High-throughput sequencing and de novo assembly of red and green forms of the Perilla frutescens var. crispa transcriptome

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Fukushima, Atsushi ^a   Nakamura, Michimi ^b   Suzuki, Hideyuki ^c   Saito, Kazuki ^a,b   Yamazaki, Mami ^b  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b CHIBA UNIVERSITY   (Japan)

^c KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHOCYANIDIN SYNTHASE; ANTHOCYANIN; COMPLEMENTARY DNA; DIHYDROFLAVONOL 4 REDUCTASE; FLAVONOID 3' HYDROXYLASE; LIMONENE SYNTHASE; OXIDOREDUCTASE; OXYGENASE; SYNTHETASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; MICROSATELLITE DNA;

ARTICLE; BIOCHEMISTRY; BIOENGINEERING; BIOTECHNOLOGY; CONTROLLED STUDY; DNA SEQUENCE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE ONTOLOGY; GENETIC TRANSCRIPTION; GREEN PERILLA; HIGH THROUGHPUT SEQUENCING; MOLECULAR BIOLOGY; MOLECULAR GENETICS; NONHUMAN; PERILLA FRUTESCENS; PHYTOCHEMISTRY; PLANT GENE; PLANT METABOLISM; RED PERILLA; RELIABILITY; RNA SEQUENCE; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCEDURES;

LAMIACEAE; PERILLA; PERILLA FRUTESCENS; PERILLA FRUTESCENS VAR. CRISPA;

ANTHOCYANINS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; METABOLIC NETWORKS AND PATHWAYS; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE ANNOTATION; PERILLA FRUTESCENS; TRANSCRIPTOME;

EID: 84936152104     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129154     Document Type: Article

References (65)

1. Winkel-Shirley B. Biosynthesis of flavonoids and effects of stress. Current opinion in plant biology. 2002; 5(3):218-23. PMID: 11960739.
2. Moura JC, Bonine CA, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P. Abiotic and biotic stresses and changes in the lignin content and composition in plants. Journal of integrative plant biology. 2010; 52(4):360-76. doi: 10.1111/j.1744-7909.2010.00892.x PMID: 20377698.
3. Koes R, Verweij W, Quattrocchio F. Flavonoids: a colorful model for the regulation and evolution of biochemical pathways. Trends in plant science. 2005; 10(5):236-42. doi: 10.1016/j.tplants.2005.03.002 PMID: 15882656.
4. Saito K, Yonekura-Sakakibara K, Nakabayashi R, Higashi Y, Yamazaki M, Tohge T, et al. The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant physiology and biochemistry: PPB / Societe francaise de physiologie vegetale. 2013; 72:21-34. doi: 10.1016/j.plaphy.2013.02.001 PMID: 23473981.
5. Tohge T, Nishiyama Y, Hirai MY, Yano M, Nakajima J, Awazuhara M, et al. Functional genomics by integrated analysis of metabolome and transcriptome of Arabidopsis plants over-expressing an MYB transcription factor. The Plant journal: for cell and molecular biology. 2005; 42(2):218-35. doi: 10.1111/j.1365-313X.2005.02371.x PMID: 15807784.
6. Yonekura-Sakakibara K, Tohge T, Matsuda F, Nakabayashi R, Takayama H, Niida R, et al. Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. The Plant cell. 2008; 20(8):2160-76. doi: 10.1105/tpc.108.058040 PMID: 18757557; PubMed Central PMCID: PMC2553606.
7. Yonekura-Sakakibara K, Fukushima A, Nakabayashi R, Hanada K, Matsuda F, Sugawara S, et al. Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. The Plant journal: for cell and molecular biology. 2012; 69(1):154-67. doi: 10.1111/j.1365-313X.2011.04779.x PMID: 21899608; PubMed Central PMCID: PMC3507004.
8. Yonekura-Sakakibara K, Nakabayashi R, Sugawara S, Tohge T, Ito T, Koyanagi M, et al. A flavonoid 3-O-glucoside:2″-O-glucosyltransferase responsible for terminal modification of pollen-specific flavonols in Arabidopsis thaliana. The Plant journal: for cell and molecular biology. 2014; 79(5):769-82. doi: 10.1111/tpj.12580 PMID: 24916675.
9. Matsuda F, Okazaki Y, Oikawa A, Kusano M, Nakabayashi R, Kikuchi J, et al. Dissection of genoty-pephenotype associations in rice grains using metabolome quantitative trait loci analysis. The Plant journal: for cell and molecular biology. 2012; 70(4):624-36. doi: 10.1111/j.1365-313X.2012.04903.x PMID: 22229385.
10. Gong L, Chen W, Gao Y, Liu X, Zhang H, Xu C, et al. Genetic analysis of the metabolome exemplified using a rice population. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110(50):20320-5. doi: 10.1073/pnas.1319681110 PMID: 24259710; PubMed Central PMCID: PMC3864304.
11. Kondo T, Tamura H, Yoshida K, Goto T. Structure of malonylshisonin, a genuine pigment in purple leaves of Perilla ocimoides L. var. crispa Benth. Agric Biol Chem. 1989; 53(3):797-800.
12. Yamazaki M, Nakajima J, Yamanashi M, Sugiyama M, Makita Y, Springob K, et al. Metabolomics and differential gene expression in anthocyanin chemo-varietal forms of Perilla frutescens. Phytochemistry. 2003; 62(6):987-95. PMID: 12590125.
13. Yamazaki M, Saito K. Differential display analysis of gene expression in plants. Cellular and molecular life sciences: CMLS. 2002; 59(8):1246-55. PMID: 12363028.
14. Saito K, Yamazaki M. Biochemistry and molecular biology of the late-stage of biosynthesis of anthocyanin: lessons from Perilla frutescens as a model plant. New Phytol. 2002; 155(1):9-23. doi: 10.1046/j.1469-8137.2002.00440.x
15. Gong ZZ, Yamazaki M, Saito K. A light-inducible Myb-like gene that is specifically expressed in red Perilla frutescens and presumably acts as a determining factor of the anthocyanin forma. Molecular & general genetics: MGG. 1999; 262(1):65-72. PMID: 10503537.
16. Gong ZZ, Yamagishi E, Yamazaki M, Saito K. A constitutively expressed Myc-like gene involved in anthocyanin biosynthesis from Perilla frutescens: molecular characterization, heterologous expression in transgenic plants and transactivation in yeast cells. Plant molecular biology. 1999; 41(1):33-44. PMID: 10561066.
17. Kitada C, Gong Z, Tanaka Y, Yamazaki M, Saito K. Differential expression of two cytochrome P450s involved in the biosynthesis of flavones and anthocyanins in chemo-varietal forms of Perilla frutescens. Plant & cell physiology. 2001; 42(12):1338-44. PMID: 11773526.
18. Saito K, Kobayashi M, Gong Z, Tanaka Y, Yamazaki M. Direct evidence for anthocyanidin synthase as a 2-oxoglutarate-dependent oxygenase: molecular cloning and functional expression of cDNA from a red forma of Perilla frutescens. The Plant journal: for cell and molecular biology. 1999; 17(2):181-9. PMID: 10074715.
19. Gong Z, Yamazaki M, Sugiyama M, Tanaka Y, Saito K. Cloning and molecular analysis of structural genes involved in anthocyanin biosynthesis and expressed in a forma-specific manner in Perilla frutescens. Plant molecular biology. 1997; 35(6):915-27. PMID: 9426610.
20. Yamazaki M, Gong Z, Fukuchi-Mizutani M, Fukui Y, Tanaka Y, Kusumi T, et al. Molecular cloning and biochemical characterization of a novel anthocyanin 5-O-glucosyltransferase by mRNA differential display for plant forms regarding anthocyanin. The Journal of biological chemistry. 1999; 274(11):7405-11. PMID: 10066805.
21. Lee SC, Lee J, Kim NH, Park JY, Kim HU, Lee HO, et al. Analysis of expressed sequence tags from a normalized cDNA library of perilla (Perilla frutescens). J Plant Biol. 2014; 57(5):312-20.
22. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nature reviews Genetics. 2009; 10(1):57-63. doi: 10.1038/nrg2484 PMID: 19015660; PubMed Central PMCID: PMC2949280.
23. Garber M, Grabherr MG, Guttman M, Trapnell C. Computational methods for transcriptome annotation and quantification using RNA-seq. Nature methods. 2011; 8(6):469-77. doi: 10.1038/nmeth.1613 PMID: 21623353.
24. Gongora-Castillo E, Buell CR. Bioinformatics challenges in de novo transcriptome assembly using short read sequences in the absence of a reference genome sequence. Natural product reports. 2013; 30(4):490-500. doi: 10.1039/c3np20099j PMID: 23377493.
25. Fukushima A, Kusano M. A network perspective on nitrogen metabolism from model to crop plants using integrated 'omics' approaches. Journal of experimental botany. 2014; 65(19):5619-30. doi: 10.1093/jxb/eru322 PMID: 25129130.
26. Gongora-Castillo E, Childs KL, Fedewa G, Hamilton JP, Liscombe DK, Magallanes-Lundback M, et al. Development of transcriptomic resources for interrogating the biosynthesis of monoterpene indole alkaloids in medicinal plant species. PloS one. 2012; 7(12):e52506. doi: 10.1371/journal.pone.0052506 PMID: 23300689; PubMed Central PMCID: PMC3530497.
27. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature biotechnology. 2011; 29(7):644-52. doi: 10.1038/nbt.1883 PMID: 21572440; PubMed Central PMCID: PMC3571712.
28. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology. 2009; 10(3):R25. doi: 10.1186/gb-2009-10-3-r25 PMID: 19261174; PubMed Central PMCID: PMC2690996.
29. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics. 2011; 12:323. doi: 10.1186/1471-2105-12-323 PMID: 21816040; PubMed Central PMCID: PMC3163565.
30. Benson DA, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic acids research. 2014. doi: 10.1093/nar/gku1216 PMID: 25414350.
31. Yamazaki M, Shibata M, Nishiyama Y, Springob K, Kitayama M, Shimada N, et al. Differential gene expression profiles of red and green forms of Perilla frutescens leading to comprehensive identification of anthocyanin biosynthetic genes. The FEBS journal. 2008; 275(13):3494-502. doi: 10.1111/j.1742-4658.2008.06496.x PMID: 18513325.
32. Suzuki H, Nakayama T, Nishino T. Proposed mechanism and functional amino acid residues of malonyl-CoA:anthocyanin 5-O-glucoside-6⌄-O-malonyltransferase from flowers of Salvia splendens, a member of the versatile plant acyltransferase family. Biochemistry. 2003; 42(6):1764-71. doi: 10.1021/bi020618g PMID: 12578391.
33. Sompornpailin K, Makita Y, Yamazaki M, Saito K. A WD-repeat-containing putative regulatory protein in anthocyanin biosynthesis in Perilla frutescens. Plant molecular biology. 2002; 50(3):485-95. PMID: 12369624.
34. Mau CJ, Karp F, Ito M, Honda G, Croteau RB. A candidate cDNA clone for (-)-limonene-7-hydroxylase from Perilla frutescens. Phytochemistry. 2010; 71(4):373-9. doi: 10.1016/j.phytochem.2009.12.002 PMID: 20079506.
35. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of molecular biology. 1990; 215(3):403-10. doi: 10.1016/S0022-2836(05)80360-2 PMID: 2231712.
36. The Gene Ontology C. Gene Ontology Consortium: going forward. Nucleic acids research. 2014. doi: 10.1093/nar/gku1179 PMID: 25428369.
37. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21(18): 3674-6. doi: 10.1093/bioinformatics/bti610 PMID: 16081474.
38. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic acids research. 2014; 42(Database issue): D199-205. doi: 10.1093/nar/gkt1076 PMID: 24214961; PubMed Central PMCID: PMC3965122.
39. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, et al. WEGO: a web tool for plotting GO annotations. Nucleic acids research. 2006; 34(Web Server issue):W293-7. doi: 10.1093/nar/gkl031 PMID: 16845012; PubMed Central PMCID: PMC1538768.
40. Hancock JM. Simple sequences in a "minimal' genome. Nature genetics. 1996; 14(1):14-5. doi: 10.1038/ng0996-14 PMID: 8782812.
41. Varshney RK, Graner A, Sorrells ME. Genic microsatellite markers in plants: features and applications. Trends in biotechnology. 2005; 23(1):48-55. doi: 10.1016/j.tibtech.2004.11.005 PMID: 15629858.
42. Thiel T, Michalek W, Varshney RK, Graner A. Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). TAG Theoretical and applied genetics Theoretische und angewandte Genetik. 2003; 106(3):411-22. doi: 10.1007/s00122-002-1031-0 PMID: 12589540.
43. Sun J, Nishiyama T, Shimizu K, Kadota K. TCC: an R package for comparing tag count data with robust normalization strategies. BMC bioinformatics. 2013; 14:219. doi: 10.1186/1471-2105-14-219 PMID: 23837715; PubMed Central PMCID: PMC3716788.
44. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics. 2005; 21(16):3448-9. doi: 10.1093/bioinformatics/bti551 PMID: 15972284.
45. Schoenbohm C, Martens S, Eder C, Forkmann G, Weisshaar B. Identification of the Arabidopsis thaliana flavonoid 3′-hydroxylase gene and functional expression of the encoded P450 enzyme. Biological chemistry. 2000; 381(8):749-53. doi: 10.1515/BC.2000.095 PMID: 11030432.
46. Shirley BW, Hanley S, Goodman HM. Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. The Plant cell. 1992; 4(3):333-47. doi: 10.1105/tpc.4.3.333 PMID: 1354004; PubMed Central PMCID: PMC160133.
47. Devic M, Guilleminot J, Debeaujon I, Bechtold N, Bensaude E, Koornneef M, et al. The BANYULS gene encodes a DFR-like protein and is a marker of early seed coat development. The Plant journal: for cell and molecular biology. 1999; 19(4):387-98. PMID: 10504561.
48. Grotewold E, Drummond BJ, Bowen B, Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994; 76(3):543-53. PMID: 8313474.
49. Procissi A, Dolfini S, Ronchi A, Tonelli C. Light-Dependent Spatial and Temporal Expression of Pigment Regulatory Genes in Developing Maize Seeds. The Plant cell. 1997; 9(9):1547-57. doi: 10.1105/tpc.9.9.1547 PMID: 12237395; PubMed Central PMCID: PMC157032.
50. Shin J, Park E, Choi G. PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. The Plant journal: for cell and molecular biology. 2007; 49(6):981-94. doi: 10.1111/j.1365-313X.2006.03021.x PMID: 17319847.
51. Carey CC, Strahle JT, Selinger DA, Chandler VL. Mutations in the pale aleurone color1 regulatory gene of the Zea mays anthocyanin pathway have distinct phenotypes relative to the functionally similar TRANSPARENT TESTA GLABRA1 gene in Arabidopsis thaliana. The Plant cell. 2004; 16(2):450-64. doi: 10.1105/tpc.018796 PMID: 14742877; PubMed Central PMCID: PMC341916.
52. Feller A, Machemer K, Braun EL, Grotewold E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. The Plant journal: for cell and molecular biology. 2011; 66(1):94-116. doi: 10.1111/j.1365-313X.2010.04459.x PMID: 21443626.
53. Hichri I, Barrieu F, Bogs J, Kappel C, Delrot S, Lauvergeat V. Recent advances in the transcriptional regulation of the flavonoid biosynthetic pathway. Journal of experimental botany. 2011; 62(8):2465-83. doi: 10.1093/jxb/erq442 PMID: 21278228.
54. Loza-Tavera H. Monoterpenes in essential oils. Biosynthesis and properties. Advances in experimental medicine and biology. 1999; 464:49-62. PMID: 10335385.
55. Degenhardt J, Kollner TG, Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry. 2009; 70(15-16):1621-37. doi: 10.1016/j.phytochem.2009.07.030 PMID: 19793600.
56. Yuba A, Yazaki K, Tabata M, Honda G, Croteau R. cDNA cloning, characterization, and functional expression of 4S-(-)-limonene synthase from Perilla frutescens. Archives of biochemistry and biophysics. 1996; 332(2):280-7. doi: 10.1006/abbi.1996.0343 PMID: 8806736.
57. Tabancaa N, Demircib B, Alia A, Alia Z, Blythec EK, Khan IA. Essential oils of green and red Perilla frutescens as potential sources of compounds for mosquito management. Ind Crop Prod. 2015; 65:36-44. doi: 10.1016/j.indcrop.2014.11.043
58. Tong W, Kwon SJ, Lee J, Choi IY, Park YJ, Choi SH, et al. Gene set by de novo assembly of Perilla species and expression profiling between P. frutescens (L.) var. frutescens and var. crispa. Gene. 2015; 559(2):155-63. doi: 10.1016/j.gene.2015.01.028 PMID: 25597767.
59. Kosuge T, Mashima J, Kodama Y, Fujisawa T, Kaminuma E, Ogasawara O, et al. DDBJ progress report: a new submission system for leading to a correct annotation. Nucleic acids research. 2014; 42(Database issue):D44-9. doi: 10.1093/nar/gkt1066 PMID: 24194602; PubMed Central PMCID: PMC3964987.
60. Goto N, Prins P, Nakao M, Bonnal R, Aerts J, Katayama T. BioRuby: bioinformatics software for the Ruby programming language. Bioinformatics. 2010; 26(20):2617-9. doi: 10.1093/bioinformatics/btq475 PMID: 20739307; PubMed Central PMCID: PMC2951089.
61. Morgan M, Anders S, Lawrence M, Aboyoun P, Pages H, Gentleman R. ShortRead: a bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics. 2009; 25(19):2607-8. doi: 10.1093/bioinformatics/btp450 PMID: 19654119; PubMed Central PMCID: PMC2752612.
62. Pages H, Aboyoun P, Gentleman R, DebRoy S. Biostrings: String objects representing biological sequences, and matching algorithms. R package version 2321. 2009.
63. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome biology. 2010; 11(3):R25. doi: 10.1186/gb-2010-11-3-r25 PMID: 20196867; PubMed Central PMCID: PMC2864565.
64. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26(1):139-40. doi: 10.1093/bioinformatics/btp616 PMID: 19910308; PubMed Central PMCID: PMC2796818.
65. Anders S, Huber W. Differential expression analysis for sequence count data. Genome biology. 2010; 11(10):R106. doi: 10.1186/gb-2010-11-10-r106 PMID: 20979621; PubMed Central PMCID: PMC3218662.