Advertisement

Molecular Biology Reports

, Volume 46, Issue 5, pp 5175–5184 | Cite as

Bioinformatics study of 1-deoxy-d-xylulose-5-phosphate synthase (DXS) genes in Solanaceae

  • Xuhao PanEmail author
  • Yiting Li
  • Guangtang Pan
  • Aiguo YangEmail author
Original Article
  • 191 Downloads

Abstract

Isoprenoids, the largest and most diverse class of secondary metabolites in plants, play an important role in plant growth and development. Isoprenoids can be synthesized by two distinct pathways: the methylerythritol-4-phosphate (MEP) pathway and the mevalonate (MVA) pathway. 1-Deoxy-d-xylulose-5-phosphate synthase (DXS) is the first step and a key regulatory enzyme of the MEP pathway in plants. The DXS gene has been reported to play a key role in seedling development, flowering, and fruit quality in plants of the Solanaceae, such as tomato, potato and tobacco. However, to improve our understanding and utilization of DXS genes, a thorough bioinformatics study is needed. In this study, 48 DXS genes were aligned and analyzed by computational tools to predict their protein properties, including molecular mass, theoretical isoelectric point (pI), signal peptides, transmembrane and conserved domains, and expression patterns. Sequence comparison analysis revealed strong conservation among the 48 DXS genes. Phylogenetic analysis indicated that all DXS genes were derived from one ancestor and could be classified into three groups with different expression patterns. Moreover, the functional divergence of DXS was restricted after gene duplication. The results suggested that the function and evolution of the DXS gene family were highly conserved and that the DXS genes of Group I may play a more important role than those of other groups.

Keywords

Bioinformatics study MEP pathway DXS gene family Solanaceae 

Notes

Acknowledgements

The authors thank Dr. Hongjun Liu and Yaou Shen for critical reviews.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11033_2019_4975_MOESM1_ESM.xls (104 kb)
Supplementary material 1 (XLS 104 kb)
11033_2019_4975_MOESM2_ESM.doc (29 kb)
Supplementary material 2 (DOC 29 kb)

References

  1. 1.
    Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70(15–16):1621–1637PubMedCrossRefGoogle Scholar
  2. 2.
    Heiling S, Schuman MC, Schoettner M, Mukerjee P, Berger B, Schneider B et al (2010) Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22(1):273PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Hasegawa M, Mitsuhara I, Seo S, Imai T, Koga J, Okada K et al (2010) Phytoalexin accumulation in the interaction between rice and the blast fungus. Mol Plant Microbe Interact 23(8):1000–1011PubMedCrossRefGoogle Scholar
  4. 4.
    Balkema-Boomstra AG, Zijlstra S, Verstappen FW, Inggamer H, Mercke PE, Jongsma MA et al (2003) Role of cucurbitacin C in resistance to spider mite (Tetranychus urticae) in cucumber (Cucumis sativus L.). J Chem Ecol 29(1):225–235PubMedCrossRefGoogle Scholar
  5. 5.
    Cieza A, Maier P, Pöppel E (2003) The effect of Ginkgo biloba on healthy elderly subjects. Fortschritte der Medizin Originalien 121(1):5–10 PubMed PMID: 15117063PubMedGoogle Scholar
  6. 6.
    Wani MC, Taylor HL, Wall ME, Coggon P, Mcphail AT (1986) Plant antitumor agents. VI. The isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 88(16):2325Google Scholar
  7. 7.
    Enfissi EM, Fraser PD, Lois LM, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnol J 3(1):17–27PubMedCrossRefGoogle Scholar
  8. 8.
    Mcgarvey DJ, Croteau R (1995) Terpenoid metabolism. Plant Cell 7(7):1015–1026PubMedPubMedCentralGoogle Scholar
  9. 9.
    Rodríguez-Concepción M, Boronat A (2002) Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol 130(3):1079PubMedCrossRefGoogle Scholar
  10. 10.
    Rohmer M, Knani M, Simonin P, Sutter B, Sahm H (1993) Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem J 295(Pt 2):517–524PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Song X, Usunow G, Lange G, Busch M, Liang T (2012) 1-Deoxy-d-xylulose 5-phosphate synthase (DXS), a crucial enzyme for isoprenoids biosynthesis. J Biolog Chem 282(4):2676Google Scholar
  12. 12.
    Lange BM, Wildung MR (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonate-independent pathway. Proc Natl Acad Sci USA 95(5):2100–2104PubMedCrossRefGoogle Scholar
  13. 13.
    Lois LM, Campos N, Putra SR, Danielsen K, Rohmer M, Boronat A (1998) Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of d-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proc Natl Acad Sci 95(5):2105–2110PubMedCrossRefGoogle Scholar
  14. 14.
    Sprenger GA, Schörken U, Wiegert T, Grolle S, de Graaf AA, Taylor SV et al (1997) Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-d-xylulose 5-phosphate precursor to isoprenoids, thiamin, and pyridoxol. Proc Natl Acad Sci 94(24):12857–12862PubMedCrossRefGoogle Scholar
  15. 15.
    Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-d-xylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276(25):22901–22909PubMedCrossRefGoogle Scholar
  16. 16.
    Zhang M, Li K, Zhang C, Gai J, Yu D (2009) Identification and characterization of class 1 DXS gene encoding 1-deoxy-d-xylulose-5-phosphate synthase, the first committed enzyme of the MEP pathway from soybean. Mol Biol Rep 36(5):879–887PubMedCrossRefGoogle Scholar
  17. 17.
    Rodriguez-Concepcion M, Boronat A (2015) Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis. Curr Opin Plant Biol 25:17–22PubMedCrossRefGoogle Scholar
  18. 18.
    Wright LP, Rohwer JM, Ghirardo A, Hammerbacher A, Ortizalcaide M, Raguschke B et al (2014) Deoxyxylulose 5-phosphate synthase controls flux through the methylerythritol 4-phosphate pathway in Arabidopsis. Plant Physiol 165(4):1488PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26(3):139–145PubMedCrossRefGoogle Scholar
  20. 20.
    Lois LM, Rodríguezconcepción M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J Cell Mol Biol 22(6):503–513CrossRefGoogle Scholar
  21. 21.
    Gang P, Chunyan W, Song S, Xiumin F, Muhammad A, Don G et al (2013) The role of 1-deoxy-d-xylulose-5-phosphate synthase and phytoene synthase gene family in citrus carotenoid accumulation. Plant Physiol Biochem 71(2):67Google Scholar
  22. 22.
    Simpson K, Quiroz LF, Rodriguez-Concepcion M, Stange CR (2016) Differential contribution of the first two enzymes of the MEP pathway to the supply of metabolic precursors for carotenoid and chlorophyll biosynthesis in carrot (Daucus carota). Front Plant Sci 7:1344PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Xiang S, Usunow G, Lange G, Busch M, Tong L (2007) Crystal structure of 1-deoxy-d-xylulose 5-phosphate synthase, a crucial enzyme for isoprenoids biosynthesis. J Biol Chem 282(4):2676PubMedCrossRefGoogle Scholar
  24. 24.
    Mandel MA, Feldmann KA, Herreraestrella L, Rochasosa M, León P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9(5):649PubMedCrossRefGoogle Scholar
  25. 25.
    Bouvier F, D’Harlingue A, Suire C, Backhaus RA, Camara B (1998) Dedicated roles of plastid transketolases during the early onset of isoprenoid biogenesis in pepper fruits. Plant Physiol 117(4):1423–1431PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Querol J, Rodríguezconcepción M, Boronat A, Imperial S (2001) Essential role of residue H49 for activity of Escherichia coli 1-deoxy-d-xylulose 5-phosphate synthase, the enzyme catalyzing the first step of the 2-C-methyl-d-erythritol 4-phosphate pathway for isoprenoid synthesis. Biochem Biophys Res Commun 289(1):155–160PubMedCrossRefGoogle Scholar
  27. 27.
    Li W, Liu W, Wei H, He Q, Chen J, Zhang B et al (2014) Species-specific expansion and molecular evolution of the 3-hydroxy-3-methylglutaryl coenzyme a reductase (hmgr) gene family in plants. PLoS ONE 9(4):e94172PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Bailey TL, Williams N, Misleh C, Li WW (2006) MEME: discovering and analyzing DNA and protein sequence motifs. Nucl Acids Res 34:W369–W373PubMedCrossRefGoogle Scholar
  29. 29.
    Petersen TN, Brunak S, Heijne GV, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Xia JX, Ikeda M, Shimizu T (2004) ConPred_elite: a highly reliable approach to transmembrane topology predication. Comput Biol Chem 28(1):51–60PubMedCrossRefGoogle Scholar
  31. 31.
    Hoon MJLD, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20(9):1453PubMedCrossRefGoogle Scholar
  32. 32.
    Walter MH, Floss DS, Hans J, Fester T, Strack D (2007) Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry 68(1):130–138PubMedCrossRefGoogle Scholar
  33. 33.
    Paetzold H, Garms S, Bartram S, Wieczorek J, Uros-Gracia EM, Rodriguez-Concepcion M et al (2010) The isogene 1-deoxy-d-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol Plant 3(5):904–916PubMedCrossRefGoogle Scholar
  34. 34.
    Gerstel DU (1960) Segregation in New Allopolyploids of Nicotiana. I. Comparison of 6x (N. Tabacum x Tomentosiformis) and 6x (N. Tabacum x Otophora). Genetics 45(12):1723–1734PubMedPubMedCentralGoogle Scholar
  35. 35.
    Gerstel DU (1963) Segregation in new allopolyploids of Nicotiana. II. Discordant ratios from individual loci in 6x (N. Tabacum x N. Sylvestris). Genetics 48(5):677PubMedPubMedCentralGoogle Scholar
  36. 36.
    Lim KY, Matyasek R, Kovarik A, Leitch AR (2004) Genome evolution in allotetraploid Nicotiana. Biol J Linn Soc 82(4):599–606CrossRefGoogle Scholar
  37. 37.
    Dehghan Nayeri F, Yarizade K (2014) Bioinformatics study of delta-12 fatty acid desaturase 2 (FAD2) gene in oilseeds. Mol Biol Rep 41(8):5077–5087PubMedCrossRefGoogle Scholar
  38. 38.
    Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adamscollier CJ et al (2007) WoLF PSORT: protein localization predictor. Nucl Acids Res 35:585CrossRefGoogle Scholar
  39. 39.
    Lee MJ, Cusinato O, Luswata R, Wheeler CH, Goldsworthy GJ (1997) Identification of prokaryotic and eukaryotic signal peptides prediction of their cleavage sites. Protein Eng 10(1):1–6CrossRefGoogle Scholar
  40. 40.
    Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43(3):228–265PubMedCrossRefGoogle Scholar
  41. 41.
    Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4(3):210–218PubMedCrossRefGoogle Scholar
  42. 42.
    Sarma AD, Sharma R (1999) Anthocyanin-DNA copigmentation complex: mutual protection against oxidative damage. Phytochemistry 52(7):1313–1318CrossRefGoogle Scholar
  43. 43.
    Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Gaspero GDI (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell Environ 30(11):1381–1399PubMedCrossRefGoogle Scholar
  44. 44.
    Katarzyna L, Sylwia J, Jan O, Jan S (2005) Ectopic expression of anthocyanin 5-O-glucosyltransferase in potato tuber causes increased resistance to bacteria. J Agric Food Chem 53(2):272CrossRefGoogle Scholar
  45. 45.
    Muñozbertomeu J, Arrillaga I, Ros R, Segura J (2006) Up-regulation of 1-deoxy-d-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142(3):890CrossRefGoogle Scholar
  46. 46.
    Rodríguezconcepción M (2004) The MEP pathway: a new target for the development of herbicides, antibiotics and antimalarial drugs. Curr Pharm Design 10(19):2391–2400CrossRefGoogle Scholar
  47. 47.
    Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Urós EM et al (2007) Functional identification and differential expression of 1-deoxy-D-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol 65(3):243–257PubMedCrossRefGoogle Scholar
  48. 48.
    Cordoba E, Porta H, Arroyo A, San RC, Medina L, Rodríguezconcepción M et al (2011) Functional characterization of the three genes encoding 1-deoxy-D-xylulose 5-phosphate synthase in maize. J Exp Bot 62(6):2023PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Tobacco Research Institute, Chinese Academy of Agricultural SciencesQingdaoPeople’s Republic of China
  2. 2.Maize Research InstituteSichuan Agricultural UniversityChengduPeople’s Republic of China

Personalised recommendations