Oil biosynthesis in a basal angiosperm: Transcriptome analysis of Persea Americana mesocarp

BMC Plant Biology

Volumn 15, Issue 1, 2015, Pages

  Kilaru, Aruna ^a,b,c   Cao, Xia ^c,d   Dabbs, Parker B ^a   Sung, Ha Jung ^a   Rahman, Md Mahbubur ^a,b   Thrower, Nicholas ^c   Zynda, Greg ^e   Podicheti, Ram ^e   Ibarra Laclette, Enrique ^f,g   Herrera Estrella, Luis ^f   Mockaitis, Keithanne ^h   Ohlrogge, John B ^c  

^a EAST TENNESSEE STATE UNIVERSITY   (United States)

^b East Tennessee State University   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d BAYER CROPSCIENCE   (United States)

^e INDIANA UNIVERSITY   (United States)

^f DEPARTAMENTO DE INGENIERÍA GENÉTICA   (Mexico)

^g INSTITUTO DE ECOLOGÍA   (Mexico)

^h INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRASSICA NAPUS; DICOTYLEDONEAE; ELAEIS; LILIOPSIDA; MAGNOLIOPHYTA; PERSEA AMERICANA;

LIPID; PLANT PROTEIN; PLANT RNA; TRANSCRIPTOME;

BIOSYNTHESIS; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PERSEA; PLANT SEED;

GENE EXPRESSION REGULATION, PLANT; LIPIDS; MOLECULAR SEQUENCE DATA; PERSEA; PLANT PROTEINS; RNA, PLANT; SEEDS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME;

EID: 84938858929     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-015-0586-2     Document Type: Article

References (93)

1. Chanderbali AS, Albert VA, Ashworth VE, Clegg MT, Litz RE, Soltis DE, et al. Persea americana (avocado): bringing ancient flowers to fruit in the genomics era. Bioessays. 2008;30(4):386-96.
2. Moore MJ, Bell CD, Soltis PS, Soltis DE. Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci U S A. 2007;104(49):19363-8.
3. Rohwer JG. Lauraceae. In: Flowering Plants Dicotyledons. Kubitzki K, Rohwer J, Bittrich V, editors. vol. 2: Springer Berlin Heidelberg; Berlin, Germany; 1993:366-391. http://link.springer.com/book/10.1007/978-3-662-02899-5/page/3 .
4. Soltis DE, Soltis PS, Clegg MT, Durbin M. rbcL sequence divergence and phylogenetic relationships in Saxifragaceae sensu lato. Proc Natl Acad Sci U S A. 1990;87(12):4640-4.
5. Schroeder CA. Growth and Development of the Fuerte Avocado Fruit. P Am Soc Hortic Sci. 1953;61:103-9.
6. Taylor NJ, Cowan AK. Plant hormone homeostais and control of avocado fruit size. Plant Growth Regul. 2001;35:247-55.
7. Kikuta Y, Erickson LC. Seasonal changes of avocado lipids during fruit development and storage. Calif Avocado So. 1968;52:102-8.
8. Liu X, Sievert J, Arpaia ML, Madore MA. Postulated physiological roles of the seven-carbon sugars, mannoheptulose, and perseitol in avocado. J Am Soc Hortic Sci. 2002;127(1):108-14.
9. FAOSTAT. Avocados, Gross production value, world-wide. In: Food and Agriculture Organization of the United Nations, Statistics Division. 2012. http://faostat.fao.org/site/339/default.aspx .
10. Lung SC, Weselake RJ. Diacylglycerol acyltransferase: a key mediator of plant triacylglycerol synthesis. Lipids. 2006;41(12):1073-88.
11. Dahlqvist A, Stahl U, Lenman M, Banas A, Lee M, Sandager L, et al. Phospholipid:diacylglycerol acyltransferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc Natl Acad Sci U S A. 2000;97(12):6487-92.
12. Stymne S, Stobart AK. Triacylglycerol biosynthesis. Biochem Plants. 1987;9:175-214.
13. Bates PD, Stymne S, Ohlrogge J. Biochemical pathways in seed oil synthesis. Curr Opin Plant Biol. 2013;16(3):358-64.
14. 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.
15. Banilas G, Karampelias M, Makariti I, Kourti A, Hatzopoulos P. The olive DGAT2 gene is developmentally regulated and shares overlapping but distinct expression patterns with DGAT1. J Exp Bot. 2011;62(2):521-32.
16. 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.
17. Ibarra-Laclette E, Méndez-Bravo A, Pérez-Torres C, Albert V, Kilaru A, López-Gómez R, et al. Deep sequencing of the Mexican avocado transcriptome, an ancient angiosperm with a high content of fatty acids. BMC Genomics. 2015. in press.
18. 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.
19. 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.
20. Horn PJ, James CN, Gidda SK, Kilaru A, Dyer JM, Mullen RT, et al. Identification of a new class of lipid droplet-associated proteins in plants. Plant Physiol. 2013;162(4):1926-36.
21. Gidda SK, Watt S, Collins-Silva J, Kilaru A, Arondel V, Yurchenko O, et al. Lipid droplet-associated proteins (LDAPs) are involved in the compartmentalization of lipophilic compounds in plant cells. Plant Signal Behav. 2013;8(11):e27141.
22. Tzen JTC. Integral Proteins in Plant Oil Bodies. ISRN Botany. 2012;2012:16.
23. Ross JHE, Sanchez J, Millan F, Murphy DJ. Differential presence of oleosins in oleogenic seed and mesocarp tissues in olive (Olea europaea) and avocado (Persea americana). Plant Sci. 1993;93(1-2):203-10.
24. Baud S, Lepiniec L. Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Biochem. 2009;47(6):448-55.
25. 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.
26. Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T. LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol. 2005;46(3):399-406.
27. Marchive CN, Krisztina T, Alexandra L, Loïc Baud S. Transcriptional regulation of fatty acid production in higher plants: Molecular bases and biotechnological outcomes. Lipid Sci Technol. 2014;116(10):1332-43.
28. 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.
29. Baud S, Mendoza MS, To A, Harscoët 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.
30. 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.
31. To A, Joubès J, Barthole G, Lécureuil 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.
32. Dussert S, Guerin C, Andersson M, Joët T, Tranbarger TJ, Pizot M, et al. Comparative transcriptome analysis of three oil palm fruit and seed tissues that differ in oil content and fatty acid composition. Plant Physiol. 2013;162(3):1337-58.
33. 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.
34. Baud S, Lepiniec L. Physiological and developmental regulation of seed oil production. Prog Lipid Res. 2010;49(3):235-49.
35. Dahan Y, Rosenfeld R, Zadiranov V, Irihimovitch V. A proposed conserved role for an avocado FW2.2-like gene as a negative regulator of fruit cell division. Planta. 2010;232(3):663-76.
36. Takenaga F, Matsuyama K, Abe S, Torii Y, Itoh S. Lipid and fatty acid composition of mesocarp and seed of avocado fruits harvested at northern range in Japan. J Oleo Sci. 2008;57(11):591-7.
37. Zou J, Abrams GD, Barton DL, Taylor DC, Pomeroy MK, Abrams SR. Induction of Lipid and Oleosin Biosynthesis by (+)-Abscisic Acid and Its Metabolites in Microspore-Derived Embryos of Brassica napus L.cv Reston (Biological Responses in the Presence of 8[prime]-Hydroxyabscisic Acid). Plant Physiol. 1995;108(2):563-71.
38. Qi Q, Rose PA, Cutler AJ. (+)-Abscisic Acid Metabolism, 3-Ketoacyl-Coenzyme A Synthase Gene Expression, and Very-Long-Chain Monounsaturated Fatty Acid Biosynthesis in Brassica napusEmbryos. Plant Physiol. 1998;117(3):979-87.
39. Chandrasekaran U, Xu W, Liu A. Transcriptome profiling identifies ABA mediated regulatory changes towards storage filling in developing seeds of castor bean (Ricinus communis L.). Cell Biosci. 2014;4:33.
40. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, et al. Acyl-lipid metabolism. Arabidopsis Book. 2013;11:e0161.
41. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, et al. A gene expression map of Arabidopsis thaliana development. Nat Genet. 2005;37(5):501-6.
42. Lutziger I, Oliver DJ. Molecular evidence of a unique lipoamide dehydrogenase in plastids: analysis of plastidic lipoamide dehydrogenase from Arabidopsis thaliana. FEBS Lett. 2000;484(1):12-6.
43. Johnston ML, Luethy MH, Miernyk JA, Randall DD. Cloning and molecular analyses of the Arabidopsis thaliana plastid pyruvate dehydrogenase subunits. Biochim Biophys Acta. 1997;1321(3):200-6.
44. Mooney BP, Miernyk JA, Randall DD. Cloning and characterization of the dihydrolipoamide S-acetyltransferase subunit of the plastid pyruvate dehydrogenase complex (E2) from Arabidopsis. Plant Physiol. 1999;120(2):443-52.
45. Beisson F, Koo AJ, Ruuska S, Schwender J, Pollard M, Thelen JJ, et al. Arabidopsis genes involved in acyl lipid metabolism. A 2003 census of the candidates, a study of the distribution of expressed sequence tags in organs, and a web-based database. Plant Physiol. 2003;132(2):681-97.
46. Ohlrogge JB, Kuo TM. Plants have isoforms for acyl carrier protein that are expressed differently in different tissues. J Biol Chem. 1985;260(13):8032-7.
47. Battey JF, Ohlrogge JB. Evolutionary and tissue-specific control of expression of multiple acyl-carrier protein isoforms in plants and bacteria. Planta. 1990;180(3):352-60.
48. Bonaventure G, Ohlrogge JB. Differential regulation of mRNA levels of acyl carrier protein isoforms in Arabidopsis. Plant Physiol. 2002;128(1):223-35.
49. Whittle E, Shanklin J. Engineering delta 9-16:0-acyl carrier protein (ACP) desaturase specificity based on combinatorial saturation mutagenesis and logical redesign of the castor delta 9-18:0-ACP desaturase. J Biol Chem. 2001;276(24):21500-5.
50. Rogge CE, Fox BG. Desaturation, chain scission, and register-shift of oxygen-substituted fatty acids during reaction with stearoyl-ACP desaturase. Biochemistry. 2002;41(31):10141-8.
51. Kachroo A, Shanklin J, Whittle E, Lapchyk L, Hildebrand D, Kachroo P. The Arabidopsis stearoyl-acyl carrier protein-desaturase family and the contribution of leaf isoforms to oleic acid synthesis. Plant Mol Biol. 2007;63(2):257-71.
52. Shockey JM, Fulda MS, Browse JA. Arabidopsis contains nine long-chain acyl-coenzyme a synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol. 2002;129(4):1710-22.
53. Schnurr JA, Shockey JM, de Boer GJ, Browse JA. Fatty acid export from the chloroplast. Molecular characterization of a major plastidial acyl-coenzyme A synthetase from Arabidopsis. Plant Physiol. 2002;129(4):1700-9.
54. Aznar-Moreno JA, Venegas Calerón M, Martínez-Force E, Garcés R, Mullen R, Gidda SK, et al. Sunflower (Helianthus annuus) long-chain acyl-coenzyme A synthetases expressed at high levels in developing seeds. Physiol Plant. 2014;150(3):363-73.
55. Zhao L, Katavic V, Li F, Haughn GW, Kunst L. Insertional mutant analysis reveals that long-chain acyl-CoA synthetase 1 (LACS1), but not LACS8, functionally overlaps with LACS9 in Arabidopsis seed oil biosynthesis. Plant J. 2010;64(6):1048-58.
56. Jessen D, Roth C, Wiermer M, Fulda M. Two Activities of Long-Chain Acyl-Coenzyme A Synthetase Are Involved in Lipid Trafficking between the Endoplasmic Reticulum and the Plastid in Arabidopsis. Plant Physiol. 2015;167(2):351-66.
57. Li N, Gugel IL, Giavalisco P, Zeisler V, Schreiber L, Soll J, et al. FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biol. 2015;13(2):e1002053.
58. Mehrshahi P, Johnny C, DellaPenna D. Redefining the metabolic continuity of chloroplasts and ER. Trends Plant Sci. 2014;19(8):501-7.
59. Tjellström H, Yang Z, Allen DK, Ohlrogge JB. Rapid kinetic labeling of Arabidopsis cell suspension cultures: implications for models of lipid export from plastids. Plant Physiol. 2012;158(2):601-11.
60. Bates PD, Ohlrogge JB, Pollard M. Incorporation of newly synthesized fatty acids into cytosolic glycerolipids in pea leaves occurs via acyl editing. J Biol Chem. 2007;282(43):31206-16.
61. Bates PD, Durrett TP, Ohlrogge JB, Pollard M. Analysis of acyl fluxes through multiple pathways of triacylglycerol synthesis in developing soybean embryos. Plant Physiol. 2009;150(1):55-72.
62. Fulda M, Shockey J, Werber M, Wolter FP, Heinz E. Two long-chain acyl-CoA synthetases from Arabidopsis thaliana involved in peroxisomal fatty acid beta-oxidation. Plant J. 2002;32(1):93-103.
63. Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J. Peroxisomal Acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell. 2004;16(2):394-405.
64. Bates PD, Browse J. The significance of different diacylgycerol synthesis pathways on plant oil composition and bioengineering. Front Plant Sci. 2012;3:147.
65. 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 U S A. 2009;106(44):18837-42.
66. Slack CR, Campbell LC, Browse JA, Roughan PG. Some evidence for the reversibility of the cholinephosphotransferasecatalysed reaction in developing linseed cotyledons in vivo. Biochim Biophys Acta. 1983;754(1):10-20.
67. Goode J, Dewey R. Characterization of aminoalcoholphosphotransferases from Arabidopsis thaliana and soybean. Plant Physiol Biochem. 1999;37(6):445-57.
68. Stymne S, Stobart AK. The biosynthesis of triacylglycerols in microsomal preparations of developing cotyledons of sunflower (Helianthus annuus L.). Biochem J. 1984;220(2):481-8.
69. Tzen JT, Huang AH. Surface structure and properties of plant seed oil bodies. J Cell Biol. 1992;117(2):327-35.
70. Frandsen GI, Mundy J, Tzen JT. Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant. 2001;112(3):301-7.
71. Lin LJ, Liao PC, Yang HH, Tzen JT. Determination and analyses of the N-termini of oil-body proteins, steroleosin, caleosin and oleosin. Plant Physiol Biochem. 2005;43(8):770-6.
72. Huang NL, Huang MD, Chen TL, Huang AH. Oleosin of subcellular lipid droplets evolved in green algae. Plant Physiol. 2013;161(4):1862-74.
73. Appleman D, Noda L. Biochemical studies of the Fuerte avocado fruits. In., vol. Yearbook 26:60: A preliminary report. Calif. Avocado Soc. 1941.
74. Davenport JB, Ellis SC. Chemical changes during growth and storage of the avocado fruit. Aust J Biol Sci. 1959;12:445-54.
75. Lee SK, Young RE, Schiffman PM, Coggins CW. Maturity studies of avocado fruit based on picking dates and dry weight. J Am Soc Horticultural Sci. 1983;108:390-4.
76. Notton BA, Blanke MM. Contribution of phosphoenolpyruvate carboxy- lase to the carbon economy of cv. Fuerte avocado fruit. In: Proc Sec World Avocado Congress. 1992: 449-455. http://faostat.fao.org/site/339/default.aspx .
77. Blanke MM, Notton BA. Kinetics and physiological significance of photosynthetic phosphoenolpyruvate carboxylase in avocado fruit. J Plant Physiol. 1991;137:553-8.
78. Whiley AW, Schaffer B, Lara SP. Carbon dioxide exchange of developing avocado (Persea americana Mill.) fruit. Tree Physiology. 1992 Jul;11(1):85-94.
79. Blanke MM. Photosynthesis of Avocado Fruit. In: Proc of Second World Avocado Congress. 1992: 179-189. http://faostat.fao.org/site/339/default.aspx .
80. Ludewig F, Flügge U-I. Role of metabolite transporters in source-sink carbon allocation. Front Plant Sci. 2013;4:231.
81. Liu X, Robinson P, Madore M, Witney G, Arpaia M. 'Hass' Avocado Carbohydrate Fluctuations. II. Fruit Growth and Ripening. J Amer Soc Hort Sci. 1999;124(6):676-81.
82. Liu X, Robinson PW, Madore MA, Witney GW, Arpaia ML. 'Hass' Avocado Carbohydrate Fluctuations. II. Fruit Growth and Ripening. J Amer Soc Hort Sci. 1999;124(6):676-81.
83. Schwender J, Hay JO. Predictive modeling of biomass component tradeoffs in Brassica napus developing oilseeds based on in silico manipulation of storage metabolism. Plant Physiol. 2012;160(3):1218-36.
84. Schwender J, Ohlrogge JB, Shachar-Hill Y. A flux model of glycolysis and the oxidative pentosephosphate pathway in developing Brassica napus embryos. J Biol Chem. 2003;278(32):29442-53.
85. Smith RG, Gauthier DA, Dennis DT, Turpin DH. Malate- and pyruvate-dependent fatty acid synthesis in leucoplasts from developing castor endosperm. Plant Physiol. 1992;98(4):1233-8.
86. Alonso AP, Dale VL, Shachar-Hill Y. Understanding fatty acid synthesis in developing maize embryos using metabolic flux analysis. Metab Eng. 2010;12(5):488-97.
87. Plaxton WC. The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol. 1996;47:185-214.
88. Hara A, Radin NS. Lipid extraction of tissues with a low-toxicity solvent. Anal Biochem. 1978;90(1):420-6.
89. Browse J, McCourt P, Somerville C. A mutant of Arabidopsis deficient in c(18:3) and c(16:3) leaf lipids. Plant Physiol. 1986;81(3):859-64.
90. Christie WW, Han X. Isolation, Separation, Identification and Lipidomic Analysis. U.K.: Oily Press, Bridgwater; 2010.
91. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644-52.
92. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947-8.
93. 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.