The Theobroma cacao B3 domain transcription factor TcLEC2plays a duel role in control of embryo development and maturation
Tóm tắt
The Arabidopsis thaliana LEC2 gene encodes a B3 domain transcription factor, which plays critical roles during both zygotic and somatic embryogenesis. LEC2 exerts significant impacts on determining embryogenic potential and various metabolic processes through a complicated genetic regulatory network. An ortholog of the Arabidopsis Leafy Cotyledon 2 gene (AtLEC2) was characterized in Theobroma cacao (TcLEC2). TcLEC2 encodes a B3 domain transcription factor preferentially expressed during early and late zygotic embryo development. The expression of TcLEC2 was higher in dedifferentiated cells competent for somatic embryogenesis (embryogenic calli), compared to non-embryogenic calli. Transient overexpression of TcLEC2 in immature zygotic embryos resulted in changes in gene expression profiles and fatty acid composition. Ectopic expression of TcLEC2 in cacao leaves changed the expression levels of several seed related genes. The overexpression of TcLEC2 in cacao explants greatly increased the frequency of regeneration of stably transformed somatic embryos. TcLEC2 overexpressing cotyledon explants exhibited a very high level of embryogenic competency and when cultured on hormone free medium, exhibited an iterative embryogenic chain-reaction. Our study revealed essential roles of TcLEC2 during both zygotic and somatic embryo development. Collectively, our evidence supports the conclusion that TcLEC2 is a functional ortholog of AtLEC2 and that it is involved in similar genetic regulatory networks during cacao somatic embryogenesis. To our knowledge, this is the first detailed report of the functional analysis of a LEC2 ortholog in a species other then Arabidopsis. TcLEC2 could potentially be used as a biomarker for the improvement of the SE process and screen for elite varieties in cacao germplasm.
Tài liệu tham khảo
Anonymous: Cocoa Market Update: World Cocoa Foundation. 2012, http://worldcocoafoundation.org/wp-content/uploads/Cocoa-Market-Update-as-of-3.20.2012.pdf,
Irizarry H, Goenaga R: Clonal selection in cacao based on early yield performance of grafted trees. J Agric Univ PR. 2000, 8 (3–4): 153-163.
Irizarry H, Rivera E: Early yield of five cacao families at three locations in Puerto Rico. J Agric Univ PR. 1999, 82 (3–4): 167-176.
Cheesman EE, Pound FJ: Uniformity trials on cacao. Trop Agric. 1932, IX (9): 277-287.
Maximova SN, Alemanno L, Young A, Ferriere N, Traore A, Guiltinan MJ: Efficiency, genotypic variability, and cellular origin of primary and secondary somatic embryogenesis of Theobroma cacao L. In Vitro Cell Dev Plant. 2002, 38 (3): 252-259. 10.1079/IVP2001257.
Pence VC, Hasegawa PM, Janick J: Asexual embryogenesis in Theobroma-cacao L. J Am Soc Hortic Sci. 1979, 104 (2): 145-148.
Lopez Baez O, Bollon H, Eskes A, Petiard V: Somatic embryogenesis and plant-regeneration from flower parts of cocoa Theobroma-cacao L. Cr Acad Sci Iii-Vie. 1993, 316 (6): 579-584.
Li ZJ, Traore A, Maximova S, Guiltinan MJ: Somatic embryogenesis and plant regeneration from floral explants of cacao (Theobroma cacao L.) using thidiazuron. In Vitro Cell Dev Plant. 1998, 34 (4): 293-299. 10.1007/BF02822737.
Lotan T, Ohto M, Yee KM, West MA, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ: Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell. 1998, 93 (7): 1195-1205. 10.1016/S0092-8674(00)81463-4.
Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ: LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci U S A. 2001, 98 (20): 11806-11811. 10.1073/pnas.201413498.
Luerssen H, Kirik V, Herrmann P, Misera S: FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J. 1998, 15 (6): 755-764. 10.1046/j.1365-313X.1998.00259.x.
Braybrook SA, Harada JJ: LECs go crazy in embryo development. Trends Plant Sci. 2008, 13 (12): 624-630. 10.1016/j.tplants.2008.09.008.
Braybrook SA, Stone SL, Park S, Bui AQ, Le BH, Fischer RL, Goldberg RB, Harada JJ: Genes directly regulated by LEAFY COTYLEDON2 provide insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci U S A. 2006, 103 (9): 3468-3473. 10.1073/pnas.0511331103.
Ledwon A, Gaj MD: LEAFY COTYLEDON2 gene expression and auxin treatment in relation to embryogenic capacity of Arabidopsis somatic cells. Plant Cell Rep. 2009, 28 (11): 1677-1688. 10.1007/s00299-009-0767-2.
Feeney M, Frigerio L, Cui Y, Menassa R: Following vegetative to embryonic cellular changes in leaves of Arabidopsis overexpressing LEAFY COTYLEDON2. Plant Physiol. 2013, 162 (4): 1881-1896. 10.1104/pp.113.220996.
Santos Mendoza M, Dubreucq B, Miquel M, Caboche M, Lepiniec L: LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett. 2005, 579 (21): 4666-4670. 10.1016/j.febslet.2005.07.037.
Baud S, Mendoza MS, To A, Harscoet E, Lepiniec L, Dubreucq B: WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J. 2007, 50 (5): 825-838. 10.1111/j.1365-313X.2007.03092.x.
Gaj MD, Zhang S, Harada JJ, Lemaux PG: Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta. 2005, 222 (6): 977-988. 10.1007/s00425-005-0041-y.
Guo FD, Liu CL, Xia H, Bi YP, Zhao CZ, Zhao SZ, Hou L, Li FG, Wang XJ: Induced expression of AtLEC1 and AtLEC2 differentially promotes somatic embryogenesis in transgenic tobacco plants. PLoS One. 2013, 8 (8): e71714-10.1371/journal.pone.0071714. doi: 10.1371/journal.pone.0071714
Zuo J, Niu QW, Ikeda Y, Chua NH: Marker-free transformation: increasing transformation frequency by the use of regeneration-promoting genes. Curr Opin Biotechnol. 2002, 13 (2): 173-180. 10.1016/S0958-1669(02)00301-4.
Fujimura T, Komamine A: Involvement of endogenous auxin in somatic embryogenesis in a carrot cell-suspension culture. Z Pflanzenphysiol. 1979, 95 (1): 13-19. 10.1016/S0044-328X(79)80023-9.
Matsuta N: Effect of auxin on somatic embryogenesis from leaf callus in Grape (Vitis-Spp). Jpn J Breed. 1992, 42 (4): 879-883. 10.1270/jsbbs1951.42.879.
Visser C, Qureshi JA, Gill R, Saxena PK: Morphoregulatory role of thidiazuron - substitution of auxin and cytokinin requirement for the induction of somatic embryogenesis in geranium hypocotyl cultures. Plant Physiol. 1992, 99 (4): 1704-1707. 10.1104/pp.99.4.1704.
Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh TF, Fischer RL, Goldberg RB, Harada JJ: Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: Implications for somatic embryogenesis. Proc Natl Acad Sci U S A. 2008, 105 (8): 3151-3156. 10.1073/pnas.0712364105.
Wojcikowska B, Jaskola K, Gasiorek P, Meus M, Nowak K, Gaj MD: LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis. Planta. 2013, 238 (3): 425-440. 10.1007/s00425-013-1892-2.
Karami O, Aghavaisi B, Mahmoudi Pour A: Molecular aspects of somatic-to-embryogenic transition in plants. J Chem Biol. 2009, 2 (4): 177-190. 10.1007/s12154-009-0028-4.
Shen B, Allen WB, Zheng PZ, Li CJ, Glassman K, Ranch J, Nubel D, Tarczynski MC: Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010, 153 (3): 980-987. 10.1104/pp.110.157537.
Tan H, Yang X, Zhang F, Zheng X, Qu C, Mu J, Fu F, Li J, Guan R, Zhang H, Wang G, Zuo J: Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiol. 2011, 156 (3): 1577-1588. 10.1104/pp.111.175000.
Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, Ishiguro S, Nakamura K: An AP2-type transcription factor, WRINKLED1, of Arabidopsis thaliana binds to the AW-box sequence conserved among proximal upstream regions of genes involved in fatty acid synthesis. Plant J. 2009, 60 (3): 476-487. 10.1111/j.1365-313X.2009.03967.x.
Sreenivasulu N, Wobus U: Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol. 2013, 64: 189-217. 10.1146/annurev-arplant-050312-120215.
Romanel EA, Schrago CG, Counago RM, Russo CA, Alves-Ferreira M: Evolution of the B3 DNA binding superfamily: new insights into REM family gene diversification. PLoS One. 2009, 4 (6): e5791-10.1371/journal.pone.0005791.
Argout X, Salse J, Aury JM, Guiltinan MJ, Droc G, Gouzy J, Allegre M, Chaparro C, Legavre T, Maximova SN, Abrouk M, Murat F, Fouet O, Poulain J, Ruiz M: The genome of Theobroma cacao. Nat Genet. 2011, 43 (2): 101-108. 10.1038/ng.736.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol. 1990, 215 (3): 403-410. 10.1016/S0022-2836(05)80360-2.
Motamayor JC, Mockaitis K, Schmutz J, Haiminen N, Livingstone D, Cornejo O, Findley SD, Zheng P, Utro F, Royaert S, Saski C, Jenkins J, Podicheti R, Zhao M, Scheffler B: The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol. 2013, 14 (6): R53-10.1186/gb-2013-14-6-r53.
Mejia LC, Guiltinan MJ, Shi Z, Landherr L, Maximova SN: Expression of designed antimicrobial peptides in Theobroma cacao L. Trees reduces leaf necrosis caused by Phytophthora spp. Acs Sym Ser. 2012, 1095: 379-395.
Patel VK, Shanklin J, Furtek DB: Changes in fatty-acid composition and stearoyl-acyl carrier protein desaturase expression in developing Theobroma-cacao L embryos. Planta. 1994, 193 (1): 83-88.
Costa LM, Gutierrez-Marcos JF, Dickinson HG: More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci. 2004, 9 (10): 507-514. 10.1016/j.tplants.2004.08.007.
Shi Z, Zhang Y, Maximova S, Guiltinan MJ: TcNPR3 from Theobroma cacao functions as a repressor of the pathogen defense response. BMC Plant Biol. 2013, 13: 204-10.1186/1471-2229-13-204.
Harding EW, Tang WN, Nichols KW, Fernandez DE, Perry SE: Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant Physiol. 2003, 133 (2): 653-663. 10.1104/pp.103.023499.
Zheng YM, Ren N, Wang H, Stromberg AJ, Perry SE: Global Identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell. 2009, 21 (9): 2563-2577. 10.1105/tpc.109.068890.
Nambara E, Naito S, Mccourt P: A mutant of arabidopsis which is defective in seed development and storage protein accumulation is a new ABI3 allele. Plant J. 1992, 2 (4): 435-441. 10.1111/j.1365-313X.1992.00435.x.
Monke G, Seifert M, Keilwagen J, Mohr M, Grosse I, Hahnel U, Junker A, Weisshaar B, Conrad U, Baumlein H, Altschmied L: Toward the identification and regulation of the Arabidopsis thaliana ABI3 regulon. Nucleic Acids Res. 2012, 40 (17): 8240-8254. 10.1093/nar/gks594.
Moreno-Risueno MÁ, González N, Díaz I, Parcy F, Carbonero P, Vicente-Carbajosa J: FUSCA3 from barley unveils a common transcriptional regulation of seed-specific genes between cereals and Arabidopsis. Plant J. 2008, 53 (6): 882-894.
Yamamoto-Toyoda A, Kagaya Y, Tanaka S, Tsutsumida K, Kagaya M, Kojima M, Sakakibara H, Hattori T: The mechanism of the regulation of seed maturation by the FUS3 transcription factor revealed by transcriptome analysis. Plant Cell Physiol. 2007, 48: S190-S190.
She MY, Yin GX, Li JR, Li X, Du LP, Ma WJ, Ye XG: Efficient regeneration potential is closely related to auxin exposure time and catalase metabolism during the somatic embryogenesis of immature embryos in Triticum aestivum L. Mol Biotechnol. 2013, 54 (2): 451-460. 10.1007/s12033-012-9583-y.
Delporte F, Muhovski Y, Pretova A, Watillon B: Analysis of expression profiles of selected genes associated with the regenerative property and the receptivity to gene transfer during somatic embryogenesis in Triticum aestivum L. Mol Biol Rep. 2013, 40 (10): 5883-5906. 10.1007/s11033-013-2696-y.
Maximova S, Miller C, Antunez de Mayolo G, Pishak S, Young A, Guiltinan MJ: Stable transformation of Theobroma cacao L. and influence of matrix attachment regions on GFP expression. Plant Cell Rep. 2003, 21 (9): 872-883.
Mejia L, Guiltinan M, Shi Z, Landherr L, Maximova S: Expression of Designed Antimicrobial Peptides in Theobroma Cacao L. Trees Reduces Leaf Necrosis Caused by Phytophthora spp. Acs Sym Ser. 2012, American Chemical Society, 1095: 379-395.
Maximova SN, Marelli JP, Young A, Pishak S, Verica JA, Guiltinan MJ: Over-expression of a cacao class I chitinase gene in Theobroma cacao L. enhances resistance against the pathogen, Colletotrichum gloeosporioides. Planta. 2006, 224: 740-749. 10.1007/s00425-005-0188-6.
Wu G-Z, Xue H-W: Arabidopsis β-ketoacyl-[acyl carrier protein] synthase I is crucial for fatty acid synthesis and plays a role in chloroplast division and embryo development. Plant Cell Online. 2010, 22 (11): 3726-3744. 10.1105/tpc.110.075564.
Moreno-Perez AJ, Venegas-Caleron M, Vaistij FE, Salas JJ, Larson TR, Garces R, Graham IA, Martinez-Force E: Reduced expression of FatA thioesterases in Arabidopsis affects the oil content and fatty acid composition of the seeds. Planta. 2012, 235 (3): 629-639. 10.1007/s00425-011-1534-5.
Lung SC, Weselake RJ: Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids. 2006, 41 (12): 1073-1088. 10.1007/s11745-006-5057-y.
Barry-Etienne D, Bertrand B, Vasquez N, Etienne H: Comparison of somatic embryogenesis-derived coffee (Coffea arabica L.) plantlets regenerated in vitro or ex vitro: morphological, mineral and water characteristics. Ann Bot. 2002, 90 (1): 77-85. 10.1093/aob/mcf149.
Kita Y, Nishizawa K, Takahashi M, Kitayama M, Ishimoto M: Genetic improvement of the somatic embryogenesis and regeneration in soybean and transformation of the improved breeding lines. Plant Cell Rep. 2007, 26 (4): 439-447. 10.1007/s00299-006-0245-z.
Samaj J, Baluska F, Pretova A, Volkmann D: Auxin deprivation induces a developmental switch in maize somatic embryogenesis involving redistribution of microtubules and actin filaments from endoplasmic to cortical cytoskeletal arrays. Plant Cell Rep. 2003, 21 (10): 940-945. 10.1007/s00299-003-0611-z.
Barthet VJ: (n-7) and (n-9) cis-Monounsaturated fatty acid contents of 12 Brassica species. Phytochemistry. 2008, 69 (2): 411-417. 10.1016/j.phytochem.2007.08.016.
Zheng P, Allen WB, Roesler K, Williams ME, Zhang S, Li J, Glassman K, Ranch J, Nubel D, Solawetz W, Bhattramakki D, Llaca V, Deschamps S, Zhong G, Tarczynski M, Shen B: A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet. 2008, 40 (3): 367-372. 10.1038/ng.85.
Shockey JM, Gidda SK, Chapital DC, Kuan JC, Dhanoa PK, Bland JM, Rothstein SJ, Mullen RT, Dyer JM: Tung tree DGAT1 and DGAT2 have nonredundant functions in triacylglycerol biosynthesis and are localized to different subdomains of the endoplasmic reticulum. Plant Cell. 2006, 18 (9): 2294-2313. 10.1105/tpc.106.043695.
Zhang Y: Recombinant expression of plant diacylglycerol acyltransferases from tissues that accumulate saturated fatty acids. 2012, Edmonton, Alberta: University of Alberta
Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32 (5): 1792-1797. 10.1093/nar/gkh340.
Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24 (8): 1596-1599. 10.1093/molbev/msm092.
Lazo GR, Stein PA, Ludwig RA: A DNA transformation-competent Arabidopsis genomic library in Agrobacterium. Biotechnology (N Y). 1991, 9 (10): 963-967. 10.1038/nbt1091-963.
Maximova SN, Dandekar AM, Guiltinan MJ: Investigation of Agrobacterium-mediated transformation of apple using green fluorescent protein: high transient expression and low stable transformation suggest that factors other than T-DNA transfer are rate-limiting. Plant Mol Biol. 1998, 37 (3): 549-559. 10.1023/A:1006041313209.
Shi Z, Maximova SN, Liu Y, Verica J, Guiltinan MJ: Functional analysis of the Theobroma cacao NPR1 gene in Arabidopsis. BMC Plant Biol. 2010, 10: 248-10.1186/1471-2229-10-248.
Stein SE: Estimating probabilities of correct identification from results of mass spectral library searches. Proc Natl Acad Sci U S A. 1997, 5 (4): 316-323.