De novo transcriptome sequencing in Bixa orellana to identify genes involved in methylerythritol phosphate, carotenoid and bixin biosynthesis

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Cárdenas Conejo, Yair ^a   Carballo Uicab, Víctor ^a   Lieberman, Meric ^b   Aguilar Espinosa, Margarita ^a   Comai, Luca ^b   Rivera Madrid, Renata ^a  

^a CENTRO DE INVESTIGACIÓN CIENTÍFICA DE YUCATÁN   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Annatto; Bixa orellana; Bixin synthesis; Carotenoids; Lipstick tree; Transcriptome

Indexed keywords

ALDEHYDE DEHYDROGENASE; CAROTENOID; COMPLEMENTARY DNA; METHYLTRANSFERASE; TRANSCRIPTOME; BIXIN; ERYTHRITOL;

ARTICLE; BIOSYNTHESIS; BIXA ORELLANA; BIXIN GENE; CACAO; CAROTENOID GENE; CONTROLLED STUDY; COTTON; DEVELOPMENTAL STAGE; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LIBRARY; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC DATABASE; MEP GENE; NONHUMAN; ONTOLOGY; PHYLOGENY; PLANT SEED; REAL TIME POLYMERASE CHAIN REACTION; SEED DEVELOPMENT; SIGNAL TRANSDUCTION; BIXACEAE; BLOOD; GENETICS; METABOLISM; MOLECULAR GENETICS;

BIXACEAE; CAROTENOIDS; ERYTHRITOL; MOLECULAR SEQUENCE DATA; SEEDS;

EID: 84945575026     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-2065-4     Document Type: Article

References (80)

1. THE ANGIOSPERM PHYLOGENY GROUP. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc. 2009;161:105-21.
2. THE ANGIOSPERM PHYLOGENY GROUP. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc. 2003;141:399-436.
3. DA Dendy V. The assay of annatto preparations by thin-layer chromatography. J Sci Food Agric. 1966;17:75-6.
4. 2) and free radicals: potential effects for human health. Acta Biochim Pol. 2012;59:27-30.
5. Zeevaart JAD, Creelman RA. Metabolism and physiology of abscisic acid. Annu Rev Plant Physiol Plant Mol Biol. 1988;39:439-73.
6. Rohmer M, Seemann M, Horbach S, Bringer-meyer S, Sahm H. Glyceraldehyde 3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J Am Chem Soc. 1996;118:2564-6.
7. Lichtenthaler HK. The 1-Deoxy-D-Xylulose-5-Phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:47-65.
8. Cunningham FX, Gantt E. Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol. 1998;49:557-83.
9. Nisar N, Li L, Lu S, Khin NC, Pogson BJ. Carotenoid metabolism in plants. Mol Plant. 2015;8:68-82.
10. Walter MH, Strack D. Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep. 2011;28:663-92.
11. Vogel JT, Tan B-C, McCarty DR, Klee HJ. The carotenoid cleavage dioxygenase 1 enzyme has broad substrate specificity, cleaving multiple carotenoids at two different bond positions. J Biol Chem. 2008;283:11364-73.
12. Bouvier F, Dogbo O, Camara B. Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science. 2003;300:2089-91.
13. Rodríguez-Ávila NL, Narvaez-Zapata JA, Ramirez-Benitez JE, Aguilar-Espinosa ML, Rivera-Madrid R. Identification and expression pattern of a new carotenoid cleavage dioxygenase gene member from Bixa orellana. J Exp Bot. 2011;62:5385-95.
14. Jako C, Coutu C, Roewer I, Reed DW, Pelcher LE, Covello PS. Probing carotenoid biosynthesis in developing seed coats of Bixa orellana (Bixaceae) through expressed sequence tag analysis. Plant Sci. 2002;163:141-5.
15. Rodríguez-Ávila NL, Narvaez-Zapata JA, Aguilar-espinosa ML, Rivera-Madrid R. Regulation of pigment-related genes during flower and fruit development of Bixa orellana. Plant Mol Biol Report. 2011;29:43-50.
16. Rodríguez-Ávila NL, Narvaez-Zapata JA, Aguilar-Espinosa ML, Rivera-Madrid R. Full-length gene enrichment by using an optimized RNA isolation protocol in Bixa orellana recalcitrant tissues. Mol Biotechnol. 2009;42:84-90.
17. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18:821-9.
18. Huang X, Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999;9:868-77.
19. Ashrafi H, Hill T, Stoffel K, Kozik A, Yao J, Chin-Wo SR, et al. De novo assembly of the pepper transcriptome (Capsicum annuum): a benchmark for in silico discovery of SNPs, SSRs and candidate genes. BMC Genomics. 2012;13:571.
20. Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011;12:444.
21. Duarte JM, Wall PK, Edger PP, Landherr LL, Ma H, Pires JC, et al. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol Biol. 2010;10:1-18.
22. Logacheva MD, Kasianov AS, Vinogradov DV, Samigullin TH, Gelfand MS, Makeev VJ, et al. De novo sequencing and characterization of floral transcriptome in two species of buckwheat (Fagopyrum). BMC Genomics. 2011;12:1-17.
23. D'Auria JC, Chen F, Pichersky E. The SABATH family of methyltransferases in Arabidopsis thaliana and other plant species. Recent Adv Phytochem. 2003;37:95-125.
24. Rivera-Madrid R, Burnell J, Aguilar-espinosa ML, Rodríguez-Ávila NL, Lugo-Cervantes E, Saenz-Carbonell LA. Control of carotenoid gene expression in Bixa orellana L. leaves treated with norflurazon. Plant Mol Biol Report. 2013;31:1422-32.
25. Soares VLF, Rodrigues SM, de Oliveira TM, de Queiroz TO, Lima LS, Hora-Júnior BT, et al. Unraveling new genes associated with seed development and metabolism in Bixa orellana L. by expressed sequence tag (EST) analysis. Mol Biol Rep. 2011;38:1329-40.
26. Hyun TK, Rim Y, Jang H-J, Kim CH, Park J, Kumar R, et al. De novo transcriptome sequencing of Momordica cochinchinensis to identify genes involved in the carotenoid biosynthesis. Plant Mol Biol. 2012;79:413-27.
27. Pan Z, Zeng Y, An J, Ye J, Xu Q, Deng X. An integrative analysis of transcriptome and proteome provides new insights into carotenoid biosynthesis and regulation in sweet orange fruits. J Proteomics. 2012;75:2670-84.
28. Grassi S, Piro G, Lee JM, Zheng Y, Fei Z, Dalessandro G, et al. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit. BMC Genomics. 2013;14:781.
29. Motamayor JC, Mockaitis K, Schmutz J, Haiminen N, Iii DL, Cornejo O, et al. The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. Genome Biol. 2013;14:r53.
30. Ming R, Hou S, Feng Y, Yu Q, Dionne-Laporte A, Saw JH, et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature. 2008;452:991-6.
31. Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, et al. Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nat Biotechnol. 2014;32:656-62.
32. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature. 2007;449:463-7.
33. Wang H, Moore MJ, Soltis PS, Bell CD, Brockington SF, Alexandre R, et al. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci U S A. 2009;106:3853-8.
34. Qiu Y-L, Li L, Wang B, Xue J-Y, Hendry TA, Li R-Q, et al. Angiosperm phylogeny inferred from sequences of four mitochondrial genes. J Syst Evol. 2010;48:391-425.
35. Morton CM. Newly sequenced nuclear gene (Xdh) for inferring angiosperm phylogeny. Ann Missouri Bot Gard. 2011;98:63-89.
36. Fay MF, Bayers C, Alverson WS, Bruijn AY, Chase MW. Plastid rbcL sequence data indicate a close affinity between Diegodendron and Bixa. Taxon. 1998;47:43-50.
37. Alverson WS, Karol KG, Baum DA, Chase MW, Swensen SM, McCourt R, et al. Circumscription of the Malvales and relationships to other Rosidae: evidence from rbcL sequence data. Am J Bot. 1998;85:876-87.
38. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Delcher AL, Jaiswal P, et al. The genome of woodland strawberry (Fragaria vesca). Nat Genet. 2011;43:109-16.
39. Zheng C, Sankoff D. Gene order in rosid phylogeny, inferred from pairwise syntenies among extant genomes. BMC Bioinformatics. 2012;13 Suppl 10:S9.
40. Rodríguez-Concepción M. Supply of precursors for carotenoid biosynthesis in plants. Arch Biochem Biophys. 2010;504:118-22.
41. Peng G, Wang C, Song S, Fu X, Azam M, Grierson D, et al. The role of 1-deoxy-d-xylulose-5-phosphate synthase and phytoene synthase gene family in citrus carotenoid accumulation. Plant Physiol Biochem. 2013;71:67-76.
42. Ruiz-Sola MÁ, Rodríguez-Concepción M. Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book. 2012;10:e0158.
43. Saladié M, Wright LP, Garcia-Mas J, Rodríguez-Concepción M, Phillips MA. The 2-C-methylerythritol 4-phosphate pathway in melon is regulated by specialized isoforms for the first and last steps. J Exp Bot. 2014;65:5077-92.
44. Floss DS, Hause B, Lange PR, Ku H, Strack D, Walter MH. Knock-down of the MEP pathway isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J. 2008;56:86-100.
45. Bramley PM. Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot. 2002;53:2073-87.
46. Giorio G, Stigliani AL, D'Ambrosio C. Phytoene synthase genes in tomato (Solanum lycopersicum L.) - New data on the structures, the deduced amino acid sequences and the expression patterns. FEBS J. 2008;275:527-35.
47. Ronen G, Cohe M, Zamir D, Hirschberg J. Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J. 1999;17:341-51.
48. Pecker I, Gabbay R, Cunningham FJ, Hirschberg J. Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol Biol. 1996;30:807-19.
49. Simkin AJ, Laboure A-M, Kuntz M, Sandmann G. Comparison of carotenoid content, gene expression and enzyme levels in tomato (Lycopersicon esculentum) leaves. Zeitschrift für Naturforsch C A J Biosci. 2003;58:371-80.
50. Corona V, Aracri B, Kosturkova G, Bartley GE, Pitto L, Giorgetti L, et al. Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J. 1996;9:505-12.
51. Auldridge ME, McCarty DR, Klee HJ. Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol. 2006;9:315-21.
52. Rodrigo MJ, Alquézar B, Alós E, Medina V, Carmona L, Bruno M, et al. A novel carotenoid cleavage activity involved in the biosynthesis of Citrus fruit-specific apocarotenoid pigments. J Exp Bot. 2013;64:4461-78.
53. Rubio A, Rambla JL, Santaella M, Gómez MD, Orzaez D, Granell A, et al. Cytosolic and plastoglobule-targeted carotenoid dioxygenases from Crocus sativus are both involved in beta-ionone release. J Biol Chem. 2008;283:24816-25.
54. Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M, Prado-Cabrero A, et al. Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci U S A. 2014;111:12246-51.
55. Priya R, Siva R. Phylogenetic analysis and evolutionary studies of plant carotenoid cleavage dioxygenase gene. Gene. 2014;548:223-33.
56. Auldridge ME, Block A, Vogel JT, Dabney-Smith C, Mila I, Bouzayen M, et al. Characterization of three members of the Arabidopsis carotenoid cleavage dioxygenase family demonstrates the divergent roles of this multifunctional enzyme family. Plant J. 2006;45:982-93.
57. Lashbrooke JG, Young PR, Dockrall SJ, Vasanth K, Vivier MA. Functional characterisation of three members of the Vitis vinifera L. carotenoid cleavage dioxygenase gene family. BMC Plant Biol. 2013;13:156.
58. Ytterberg AJ, Peltier J, Van Wijk KJ. Protein profiling of plastoglobules in chloroplasts and chromoplasts. A surprising site for differential accumulation of metabolic enzymes. Plant Physiol. 2006;140(March):984-97.
59. Vallabhaneni R, Bradbury LMT, Wurtzel ET. The carotenoid dioxygenase gene family in maize, sorghum, and rice. Arch Biochem Biophys. 2010;504:104-11.
60. Floss DS, Walter MH. Role of carotenoid cleavage dioxygenase 1 (CCD1) in apocarotenoid biogenesis revisited. Plant Signal Behav. 2009;4:172-5.
61. Floss DS, Schliemann W, Schmidt J, Strack D, Walter MH. RNA interference-mediated repression of MtCCD1 in mycorrhizal roots of Medicago truncatula causes accumulation of C27 apocarotenoids, shedding light on the functional role of CCD1. Plant Physiol. 2008;148(November):1267-82.
62. Brocker C, Vasiliou M, Carpenter S, Carpenter C, Zhang Y, Wang X, et al. Aldehyde dehydrogenase (ALDH) superfamily in plants: gene nomenclature and comparative genomics. Planta. 2013;237:189-210.
63. Nair RB, Bastress KL, Ruegger MO, Denault JW, Chapple C. The Arabidopsis thaliana REDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell. 2004;16:544-54.
64. Kotchoni SO, Jimenez-Lopez JC, Kayodé APP, Gachomo EW, Baba-Moussa L. The soybean aldehyde dehydrogenase (ALDH) protein superfamily. Gene. 2012;495:128-33.
65. Hou Q, Bartels D. Comparative study of the aldehyde dehydrogenase (ALDH) gene superfamily in the glycophyte Arabidopsis thaliana and Eutrema halophytes. Ann Bot. 2014;22:1-15.
66. Jimenez-Lopez JC, Gachomo EW, Seufferheld MJ, Kotchoni SO. The maize ALDH protein superfamily: linking structural features to functional specificities. BMC Struct Biol. 2010;10:43.
67. Stiti N, Missihoun TD, Kotchoni SO, Kirch H-H, Bartels D. Aldehyde dehydrogenases in Arabidopsis thaliana: biochemical requirements, metabolic pathways, and functional analysis. Front Plant Sci. 2011;2:1-11.
68. Huang W, Ma X, Wang Q, Gao Y, Xue Y, Niu X, et al. Significant improvement of stress tolerance in tobacco plants by overexpressing a stress-responsive aldehyde dehydrogenase gene from maize (Zea mays). Plant Mol Biol. 2008;68:451-63.
69. Trautmann D, Beyer P, Al-Babili S. The ORF slr0091 of Synechocystis sp. PCC6803 encodes a high-light induced aldehyde dehydrogenase converting apocarotenals and alkanals. FEBS J. 2013;280:3685-96.
70. Estrada AF, Youssar L, Scherzinger D, Al-Babili S, Avalos J. The ylo-1 gene encodes an aldehyde dehydrogenase responsible for the last reaction in the Neurospora carotenoid pathway. Mol Microbiol. 2008;69:1207-20.
71. Díaz-Sánchez V, Estrada AF, Trautmann D, Al-Babili S, Avalos J. The gene carD encodes the aldehyde dehydrogenase responsible for neurosporaxanthin biosynthesis in Fusarium fujikuroi. FEBS J. 2011;278:3164-76.
72. Rivera-Madrid R, Escobedo-GM RM, Balam-Galera E, Vera-Ku M, Harries H. Preliminary studies toward genetic improvement of annatto (Bixa orellana L.). Sci Hortic (Amsterdam). 2006;109:165-72.
73. Bradnam KR, Fass JN, Alexandrov A, Baranay P, Bechner M, Birol I, et al. Assemblathon 2: evaluating de novo methods of genome assembly in three vertebrate species. Gigascience. 2013;2:10.
74. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.
75. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21:3674-6.
76. Moriya Y, Itoh M, Okuda S, Yoshizagua A, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35:182-5.
77. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25:1307-20.
78. Jones D, Taylor W, Thornton J. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992;8:275-82.
79. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731-9.
80. Kutmon M, van Iersel MP, Bohler A, Kelder T, Nunes N, Pico AR, et al. PathVisio 3: an extendable pathway analysis toolbox. PLOS Comput Biol. 2015;11:e1004085.