (2008) The Gene Ontology project in 2008. Nucleic Acids Res 36:D440–D444. doi: 10.1093/nar/gkm883 CrossRefGoogle Scholar
  15. Cordewener J, Booij H, Zandt H, Engelen F, Kammen A, Vries S (1991) Tunicamycin-inhibited carrot somatic embryogenesis can be restored by secreted cationic peroxidase isoenzymes. Planta 184:478–486. doi: 10.1007/BF00197895 CrossRefGoogle Scholar
  16. Corley RHV, Tinker PB (2003) The oil palm, 4th edn. Blackwell Science, OxfordGoogle Scholar
  17. de Touchet B, Duval Y, Pannetier C (1991) Plant regeneration from embryogenic suspension culture of oil palm (Elaeis guineensis Jacq). Plant Cell Rep 10:529–532CrossRefGoogle Scholar
  18. Diatchenko L, Lau YF, Campbell AP, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov K, Gurskaya N, Sverdlov ED, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030. doi: 10.1073/pnas.93.12.6025 PubMedCrossRefGoogle Scholar
  19. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:reviews3004.1–3004.10Google Scholar
  20. Dong JZ, Dunstan DI (1996) Expression of abundant mRNAs during somatic embryogenesis of white spruce [Picea glauca (Moench) Voss]. Planta 199:459–466. doi: 10.1007/BF00195740 PubMedCrossRefGoogle Scholar
  21. Duval Y, Engelmann F, Durand-Gasselin T (1995) Somatic embryogenesis in oil palm (Elaeis guineensis Jacq.). Springer, BerlinGoogle Scholar
  22. Feher A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228. doi: 10.1023/A:1024033216561 CrossRefGoogle Scholar
  23. Freeman WM, Robertson DJ, Vrana KE (2000) Fundamentals of DNA hybridization arrays for gene expression analysis. Biotechniques 29:1042–1046, 1048–1055Google Scholar
  24. Gaj MD (2004) Factors influencing somatic embryogenesis induction and plant regeneration with particular reference to Arabidopsis thaliana (L.) Heynh. Plant Growth Regul 43:27–47. doi: 10.1023/B:GROW.0000038275.29262.fb CrossRefGoogle Scholar
  25. Galland R, Randoux B, Vasseur J, Hilbert J (2001) A glutathione S-transferase cDNA identified by mRNA differential display is upregulated during somatic embryogenesis in Cichorium. Biochim Biophys Acta 1522:212–216PubMedGoogle Scholar
  26. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230. doi: 10.1016/S0092-8674(03)00003-5 PubMedCrossRefGoogle Scholar
  27. Gray DJ (2005) Propagation from nonmeristematic tissues: nonzygotic embryogenesis. CRC Press Inc., Boca RatonGoogle Scholar
  28. Groth D, Lehrach H, Hennig S (2004) GOblet: a platform for Gene Ontology annotation of anonymous sequence data. Nucleic Acids Res 32:313–317. doi: 10.1093/nar/gkh406 CrossRefGoogle Scholar
  29. Guo WJ, Meetam M, Goldsbrough PB (2008) Examining the specific contributions of individual Arabidopsis metallothioneins to copper distribution and metal tolerance. Plant Physiol 146:1697–1706. doi: 10.1104/pp.108.115782 PubMedCrossRefGoogle Scholar
  30. Helleboid S, Chapman A, Hendriks T, Inze D, Vasseur J, Hilbert JL (2000a) Cloning of ß-1, 3-glucanases expressed during Cichorium somatic embryogenesis. Plant Mol Biol 42:377–386. doi: 10.1023/A:1006344024877 PubMedCrossRefGoogle Scholar
  31. Helleboid S, Hendriks T, Bauw G, Inze D, Vasseur J, Hilbert JL (2000b) Three major somatic embryogenesis related proteins in Cichorium identified as PR proteins. J Exp Bot 51:1189–1200. doi: 10.1093/jexbot/51.348.1189 PubMedCrossRefGoogle Scholar
  32. Ho CL, Kwan YY, Choi MC, Tee SS, Ng WH, Lim KA, Lee YP, Ooi SE, Lee WW, Tee JM, Tan SH, Kulaveerasingam H, Alwee SS, Abdullah MO (2007) Analysis and functional annotation of expressed sequence tags (ESTs) from multiple tissues of oil palm (Elaeis guineensis Jacq.). BMC Genomics 8:381. doi: 10.1186/1471-2164-8-381 PubMedCrossRefGoogle Scholar
  33. Ikeda-Iwai M, Umehara M, Satoh S, Kamada H (2003) Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 34:107–114. doi: 10.1046/j.1365-313X.2003.01702.x PubMedCrossRefGoogle Scholar
  34. Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-benzylaminopurine and 1-naphthaleneacetic acid treatments. Plant Physiol 137:1250–1260. doi: 10.1104/pp.104.055277 PubMedCrossRefGoogle Scholar
  35. Joosen R, Cordewener J, Supena ED, Vorst O, Lammers M, Maliepaard C, Zeilmaker T, Miki B, America T, Custers J, Boutilier K (2007) Combined transcriptome and proteome analysis identifies pathways and markers associated with the establishment of rapeseed microspore-derived embryo development. Plant Physiol 144:155–172. doi: 10.1104/pp.107.098723 PubMedCrossRefGoogle Scholar
  36. Jouannic S, Argout X, Lechauve F, Fizames C, Borgel A, Morcillo F, Aberlenc-Bertossi F, Duval Y, Tregear J (2005) Analysis of expressed sequence tags from oil palm (Elaeis guineensis). FEBS Lett 579:2709–2714. doi: 10.1016/j.febslet.2005.03.093 PubMedCrossRefGoogle Scholar
  37. Legrand S, Hendriks T, Hilbert JL, Quillet MC (2007) Characterization of expressed sequence tags obtained by SSH during somatic embryogenesis in Cichorium intybus L. BMC Plant Biol 7:27. doi: 10.1186/1471-2229-7-27 PubMedCrossRefGoogle Scholar
  38. Lippert D, Zhuang J, Ralph S, Ellis DE, Gilbert M, Olafson R, Ritland K, Ellis B, Douglas CJ, Bohlmann J (2005) Proteome analysis of early somatic embryogenesis in Picea glauca. Proteomics 5:461–473. doi: 10.1002/pmic.200400986 PubMedCrossRefGoogle Scholar
  39. Low ET, Alias H, Boon SH, Shariff EM, Tan CY, Ooi LC, Cheah SC, Raha AR, Wan KL, Singh R (2008) Oil palm (Elaeis guineensis Jacq.) tissue culture ESTs: identifying genes associated with callogenesis and embryogenesis. BMC Plant Biol 8:62. doi: 10.1186/1471-2229-8-62 PubMedCrossRefGoogle Scholar
  40. Malik MR, Wang F, Dirpaul JM, Zhou N, Polowick PL, Ferrie AM, Krochko JE (2007) Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol 144:134–154. doi: 10.1104/pp.106.092932 PubMedCrossRefGoogle Scholar
  41. Malinowski R, Filipecki M (2002) The role of cell wall in plant embryogenesis. Cell Mol Biol Lett 7:1137–1151PubMedGoogle Scholar
  42. Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300. doi: 10.1105/tpc.105.036723 PubMedCrossRefGoogle Scholar
  43. Pasternak TP, Prinsen E, Ayaydin F, Miskolczi P, Potters G, Asard H, Van Onckelen HA, Dudits D, Feher A (2002) The Role of auxin, pH, and stress in the activation of embryogenic cell division in leaf protoplast-derived cells of alfalfa. Plant Physiol 129:1807–1819. doi: 10.1104/pp.000810 PubMedCrossRefGoogle Scholar
  44. Schrick K, Mayer U, Martin G, Bellini C, Kuhnt C, Schmidt J, Jurgens G (2002) Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J 31:61–73. doi: 10.1046/j.1365-313X.2002.01333.x PubMedCrossRefGoogle Scholar
  45. Seo PJ, Lee AK, Xiang F, Park CM (2008) Molecular and functional profiling of Arabidopsis pathogenesis-related genes: insights into their roles in salt response of seed germination. Plant Cell Physiol 49:334–344. doi: 10.1093/pcp/pcn011 PubMedCrossRefGoogle Scholar
  46. Sharma SK, Millam S, Hedley PE, McNicol J, Bryan GJ (2008) Molecular regulation of somatic embryogenesis in potato: an auxin led perspective. Plant Mol Biol, 16 Jun 2008. Epub ahead of printGoogle Scholar
  47. Singla B, Tyagi AK, Khurana JP, Khurana P (2007) Analysis of expression profile of selected genes expressed during auxin-induced somatic embryogenesis in leaf base system of wheat (Triticum aestivum) and their possible interactions. Plant Mol Biol 65:677–692. doi: 10.1007/s11103-007-9234-z PubMedCrossRefGoogle Scholar
  48. Stasolla C, van Zyl L, Egertsdotter U, Craig D, Liu W, Sederoff RR (2003) The effects of polyethylene glycol on gene expression of developing white spruce somatic embryos. Plant Physiol 131:49–60. doi: 10.1104/pp.015214 PubMedCrossRefGoogle Scholar
  49. Stasolla C, Bozhkov PV, Chu TM, Van Zyl L, Egertsdotter U, Suarez MF, Craig D, Wolfinger RD, Von Arnold S, Sederoff RR (2004) Variation in transcript abundance during somatic embryogenesis in gymnosperms. Tree Physiol 24:1073–1085PubMedGoogle Scholar
  50. Su N, He K, Jiao Y, Chen C, Zhou J, Li L, Bai S, Li X, Deng XW (2007) Distinct reorganization of the genome transcription associates with organogenesis of somatic embryo, shoots, and roots in rice. Plant Mol Biol 63:337–349. doi: 10.1007/s11103-006-9092-0 PubMedCrossRefGoogle Scholar
  51. Takeda H, Kotake T, Nakagawa N, Sakurai N, Nevins DJ (2003) Expression and function of cell wall-bound cationic peroxidase in asparagus somatic embryogenesis. Plant Physiol 131:1765–1774. doi: 10.1104/pp.102.014654 PubMedCrossRefGoogle Scholar
  52. Thibaud-Nissen F, Shealy RT, Khanna A, Vodkin LO (2003) Clustering of microarray data reveals transcript patterns associated with somatic embryogenesis in soybean. Plant Physiol 132:118–136. doi: 10.1104/pp.103.019968 PubMedCrossRefGoogle Scholar
  53. Thomann A, Dieterle M, Genschik P (2005a) Plant CULLIN-based E3s: phytohormones come first. FEBS Lett 579:3239–3245. doi: 10.1016/j.febslet.2005.02.068 PubMedCrossRefGoogle Scholar
  54. Thomann A, Brukhin V, Dieterle M, Gheyeselinck J, Vantard M, Grossniklaus U, Genschik P (2005b) Arabidopsis CUL3A and CUL3B genes are essential for normal embryogenesis. Plant J 43:437–448. doi: 10.1111/j.1365-313X.2005.02467.x PubMedCrossRefGoogle Scholar
  55. Tregear JW, Morcillo F, Richaud F, Berger A, Singh R, Cheah SC, Hartmann C, Rival A, Duval Y (2002) Characterization of a defensin gene expressed in oil palm inflorescences: induction during tissue culture and possible association with epigenetic somaclonal variation events. J Exp Bot 53:1387–1396. doi: 10.1093/jexbot/53.373.1387 PubMedCrossRefGoogle Scholar
  56. Tsuwamoto R, Fukuoka H, Takahata Y (2007) Identification and characterization of genes expressed in early embryogenesis from microspores of Brassica napus. Planta 225:641–652. doi: 10.1007/s00425-006-0388-8 PubMedCrossRefGoogle Scholar
  57. van Zyl L, Bozhkov PV, Clapham DH, Sederoff RR, von Arnold S (2003) Up, down and up again is a signature global gene expression pattern at the beginning of gymnosperm embryogenesis. Gene Expr Patterns 3:83–91. doi: 10.1016/S1567-133X(02)00068-6 PubMedCrossRefGoogle Scholar
  58. Verdeil JL, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252. doi: 10.1016/j.tplants.2007.04.002 PubMedCrossRefGoogle Scholar
  59. Vidali L, Augustine RC, Kleinman KP, Bezanilla M (2007) Profilin is essential for tip growth in the moss Physcomitrella patens. Plant Cell 19:3705–3722. doi: 10.1105/tpc.107.053413 PubMedCrossRefGoogle Scholar
  60. von Arnold S, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249. doi: 10.1023/A:1015673200621 CrossRefGoogle Scholar
  61. Vrinten PL, Nakamura T, Kasha KJ (1999) Characterization of cDNAs expressed in the early stages of microspore embryogenesis in barley (Hordeum vulgare) L. Plant Mol Biol 41:455–463. doi: 10.1023/A:1006383724443 PubMedCrossRefGoogle Scholar
  62. Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B (2003) Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15:612–625. doi: 10.1105/tpc.008433 PubMedCrossRefGoogle Scholar
  63. Xu J, Scheres B (2005) Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity. Plant Cell 17:525–536. doi: 10.1105/tpc.104.028449 PubMedCrossRefGoogle Scholar
  64. Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y (2006) Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 60:167–183. doi: 10.1007/s11103-005-3381-x PubMedCrossRefGoogle Scholar
  65. Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WHIII, Ye ZH (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466. doi: 10.1105/tpc.105.031377 PubMedCrossRefGoogle Scholar
  66. Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5:1411–1423PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Hsiang-Chun Lin
    • 1
    • 4
  • Fabienne Morcillo
    • 2
  • Stéphane Dussert
    • 3
  • Christine Tranchant-Dubreuil
    • 3
  • James W. Tregear
    • 1
  • Timothy John Tranbarger
    • 1
  1. 1.IRD, UMR DIAPC, IRD/CIRAD Palm Development GroupMontpellier Cedex 5France
  2. 2.CIRAD, UMR DIAPC, IRD/CIRAD Palm Development GroupMontpellier Cedex 5France
  3. 3.IRD, UMR DIAPCMontpellier Cedex 5France
  4. 4.ETH ZurichInstitute of Plant ScienceZurichSwitzerland

Personalised recommendations