Draft genome assembly and annotation of Glycyrrhiza uralensis, a medicinal legume

Plant Journal

Volumn 89, Issue 2, 2017, Pages 181-194

  Mochida, Keiichi ^a,b,c   Sakurai, Tetsuya ^a,d   Seki, Hikaru ^a,e   Yoshida, Takuhiro ^a   Takahagi, Kotaro ^a,c   Sawai, Satoru ^a,e   Uchiyama, Hiroshi ^f   Muranaka, Toshiya ^a,e   Saito, Kazuki ^a,g  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b OKAYAMA UNIVERSITY   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d KOCHI UNIVERSITY   (Japan)

^e OSAKA UNIVERSITY   (Japan)

^f NIHON UNIVERSITY   (Japan)

^g CHIBA UNIVERSITY   (Japan)

Author keywords

flavonoid; genome sequence; Glycyrrhiza uralensis; liquorice licorice; P450; PRJDB3943; synteny; UDP dependent glycosyltransferases

Indexed keywords

BIOCHEMISTRY; BIOSYNTHESIS; FLAVONOIDS; GENETIC ENGINEERING; PLANTS (BOTANY);

FLAVONOID; GENOME SEQUENCES; GLYCOSYLTRANSFERASES; GLYCYRRHIZA URALENSIS; LIQUORICE/LICORICE; P450; PRJDB3943; SYNTENY;

GENE EXPRESSION;

CYTOCHROME P450; FLAVONOID; GLUCURONOSYLTRANSFERASE; GLYCYRRHIZIC ACID; ISOFLAVONE 7-O-METHYLTRANSFERASE; METHYLTRANSFERASE; PLANT PROTEIN;

BARREL MEDIC; BIOSYNTHESIS; CICER; GENETICS; GLYCYRRHIZA URALENSIS; MEDICINAL PLANT; METABOLISM; MOLECULAR GENETICS; PLANT GENOME;

CICER; CYTOCHROME P-450 ENZYME SYSTEM; FLAVONOIDS; GENOME, PLANT; GLUCURONOSYLTRANSFERASE; GLYCYRRHIZA URALENSIS; GLYCYRRHIZIC ACID; MEDICAGO TRUNCATULA; METHYLTRANSFERASES; MOLECULAR SEQUENCE ANNOTATION; PLANT PROTEINS; PLANTS, MEDICINAL;

EID: 85002246077     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.13385     Document Type: Article

References (69)

1. Achnine, L., Huhman, D.V., Farag, M.A., Sumner, L.W., Blount, J.W. and Dixon, R.A. (2005) Genomics-based selection and functional characterization of triterpene glycosyltransferases from the model legume Medicago truncatula. Plant J. 41, 875–887.
2. Afendi, F.M., Okada, T., Yamazaki, M. et al. (2012) KNApSAcK family databases: integrated metabolite-plant species databases for multifaceted plant research. Plant Cell Physiol. 53, e1.
3. Arendt, P., Pollier, J., Callewaert, N. and Goossens, A. (2016) Synthetic biology for production of natural and new-to-nature terpenoids in photosynthetic organisms. Plant J. 87, 16–37.
4. Asl, M.N. and Hosseinzadeh, H. (2008) Review of pharmacological effects of Glycyrrhiza sp. and its bioactive compounds. Phytother. Res. 22, 709–724.
5. Bertioli, D.J., Cannon, S.B., Froenicke, L. et al. (2016) The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nat. Genet. 48, 438–446.
6. Boycheva, S., Daviet, L., Wolfender, J.L. and Fitzpatrick, T.B. (2014) The rise of operon-like gene clusters in plants. Trends Plant Sci. 19, 447–459.
7. Campbell, M.S., Law, M., Holt, C. et al. (2014) MAKER-P: a tool kit for the rapid creation, management, and quality control of plant genome annotations. Plant Physiol. 164, 513–524.
8. Cannon, S.B., May, G.D. and Jackson, S.A. (2009) Three sequenced legume genomes and many crop species: rich opportunities for translational genomics. Plant Physiol. 151, 970–977.
9. Chae, L., Kim, T., Nilo-Poyanco, R. and Rhee, S.Y. (2014) Genomic signatures of specialized metabolism in plants. Science, 344, 510–513.
10. Chaisson, M.J. and Tesler, G. (2012) Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): application and theory. BMC Bioinformatics, 13, 238.
11. Cingolani, P., Platts, A., Wang le, L., Coon, M., Nguyen, T., Wang, L., Land, S.J., Lu, X. and Ruden, D.M. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin), 6, 80–92.
12. De Luca, V., Salim, V., Atsumi, S.M. and Yu, F. (2012) Mining the biodiversity of plants: a revolution in the making. Science, 336, 1658–1661.
13. De Vega, J.J., Ayling, S., Hegarty, M. et al. (2015) Red clover (Trifolium pratense L.) draft genome provides a platform for trait improvement. Sci. Rep. 5, 17394.
14. English, A.C., Richards, S., Han, Y. et al. (2012) Mind the gap: upgrading genomes with Pacific Biosciences RS long-read sequencing technology. PLoS ONE, 7, e47768.
15. Fukushima, A., Kusano, M., Redestig, H., Arita, M. and Saito, K. (2009) Integrated omics approaches in plant systems biology. Curr. Opin. Chem. Biol. 13, 532–538.
16. Fukushima, E.O., Seki, H., Sawai, S., Suzuki, M., Ohyama, K., Saito, K. and Muranaka, T. (2013) Combinatorial biosynthesis of legume natural and rare triterpenoids in engineered yeast. Plant Cell Physiol. 54, 740–749.
17. Gnerre, S., Maccallum, I., Przybylski, D. et al. (2011) High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA, 108, 1513–1518.
18. Hane, J.K., Ming, Y., Kamphuis, L.G. et al. (2016) A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant-microbe interactions and legume evolution. Plant Biotechnol. J., doi: 10.1111/pbi.12615.
19. Hayashi, H. and Sudo, H. (2009) Economic importance of licorice. Plant Biotechnol. 26, 101–104.
20. Hosseinzadeh, H. and Nassiri-Asl, M. (2015) Pharmacological effects of Glycyrrhiza spp. and its bioactive constituents: update and review. Phytother. Res. 29, 1868–1886.
21. Hunt, M., Kikuchi, T., Sanders, M., Newbold, C., Berriman, M. and Otto, T.D. (2013) REAPR: a universal tool for genome assembly evaluation. Genome Biol. 14, R47.
22. Jain, M., Misra, G., Patel, R.K. et al. (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J. 74, 715–729.
23. Ji, S., Li, Z., Song, W. et al. (2016) Bioactive constituents of Glycyrrhiza uralensis (Licorice): discovery of the effective components of a traditional herbal medicine. J. Nat. Prod. 79, 281–292.
24. Kang, Y.J., Kim, S.K., Kim, M.Y. et al. (2014) Genome sequence of mungbean and insights into evolution within Vigna species. Nat. Commun. 5, 5443.
25. Kao, T.C., Wu, C.H. and Yen, G.C. (2014) Bioactivity and potential health benefits of licorice. J. Agric. Food Chem. 62, 542–553.
26. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S.L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.
27. Koren, S., Schatz, M.C., Walenz, B.P. et al. (2012) Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotechnol. 30, 693–700.
28. Krokida, A., Delis, C., Geisler, K., Garagounis, C., Tsikou, D., Pena-Rodriguez, L.M., Katsarou, D., Field, B., Osbourn, A.E. and Papadopoulou, K.K. (2013) A metabolic gene cluster in Lotus japonicus discloses novel enzyme functions and products in triterpene biosynthesis. New Phytol. 200, 675–690.
29. Li, H. and Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754–1760.
30. Li, L., Stoeckert, C.J. Jr and Roos, D.S. (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13, 2178–2189.
31. Lohse, M., Drechsel, O., Kahlau, S. and Bock, R. (2013) OrganellarGenomeDRAW–a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 41, W575–W581.
32. Lomsadze, A., Ter-Hovhannisyan, V., Chernoff, Y.O. and Borodovsky, M. (2005) Gene identification in novel eukaryotic genomes by self-training algorithm. Nucleic Acids Res. 33, 6494–6506.
33. Lukashin, A.V. and Borodovsky, M. (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res. 26, 1107–1115.
34. Mochida, K., Yoshida, T., Sakurai, T., Yamaguchi-Shinozaki, K., Shinozaki, K. and Tran, L.S. (2010) LegumeTFDB: an integrative database of Glycine max, Lotus japonicus and Medicago truncatula transcription factors. Bioinformatics, 26, 290–291.
35. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A.C. and Kanehisa, M. (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 35, W182–W185.
36. Murat, F., Louis, A., Maumus, F., Armero, A., Cooke, R., Quesneville, H., Roest Crollius, H. and Salse, J. (2015) Understanding Brassicaceae evolution through ancestral genome reconstruction. Genome Biol. 16, 262.
37. Naoumkina, M.A., Modolo, L.V., Huhman, D.V., Urbanczyk-Wochniak, E., Tang, Y., Sumner, L.W. and Dixon, R.A. (2010) Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell, 22, 850–866.
38. Nutzmann, H.W. and Osbourn, A. (2014) Gene clustering in plant specialized metabolism. Curr. Opin. Biotechnol. 26, 91–99.
39. Nutzmann, H.W., Huang, A. and Osbourn, A. (2016) Plant metabolic clusters - from genetics to genomics. New Phytol. 211, 771–789.
40. Ober, D. (2005) Seeing double: gene duplication and diversification in plant secondary metabolism. Trends Plant Sci. 10, 444–449.
41. Osbourn, A.E. (2003) Saponins in cereals. Phytochemistry, 62, 1–4.
42. Parra, G., Bradnam, K. and Korf, I. (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics, 23, 1061–1067.
43. Pfosser, M., Amon, A., Lelley, T. and Heberlebors, E. (1995) Evaluation of sensitivity of flow-cytometry in detecting aneuploidy in wheat using disomic and ditelosomic wheat-rye addition lines. Cytometry, 21, 387–393.
44. Quinlan, A.R. and Hall, I.M. (2010) BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics, 26, 841–842.
45. Rai, A. and Saito, K. (2016) Omics data input for metabolic modeling. Curr. Opin. Biotechnol. 37, 127–134.
46. Ramilowski, J.A., Sawai, S., Seki, H., Mochida, K., Yoshida, T., Sakurai, T., Muranaka, T., Saito, K. and Daub, C.O. (2013) Glycyrrhiza uralensis transcriptome landscape and study of phytochemicals. Plant Cell Physiol. 54, 697–710.
47. Renault, H., Bassard, J.E., Hamberger, B. and Werck-Reichhart, D. (2014) Cytochrome P450-mediated metabolic engineering: current progress and future challenges. Curr. Opin. Plant Biol. 19, 27–34.
48. Salse, J., Abrouk, M., Bolot, S., Guilhot, N., Courcelle, E., Faraut, T., Waugh, R., Close, T.J., Messing, J. and Feuillet, C. (2009) Reconstruction of monocotelydoneous proto-chromosomes reveals faster evolution in plants than in animals. Proc. Natl Acad. Sci. USA, 106, 14908–14913.
49. Sato, S., Nakamura, Y., Kaneko, T. et al. (2008) Genome structure of the legume, Lotus japonicus. DNA Res. 15, 227–239.
50. Sawai, S. and Saito, K. (2011) Triterpenoid biosynthesis and engineering in plants. Front. Plant Sci. 2, 25.
51. Schmutz, J., Cannon, S.B., Schlueter, J. et al. (2010) Genome sequence of the palaeopolyploid soybean. Nature, 463, 178–183.
52. Seki, H., Ohyama, K., Sawai, S., Mizutani, M., Ohnishi, T., Sudo, H., Akashi, T., Aoki, T., Saito, K. and Muranaka, T. (2008) Licorice beta-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc. Natl Acad. Sci. USA, 105, 14204–14209.
53. Seki, H., Sawai, S., Ohyama, K. et al. (2011) Triterpene functional genomics in licorice for identification of CYP72A154 involved in the biosynthesis of glycyrrhizin. Plant Cell, 23, 4112–4123.
54. Seki, H., Tamura, K. and Muranaka, T. (2015) P450s and UGTs: key players in the structural diversity of Triterpenoid Saponins. Plant Cell Physiol. 56, 1463–1471.
55. Soderlund, C., Bomhoff, M. and Nelson, W.M. (2011) SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res. 39, e68.
56. Stanke, M., Keller, O., Gunduz, I., Hayes, A., Waack, S. and Morgenstern, B. (2006) AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res. 34, W435–W439.
57. Sudo, H., Seki, H., Sakurai, N. et al. (2009) Expressed sequence tags from rhizomes of Glycyrrhiza uralensis. Plant Biotechnol. 26, 105–107.
58. Sumner, L.W., Lei, Z., Nikolau, B.J. and Saito, K. (2015) Modern plant metabolomics: advanced natural product gene discoveries, improved technologies, and future prospects. Nat. Prod. Rep. 32, 212–229.
59. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.
60. Tang, H., Bowers, J.E., Wang, X. and Paterson, A.H. (2010) Angiosperm genome comparisons reveal early polyploidy in the monocot lineage. Proc. Natl Acad. Sci. USA, 107, 472–477.
61. Tang, Z.H., Li, T., Tong, Y.G., Chen, X.J., Chen, X.P., Wang, Y.T. and Lu, J.J. (2015) A systematic review of the anticancer properties of compounds isolated from Licorice (Gancao). Planta Med. 81, 1670–1687.
62. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L. and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578.
63. Varshney, R.K., Chen, W., Li, Y. et al. (2012) Draft genome sequence of pigeonpea (Cajanus cajan), an orphan legume crop of resource-poor farmers. Nat. Biotechnol. 30, 83–89.
64. Varshney, R.K., Song, C., Saxena, R.K. et al. (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat. Biotechnol. 31, 240–246.
65. Wang, L., Yang, R., Yuan, B., Liu, Y. and Liu, C. (2015) The antiviral and antimicrobial activities of licorice, a widely-used Chinese herb. Acta Pharm. Sin. B, 5, 310–315.
66. Wu, T.D. and Watanabe, C.K. (2005) GMAP: A Genomic Mapping and Alignment Program for mRNA and EST sequences. Bioinformatics, 21, 1859–1875.
67. Wyman, S.K., Jansen, R.K. and Boore, J.L. (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics, 20, 3252–3255.
68. Yonekura-Sakakibara, K. and Saito, K. (2009) Functional genomics for plant natural product biosynthesis. Nat. Prod. Rep. 26, 1466–1487.
69. Young, N.D., Debelle, F., Oldroyd, G.E. et al. (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature, 480, 520–524.