Candidate enzymes for saffron crocin biosynthesis are localized in multiple cellular compartments

Plant Physiology

Volumn 177, Issue 3, 2018, Pages 990-1006

  Demurtas, Olivia Costantina ^a   Frusciante, Sarah ^a   Ferrante, Paola ^a   Diretto, Gianfranco ^a   Azad, Noraddin Hosseinpour ^b   Pietrella, Marco ^a,c   Aprea, Giuseppe ^a   Taddei, Anna Rita ^d   Romano, Elena ^e   Mi, Jianing ^f   Al Babili, Salim ^f   Frigerio, Lorenzo ^g   Giuliano, Giovanni ^a  

^a ENEA   (Italy)

^b UNIVERSITY OF MOHAGHEGH ARDABILI   (Iran)

^c CREA Research Centre for Olive   (Italy)

^d UNIVERSITY OF TUSCIA   (Italy)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

^f KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^g UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CAROTENOID; CROCETIN; CROCIN; GLYCOSYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; PLANT PROTEIN;

ANTIBODY SPECIFICITY; BIOSYNTHESIS; CONFOCAL MICROSCOPY; CROCUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GLYCOSYLATION; IMMUNOHISTOCHEMISTRY; METABOLISM; PROCEDURES; TOBACCO; TRANSGENIC PLANT;

ALDEHYDE DEHYDROGENASE; CAROTENOIDS; CROCUS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GLYCOSYLATION; GLYCOSYLTRANSFERASES; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, CONFOCAL; ORGAN SPECIFICITY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; TOBACCO;

EID: 85050182415     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.17.01815     Document Type: Article

References (60)

1. Ahrazem O, Rubio-Moraga A, Trapero-Mozos A, Climent MF, Gómez-Cadenas A, Gómez-Gómez L (2015) Ectopic expression of a stress-inducible glycosyltransferase from saffron enhances salt and oxidative stress tolerance in Arabidopsis while alters anchor root formation. Plant Sci 234: 60–73
2. Ahrazem O, Rubio-Moraga A, Berman J, Capell T, Christou P, Zhu C, Gómez-Gómez L (2016) The carotenoid cleavage dioxygenase CCD2 cata-lysing the synthesis of crocetin in spring crocuses and saffron is a plastidial enzyme. New Phytol 209: 650–663
3. Alavizadeh SH, Hosseinzadeh H (2014) Bioactivity assessment and toxicity of crocin: a comprehensive review. Food Chem Toxicol 64: 65–80
4. Al-Babili S, von Lintig J, Haubruck H, Beyer P (1996) A novel, soluble form of phytoene desaturase from Narcissus pseudonarcissus chromoplasts is Hsp70-complexed and competent for flavinylation, membrane association and enzymatic activation. Plant J 9: 601–612
5. Alboresi A, Perin G, Vitulo N, Diretto G, Block M, Jouhet J, Meneghesso A, Valle G, Giuliano G, Maréchal E, (2016) Light remodels lipid biosynthesis in Nannochloropsis gaditana by modulating carbon partitioning between organelles. Plant Physiol 171: 2468–2482
6. Azama K, Abe S, Sugimoto H, Davies E (2003) Lysine-containing proteins in maize endosperm: a major contribution from cytoskeleton-associated car-bohydrate-metabolizing enzymes. Planta 217: 628–638
7. Bathaie SZ, Farajzade A, Hoshyar R (2014) A review of the chemistry and uses of crocins and crocetin, the carotenoid natural dyes in saffron, with particular emphasis on applications as colorants including their use as biological stains. Biotech Histochem 89: 401–411
8. Benghezal M, Wasteneys GO, Jones DA (2000) The C-terminal dilysine motif confers endoplasmic reticulum localization to type I membrane proteins in plants. Plant Cell 12: 1179–1201
9. Bisti S, Maccarone R, Falsini B (2014) Saffron and retina: neuroprotection and pharmacokinetics. Vis Neurosci 31: 355–361
10. Bouvier F, Dogbo O, Camara B (2003a) Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Science 300: 2089–2091
11. Bouvier F, Suire C, Mutterer J, Camara B (2003b) Oxidative remodeling of chromoplast carotenoids: identification of the carotenoid dioxygenase CsC-CD and CsZCD genes involved in Crocus secondary metabolite biogenesis. Plant Cell 15: 47–62
12. Brandle JE, Telmer PG (2007) Steviol glycoside biosynthesis. Phytochemistry 68: 1855–1863
13. Brocker C, Vasiliou M, Carpenter S, Carpenter C, Zhang Y, Wang X, Kotchoni SO, Wood AJ, Kirch HH, Kopečný D, (2013) Aldehyde dehydrogenase (ALDH) superfamily in plants: gene nomenclature and comparative genomics. Planta 237: 189–210
14. Chryssanthi DG, Lamari FN, Georgakopoulos CD, Cordopatis P (2011) A new validated SPE-HPLC method for monitoring crocetin in human plasma: application after saffron tea consumption. J Pharm Biomed Anal 55: 563–568
15. Cinelli RA, Ferrari A, Pellegrini V, Tyagi M, Giacca M, Beltram F (2000) The enhanced green fluorescent protein as a tool for the analysis of protein dynamics and localization: local fluorescence study at the single-molecule level. Photochem Photobiol 71: 771–776
16. Cote F, Cormier F, Dufresne C, Willemot C (2001) A highly specific glucosyltransferase is involved in the synthesis of crocetin glucosylesters in Crocus sativus cultured cells. J Plant Physiol 158: 553–560
17. D’Esposito D, Ferriello F, Molin AD, Diretto G, Sacco A, Minio A, Barone A, Di Monaco R, Cavella S, Tardella L, (2017) Unraveling the complexity of transcriptomic, metabolomic and quality environmental response of tomato fruit. BMC Plant Biol 17: 66
18. Demurtas OC, Massa S, Illiano E, De Martinis D, Chan PK, Di Bonito P, Franconi R (2016) Antigen production in plant to tackle infectious diseases flare up: the case of SARS. Front Plant Sci 7: 54
19. Díaz-Sánchez V, Estrada AF, Trautmann D, Al-Babili S, Avalos J (2011) The gene carD encodes the aldehyde dehydrogenase responsible for neurospo-raxanthin biosynthesis in Fusarium fujikuroi. FEBS J 278: 3164–3176
20. Diretto G, Al-Babili S, Tavazza R, Scossa F, Papacchioli V, Migliore M, Beyer P, Giuliano G (2010) Transcriptional-metabolic networks in β-carotene-en-riched potato tubers: the long and winding road to the Golden phenotype. Plant Physiol 154: 899–912
21. Dong T, Hwang I (2014) Contribution of ABA UDP-glucosyltransferases in coordination of ABA biosynthesis and catabolism for ABA homeostasis. Plant Signal Behav 9: e28888
22. Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, ho-moeostasis and signalling. Essays Biochem 58: 29–48
23. Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300: 1005–1016
24. Estrada AF, Youssar L, Scherzinger D, Al-Babili S, Avalos J (2008) The ylo-1 gene encodes an aldehyde dehydrogenase responsible for the last reaction in the Neurospora carotenoid pathway. Mol Microbiol 69: 1207–1220
25. Fasano C, Diretto G, Aversano R, D’Agostino N, Di Matteo A, Frusciante L, Giuliano G, Carputo D (2016) Transcriptome and metabolome of synthetic Solanum autotetraploids reveal key genomic stress events following poly-ploidization. New Phytol 210: 1382–1394
26. Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M, Prado-Cabrero A, Rubio-Moraga A, Beyer P, Gomez-Gomez L, Al-Babili S, (2014) Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci USA 111: 12246–12251
27. Gachon CM, Langlois-Meurinne M, Saindrenan P (2005) Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci 10: 542–549
28. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA III, Smith HO (2009) Enzymatic assembly of DNA molecules up to several hundred ki-lobases. Nat Methods 6: 343–345
29. Gómez-Gómez L, Parra-Vega V, Rivas-Sendra A, Seguí-Simarro JM, Molina RV, Pallotti C, Rubio-Moraga Á, Diretto G, Prieto A, Ahrazem O (2017) Unraveling massive crocins transport and accumulation through proteome and microscopy tools during the development of saffron stigma. Int J Mol Sci 18: E76
30. Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in post-transcriptional gene silencing in plants. Science 286: 950–952
31. Jain M, Srivastava PL, Verma M, Ghangal R, Garg R (2016) De novo transcriptome assembly and comprehensive expression profiling in Crocus sativus to gain insights into apocarotenoid biosynthesis. Sci Rep 6: 22456
32. Kirch HH, Bartels D, Wei Y, Schnable PS, Wood AJ (2004) The ALDH gene superfamily of Arabidopsis. Trends Plant Sci 9: 371–377
33. Kotchoni SO, Kuhns C, Ditzer A, Kirch HH, Bartels D (2006) Over-expression of different aldehyde dehydrogenase genes in Arabidopsis thaliana confers tolerance to abiotic stress and protects plants against lipid peroxidation and oxidative stress. Plant Cell Environ 29: 1033–1048
34. Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870–1874
35. Lätari K, Wüst F, Hübner M, Schaub P, Beisel KG, Matsubara S, Beyer P, Welsch R (2015) Tissue-specific apocarotenoid glycosylation contributes to carotenoid homeostasis in Arabidopsis leaves. Plant Physiol 168: 1550–1562
36. Lee H, Sparkes I, Gattolin S, Dzimitrowicz N, Roberts LM, Hawes C, Frigerio L (2013) An Arabidopsis reticulon and the atlastin homologue RHD3-like2 act together in shaping the tubular endoplasmic reticulum. New Phytol 197: 481–489
37. Liu M, Diretto G, Pirrello J, Roustan JP, Li Z, Giuliano G, Regad F, Bouzayen M (2014) The chimeric repressor version of an Ethylene Response Factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol 203: 206–218
38. Martinoia E, Maeshima M, Neuhaus HE (2007) Vacuolar transporters and their essential role in plant metabolism. J Exp Bot 58: 83–102
39. Masaki R, Yamamoto A, Tashiro Y (1994) Microsomal aldehyde dehydrogenase is localized to the endoplasmic reticulum via its carboxyl-terminal 35 amino acids. J Cell Biol 126: 1407–1420
40. Mehrshahi P, Stefano G, Andaloro JM, Brandizzi F, Froehlich JE, DellaPenna D (2013) Transorganellar complementation redefines the biochemical continuity of endoplasmic reticulum and chloroplasts. Proc Natl Acad Sci USA 110: 12126–12131
41. Moraga AR, Nohales PF, Pérez JA, Gómez-Gómez L (2004) Glucosylation of the saffron apocarotenoid crocetin by a glucosyltransferase isolated from Crocus sativus stigmas. Planta 219: 955–966
42. Moraga AR, Mozos AT, Ahrazem O, Gómez-Gómez L (2009) Cloning and characterization of a glucosyltransferase from Crocus sativus stigmas involved in flavonoid glucosylation. BMC Plant Biol 9: 109
43. Nagatoshi M, Terasaka K, Owaki M, Sota M, Inukai T, Nagatsu A, Mizukami H (2012) UGT75L6 and UGT94E5 mediate sequential glucosylation of crocetin to crocin in Gardenia jasminoides. FEBS Lett 586: 1055–1061
44. Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56: 165–185
45. Nishihara K, Kanemori M, Kitagawa M, Yanagi H, Yura T (1998) Chaperone coexpression plasmids: differential and synergistic roles of DnaK-DnaJ-GrpE and GroEL-GroES in assisting folding of an allergen of Japanese cedar pollen, Cryj2, in Escherichia coli. Appl Environ Microbiol 64: 1694–1699
46. Ponti G, Palombi F, Abate D, Ambrosino F, Aprea G, Bastianelli T, Beone F, Bertini R, Bracco G, Caporicci M (2014) The role of medium size facilities in the HPC ecosystem: the case of the new CRESCO4 cluster integrated in the ENEAGRID infrastructure. In S Bassini, M Nygard, eds, 2014 International Conference on High Performance Computing & Simulation (HPCS). IEEE, New York, NY, pp 1030–1033 10.1109/HPCSim.2014.6903807
47. Rambla JL, Trapero-Mozos A, Diretto G, Rubio-Moraga A, Granell A, Gómez-Gómez L, Ahrazem O (2016) Gene-metabolite networks of volatile metabolism in Airen and Tempranillo grape cultivars revealed a distinct mechanism of aroma bouquet production. Front Plant Sci 7: 1619
48. Ross J, Li Y, Lim EK, Bowles DJ (2001) Higher plant glycosyltransferases. Genome Biol 2: REVIEWS3004
49. Rubio-Moraga A, Trapero A, Ahrazem O, Gómez-Gómez L (2010) Crocins transport in Crocus sativus: the long road from a senescent stigma to a newborn corm. Phytochemistry 71: 1506–1513
50. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425
51. Shao H, He X, Achnine L, Blount JW, Dixon RA, Wang X (2005) Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17: 3141–3154
52. Stiti N, Adewale IO, Petersen J, Bartels D, Kirch HH (2011a) Engineering the nucleotide coenzyme specificity and sulfhydryl redox sensitivity of two stress-responsive aldehyde dehydrogenase isoenzymes of Arabidopsis thaliana. Biochem J 434: 459–471
53. Stiti N, Missihoun TD, Kotchoni SO, Kirch HH, Bartels D (2011b) Aldehyde dehydrogenases in Arabidopsis thaliana: biochemical requirements, metabolic pathways, and functional analysis. Front Plant Sci 2: 65
54. Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of mi-croarray data. Bioinformatics 18: 207–208
55. Su L, Diretto G, Purgatto E, Danoun S, Zouine M, Li Z, Roustan JP, Bouzayen M, Giuliano G, Chervin C (2015) Carotenoid accumulation during tomato fruit ripening is modulated by the auxin-ethylene balance. BMC Plant Biol 15: 114
56. Tarantilis PA, Tsoupras G, Polissiou M (1995) Determination of saffron (Cro-cus sativus L.) components in crude plant extract using high-performance liquid chromatography-UV-visible photodiode-array detection-mass spectrometry. J Chromatogr A 699: 107–118
57. Trapero A, Ahrazem O, Rubio-Moraga A, Jimeno ML, Gómez MD, Gómez-Gómez L (2012) Characterization of a glucosyltransferase enzyme involved in the formation of kaempferol and quercetin sophorosides in Crocus sativus. Plant Physiol 159: 1335–1354
58. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7: 562–578
59. Trautmann D, Beyer P, Al-Babili S (2013) The ORF slr0091 of Synechocystis sp. PCC6803 encodes a high-light induced aldehyde dehydrogenase converting apocarotenals and alkanals. FEBS J 280: 3685–3696
60. Wang X (2009) Structure, mechanism and engineering of plant natural product glycosyltransferases. FEBS Lett 583: 3303–3309