A metabolic gene cluster in Lotus japonicus discloses novel enzyme functions and products in triterpene biosynthesis

New Phytologist

Volumn 200, Issue 3, 2013, Pages 675-690

  Krokida, Afrodite ^a   Delis, Costas ^a   Geisler, Katrin ^b   Garagounis, Constantine ^a   Tsikou, Daniela ^a   Peña Rodríguez, Luis M ^c   Katsarou, Dimitra ^a   Field, Ben ^b   Osbourn, Anne E ^b   Papadopoulou, Kalliope K ^a  

^a UNIVERSITY OF THESSALY   (Greece)

^b JOHN INNES CENTRE   (United Kingdom)

^c CENTRO DE INVESTIGACIÓN CIENTÍFICA DE YUCATÁN   (Mexico)

Author keywords

Cytochrome P450; Lotus japonicus; Nodule; Transcriptional silencing; Triterpene

Indexed keywords

CYTOCHROME; ENVIRONMENTAL CONDITIONS; ENZYME; GENE; GENE EXPRESSION; LEGUME; METABOLISM; NODULATION; OXIDATION; WILD POPULATION;

ARABIDOPSIS THALIANA; LOTUS CORNICULATUS VAR. JAPONICUS; NICOTIANA BENTHAMIANA;

CYTOCHROME P450; TRITERPENE; VEGETABLE PROTEIN;

ARTICLE; ENZYMOLOGY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; LOTUS; LOTUS JAPONICUS; METABOLISM; NODULATION; NODULE; PLANT DEVELOPMENT; PLANT GENE; PLANT ROOT; TRANSCRIPTIONAL SILENCING;

CYTOCHROME P450; LOTUS JAPONICUS; NODULE; TRANSCRIPTIONAL SILENCING; TRITERPENE;

CYTOCHROME P-450 ENZYME SYSTEM; GENE EXPRESSION; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENES, PLANT; LOTUS; PLANT DEVELOPMENT; PLANT PROTEINS; PLANT ROOT NODULATION; PLANT ROOTS; ROOT NODULES, PLANT; TRITERPENES;

EID: 84885433874     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12414     Document Type: Article

References (83)

1. Altschul SF, Boguski MS, Gish W, Wootton JC. 1994. Issues in searching molecular sequence databases. Nature Genetics 6: 119-129.
2. Anzai Y, Li SY, Chaulagain MR, Kinoshita K, Kato F, Montgomery J, Sherman DH. 2008. Functional analysis of MycCI and MycG, cytochrome P450 enzymes involved in biosynthesis of mycinamicin macrolide antibiotics. Chemistry and Biology 15: 950-959.
3. Augustin JM, Kuzina V, Andersen SB, Bak S. 2011. Molecular activities, biosynthesis and evolution of triterpenoid saponins. Phytochemistry 72: 435-457.
4. Baisted DJ. 1971. Sterol and triterpene synthesis in developing and germinating pea seed. Biochemical Journal 124: 375-383.
5. Bak S, Kahn RA, Olsen CE, Halkier BA. 1997. Cloning and expression in Escherichia coli of the obtusifoliol 14 alpha-demethylase of Sorghum bicolor (L.) Moench, a cytochrome P450 orthologous to the sterol 14 alpha-demethylases (CYP51) from fungi and mammals. Plant Journal 11: 191-201.
6. Barbulova A, Chiurazzi M. 2005. A procedure for in vitro nodulation studies. In: Márquez AJ, The Lotus japonicus handbook. Dordrecht, the Netherlands: Springer, 83-86.
7. Budzikiewicz H, Djerassi C, Williams DH. 1964. Structure elucidation of natural products by mass spectrometry, v. II, Steroids, terpenoids, sugars, and miscellaneous classes. San Francisco, CA, USA: Holden-Day.
8. Burge CB, Karlin S. 1998. Finding the genes in genomic DNA. Current Opinion in Structural Biology 8: 346-354.
9. Canizares MC, Liu L, Perrin Y, Tsakiris E, Lomonossoff GP. 2006. A bipartite system for the constitutive and inducible expression of high levels of foreign proteins in plants. Plant Biotechnology Journal 4: 183-193.
10. Carlson JC, Fortman JL, Anzai Y, Li SY, Burr DA, Sherman DH. 2010. Identification of the tirandamycin biosynthetic gene cluster from Streptomyces sp 307-9. ChemBioChem 11: 564-572.
11. Chu HY, Wegel E, Osbourn A. 2011. From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants. Plant Journal 66: 66-79.
12. Cole BJW, Bentley MD, Hua Y, Bu L. 1991. Triterpenoid constituents in the outer bark of Betula alleghaniensis (Yellow Birch). Journal of Wood Chemistry and Technology 11: 209-223.
13. Confalonieri M, Cammareri M, Biazzi E, Pecchia P, Fevereiro MP, Balestrazzi A, Tava A, Conicella C. 2009. Enhanced triterpene saponin biosynthesis and root nodulation in transgenic barrel medic (Medicago truncatula Gaertn.) expressing a novel beta-amyrin synthase (AsOXA1) gene. Plant Biotechnology Journal 7: 172-182.
14. Dalakouras A, Wassenegger M. 2013. Revisiting RNA-directed DNA methylation. RNA Biology 10: 453-455.
15. Dantanarayana AP, Kumar NS, Sultanbawa MUS, Balasubramaniam S. 1981. Structures of four new oxygenated lupanes from Pleurostyliaopposita (Celastraceae). Journal of the Chemical Society, Perkin Transactions 10: 2717-2723.
16. Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke AJ, Matzke M. 2009. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO Journal 28: 48-57.
17. Delis C, Dimou M, Flemetakis E, Aivalakis G, Katinakis P. 2006. A root- and hypocotyl-specific gene coding for copper-containing amine oxidase is related to cell expansion in soybean seedlings. Journal of Experimental Botany 57: 101-111.
18. Delis C, Krokida A, Georgiou S, Pena-Rodriguez LM, Kavroulakis N, Ioannou E, Roussis V, Osbourn AE, Papadopoulou KK. 2011. Role of lupeol synthase in Lotus japonicus nodule formation. New Phytologist 189: 335-346.
19. Eamens A, Wang MB, Smith NA, Waterhouse PM. 2008. RNA silencing in plants: yesterday, today, and tomorrow. Plant Physiology 147: 456-468.
20. Ehlting J, Sauveplane V, Olry A, Ginglinger JF, Provart NJ, Werck-Reichhart D. 2008. An extensive (co-)expression analysis tool for the cytochrome P450 superfamily in Arabidopsis thaliana. BMC Plant Biology 8: 47.
21. van Engelen FA, Molthoff JW, Conner AJ, Nap JP, Pereira A, Stiekema WJ. 1995. pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Research 4: 288-290.
22. Field B, Fiston-Lavier AS, Kemen A, Geisler K, Quesneville H, Osbourn AE. 2011. Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proceedings of the National Academy of Sciences, USA 108: 16116-16121.
23. Field B, Osbourn AE. 2008. Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320: 543-547.
24. Grandmougin-Ferjani A, Dalpe Y, Hartmann MA, Laruelle F, Sancholle M. 1999. Sterol distribution in arbuscular mycorrhizal fungi. Phytochemistry 50: 1027-1031.
25. Helliwell CA, Chandler PM, Poole A, Dennis ES, Peacock WJ. 2001. The CYP88A cytochrome P450, ent-kaurenoic acid oxidase, catalyzes three steps of the gibberellin biosynthesis pathway. Proceedings of the National Academy of Sciences, USA 98: 2065-2070.
26. Henderson IR, Jacobsen SE. 2008. Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes and Development 22: 1597-1606.
27. Hernandez LE, Cooke DT. 1996. Lipid composition of symbiosomes from pea root nodules. Phytochemistry 42: 341-346.
28. Huhman DV, Sumner LW. 2002. Metabolic profiling of saponins in Medicago sativa and Medicago truncatula using HPLC coupled to an electrospray ion-trap mass spectrometer. Phytochemistry 59: 347-360.
29. Iturbe-Ormaetxe I, Haralampidis K, Papadopoulou K, Osbourn AE. 2003. Molecular cloning and characterization of triterpene synthases from Medicago truncatula and Lotus japonicus. Plant Molecular Biology 51: 731-743.
30. Kliebenstein DJ, Osbourn A. 2012. Making new molecules - evolution of pathways for novel metabolites in plants. Current Opinion in Plant Biology 5: 415-423.
31. Kudo F, Motegi A, Mizoue K, Eguchi T. 2010. Cloning and characterization of the biosynthetic gene cluster of 16-membered macrolide antibiotic FD-891: involvement of a dual functional cytochrome P450 monooxygenase and hydroxylation. ChemBioChem 11: 1574-1582.
32. Latunde-Dada AO, Cabello-Hurtado F, Czittrich N, Didierjean L, Schopfer C, Hertkorn N, Werck-Reichhart D, Ebel J. 2001. Flavonoid 6-hydroxylase from soybean (Glycine max L.), a novel plant P-450 monooxygenase. Journal of Biological Chemistry 276: 1688-1695.
33. Liu L, Lomonossoff G. 2002. Agroinfection as a rapid method for propagating Cowpea mosaic virus-based constructs. Journal of Virological Methods 105: 343-348.
34. Lombari P, Ercolano E, El Alaoui H, Chiurazzi M. 2003. A new transformation-regeneration procedure in the model legume Lotus japonicus: root explants as a source of large numbers of cells susceptible to Agrobacterium-mediated transformation. Plant Cell Reports 21: 771-777.
35. Lupien S, Karp F, Wildung M, Croteau R. 1999. Regiospecific cytochrome P450 limonene hydroxylases from mint (Mentha) species: cDNA isolation, characterization, and functional expression of (-)-4S-limonene-3-hydroxylase and (-)-4S-limonene-6-hydroxylase. Archives of Biochemistry and Biophysics 368: 181-192.
36. Lyons E, Freeling M. 2008 How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant Journal 53: 661-673.
37. Maekawa T, Kusakabe M, Shimoda Y, Sato S, Tabata S, Murooka Y, Hayashi M. 2008. Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Molecular Plant-Microbe Interactions 21: 375-382.
38. Martirani L, Stiller J, Mirabella R, Alfano F, Lamberti A, Radutoiu S, Iaccarino M, Gresshoff PM, Chiurazzi M. 1999. T-DNA tagging of nodulation- and root-related genes in Lotus japonicus: expression patterns and potential for promoter trapping and insertional mutagenesis. Molecular Plant-Microbe Interactions 12: 275-284.
39. Mylona P, Owatworakit A, Papadopoulou K, Jenner H, Qin B, Findlay K, Hill L, Qi X, Bakht S, Melton R et al. 2008. Sad3 and Sad4 are required for saponin biosynthesis and root development in oat. Plant Cell 20: 210-212.
40. Naoumkina MA, Modolo LV, Huhman DV, Urbanczyk-Wochniak E, Tang Y, Sumner LW, Dixon RA. 2010. Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell 22: 850-866.
41. Nelson D, Werck-Reichhart D. 2011. A P450-centric view of plant evolution. Plant Journal 66: 194-211.
42. Ohyama K, Suzuki M, Kikuchi J, Saito K, Muranaka T. 2009. Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106: 725-730.
43. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H. 2009. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoidphytoalexins in rice. Journal of Biological Chemistry 284: 26510-26518.
44. Osbourn A. 2010. Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends in Genetics 26: 449-457.
45. Osbourn AE, Field B. 2009. Operons. Cellular and Molecular Life Science 66: 3755-3775.
46. Osbourn A, Goss RJ, Field RA. 2011. The saponins: polar isoprenoids with important and diverse biological activities. Natural Product Reports 28: 1261-1268.
47. Papadopoulou K, Melton RE, Leggett M, Daniels MJ, Osbourn AE. 1999. Compromised disease resistance in saponin-deficient plants. Proceedings of the National Academy of Sciences, USA 96: 12923-12928.
48. Pauwels L, Inze D, Goossens A. 2009. Jasmonate-inducible gene: what does it mean? Trends in Plant Science 1: 87-91.
49. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29: e45.
50. Phillips DR, Rasbery JM, Bartel B, Matsuda SPT. 2006. Biosynthetic diversity in plant triterpene cyclization. Current Opinion in Plant Biology 9: 305-314.
51. Pollier J, Morreel K, Geelen D, Goossens A. 2011. Metabolite profiling of triterpene saponins in Medicago truncatula hairy roots by liquid chromatography Fourier transform ion cyclotron resonance mass spectrometry. Journal of Natural Products 74: 1462-1476.
52. Qi X, Bakht S, Leggett M, Maxwell C, Melton R, Osbourn A. 2004. A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proceedings of the National Academy of Sciences, USA 101: 8233-8238.
53. Qi X, Bakht S, Qin B, Leggett M, Hemmings A, Mellon F, Eagles J, Werck-Reichhart D, Schaller H, Lesot A et al. 2006. A different function for a member of an ancient and highly conserved cytochrome P450 family: from essential sterols to plant defense. Proceedings of the National Academy of Sciences, USA 103: 18848-18853.
54. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. 2003. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters 339: 62-66.
55. Rochfort S, Panozzo J. 2007. Phytochemicals for health, the role of pulses. Journal of Agricultural and Food Chemistry 55: 7981-7994.
56. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K et al. 2008. Genome structure of the legume, Lotus japonicus. DNA Research 15: 227-239.
57. Sawai S, Saito K. 2011. Triterpenoid biosynthesis and engineering in plants. Frontiers in Plant Science 2: 25.
58. Sawai S, Shindo T, Sato S, Kaneko T, Tabata S, Ayabe S, Aoki T. 2006. Functional and structural analysis of genes encoding oxidosqualene cyclases of Lotus japonicus. Plant Science 170: 247-257.
59. Schult K, Meierhoff K, Paradies S, Toller T, Wolff P, Westhoff P. 2007. The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19: 1329-1346.
60. Seki H, Ohyama K, Sawai S, Mizutani M, Ohnishi T, Sudo H, Akashi T, Aoki T, Saito K, Muranaka T. 2008. Licorice beta-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proceedings of the National Academy of Sciences, USA 105: 14204-14209.
61. Seki H, Sawai S, Ohyama K, Mizutani M, Ohnishi T, Sudo H, Fukushima EO, Akashi T, Aoki T, Saito K, Muranaka T. 2011. Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. The Plant Cell 23: 4112-4123.
62. Shimura K, Okada A, Okada K, Jikumaru Y, Ko KW, Toyomasu T, Sassa T, Hasegawa M, Kodama O, Shibuya N et al. 2007. Identification of a biosynthetic gene cluster in rice for momilactones. Journal of Biological Chemistry 282: 34013-34018.
63. Suzuki H, Achnine L, Xu R, Matsuda SP, Dixon RA. 2002. A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula. Plant Journal 32: 1033-1048.
64. Swaminathan S, Morrone D, Wang Q, Fulton DB, Peters RJ. 2009. CYP76M7 is an ent-cassadiene C11alpha-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell 21: 3315-3325.
65. Takahashi Y, Nishida Y, Ishii Y, Ishikawa K, Asai S. 2005. Monitoring expression of cytochrome P450 genes during postischemic rat liver reperfusion using DNA microarrays. Journal of Pharmacological Sciences 97: 153-156.
66. Takos AM, Knudsen C, Lai D, Kannangara R, Mikkelsen L, Motawia MS, Olsen CE, Sato S, Tabata S, Jorgensen K et al. 2011. Genomic clustering of cyanogenicglucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway. Plant Journal 68: 273-286.
67. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
68. Tokai T, Koshino H, Takahashi-Ando N, Sato M, Fujimura M, Kimura M. 2007. Fusarium Tri4 encodes a key multifunctional cytochrome P450 monooxygenase for four consecutive oxygenation steps in trichothecene biosynthesis. Biochemical and Biophysical Research Communications 353: 412-417.
69. Tsichritzis F, Jakupovic J. 1990. Diterpenes and other constituents from Relhania species. Phytochemistry 29: 3173-3187.
70. Ulubelen A, Topcu G, Lotter H, Wagner H, Eris C. 1994. Triterpenoids from the aerial parts of Salvia montbretii. Phytochemistry 36: 413-415.
71. Urbanski DF, Malolepszy A, Stougaard J, Andersen SU. 2012. Genome-wide LORE1 retrotransposon mutagenesis and high-throughput insertion detection in Lotus japonicus. Plant Journal 69: 731-741.
72. Vaistij FE, Jones L, Baulcombe DC. 2002. Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14: 857-867.
73. Voinnet O. 2008. Post-transcriptional RNA silencing in plant-microbe interactions: a touch of robustness and versatility. Current Opinion in Plant Biology 11: 464-470.
74. Voinnet O, Rivas S, Mestre P, Baulcombe D. 2003. An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant Journal 33: 949-956.
75. Wassenegger M, Heimes S, Riedel L, Sanger HL. 1994. RNA-directed de novo methylation of genomic sequences in plants. Cell 76: 567-576.
76. Wegel E, Koumproglou R, Shaw P, Osbourn A. 2009. Cell type-specific chromatin decondensation of a metabolic gene cluster in oats. Plant Cell 21: 3926-3936.
77. Whitmer S, Verpoorte R, Canel C. 1998. Influence of auxins on alkaloid accumulation by a transgenic cell line of Catharanthusroseus. Plant Cell, Tissue and Organ Culture 53: 135-141.
78. Wilderman PR, Xu M, Jin Y, Coates RM, Peters RJ. 2004. Identification of syn-pimara-7, 15-diene synthase reveals functional clustering of terpene synthases involved in rice phytoalexin/allelochemical biosynthesis. Plant Physiology 135: 2098-2105.
79. Wink M, Mohamed GIA. 2003. Evolution of chemical defense traits in the Leguminosae: mapping of distribution patterns of secondary metabolites on a molecular phylogeny inferred from nucleotide sequences of the rbcL gene. Biochemical Systematics and Ecology 31: 897-917.
80. Winzer T, Gazda V, He Z, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE et al. 2012. A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336: 1704-1708.
81. Xu R, Fazio GC, Matsuda SP. 2004. On the origins of triterpenoid skeletal diversity. Phytochemistry 65: 261-291.
82. Yahia A, Kevers C, Gaspar T, Chenieux J-C, Rideau M, Creche Jl. 1998. Cytokinins and ethylene stimulate indole alkaloid accumulation in cell suspension cultures of Catharanthus roseus by two distinct mechanisms. Plant Science 133: 9-15.
83. Zhao J, Davis LC, Verpoorte R. 2005. Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances 23: 283-333.