Comparative transcriptomics unravel biochemical specialization of leaf tissues of Stevia for diterpenoid production

Plant Physiology

Volumn 169, Issue 4, 2015, Pages 2462-2480

  Kim, Mi Jung ^a   Jin, Jingjing ^a   Zheng, Junshi ^a   Wong, Limsoon ^a   Chua, Nam Hai ^b   Jang, In Cheol ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2-C-METHYLERYTHRITOL 4-PHOSPHATE; DITERPENE; ENT-KAURENE SYNTHETASE A; ERYTHRITOL; ERYTHRITOL 4-PHOSPHATE; GLUCOSIDE; KAURANE DERIVATIVE; KAURENE; KAURENE SYNTHETASE; MANOYL OXIDE; PLANT PROTEIN; STEVIOL; STEVIOSIDE; SUGAR PHOSPHATE; TRANSCRIPTOME; TRANSFERASE;

ANALOGS AND DERIVATIVES; ANTIBODY SPECIFICITY; COMPARATIVE STUDY; GENETICS; METABOLISM; METABOLOME; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT LEAF; SEQUENCE ANALYSIS; STEVIA; TRICHOME; ULTRASTRUCTURE;

ALKYL AND ARYL TRANSFERASES; BASE SEQUENCE; DITERPENES; DITERPENES, KAURANE; ERYTHRITOL; GLUCOSIDES; METABOLOME; MOLECULAR SEQUENCE DATA; MUTATION; ORGAN SPECIFICITY; PHYLOGENY; PLANT LEAVES; PLANT PROTEINS; SEQUENCE ANALYSIS, RNA; STEVIA; SUGAR PHOSPHATES; TRANSCRIPTOME; TRICHOMES;

EID: 84949604823     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01353     Document Type: Article

References (65)

1. Adam P, Hecht S, Eisenreich W, Kaiser J, Grawert T, Arigoni D, Bacher A, Rohdich F (2002) Biosynthesis of terpenes: studies on 1-hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase. Proc Natl Acad Sci USA 99: 12108-12113
2. Adams RP (2007) Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry, Ed 4. Allured Publishing Corporation, Carol Stream, IL
3. Alvarez MA (2014) Plant Biotechnology for Health: From Secondary Metabolites to Molecular Farming. Springer International Publishing, Cham, Switzerland, pp 33-59
4. Armstrong DW, Zhou EY, Zukowski J, Kosmowska-Ceranowicz B (1996) Enantiomeric composition and prevalence of some bicyclic monoterpenoids in amber. Chirality 8: 39-48
5. Beck G, Coman D, Herren E, Ruiz-Sola MA, Rodríguez-Concepción M, Gruissem W, Vranová E (2013) Characterization of the GGPP synthase gene family in Arabidopsis thaliana. Plant Mol Biol 82: 393-416
6. Bleeker PM, Spyropoulou EA, Diergaarde PJ, Volpin H, De Both MT, Zerbe P, Bohlmann J, Falara V, Matsuba Y, Pichersky E, et al (2011) RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol Biol 77: 323-336
7. Boutanaev AM, Moses T, Zi J, Nelson DR, Mugford ST, Peters RJ, Osbourn A (2015) Investigation of terpene diversification across multiple sequenced plant genomes. Proc Natl Acad Sci USA 112: E81-E88
8. Brandle JE, Richman A, Swanson AK, Chapman BP (2002) Leaf Ests from Stevia rebaudiana: a resource for gene discovery in diterpene synthesis. Plant Mol Biol 50: 613-622
9. Brandle JE, Rosa N (1992) Heritability for yield, leaf:stem ratio and stevioside content estimated from a landrace cultivar of Stevia rebaudiana. Can J Plant Sci 72: 1263-1266
10. Brandle JE, Telmer PG (2007) Steviol glycoside biosynthesis. Phytochemistry 68: 1855-1863
11. Caniard A, Zerbe P, Legrand S, Cohade A, Valot N, Magnard JL, Bohlmann J, Legendre L (2012) Discovery and functional characterization of two diterpene synthases for sclareol biosynthesis in Salvia sclarea (L.) and their relevance for perfume manufacture. BMC Plant Biol 12: 119
12. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66: 212-229
13. Chen J, Hou K, Qin P, Liu H, Yi B, Yang W, Wu W (2014) RNA-seq for gene identification and transcript profiling of three Stevia rebaudiana genotypes. BMC Genomics 15: 571
14. Cho BO, Ryu HW, So Y, Cho JK, Woo HS, Jin CH, Seo KI, Park JC, Jeong IY (2013) Anti-inflammatory effect of austroinulin and 6-O-acetyl-austroinulin from Stevia rebaudiana in lipopolysaccharide-stimulated RAW264.7 macrophages. Food Chem Toxicol 62: 638-644
15. Cordoba E, Porta H, Arroyo A, San Román C, Medina L, Rodríguez-Concepción M, León P (2011) Functional characterization of the three genes encoding 1-deoxy-D-xylulose 5-phosphate synthase in maize. J Exp Bot 62: 2023-2038
16. Cordoba E, Salmi M, León P (2009) Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. J Exp Bot 60: 2933-2943
17. Cui G, Duan L, Jin B, Qian J, Xue Z, Shen G, Snyder JH, Song J, Chen S, Huang L, et al (2015) Functional divergence of diterpene syntheses in the medicinal plant Salvia miltiorrhiza. Plant Physiol 169: 1607-1618
18. Cui H, Zhang ST, Yang HJ, Ji H, Wang XJ (2011) Gene expression profile analysis of tobacco leaf trichomes. BMC Plant Biol 11: 76-86
19. De S, Mondal S, Banerjee S (2013) Introduction to stevioside. In Stevioside: Technology, Applications and Health. John Wiley & Sons, Oxford, pp 1-18
20. Falara V, Pichersky E, Kanellis AK (2010) A copal-8-ol diphosphate synthase from the angiosperm Cistus creticus subsp. creticus is a putative key enzyme for the formation of pharmacologically active, oxygencontaining labdane-type diterpenes. Plant Physiol 154: 301-310
21. Gang DR, Beuerle T, Ullmann P, Werck-Reichhart D, Pichersky E (2002) Differential production of meta hydroxylated phenylpropanoids in sweet basil peltate glandular trichomes and leaves is controlled by the activities of specific acyltransferases and hydroxylases. Plant Physiol 130: 1536-1544
22. Geuns JM (2003) Stevioside. Phytochemistry 64: 913-921
23. Glas JJ, Schimmel BC, Alba JM, Escobar-Bravo R, Schuurink RC, Kant MR (2012) Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci 13: 17077-17103
24. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29: 644-652
25. Guo J, Zhou YJ, Hillwig ML, Shen Y, Yang L, Wang Y, Zhang X, Liu W, Peters RJ, Chen X, et al (2013) CYP76AH1 catalyzes turnover of miltiradiene in tanshinones biosynthesis and enables heterologous production of ferruginol in yeasts. Proc Natl Acad Sci USA 110: 12108-12113
26. Guo Z, Severson RF, Wagner GJ (1994) Biosynthesis of the diterpene cisabienol in cell-free extracts of tobacco trichomes. Arch Biochem Biophys 308: 103-108
27. Harada E, Kim JA, Meyer AJ, Hell R, Clemens S, Choi YE (2010) Expression profiling of tobacco leaf trichomes identifies genes for biotic and abiotic stresses. Plant Cell Physiol 51: 1627-1637
28. Hedden P, Phillips AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5: 523-530
29. Huang K, Armstrong DW (2009) GC-MS analysis of crocetane, phytane and some of their stereoisomers using cyclodextrin-based stationary phases. Org Geochem 40: 283-286
30. Humphrey TV, Richman AS, Menassa R, Brandle JE (2006) Spatial organisation of four enzymes from Stevia rebaudiana that are involved in steviol glycoside synthesis. Plant Mol Biol 61: 47-62
31. Hunter WN (2007) The non-mevalonate pathway of isoprenoid precursor biosynthesis. J Biol Chem 282: 21573-21577
32. Ibrahim NA, El-Gengaihi S, Motawe H, Riad SA (2007) Phytochemical and biological investigation of Stevia rebaudiana Bertoni; 1-labdane-type diterpene. Eur Food Res Technol 224: 483-488
33. Jin J, Kim MJ, Dhandapani S, Tjhang JG, Yin JL, Wong L, Sarojam R, Chua NH, Jang IC (2015) The floral transcriptome of ylang ylang (Cananga odorata var. fruticosa) uncovers biosynthetic pathways for volatile organic compounds and a multifunctional and novel sesquiterpene synthase. J Exp Bot 66: 3959-3975
34. Jin J, Panicker D, Wang Q, Kim MJ, Liu J, Yin JL, Wong L, Jang IC, Chua NH, Sarojam R (2014) Next generation sequencing unravels the biosynthetic ability of spearmint (Mentha spicata) peltate glandular trichomes through comparative transcriptomics. BMC Plant Biol 14: 292
35. Kandra L, Wagner GJ (1988) Studies of the site and mode of biosynthesis of tobacco trichome exudate components. Arch Biochem Biophys 265: 425-432
36. Keene CK, Wagner GJ (1985) Direct demonstration of duvatrienediol biosynthesis in glandular heads of tobacco trichomes. Plant Physiol 79: 1026-1032
37. King AJ, Brown GD, Gilday AD, Larson TR, Graham IA (2014) Production of bioactive diterpenoids in the Euphorbiaceae depends on evolutionarily conserved gene clusters. Plant Cell 26: 3286-3298
38. Kumar H, Kaul K, Bajpai-Gupta S, Kaul VK, Kumar S (2012) A comprehensive analysis of fifteen genes of steviol glycosides biosynthesis pathway in Stevia rebaudiana (Bertoni). Gene 492: 276-284
39. Lange BM, Wildung MR, Stauber EJ, Sanchez C, Pouchnik D, Croteau R (2000) Probing essential oil biosynthesis and secretion by functional evaluation of expressed sequence tags from mint glandular trichomes. Proc Natl Acad Sci USA 97: 2934-2939
40. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359
41. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics 12: 323
42. Liang PH, Ko TP, Wang AHJ (2002) Structure, mechanism and function of prenyltransferases. Eur J Biochem 269: 3339-3354
43. Markovi_c IS, Đarmati ZA, Abramovi_c BF (2008) Chemical composition of leaf extracts of Stevia rebaudiana Bertoni grown experimentally in Vojvodina. J Serb Chem Soc 73: 283-297
44. McGarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7: 1015-1026
45. Obtani K, Yamasaki K (2002) Methods to improve the taste of the sweet principles of Stevia rebaudiana. In AD Kinghorn, ed, Stevia: The Genus Stevia. Taylor and Francis, London and New York, pp 138-159
46. Pateraki I, Andersen-Ranberg J, Hamberger B, Heskes AM, Martens HJ, Zerbe P, Bach SS, Møller BL, Bohlmann J, Hamberger B (2014) Manoyl oxide (13R), the biosynthetic precursor of forskolin, is synthesized in specialized root cork cells in Coleus forskohlii. Plant Physiol 164: 1222-1236
47. Peters RJ (2010) Two rings in them all: the labdane-related diterpenoids. Nat Prod Rep 27: 1521-1530
48. Philippe RN, De Mey M, Anderson J, Ajikumar PK (2014) Biotechnological production of natural zero-calorie sweeteners. Curr Opin Biotechnol 26: 155-161
49. Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Urós EM, Boland W, Strack D, Rodríguez-Concepción M, Bohlmann J, et al (2007) Functional identification and differential expression of 1-deoxy-Dxylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol 65: 243-257
50. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R (2005) InterProScan: protein domains identifier. Nucleic Acids Res 33: W116-W120
51. Richman A, Swanson A, Humphrey T, Chapman R, McGarvey B, Pocs R, Brandle J (2005) Functional genomics uncovers three glucosyltransferases involved in the synthesis of the major sweet glucosides of Stevia rebaudiana. Plant J 41: 56-67
52. Richman AS, Gijzen M, Starratt AN, Yang Z, Brandle JE (1999) Diterpene synthesis in Stevia rebaudiana: recruitment and up-regulation of key enzymes from the gibberellin biosynthetic pathway. Plant J 19: 411-421
53. Sallaud C, Giacalone C, Töpfer R, Goepfert S, Bakaher N, Rösti S, Tissier A (2012) Characterization of two genes for the biosynthesis of the labdane diterpene Z-abienol in tobacco (Nicotiana tabacum) glandular trichomes. Plant J 72: 1-17
54. Starratt AN, Kirby CW, Pocs R, Brandle JE (2002) Rebaudioside F, a diterpene glycoside from Stevia rebaudiana. Phytochemistry 59: 367-370
55. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729
56. Totté N, Charon L, Rohmer M, Compernolle F, Baboeuf I, Geuns JMC (2000) Biosynthesis of the diterpenoid steviol, an ent-kaurene derivative from Stevia rebaudiana Bertoni, via the methylerythritol phosphate pathway. Tetrahedron Lett 41: 6407-6410
57. Totté N, Van den Ende W, Damme EJMV, Compernolle F, Baboeuf I, Geuns JMC (2003) Cloning and heterologous expression of early genes in gibberellin and steviol biosynthesis via the methylerythritol phosphate pathway in Stevia rebaudiana. Can J Bot 81: 517-522
58. Toyomasu T, Sassa T (2010) Diterpenes. In L Mander, HW Lui, eds, Comprehensive Natural Products II. Chemistry and Biology, Vol 1. Elsevier, Oxford, pp 643-672
59. Turner GW, Gershenzon J, Croteau RB (2000) Distribution of peltate glandular trichomes on developing leaves of peppermint. Plant Physiol 124: 655-664
60. Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-D-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31: 243-254
61. Wang E, Wang R, DeParasis J, Loughrin JH, Gan S, Wagner GJ (2001) Suppression of a P450 hydroxylase gene in plant trichome glands enhances natural-product-based aphid resistance. Nat Biotechnol 19: 371-374
62. Zerbe P, Bohlmann J (2015) Plant diterpene synthases: exploring modularity and metabolic diversity for bioengineering. Trends Biotechnol 33: 419-428
63. Zerbe P, Hamberger B, Yuen MM, Chiang A, Sandhu HK, Madilao LL, Nguyen A, Hamberger B, Bach SS, Bohlmann J (2013) Gene discovery of modular diterpene metabolism in nonmodel systems. Plant Physiol 162: 1073-1091
64. Zi J, Mafu S, Peters RJ (2014) To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism. Annu Rev Plant Biol 65: 259-286
65. Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52: 86-97