Transcriptional transitions in Nicotiana benthamiana leaves upon induction of oil synthesis by WRINKLED1 homologs from diverse species and tissues

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Grimberg, Åsa ^a   Carlsson, Anders S ^a   Marttila, Salla ^a   Bhalerao, Rishikesh ^b   Hofvander, Per ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b Umea Plant Science Center   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; TRANSCRIPTION FACTOR; WRINKLED1 PROTEIN, ARABIDOPSIS;

AVENA; CARBOHYDRATE METABOLISM; CYPERUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT LEAF; POPULUS; POTATO; REAL TIME POLYMERASE CHAIN REACTION; TOBACCO; TRANSGENIC PLANT;

ARABIDOPSIS PROTEINS; AVENA; CARBOHYDRATE METABOLISM; CYPERUS; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; POPULUS; REAL-TIME POLYMERASE CHAIN REACTION; SOLANUM TUBEROSUM; TOBACCO; TRANSCRIPTION FACTORS;

EID: 84938591507     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0579-1     Document Type: Article

References (69)

1. Vanhercke T, Wood CC, Stymne S, Singh SP, Green AG. Metabolic engineering of plant oils and waxes for use as industrial feedstocks. Plant Biotechnol J. 2013;11(2):197-210.
2. Carlsson AS, Yilmaz JL, Green AG, Stymne S, Hofvander P. Replacing fossil oil with fresh oil-with what and for what? Eur J Lipid Sci Technol. 2011;113(7):812-31.
3. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, et al. Acyl-lipid metabolism. Arabidopsis Book. 2010;8(10):11.
4. Focks N, Benning C. Wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol. 1998;118(1):91-101.
5. Cernac A, Benning C. WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J. 2004;40(4):575-85.
6. Riechmann JL, Meyerowitz EM. The AP2/EREBP family of plant transcription factors. Biol Chem. 1998;379(6):633-46.
7. Ruuska SA, Girke T, Benning C, Ohlrogge JB. Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell. 2002;14(6):1191-206.
8. Maeo K, Tokuda T, Ayame A, Mitsui N, Kawai T, Tsukagoshi H, et al. 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):476-87.
9. Baud S, Wuilleme S, To A, Rochat C, Lepiniec L. Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J. 2009;60(6):933-47.
10. 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):825-38.
11. Liu J, Hua W, Zhan G, Wei F, Wang X, Liu G, et al. Increasing seed mass and oil content in transgenic Arabidopsis by the overexpression of wri1-like gene from Brassica napus. Plant Physiol Biochem. 2010;48(1):9-15.
12. Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, et al. Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol. 2010;153(3):980-7.
13. Bourgis F, Kilaru A, Cao X, Ngando-Ebongue GF, Drira N, Ohlrogge JB, et al. Comparative transcriptome and metabolite analysis of oil palm and date palm mesocarp that differ dramatically in carbon partitioning. Proc Natl Acad Sci U S A. 2011;108(30):12527-32.
14. FAOSTAT. ProdSTAT, Crops processed. Rome: Food and Agriculture Organization of the United Nations; 2012.
15. Baud S, Lepiniec L. Physiological and developmental regulation of seed oil production. Prog Lipid Res. 2010;49(3):235-49.
16. Troncoso-Ponce MA, Kilaru A, Cao X, Durrett TP, Fan J, Jensen JK, et al. Comparative deep transcriptional profiling of four developing oilseeds. Plant J. 2011;68(6):1014-27.
17. Tranbarger TJ, Dussert S, Joët T, Argout X, Summo M, Champion A, et al. Regulatory mechanisms underlying oil palm fruit mesocarp maturation, ripening, and functional specialization in lipid and carotenoid metabolism. Plant Physiol. 2011;156(2):564-84.
18. Turesson H, Marttila S, Gustavsson KE, Hofvander P, Olsson ME, Bulow L, et al. Characterization of oil and starch accumulation in tubers of Cyperus esculentus var. sativus (Cyperaceae): a novel model system to study oil reserves in nonseed tissues. Am J Bot. 2010;97(11):1884-93.
19. Linssen JPH, Cozijnsen JL, Pilnik W. Chufa (cyperus esculentus): a new source of dietary fibre. J Sci Food Agric. 1989;49(3):291-6.
20. Banas A, Debski H, Banas W, Heneen WK, Dahlqvist A, Bafor M, et al. Lipids in grain tissues of oat (Avena sativa): differences in content, time of deposition, and fatty acid composition. J Exp Bot. 2007;58(10):2463-70.
21. Peterson DM, Wood DF. Composition and structure of high-oil oat. J Cereal Sci. 1997;26(1):121-8.
22. Hayden DM, Rolletschek H, Borisjuk L, Corwin J, Kliebenstein DJ, Grimberg A, et al. Cofactome analyses reveal enhanced flux of carbon into oil for potential biofuel production. Plant J. 2011;67(6):1018-28.
23. Norlin LH. Tall Oil. In: Ullmann's Encyclopedia of Industrial Chemistry. vol. 35: Wiley-VCH Verlag GmbH & Co.; 2002: 583-596.
24. Robards AW, Kidwai A. A comparative study of the ultrastructure of resting and active cambium of Salix fragilis L. Planta. 1969;84:239-49.
25. Druart N, Johansson A, Baba K, Schrader J, Sjodin A, Bhalerao RR, et al. Environmental and hormonal regulation of the activity-dormancy cycle in the cambial meristem involves stage-specific modulation of transcriptional and metabolic networks. Plant J. 2007;50(4):557-73.
26. Sjödin A, Street NR, Sandberg G, Gustafsson P, Jansson S. The Populus Genome Integrative Explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytol. 2009;182(4):1013-25.
27. Mu J, Tan H, Zheng Q, Fu F, Liang Y, Zhang J, et al. LEAFY COTYLEDON1 is a key regulator of fatty acid biosynthesis in Arabidopsis. Plant Physiol. 2008;148(2):1042-54.
28. To A, Joubes J, Barthole G, Lecureuil A, Scagnelli A, Jasinski S, et al. WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell. 2012;24(12):5007-23.
29. Ma W, Kong Q, Arondel V, Kilaru A, Bates PD, Thrower NA, et al. WRINKLED1, a ubiquitous regulator in oil accumulating tissues from Arabidopsis embryos to oil palm mesocarp. PLoS ONE. 2013;8(7):e68887.
30. Fan J, Yan C, Zhang X, Xu C. Dual role for phospholipid:diacylglycerol acyltransferase: enhancing fatty acid synthesis and diverting fatty acids from membrane lipids to triacylglycerol in Arabidopsis leaves. Plant Cell. 2013;25(9):3506-18.
31. Vanhercke T, El Tahchy A, Liu Q, Zhou XR, Shrestha P, Divi UK, et al. Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves. Plant Biotechnol J. 2014;12(2):231-9.
32. Hofer R, Dong L, Andre F, Ginglinger JF, Lugan R, Gavira C, et al. Geraniol hydroxylase and hydroxygeraniol oxidase activities of the CYP76 family of cytochrome P450 enzymes and potential for engineering the early steps of the (seco)iridoid pathway. Metab Eng. 2013;20:221-32.
33. Liu Q, Manzano D, Tanic N, Pesic M, Bankovic J, Pateraki I, et al. Elucidation and in planta reconstitution of the parthenolide biosynthetic pathway. Metab Eng. 2014;23:145-53.
34. Petrie JR, Shrestha P, Mansour MP, Nichols PD, Liu Q, Singh SP. Metabolic engineering of omega-3 long-chain polyunsaturated fatty acids in plants using an acyl-CoA Delta6-desaturase with omega3-preference from the marine microalga Micromonas pusilla. Metab Eng. 2010;12(3):233-40.
35. Wood CC, Petrie JR, Shrestha P, Mansour MP, Nichols PD, Green AG, et al. A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. Plant Biotechnol J. 2009;7(9):914-24.
36. Lonien J, Schwender J. Analysis of metabolic flux phenotypes for two arabidopsis mutants with severe impairment in seed storage lipid synthesis. Plant Physiol. 2009;151(3):1617-34.
37. Baud S, Graham IA. A spatiotemporal analysis of enzymatic activities associated with carbon metabolism in wild-type and mutant embryos of Arabidopsis using in situ histochemistry. Plant J. 2006;46(1):155-69.
38. Lu C, Xin Z, Ren Z, Miquel M, Browse J. An enzyme regulating triacylglycerol composition is encoded by the ROD1 gene of Arabidopsis. Proc Natl Acad Sci. 2009;106(44):18837-42.
39. Nandi A, Welti R, Shah J. The Arabidopsis thaliana dihydroxyacetone phosphate reductase gene SUPPRESSSOR OF FATTY ACID DESATURASE DEFICIENCY1 is required for glycerolipid metabolism and for the activation of systemic acquired resistance. Plant Cell. 2004;16(2):465-77.
40. Wei Y, Periappuram C, Datla R, Selvaraj G, Zou J. Molecular and biochemical characterizations of a plastidic glycerol-3-phosphate dehydrogenase from Arabidopsis. Plant Physiol Biochem. 2001;39(10):841-8.
41. Kawai H, Ishikawa T, Mitsui T, Koreeda S, Yamada-Kawai M, Ohnishi J.-I. Arabidopsis glycerol-3-phosphate permease 4 is localized in the plastids and involved in the accumulation of seed oil. Plant Biotechnology. 2014;31(2):159-65.
42. Pouvreau B, Baud S, Vernoud V, Morin V, Py C, Gendrot G, et al. Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol. 2011;156(2):674-86.
43. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ. An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE. 2007;2(8):e718.
44. Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L. Storage reserve accumulation in arabidopsis: metabolic and developmental control of seed filling. The Arabidopsis Book. 2008;6:e0113.
45. Weber AP, Linka N. Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol. 2011;62:53-77.
46. Flugge UI, Hausler RE, Ludewig F, Gierth M. The role of transporters in supplying energy to plant plastids. J Exp Bot. 2011;62(7):2381-92.
47. Da Silva PMFR, Eastmond PJ, Hill LM, Smith AM, Rawsthorne S. Starch metabolism in developing embryos of oilseed rape. Planta. 1997;203(4):480-7.
48. Lu S, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA. Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J. 2009;59(4):553-64.
49. Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D. Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell. 2000;12(10):2001-8.
50. Pascal S, Bernard A, Sorel M, Pervent M, Vile D, Haslam RP, et al. The Arabidopsis cer26 mutant, like the cer2 mutant, is specifically affected in the very long chain fatty acid elongation process. Plant J. 2013;73(5):733-46.
51. Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A. Molecular characterization of the CER1 gene of arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell. 1995;7(12):2115-27.
52. Panikashvili D, Shi JX, Schreiber L, Aharoni A. The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol. 2009;151(4):1773-89.
53. Li Y, Beisson F, Koo AJK, Molina I, Pollard M, Ohlrogge J. Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci. 2007;104(46):18339-44.
54. Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, Tang X, et al. Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J. 2004;23(14):2903-13.
55. Eastmond PJ. Glycerol-insensitive Arabidopsis mutants: gli1 seedlings lack glycerol kinase, accumulate glycerol and are more resistant to abiotic stress. Plant J. 2004;37(4):617-25.
56. Eastmond PJ, Dennis DT, Rawsthorne S. Evidence that a malate/inorganic phosphate exchange translocator imports carbon across the leucoplast envelope for fatty acid synthesis in developing castor seed endosperm. Plant Physiol. 1997;114(3):851-6.
57. Neuhaus HE, Emes MJ. Nonphotosynthetic metabolism in plastids. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:111-40.
58. Schaffer JE. Lipotoxicity: when tissues overeat. Curr Opin Lipidol. 2003;14(3):281-7.
59. Eastmond PJ, van Dijken AJ, Spielman M, Kerr A, Tissier AF, Dickinson HG, et al. Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J. 2002;29(2):225-35.
60. Gomez LD, Baud S, Gilday A, Li Y, Graham IA. Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J. 2006;46(1):69-84.
61. Gomez LD, Baud S, Graham IA. The role of trehalose-6-phosphate synthase in Arabidopsis embryo development. Biochem Soc Trans. 2005;33(Pt 1):280-2.
62. Bao F, Azhakanandam S, Franks RG. SEUSS and SEUSS-LIKE transcriptional adaptors regulate floral and embryonic development in Arabidopsis. Plant Physiol. 2010;152(2):821-36.
63. Jolivet P, Roux E, d'Andrea S, Davanture M, Negroni L, Zivy M, et al. Protein composition of oil bodies in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem. 2004;42(6):501-9.
64. Liu D, Shi L, Han C, Yu J, Li D, Zhang Y. Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS ONE. 2012;7(9):e46451.
65. Santos-Mendoza M, Dubreucq B, Baud S, Parcy F, Caboche M, Lepiniec L. Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. Plant J. 2008;54(4):608-20.
66. Bligh EG, Dyer WJ. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959;37(8):911-7.
67. Leonova S, Shelenga T, Hamberg M, Konarev AV, Loskutov I, Carlsson AS. Analysis of oil composition in cultivars and wild species of oat (Avena sp.). J Agric Food Chem. 2008;56(17):7983-91.
68. Leonova S, Grimberg Å, Marttila S, Stymne S, Carlsson AS. Mobilization of lipid reserves during germination of oat (Avena sativa L.), a cereal rich in endosperm oil. J Exp Bot. 2010;61(11):3089-99.
69. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, et al. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 2012;40(D1):D1202-10.