An unusual abscisic acid and gibberellic acid synergism increases somatic embryogenesis, facilitates its genetic analysis and improves transformation in Medicago truncatula

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Nolan, Kim E ^a   Song, Youhong ^a   Liao, Siyang ^a   Saeed, Nasir A ^a,b   Zhang, Xiyi ^a   Rose, Ray J ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b NATIONAL INSTITUTE FOR BIOTECHNOLOGY AND GENETIC ENGINEERING NIBGE   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; GIBBERELLIC ACID; GIBBERELLIN; PHYTOHORMONE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BARREL MEDIC; CONTROLLED STUDY; DOWN REGULATION; GA2OX GENE; GENE EXPRESSION REGULATION; GENETIC SCREENING; HORMONE ACTION; NONHUMAN; PICKLE GENE; PLANT DEVELOPMENT; PLANT GENE; PLANT GENETICS; PLANT REGENERATION; REGULATOR GENE; REPRESSOR GENE; SOMATIC EMBRYOGENESIS; DRUG POTENTIATION; GENE EXPRESSION; GENETIC TRANSFORMATION; GENETICS; METABOLISM; PHYSIOLOGY;

ABSCISIC ACID; DRUG SYNERGISM; GENE EXPRESSION; GENES, PLANT; GIBBERELLINS; MEDICAGO TRUNCATULA; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT SOMATIC EMBRYOGENESIS TECHNIQUES; TRANSFORMATION, GENETIC;

EID: 84903287455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099908     Document Type: Article

References (57)

1. Halperin W (1964) Morphogenetic studies with partially synchronized cultures of carrot embryos. Science 146: 408-410.
2. Dudits D, Bögre L, Györgyey J (1991) Molecular and cellular approaches to the analysis of plant embryo development from somatic cells in vitro. J Cell Sci 99: 475-484.
3. Nolan KE, Rose RJ, Gorst JR (1989) Regeneration of Medicago truncatula from tissue culture: increased somatic embryogenesis from regenerated plants. Plant Cell Rep 8: 278-281.
4. Rose RJ, Nolan KE, Bicego L (1999) The development of the highly regenerable seed line Jemalong 2HA for transformation of Medicago truncatula - Implications for regenerability via somatic embryogenesis. J Plant Physiol 155: 788-791. (Pubitemid 30044603)
5. Rose RJ, Wang X-D, Nolan KE, Rolfe BG (2006) Root meristems in Medicago truncatula tissue culture arise from vascular-derived procambial-like cells in a process regulated by ethylene. J Exp Bot 57: 2227-2235. (Pubitemid 44289118)
6. Fehér A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue & Organ Cult 74: 201-228. (Pubitemid 36784822)
7. Nolan KE, Saeed NA, Rose RJ (2006) The stress kinase gene MtSK1 in Medicago truncatula with particular reference to somatic embryogenesis. Plant Cell Rep 25: 711-722. (Pubitemid 44124473)
8. Kamada H, Ishikawa K, Saga H, Harada H (1993) Induction of somatic embryogenesis in carrot by osmotic stress. Plant Tiss Cult Lett 10: 38-44.
9. Nishiwaki M, Fujino K, Koda Y, Masuda K, Kikuta Y (2000) Somatic embryogenesis induced by the simple application of abscisic acid. Planta 211: 756-759.
10. Nolan KE, Rose RJ (1998) Plant regeneration from cultured Medicago truncatula with particular reference to abscisic acid and light treatments. Aust J Bot 46: 151-160. (Pubitemid 28205435)
11. Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459: 1071-1078.
12. Zheng Q, Zheng Y, Perry SE (2013) AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and soybean in part by the control of ethylene biosynthesis and response. Plant Physiol 161: 2113-2127.
13. Mantiri FR, Kurdyukov S, Lohar DP, Sharapova N, Saeed NA, et al. (2008) The transcription factor MtSERF1 of the ERF subfamily identified by transcriptional profiling is required for somatic embryogenesis induced by auxin plus cytokinin in Medicago truncatula. Plant Physiol 146: 1622-1636. (Pubitemid 352844063)
14. Wang H, Caruso LV, Downie AB, Perry SE (2004) The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16: 1206-1219. (Pubitemid 38641515)
15. Tokuji Y, Kuriyama K (2003) Involvement of gibberellin and cytokinin in the formation of embryogenic cell clumps in carrot (Daucus carota). J Plant Physiol 160: 133-141. (Pubitemid 36242501)
16. Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277: 91- 94.
17. 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. (Pubitemid 36524309)
18. Su YH, Zhao XY, Liu YB, Zhang CL, O'Neill SD, et al. (2009) Auxin-induced WUS expression is essential for embryonic stem cell renewal during somatic embryogenesis in Arabidopsis. Plant J 59: 448-460.
19. Rose RJ, Mantiri FR, Kurdyukov S, Chen S-G, Wang X-D, et al. (2010) The developmental biology of somatic embryogenesis. In: Pua EC, Davey MR, editors. Plant developmental biology: biotechnology perspectives. Volume 2. Berlin: Springer-Verlag. 3-26.
20. Gaj MD, Trojanowska A, Ujzak A, Me?drek M, Koziol A, et al. (2006) Hormone-response mutants of Arabidopsis thaliana (L.) Heynh. impaired in somatic embryogenesis. Plant Growth Regul 49: 183-197. (Pubitemid 46237455)
21. Chen S-K, Kurdyukov S, Kereszt A, Wang X-D, Gresshoff PM, et al. (2009) The association of homeobox gene expression with stem cell formation and morphogenesis in cultured Medicago truncatula. Planta 230: 827-840.
22. Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, et al. (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127: 803-816. (Pubitemid 33112143)
23. Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133: 218-230. (Pubitemid 37144095)
24. Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends in Plant Sci 13: 624-630.
25. Curaba J, Moritz T, Blervaque R, Parcy F, Raz V, et al. (2004) AtGA3ox2, a key gene responsible for bioactive gibberellin synthesis, is regulated during embryogenesis by LEAFCOTYLEDON2 and FUSCA3 in Arabidopsis. Plant Physiol 136: 3660-3669. (Pubitemid 41075804)
26. Weis D, Ori N (2007) Mechanism of cross-talk between gibberellin and other hormones. Plant Physiol 144: 1240-1246.
27. Song Y, Nolan KE, Rose RJ (2013) Stable transformation of Medicago truncatula cv. Jemalong for gene analysis using Agrobacterium tumefaciens. In: Rose RJ, editor, Legume genomics, methods and protocols, methods in molecular biology series 1069. New York: Humana Press, Springer. 203-214.
28. Wang X-D, Song Y, Sheahan MB, Garg ML, Rose RJ (2012) From embryo sac to oil and protein bodies: embryo development in the model legume Medicago truncatula. New Phytol 193: 327-338.
29. Mantiri FR, Kurdyukov S, Chen S-K, Rose RJ (2008) The transcription factor MtSERF1 may function as a nexus between stress and development in somatic embryogenesis in Medicago truncatula. Plant Signal & Behav, 37: 498-500.
30. Thomas MR, Rose RJ, Nolan KE (1992) Genetic transformation of Medicago truncatula using Agrobacterium with genetically modified Ri and disarmed Ti plasmids. Plant Cell Rep 11: 113-117.
31. Wang JH, Rose RJ, Donaldson BI (1996) Agrobacterium-mediated transformation and expression of foreign genes in Medicago truncatula . Aust J Plant Physiol 23: 265-270.
32. Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn.) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the gus reporter gene. Plant Cell Rep 15: 305-310.
33. Yamada T, Takagi K, Ishimoto M (2012) Recent advances in soybean transformation and their application to molecular breeding and genomic analysis. Breeding Sci 61: 480-494.
34. Nolan KE, Kurdyukov S, Rose RJ (2009) Expression of the Somatic Embryogenesis Receptor-Like Kinase 1 (SERK1) gene is associated with developmental change in the life cycle of the model legume Medicago truncatula. J Exp Bot 60: 1759-1771.
35. Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21: 3493-3505.
36. Pasternak TP, Ötvös K, Domoki D, Fehér A (2007) Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin. Plant Growth Regul 51: 109-117.
37. Rose RJ, Sheahan MB, Tiew TW-Y (2013) Connecting stress to development in the induction of somatic embryogenesis. In: Aslam J, Srivastava PS, Sharma MP, Somatic embryogenesis and gene expression. New Delhi: Narosa Publishing House. 146-165.
38. Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5: 388-395. (Pubitemid 34961400)
39. Henderson JT, Li HC, Rider SD, Mordhorst AP, Romero-Severson J, et al. (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134: 995-1005.
40. Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5: 523-530. (Pubitemid 32099970)
41. Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, et al. (2008) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20: 2420-2436. (Pubitemid 352844608)
42. Lotan T, Ohto M, Yee KM, West MAL, Lo R, et al. (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195-1205.
43. Zhang H, Bishop B, Ringenberg W, Muir WM, Ogas J (2012) The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27. Plant Physiol 159: 418-432.
44. Zhang H, Rider Jr SD, Henderson JT, Fountain N, Chuang K, et al. (2008) The CHD3 remodeler PICKLE promotes trimethylation of histone H3 Lysine 27. J Biol Chem 283: 22637-22648.
45. Zheng Q, Zheng Y, Perry SE (2013) Decreased GmAGL1 expression and reduced ethylene synthesis may contribute to reduced somatic embryogenesis in a poorly embryogenic cultivar of Glycine max . Plant Signal Behav 8: e25422.
46. Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, et al. (2006) Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA 103: 3468-3473. (Pubitemid 43346492)
47. Gliwicka M, Nowak K, Balazadeh S, Mueller-Roeber B, Gaj MD (2013) Extemsive modulation of the transcription factor transcriptome during somatic embryogenesis in Arabidopsis thaliana. Plos one 8: e69261.
48. Elhiti M, Tahir M, Gulden RH, Khamis K, Stassola C (2010) Modulation of embryo-forming capacity in culture through the expression of Brassica genes involved in the regulation of the shoot apical meristem. J Exp Bot 61: 4069- 4085.
49. Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP, et al. (2004) VEIDase is a principal caspase-like activity involverd in plant programmed cell death and essential for embryonc pattern formation. Cell Death and Differentiation 11: 175-182. (Pubitemid 38159641)
50. 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 68: 185-201.
51. Piyatrakul P, Putrano R-A, Martin F, Rio M, Dessailly F, et al. (2012) Some ethylene biosynthesis and AP2/ERF genes reveal a specific pattern of expression during somatic embryogenesis in Hevea brasiliensis. BMC Plant Biology 12: 244.
52. Nolan KE, Rose RJ (2010) Plant regeneration - somatic embryogenesis. In: Davey MR, Anthony P, editors, Plant cell culture. essential methods. Chichester U.K: John Wiley & Sons Ltd. 39-59.
53. Song Y (2013) Genetic regulation of embryo development and formation of seed storage products in the legume model Medicago truncatula. PhD thesis. The University of Newcastle. Callaghan, NSW, Australia.
54. Marino D, Andrio E, Danchin EGJ, Oger E, Gucciardo S, et al. (2011) A Medicago truncatula NADPH oxidase is involved in symbiotic nodule functioning. New Phytol 189: 580-592.
55. Verdier J, Kakar K, Gallardo K, Le Signor C, Aubert G., et al. (2008) Gene expression profiling of M. truncatula transcription factors identifies putative regulators of grain legume seed filling. Plant Mol Biol 67: 567-580.
56. Ramakers C, Ruijter JM, Lekanne Deprez RH, Moorman AFM (2003): Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Lett 339: 62-66. (Pubitemid 36263221)
57. Pfaffl MW (2001): A new mathematical model for relative quantification in realtime RT-PCR. Nucleic Acids Res 29: e45.