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Characterization of mango (Mangifera indica L.) transcriptome and chloroplast genome

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Abstract

We characterized mango leaf transcriptome and chloroplast genome using next generation DNA sequencing. The RNA-seq output of mango transcriptome generated >12 million reads (total nucleotides sequenced >1 Gb). De novo transcriptome assembly generated 30,509 unigenes with lengths in the range of 300 to ≥3,000 nt and 67× depth of coverage. Blast searching against nonredundant nucleotide databases and several Viridiplantae genomic datasets annotated 24,593 mango unigenes (80 % of total) and identified Citrus sinensis as closest neighbor of mango with 9,141 (37 %) matched sequences. The annotation with gene ontology and Clusters of Orthologous Group terms categorized unigene sequences into 57 and 25 classes, respectively. More than 13,500 unigenes were assigned to 293 KEGG pathways. Besides major plant biology related pathways, KEGG based gene annotation pointed out active presence of an array of biochemical pathways involved in (a) biosynthesis of bioactive flavonoids, flavones and flavonols, (b) biosynthesis of terpenoids and lignins and (c) plant hormone signal transduction. The mango transcriptome sequences revealed 235 proteases belonging to five catalytic classes of proteolytic enzymes. The draft genome of mango chloroplast (cp) was obtained by a combination of Sanger and next generation sequencing. The draft mango cp genome size is 151,173 bp with a pair of inverted repeats of 27,093 bp separated by small and large single copy regions, respectively. Out of 139 genes in mango cp genome, 91 found to be protein coding. Sequence analysis revealed cp genome of C. sinensis as closest neighbor of mango. We found 51 short repeats in mango cp genome supposed to be associated with extensive rearrangements. This is the first report of transcriptome and chloroplast genome analysis of any Anacardiaceae family member.

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References

  1. Adams MD, Kelley JM, Gocayne JD, Dubnick M, Polymeropoulos MH, Xiao H, Merril CR, Wu A, Olde B, Moreno RF et al (1991) Complementary DNA sequencing: expressed sequence tags and human genome project. Science 252(5013):1651–1656

  2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

  3. Andrade Jde M, Toledo TT, Nogueira SB, Cordenunsi BR, Lajolo FM, do Nascimento JR (2012) 2D-DIGE analysis of mango (Mangifera indica L.) fruit reveals major proteomic changes associated with ripening. J Proteomics 75:3331–3341

  4. Asif H, Khan A, Iqbal A, Khan IA, Heinze B, Azim MK (2013) The chloroplast genome sequence of Syzygium cumini (L.) and its relationship with other angiosperms. Tree Genet Genomes 9:867–877

  5. Bausher MG, Singh ND, Lee SB, Jansen RK, Daniell H (2006) The complete chloroplast genome sequence of Citrus sinensis (L.) Osbeck var ‘Ridge Pineapple’: organization and phylogenetic relationships to other angiosperms. BMC Plant Biol 6:21. doi:10.1186/1471-2229-6-21

  6. Bleecker AB, Esch JJ, Hall AE, Rodríguez FI, Binder BM (1998) The ethylene-receptor family from Arabidopsis: structure and function. Philos Trans R Soc Lond B Biol Sci 353(1374):1405–1412

  7. Chinag YC, Tasi CM, Chen YK, Lee SR, Chen CH, Lin YS, Tasi CC (2012) Development and characterization of 20 new polymorphic microsatellite markers from mangifera indica (Anacardiaceae). Am J Bot 99(3):e117–e119

  8. Chung HJ, Jung JD, Park HW, Kim JH, Cha HW, Min SR, Jeong WJ, Liu JR (2006) The complete chloroplast genome sequences of Solanum tuberosum and comparative analysis of with solanaceae species identified the presence of 241 bp deletion in cultivated potato chloroplast DNA sequence. Plant Cell Rep. doi:10.1007/s0029-006-0196-4

  9. Conant GC, Wolfe KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24:861–862

  10. Conesa A, Gotz S et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676

  11. Dhingra A, Folta KM (2005) ASAP: amplification, sequencing and annotation of plastomes. BMC Genom 6:176

  12. Duangjit J, Bohanec B, Chan AP, Town CD, Havey MJ (2013) Transcriptome sequencing to produce SNP-based genetic maps of onion. Theor Appl Genet. doi:10.1007/s00122-013-2121-x

  13. Duval M, Bunel FJ, Sitbon C, Risterucci AM (2005) Development of microsatellite markers for mango (Mangifera indica L.). Mol Ecol Notes 5:823

  14. Edwards RL, Lyon T, Litwin SE, Rabovsky A, Symons JD, Jalili T (2007) Quercetin reduces blood pressure in hypertensive subjects. J Nutr 137(11):2405–2411

  15. Fahey JW, Stephenson KK (2002) Pinostrobin from honey and Thai ginger (Boesenbergia pandurata): a potent flavonoid inducer of mammalian phase 2 chemoprotective and antioxidant enzymes. J Agric Food Chem 50(25):7472–7476

  16. Frazer KA, Pachter L, Poliakov A, Rubin EM, Dubchak I (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32:W273–W275

  17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652

  18. Haas BJ, Zody MC (2010) Advancing RNA-seq analysis. Nat Biotechnol 28(5):421–423

  19. Haberle RC, Fourcade HM, Boore JL, Jansen RK (2008) Extensive rearrangements in the chloroplast genome of Trachelium caeruleum are associated with repeats and trna genes. J Mol Evol 66:350–361

  20. Hirano R, Htun Oo T, Watanabe KN (2010) Myanmar mango landraces reveal genetic uniqueness over common cultivars from Florida, India, and Southeast Asia. Genome 53(4):321

  21. Ibrahim RIH, Azuma JI, Sakamoto M (2006) Complete nucleotide sequence of the cotton (Gossypium barbadense L.) chloroplast genome with a comparative analysis of sequences among 9 dicot plants. Genes Genet Syst 81:311–321

  22. Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc Int Conf Intell Syst Mol Biol 138–148

  23. Kanehisa M, Araki M et al (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36(Database issue):D480–D484

  24. Khan IA, Azim MK (2011) Variations in intergenic spacer rpl20-rps12 of Mango (Mangifera indica) chloroplast DNA: implications in cultivar identification. Plant Evol Syst 292(3–4):249–255

  25. Khan A, Khan IA, Heinze B, Azim MK (2012) The chloroplast genome sequence of date palm (Phoenix dactylifera L. cv. ‘Aseel’). Plant Mol Biol Rep 30:666–678

  26. Krishna H, Singh SK (2007) Biotechnological advances in mango (Mangifera indica L.) and their future implication in crop improvement: a review. Biotechnol Adv 25:223–243

  27. Kulkarni R, Pandit S, Chidley H, Nagel R, Schmidt A, Gershenzon J, Pujari K, Giri A, Gupta V (2013) Characterization of three novel isoprenyl diphosphate synthases from the terpenoid rich mango fruit. Plant Physiol Biochem 71:121–131

  28. Kurtz S, Choudhuri JV, Ohlebusch E, Schleiermacher C, Stoye J, Giegerich R (2001) REPuter: the manifold applications of repeat analysis on a genomic scale. Nucleic Acids Res 29(22):4633–4642

  29. Lam KC, Ibrahim RK, Behdad B, Dayanandan S (2007) Structure, function, and evolution of plant O-methyltransferases. Genome 50(11):1001–1013

  30. Lee EH, Song DG, Lee JY, Pan CH, Um BH, Jung SH (2008) Inhibitory effect of the compounds isolated from Rhus verniciflua on aldose reductase and advanced glycation endproducts. Biol Pharm Bull 31(8):1626–1630

  31. Lewinshon E, Schalechet F, Wilkinson J, Matsui K, Tadmor Y, Nam K, Amar O, Lastochkin E, Larkov O, Ravid U, Hiatt W, Gepstein S, Pichersky E (2001) Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol 127:1256–1265

  32. Ley JP, Krammer G, Reinders G, Gatfield IL, Bertram HJ (2005) Evaluation of bitter masking flavanones from Herba Santa (Eriodictyon californicum (H. and A.) Torr., Hydrophyllaceae. J Agric Food Chem 53(15):6061–6066

  33. Li B, Ruotti V, Stewart RM, Thomson JA, Dewey CN (2010) RNASeq gene expression estimation with read mapping uncertainty. Bioinformatics 26(4):493–500

  34. López-Lázaro M (2009) Distribution and biological activities of the flavonoid luteolin. Mini Rev Med Chem 9(1):31–59

  35. Mehrnoush A, Mustafa S, Sarker MZ, Yazid AM (2012) Optimization of serine protease purification from mango (Mangifera indica cv. Chokanan) peel in polyethylene glycol/dextran aqueous two phase system. Int J Mol Sci 13:3636–3649

  36. Michal G (1999) Biochemical pathways, an atlas of biochemistry and molecular biology. Spektrum Akademischer, Heidelberg

  37. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-seq. Nat Methods 5(7):621–628

  38. Mukherjee SK (1950) Mango: its allopolyploid nature. Nature 4213:196–197

  39. Mukherjee SK, Litz RE (2009) Introduction: Botany and Importance. In: Litz RE (ed) The mango botany, production and uses, 2nd edn. CBI International, Wallingford, pp 1–18

  40. Mulvihill EE, Allister EM, Sutherland BG, Telford DE, Sawyez CG, Edwards JY, Markle JM, Hegele RA, Huff MW (2009) Naringenin prevents dyslipidemia, apolipoprotein B overproduction, and hyperinsulinemia in LDL receptor-null mice with diet-induced insulin resistance. Diabetes 58(10):2198–2210

  41. Pandit SS, Kulkarni RS, Giri AP, Kollner TG, Degenhardt J, Gershenzon J, Gupta VS (2010) Expression profiling of various genes during the fruit development and ripening of mango. Plant Physiol Biochem 48:426–433

  42. Park KY, Jung GO, Lee KT, Choi J, Choi MY, Kim GT, Jung HJ, Park HJ (2004) Antimutagenic activity of flavonoids from the heartwood of Rhus verniciflua. J Ethnopharmacol 90(1):73–79

  43. Park BC, Lee YS, Park HJ, Kwak MK, Yoo BK, Kim JY, Kim JA (2007) Protective effects of fustin, a flavonoid from Rhus verniciflua Stokes, on 6-hydroxydopamine-induced neuronal cell death. Exp Mol Med 39(3):316–326

  44. Ravishankar KV, Mani BH, Anand L, Dinesh MR (2011) Development of new microsatellite markers from mango (Mangifera indica) and cross-species amplification. Am J Bot 98(4):e96–e99

  45. Renuse S, Harsha HC, Kumar P, Acharya PK, Sharma J, Goel R, Kumar GSS, Raju R, Prasad TSK, Slotta T, Pandey A (2012) Proteomic analysis of an unsequenced plant-Mangifera indica. J Proteomics 75:5793–5796

  46. Rocha A, Salomao LC, Salomao TM, Cruz CD, de Siqueira DL (2012) Genetic diversity of ‘uba’ mango tree using ISSR markers. Mol Biotechnol 50(2):108–113

  47. Sara Z, Alberto F, Enrico G, Luciano X, Marianna F, Giovanni M, Diana B, Mario P, Massimo D (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-seq. Plant Physiol 152:1787–1795

  48. Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (1999) Complete structure of the chloroplast Genome of Arabidopsis thaliana. DNA Res 6:283–290

  49. Schnell RJ, Olano CT, Quintanilla WE, Meerow AW (2005) Isolation and characterization of 15 microsatellite loci from mango (Mangifera indica L.) and cross-species amplification in closely related taxa. Mol Ecol Notes 5:625

  50. Schnell RJ, Brown JS, Olano CT, Meerow AW, Campbell RJ, Kuhn DN (2006) Mango genetic diversity analysis and pedigree inferences for Florida cultivars using microsatellite markers. J Am Soc Hort Sci 131:214

  51. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, Matsubayashi T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki J, Ohto C, Torazawa K, Meng BY, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kato A, Tohdoh N, Shimada H, Sugiura M (1986) The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J 5:2043–2049

  52. Souza IG, Valente SE, Britto FB, de Souza VA, Lima PS (2011) RAPD analysis of the genetic diversity of mango (Mangifera indica) germplasm in Brazil. Genet Mol Res 10(4):3080–3089

  53. Srivastava N, Bajpai A, Chandra R, Rajan S, Muthukumar M, Srivastava MK (2012) Comparison of PCR based marker systems for genetic analysis in different cultivars of mango. J Environ Biol 33(2):159–166

  54. Strickler SR, Aureliano Bombarely A, Mueller LA (2012) Designing a transcriptome next-generation sequencing project for a nonmodel plant species. Am J Bot 99(2):257–266

  55. Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62:113–123

  56. Viruel MA, Escribano P, Barbieri M, Ferri M, Hormaza JI (2005) Fingerprinting, embryo type and geographic differentiation in mango (Mangifera indica L., Anacardiaceae) with microsatellites. Mol Breeding 15:383

  57. Wang Y (2005) The plant polyphenol butein inhibits testosterone-induced proliferation in breast cancer cells expressing aromatase. Life Sci 77(1):39–51

  58. Wang Z, Gerstein M, Snyder M (2009) RNA-seq: a revolutionary tool for transcriptomics. Nat Rev 10(1):57–63

  59. Wilhelm BT, Marguerat S, Goodhead I, Bahler J (2010) Defining transcribed regions using RNA-seq. Nat Protoc 5(2):255–266

  60. Wyman SK, Jansen RK, Boore JL (2004) Automatic annotation of organellar genomes with DOGMA. Bioinformatics 20(17):3252–3255

  61. Xu J, Li Y, Ma X, Ding J, Wang K, Wang S, Tian Y, Zhang H, Zhu X-G (2013) Whole transcriptome analysis using next-generation sequencing of model species Setaria viridis to support C4 photosynthesis research. Plant Mol Biol. doi:10.1007/s11103-013-0025-4

  62. Ye J, Fang L et al (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293–W297

  63. Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7(1–2):203–214

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Correspondence to M. Kamran Azim.

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Azim, M.K., Khan, I.A. & Zhang, Y. Characterization of mango (Mangifera indica L.) transcriptome and chloroplast genome. Plant Mol Biol 85, 193–208 (2014). https://doi.org/10.1007/s11103-014-0179-8

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Keywords

  • Transcriptome analysis
  • RNA-seq
  • Anacardiaceae
  • Plant genome