The bitter side of the nightshades: Genomics drives discovery in Solanaceae steroidal alkaloid metabolism

Phytochemistry

Volumn 113, Issue , 2015, Pages 24-32

  Cardenas P D ^a,b   Sonawane, P D ^a   Heinig, U ^a   Bocobza, S E ^a   Burdman, S ^b   Aharoni, A ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Metabolic gene clusters; Solanaceae; Steroidal alkaloids

Indexed keywords

SOLANUM ALKALOID; STEROID;

ANIMAL; BIOSYNTHESIS; CHEMISTRY; CROP; GENETIC ENGINEERING; GENETICS; GENOMICS; HUMAN; METABOLISM; POTATO; SOLANUM; TOMATO;

ANIMALS; BIOSYNTHETIC PATHWAYS; CROPS, AGRICULTURAL; GENETIC ENGINEERING; GENOMICS; HUMANS; LYCOPERSICON ESCULENTUM; SOLANACEOUS ALKALOIDS; SOLANUM; SOLANUM TUBEROSUM; STEROIDS;

EID: 84939999961     PISSN: 00319422     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.phytochem.2014.12.010     Document Type: Review

References (79)

1. L. Arnqvist, P.C. Dutta, L. Jonsson, and F. Sitbon Reduction of cholesterol and glycoalkaloid levels in transgenic potato plants by overexpression of a type 1 sterol methyltransferase cDNA Plant Physiol. 131 2003 1792 1799
2. D. Arthan, P. Kittakoop, A. Esen, and J. Svasti Furostanol glycoside 26-O-β-glucosidase from the leaves of Solanum torvum Phytochemistry 67 2006 27 33
3. Atta-ur-Rahman, and M.I. Choudhary Diterpenoid and steroidal alkaloids Nat. Prod. Rep. 16 1999 619 635
4. Y. Bai, and P. Lindhout Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann. Bot. 100 2007 1085 1094
5. M. Baup Extrait d'une lettre Ann. Chim. Phys. 31 1826 108 109
6. S. Boycheva, L. Daviet, J.L. Wolfender, and T.B. Fitzpatrick The rise of operon-like gene clusters in plants Trends Plant Sci. 2014 http://dx.doi.org/10.1016/j.tplants.2014.01.013
7. A.A. Bushway, R.J. Bushway, and C.H. Kim Isolation, partial purification and characterization of a potato peel glycoalkaloid glycosidase Am. Potato J. 65 1988 621 631
8. A.A. Bushway, R.J. Bushway, and C.H. Kim Isolation, partial purification and characterization of a potato peel α-solanine cleaving glycosidase Am. Potato J. 67 1990 233 238
9. R.J. Bushway, L.B. Perkins, L.R. Paradis, and S. Vanderpant High-performance liquid chromatographic determination of the tomato glycoalkaloid, tomatine, in green and red tomatoes J. Agric. Food Chem. 42 1994 2824 2829
10. M. Desfosses Extrait d'une lettre J. Pharm. 6 1820 374 376
11. L.C. Dolan, R.A. Matulka, and G.A. Burdock Naturally occurring food toxins Toxins 2 2010 2289 2332
12. E. Eich Solanaceae and Convolvulaceae: Secondary Metabolites 2008 Springer Berlin
13. B. Field, A.S. Fiston-Lavier, A. Kemen, K. Geisler, H. Quesneville, and A.E. Osbourn Formation of plant metabolic gene clusters within dynamic chromosomal regions Proc. Natl. Acad. Sci. U.S.A. 108 2011 16116 16121
14. B. Field, and A.E. Osbourn Metabolic diversification-independent assembly of operon-like gene clusters in different plants Science 320 2008 543 547
15. T.D. Fontaine, G.W. Irving, R. Ma, J.B. Poole, and S.P. Doolittle Isolation and partial characterization of crystalline tomatine, an antibiotic agent from the tomato plant Arch. Biochem. 18 1948 467 475
16. J.E. Ford, D.J. McCance, and R.B. Drysdale The detoxification of α-tomatine by Fusarium oxysporum f. sp. lycopersici Phytochemistry 16 1977 545 546
17. M. Frey, P. Chomet, E. Glawischnig, C. Stettner, S. Grun, A. Winklmair, W. Eisenreich, A. Bacher, R.B. Meeley, S.P. Briggs, K. Simcox, and A. Gierl Analysis of a chemical plant defense mechanism in grasses Science 277 1997 696 699
18. M. Friedman Tomato glycoalkaloids: role in the plant and in the diet J. Agric. Food Chem. 50 2002 5751 5780
19. M. Friedman, C.E. Levin, and G.M. McDonald α-Tomatine determination in tomatoes by HPLC using pulsed amperometric detection J. Agric. Food Chem. 42 1994 1959 1964
20. Y. Fujiwara, A. Takaki, Y. Uehara, T. Ikeda, M. Okawa, K. Yamauchi, M. Ono, H. Yoshimitsu, and T. Nohara Tomato steroidal alkaloid glycosides, esculeosides A and B, from ripe fruits Tetrahedron 60 2004 4915 4920
21. Y. Fujiwara, S. Yahara, T. Ikeda, M. Ono, and T. Nohara Cytotoxic major saponin from tomato fruits Chem. Pharm. Bull. 51 2003 234 235
22. I. Ginzberg, M. Thippeswamy, E. Fogelman, U. Demirel, A.M. Mweetwa, J. Tokuhisa, and R.E. Veilleux Induction of potato steroidal glycoalkaloid biosynthetic pathway by overexpression of cDNA encoding primary metabolism HMG-CoA reductase and squalene synthase Planta 235 2012 1341 1353
23. E. Heftmann Review of steroids in Solanaceae Phytochemistry 22 1983 1843 1860
24. R.E. Hoagland Toxicity of tomatine and tomatidine on weeds, crops and phytopathogenetic fungi Allelopathy J. 23 2009 425 436
25. Y. Iijima, Y. Fujiwara, T. Tokita, T. Ikeda, T. Nohara, K. Aoki, and D. Shibata Involvement of ethylene in the accumulation of esculeoside A during fruit ripening of tomato (Solanum lycopersicum) J. Agric. Food Chem. 57 2009 3247 3252
26. Y. Iijima, Y. Nakamura, Y. Ogata, K. Tanaka, N. Sakurai, K. Suda, T. Suzuki, H. Suzuki, K. Okazaki, M. Kitayama, S. Kanaya, K. Aoki, and D. Shibata Metabolite annotations based on the integration of mass spectral information Plant J. 54 2008 949 962
27. Y. Iijima, B. Watanabe, R. Sasaki, M. Takenaka, H. Ono, N. Sakurai, N. Umemoto, H. Suzuki, D. Shibata, and K. Aoki Steroidal glycoalkaloid profiling and structures of glycoalkaloids in wild tomato fruit Phytochemistry 95 2013 145 157
28. G.W. Irving, T.D. Fontaine, and S.P. Doolittle Lycopersicin, a fungistatic agent from the tomato plant Science 102 1945 9 11
29. G.W. Irving, T.D. Fontaine, and S.P. Doolittle Partial antibiotic spectrum of tomatin, an antibiotic agent from tomato plant J. Bacteriol. 52 1946 601 607
30. M. Itkin, U. Heinig, O. Tzfadia, A.J. Bhide, B. Shinde, P.D. Cardenas, S.E. Bocobza, T. Unger, S. Malitsky, R. Finkers, Y. Tikunov, A. Bovy, Y. Chikate, P. Singh, I. Rogachev, J. Beekwilder, A.P. Giri, and A. Aharoni Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes Science 341 2013 175 179
31. M. Itkin, I. Rogachev, N. Alkan, T. Rosenberg, S. Malitsky, L. Masini, S. Meir, Y. Iijima, K. Aoki, R. de Vos, D. Prusky, S. Burdman, J. Beekwilder, and A. Aharoni GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato Plant Cell 23 2011 4507 4525
32. K. Kaneko, M.W. Tanaka, and H. Mitsuhashi Origin of the nitrogen in the biosynthesis of solanidine by Veratrum grandiflorum Phytochemistry 15 1976 1391 1393
33. K. Kaneko, M.W. Tanaka, and H. Mitsuhashi Dormantinol, a possible precursor in solanidine biosynthesis, from budding Veratrum grandiflorum Phytochemistry 16 1977 1247 1251
34. K. Kaneko, M. Watanabe, S. Taira, and H. Mitsuhashi Conversion of solanidine to jerveratrum alkaloids in Veratrum grandiflorum Phytochemistry 11 1972 3199 3202
35. O. Kaup, I. Gräfen, E.M. Zellermann, R. Eichenlaub, and K.H. Gartemann Identification of a tomatinase in the tomato-pathogenic actinomycete Clavibacter michiganensis subsp. michiganensis NCPPB382 Mol. Plant-Microbe Interact. 18 2005 1090 1098
36. P. Krits, E. Fogelman, and I. Ginzberg Potato steroidal glycoalkaloid levels and the expression of key isoprenoid metabolic genes Planta 227 2007 143 150
37. A. Krokida, C. Delis, K. Geisler, C. Garagounis, D. Tsikou, L.M. Peña-Rodríguez, D. Katsarou, B. Field, A.E. Osbourn, and K.K. Papadopoulou A metabolic gene cluster in Lotus japonicus discloses novel enzyme functions and products in triterpene biosynthesis New Phytol. 200 2013 675 690
38. R. Kuhn, and I. Low Die Konstitution des Solanins Angew. Chem. 66 1954 639 640
39. R. Ma, and T.D. Fontaine Identification of the sugars in crystalline tomatin Arch. Biochem. 27 1950 461 462
40. K.F. McCue, P.V. Allen, L.V.T. Shepherd, A. Blake, M.M. Maccree, D.R. Rockhold, R.G. Novy, D. Stewart, H.V. Davies, and W.R. Belknap Potato glycosterol rhamnosyltransferase, the terminal step in triose side-chain biosynthesis Phytochemistry 68 2007 327 334
41. K.F. McCue, P.V. Allen, L.V.T. Shepherd, A. Blake, J. Whitworth, M.M. Maccree, D.R. Rockhold, D. Stewart, H.V. Davies, and W.R. Belknap The primary in vivo steroidal alkaloid glucosyltransferase from potato Phytochemistry 67 2006 1590 1597
42. K.F. McCue, L.V.T. Shepherd, P.V. Allen, M.M. Maccree, D.R. Rockhold, D.L. Corsini, H.V. Davies, and W.R. Belknap Metabolic compensation of steroidal glycoalkaloid biosynthesis in transgenic potato tubers: using reverse genetics to confirm the in vivo enzyme function of a steroidal alkaloid galactosyltransferase Plant Sci. 168 2005 267 273
43. G. Mennella, R. Lo Scalzo, M. Fibiani, A. D'Alessandro, G. Francese, L. Toppino, N. Acciarri, A.E. de Almeida, and G.L. Rotino Chemical and bioactive quality traits during fruit ripening in eggplant (S. melongena L.) and allied species J. Agric. Food Chem. 60 2012 11821 11831
44. S.E. Milner, N.P. Brunton, P.W. Jones, N.M. O'Brien, S.G. Collins, and A.R. Maguire Bioactivities of glycoalkaloids and their aglycones from Solanum species J. Agric. Food Chem. 59 2011 3454 3484
45. S. Mintz-Oron, T. Mandel, I. Rogachev, L. Feldberg, O. Lotan, M. Yativ, Z. Wang, R. Jetter, I. Venger, A. Adato, and A. Aharoni Gene expression and metabolism in tomato fruit surface tissues Plant Physiol. 147 2008 823 851
46. S. Moco, R.J. Bino, O. Vorst, H.A. Verhoeven, J. de Groot, T.A. van Beek, J. Vervoort, and C.H.R. de Vos A liquid chromatography-mass spectrometry-based metabolome database for tomato Plant Physiol. 141 2006 1205 1218
47. C.P. Moehs, P.V. Allen, M. Friedman, and W.R. Belknap Cloning and expression of solanidine UDP-glucose glucosyltransferase from potato Plant J. 11 1997 227 236
48. L.A. Mueller, T.H. Solow, N. Taylor, B. Skwarecki, R. Buels, J. Binns, C. Lin, M.H. Wright, R. Ahrens, Y. Wang, E.V. Herbst, E.R. Keyder, N. Menda, D. Zamir, and S.D. Tanksley The SOL Genomics Network. A comparative resource for Solanaceae biology and beyond Plant Physiol. 138 2005 1310 1317
49. W.D. Nes Biosynthesis of cholesterol and other sterols Chem. Rev. 111 2011 6423 6451
50. T. Nohara, T. Ikeda, Y. Fujiwara, S. Matsushita, E. Noguchi, H. Yoshimitsu, and M. Ono Physiological functions of solanaceous and tomato steroidal glycosides J. Nat. Med. 61 2006 1 13
51. K. Ohyama, A. Okawa, Y. Moriuchi, and Y. Fujimoto Biosynthesis of steroidal alkaloids in Solanaceae plants: involvement of an aldehyde intermediate during C-26 amination Phytochemistry 89 2013 26 31
52. K. Ohyama, M. Suzuki, J. Kikuchi, K. Saito, and T. Muranaka Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis Proc. Natl. Acad. Sci. U.S.A. 106 2009 725 730
53. B. Ökmen, D.W. Etalo, M.H. Joosten, H.J. Bouwmeester, R.C.H. de Vos, J. Collemare, and P.J.G.M. de Wit Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato New Phytol. 198 2013 1203 1214
54. R.G. Olmstead, L. Bohs, H.A. Migid, E. Santiago-Valentin, V.F. Garcia, and S.M. Collier A molecular phylogeny of the Solanaceae Taxon 57 2008 1159 1181
55. D. Orzaez, A. Medina, S. Torre, J.P. Fernández-Moreno, J.L. Rambla, A. Fernández-Del-Carmen, E. Butelli, C. Martin, and A. Granell A visual reporter system for virus-induced gene silencing in tomato fruit based on anthocyanin accumulation Plant Physiol. 150 2009 1122 1134
56. A. Osbourn Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation Trends Genet. 26 2010 449 457
57. A. Osbourn Gene clusters for secondary metabolic pathways: an emerging theme in plant biology Plant Physiol. 154 2010 531 535
58. K. Patel, M. Gadewar, V. Tahilyani, and D.K. Patel A review on pharmacological and analytical aspects of diosgenin: a concise report Nat. Prod. Bioprospect. 2 2012 46 52
59. E.V. Petersson, N. Nahar, P. Dahlin, A. Broberg, R. Tröger, P.C. Dutta, L. Jonsson, and F. Sitbon Conversion of exogenous cholesterol into glycoalkaloids in potato shoots, using two methods for sterol solubilisation PLoS One 8 2013 e82955
60. X. Qi, S. Bakht, M. Leggett, C. Maxwell, R. Melton, and A. Osbourn A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants Proc. Natl. Acad. Sci. U.S.A. 101 2004 8233 8238
61. J.G. Roddick Intracellular distribution of the steroidal glycoalkaloid α-tomatine in Lycopersicon esculentum fruit Phytochemistry 16 1976 475 477
62. J.G. Roddick Subcellular localization of steroidal glycoalkaloids in vegetative organs of Lycopersicon esculentum and Solanum tuberosum Phytochemistry 16 1977 805 807
63. J.G. Roddick Steroidal glycoalkaloids: nature and consequences of bioactivity Adv. Exp. Med. Biol. 404 1996 277 295
64. M.C. Sánchez-Mata, W.E. Yokoyama, Y.J. Hong, and J. Prohens α-Solasonine and α-solamargine contents of gboma (Solanum macrocarpon L.) and scarlet (Solanum aethiopicum L.) eggplants J. Agric. Food Chem. 58 2010 5502 5508
65. S. Sawai, K. Ohyama, S. Yasumoto, H. Seki, T. Sakuma, T. Yamamoto, Y. Takebayashi, M. Kojima, H. Sakakibara, T. Aoki, T. Muranaka, K. Saito, and N. Umemoto Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato Plant Cell 26 2014 3763 3774
66. R. Schakirov, and M.S. Yunusov Steroidal alkaloids Nat. Prod. Rep. 7 1990 557 564
67. R. Shakya, and D.A. Navarre LC-MS analysis of solanidane glycoalkaloid diversity among tubers of four wild potato species and three cultivars (Solanum tuberosum) J. Agric. Food Chem. 56 2008 6949 6958
68. M. Suzuki, and T. Muranaka Molecular genetics of plant sterol backbone synthesis Lipids 42 2007 47 54
69. A.P. Swain, T.J. Fitzpatrick, E.A. Talley, S.F. Herb, and S.F. Osman Enzymatic hydrolysis of α-chaconine and α-solanine Phytochemistry 17 1978 8 9
70. S. Swaminathan, D. Morrone, Q. Wang, D.B. Fulton, and R.J. Peters CYP76M7 is an ent-cassadiene C11α-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice Plant Cell 21 2009 3315 3325
71. A.M. Takos, C. Knudsen, D. Lai, R. Kannangara, L. Mikkelsen, M.S. Motawia, C.E. Olsen, S. Sato, S. Tabata, K. Jorgensen, B.L. Moller, and F. Rook Genomic clustering of cyanogenic glucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway Plant J. 68 2011 273 286
72. Umemoto, N., Sasaki, K., 2012. Protein having glycoalkaloid biosynthetic enzyme activity and gene encoding the same. U.S. patent application 2012/0159676 A1.
73. E. Wegel, R. Koumproglou, P. Shaw, and A. Osbourn Cell type-specific chromatin decondensation of a metabolic gene cluster in oats Plant Cell 21 2009 3926 3936
74. P.R. Wilderman, M. Xu, Y. Jin, R.M. Coates, and R.J. Peters Identification of syn-pimara-7,15-diene synthase reveals functional clustering of terpene synthases involved in rice phytoalexin/allelochemical biosynthesis Plant Physiol. 135 2004 2098 2105
75. T. Winzer, V. Gazda, Z. He, F. Kaminski, M. Kern, T.R. Larson, Y. Li, F. Meade, R. Teodor, F.E. Vaistij, C. Walker, T.A. Bowser, and I.A. Graham A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine Science 336 2012 1704 1708
76. S. Yahara, N. Uda, and T. Nohara Lycoperosides A-C, three steroisomeric 23-acetoxyspirosolan-3β-ol β-lycotetraosides from Lycopersicon esculetum Phytochemistry 42 1996 169 172
77. S. Yahara, N. Uda, E. Yoshio, and E. Yae Steroidal alkaloid glycosides from tomato (Lycopersicon esculentum) J. Nat. Prod. 67 2004 500 502
78. T. Yamanaka, J.P. Vincken, H. Zuilhof, A. Legger, N. Takada, and H. Gruppen C22 isomerization in α-tomatine-to-esculeoside A conversion during tomato ripening is driven by C27 hydroxylation of triterpenoidal skeleton J. Agric. Food Chem. 57 2009 3786 3791
79. C. Zwenger, and A. Kind Über das Solanin und dessen Spaltungsprodukte Ann. Chem. Pharm. 118 1861 129 151