Advertisement

Planta

, Volume 243, Issue 6, pp 1429–1440 | Cite as

On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27

  • Mark Bruno
  • Salim Al-Babili
Original Article
Part of the following topical collections:
  1. Strigolactones

Abstract

Main conclusion

The β-carotene isomerase OsDWARF27 is stereo- and double bond-specific. It converts bicyclic carotenoids with at least one unsubstituted β-ionone ring. OsDWARF27 may contribute to the formation of α-carotene-based strigolactone-like compounds.

Strigolactones (SLs) are synthesized from all-trans-β-carotene via a pathway involving the β-carotene isomerase DWARF27, the carotenoid cleavage dioxygenases 7 and 8 (CCD7, CCD8), and cytochrome P450 enzymes from the 711 clade (MAX1 in Arabidopsis). The rice enzyme DWARF27 was shown to catalyze the reversible isomerization of all-trans- into 9-cis-β-carotene in vitro. β-carotene occurs in different cis-isomeric forms, and plants accumulate other carotenoids, which may be substrates of DWARF27. Here, we investigated the stereo and substrate specificity of the rice enzyme DWARF27 in carotenoid-accumulating E. coli strains and in in vitro assays performed with heterologously expressed and purified enzyme. Our results suggest that OsDWARF27 is strictly double bond-specific, solely targeting the C9–C10 double bond. OsDWARF27 did not introduce a 9-cis-double bond in 13-cis- or 15-cis-β-carotene. Substrates isomerized by OsDWARF27 are bicyclic carotenoids, including β-, α-carotene and β,β-cryptoxanthin, that contain at least one unsubstituted β-ionone ring. Accordingly, OsDWARF27 did not produce the abscisic acid precursors 9-cis-violaxanthin or -neoxanthin from the corresponding all-trans-isomers, excluding a direct role in the formation of this carotenoid derived hormone. The conversion of all-trans-α-carotene yielded two different isomers, including 9′-cis-α-carotene that might be the precursor of strigolactones with an ε-ionone ring, such as the recently identified heliolactone.

Keywords

Apocarotenoids Carotenoids Carotenoid cleavage dioxygenase Carotene isomerase Carlactone Strigolactones 

Abbreviations

CCD

Carotenoid cleavage dioxygenase

MBP

Maltose binding protein

SL

Strigolactone

Notes

Acknowledgments

We thank Dr. Peter Beyer, University of Freiburg, Germany, for valuable discussions and Dr. Hansgeorg Ernst, BASF, Germany, for providing the synthetic apocarotenoid substrates. The research reported in this publication was supported by funding from King Abdullah University of Science and Technology (KAUST) and the EU (METAPRO; FP7 KBBE-2009-3-1-01).

Supplementary material

425_2016_2487_MOESM1_ESM.pptx (99 kb)
Suppl. Fig. S1 SDS PAGE of maltose binding protein (MBP) purified D27-fusion protein. Lanes represent: M, molecular marker (size in kDa on the left). a Solubilized total lysate of control cells expressing MBP after French press. b Total lysate of MBP-OsD27 producing cells. c Supernatant from (b) after centrifugation. d Flow through obtained after (C) binding to amylose resin. e Eluate of control, (2) indicating the expressed MBP. f Eluate from amylose resin of OsD27-fusion protein; (1) pMAL-OsD27 fusion protein (PPTX 99 kb)
425_2016_2487_MOESM2_ESM.pptx (68 kb)
Suppl. Fig. S2 HPLC analysis of in vitro assays with apocarotenoids: We did not observe any isomerization of all-trans β-apo-8′-carotenal (a) or for all-trans β-apo-10′-carotenal (b). UV/Vis spectra of substrates are summarized in Suppl. Fig. S5, for chemical structures see Fig. 1. HPLC system 1 was employed for separation (PPTX 67 kb)
425_2016_2487_MOESM3_ESM.pptx (68 kb)
Suppl. Fig. S3 In vitro activity of MBP-OsD27 with linear and monocyclic carotenes: No conversion was observed when purified MBP-fusion protein was incubated with the linear all-trans-lycopene (a) or the monocyclic γ-carotene (b). For separation, we used systems 2 (a) and 1 (b). UV/Vis spectra of substrates are summarized in Suppl. Fig. S5, for chemical structures see Fig. 1 (PPTX 68 kb)
425_2016_2487_MOESM4_ESM.pptx (106 kb)
Suppl. Fig. S4 In vitro activity of MBP-OsD27 with xanthophylls: The MBP-OsD27 did not convert the dihydroxylated all-trans zeaxanthin (a) and all-trans-lutein (b), nor the epoxydized all-trans-viola- (c) and neoxanthin (d). UV/Vis spectra of substrates are summarized in Suppl. Fig. S5, for chemical structures see Fig. 1. We used HPLC system 1 for analysis (PPTX 106 kb)
425_2016_2487_MOESM5_ESM.pptx (92 kb)
Suppl. Fig. S5 UV/Vis spectra of substrates and products: (I) all-trans-β-carotene, (II) 9-cis-β-carotene, (III) 13-cis-β-carotene, (IV) 15-cis-β-carotene, (V) all-trans-α-carotene, (VI) 9-cis-α-carotene, (VII) 9′-cis-α-carotene, (VIII) all-trans-ε,ε-carotene, (IX) all-trans-β,β-cryptoxanthin, (X) 9-cis-β,β-cryptoxanthin, (XI) all-trans-zeaxanthin, (XII) all-trans-lutein, (XIII) all-trans-violaxanthin, (XIV) all-trans-neoxanthin, (XV) all-trans-lycopene, (XVI) all-trans-γ-carotene, (XVII) all-trans-β-apo-8′-carotenal, (XVIII) β-apo-10′-carotenal (PPTX 92 kb)

References

  1. Abe A, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y, Yamaguchi S, Akiyama K, Yoneyama K, Nomura T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111:18084–18089CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827CrossRefPubMedGoogle Scholar
  3. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186CrossRefPubMedGoogle Scholar
  4. Alder A, Holdermann I, Beyer P, Al-Babili S (2008) Carotenoid oxygenases involved in plant branching catalyse a highly specific conserved apocarotenoid cleavage reaction. Biochem J 416:289–296CrossRefPubMedGoogle Scholar
  5. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351CrossRefPubMedGoogle Scholar
  6. Aman R, Schieber A, Carle R (2005) Effects of heating and illumination on trans-cis isomerization and degradation of beta-carotene and lutein in isolated spinach chloroplasts. J Agric Food Chem 53:9512–9518CrossRefPubMedGoogle Scholar
  7. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321CrossRefPubMedGoogle Scholar
  8. Avendano-Vazquez AO, Cordoba E, Llamas E, San Roman C, Nisar N, De la Torre S, Ramos-Vega M, Gutierrez-Nava MD, Cazzonelli CI, Pogson BJ, Leon P (2014) An uncharacterized apocarotenoid-derived signal generated in zeta-carotene desaturase mutants regulates leaf development and the expression of chloroplast and nuclear genes in Arabidopsis. Plant Cell 26:2524–2537CrossRefPubMedPubMedCentralGoogle Scholar
  9. Booker J, Auldridge M, Wills S, McCarty D, Klee H, Leyser O (2004) MAX3/CCD7 is a carotenoid cleavage dioxygenase required for the synthesis of a novel plant signaling molecule. Curr Biol 14:1232–1238CrossRefPubMedGoogle Scholar
  10. Bouvier F, Isner JC, Dogbo O, Camara B (2005) Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci 10:187–194CrossRefPubMedGoogle Scholar
  11. Breitenbach J, Sandmann G (2005) zeta-Carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta 220:785–793CrossRefPubMedGoogle Scholar
  12. Britton G (1995) Carotenoids, vol 1b: Spectroscopy. Birkhäuser Verlag, BaselGoogle Scholar
  13. Bruno M, Hofmann M, Vermathen M, Alder A, Beyer P, Al-Babili S (2014) On the substrate- and stereospecificity of the plant carotenoid cleavage dioxygenase 7. FEBS Lett 588:1802–1807CrossRefPubMedGoogle Scholar
  14. Bruno M, Beyer P, Al-Babili S (2015) The potato carotenoid cleavage dioxygenase 4 catalyzes a single cleavage of beta-ionone ring-containing carotenes and non-epoxidated xanthophylls. Arch Biochem Biophys 572:126–133CrossRefPubMedGoogle Scholar
  15. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190CrossRefPubMedGoogle Scholar
  16. Cunningham FX, Chamovitz D, Misawa N, Gantt E, Hirschberg J (1993) Cloning and functional expression in Escherichia coli of a cyanobacterial gene for lycopene cyclase, the enzyme that catalyzes the biosynthesis of β-carotene. FEBS Lett 328:130–138CrossRefPubMedGoogle Scholar
  17. de Saint Germain A, Bonhomme S, Boyer FD, Rameau C (2013) Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol 16:583–589CrossRefGoogle Scholar
  18. Emenhiser C, Englert G, Sander LC, Ludwig B, Schwartz SV (1996) Isolation and structural elucidation of the predominant geometrical isomers of alpha-carotene. J Chromatogr A 719:333–343CrossRefPubMedGoogle Scholar
  19. Estrada AF, Maier D, Scherzinger D, Avalos J, Al-Babili S (2008) Novel apocarotenoid intermediates in Neurospora crassa mutants imply a new biosynthetic reaction sequence leading to neurosporaxanthin formation. Fungal Genet Biol 45:1497–1505CrossRefPubMedGoogle Scholar
  20. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265CrossRefPubMedGoogle Scholar
  21. Frusciante S, Diretto G, Bruno M, Ferrante P, Pietrella M, Prado-Cabrero A, Rubio-Moraga A, Beyer P, Gomez-Gomez L, Al-Babili S, Giuliano G (2014) Novel carotenoid cleavage dioxygenase catalyzes the first dedicated step in saffron crocin biosynthesis. Proc Natl Acad Sci USA 111:12246–12251CrossRefPubMedPubMedCentralGoogle Scholar
  22. Giuliano G, Al-Babili S, Von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149CrossRefPubMedGoogle Scholar
  23. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194CrossRefPubMedGoogle Scholar
  24. Harrison PJ, Newgas SA, Descombes F, Shepherd SA, Thompson AJ, Bugg TD (2015) Biochemical characterization and selective inhibition of beta-carotene cis-trans isomerase D27 and carotenoid cleavage dioxygenase CCD8 on the strigolactone biosynthetic pathway. FEBS J 282:3986–4000CrossRefPubMedGoogle Scholar
  25. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218CrossRefPubMedGoogle Scholar
  26. Ilg A, Beyer P, Al-Babili S (2009) Characterization of the rice carotenoid cleavage dioxygenase 1 reveals a novel route for geranial biosynthesis. FEBS J 276:736–747CrossRefPubMedGoogle Scholar
  27. Ilg A, Bruno M, Beyer P, Al-Babili S (2014) Tomato carotenoid cleavage dioxygenases 1A and 1B: relaxed double bond specificity leads to a plenitude of dialdehydes, mono-apocarotenoids and isoprenoid volatiles. FEBS Open Biol 4:584–593CrossRefGoogle Scholar
  28. Isaacson T, Ohad I, Beyer P, Hirschberg J (2004) Analysis in vitro of the enzyme CRTISO establishes a poly-cis-carotenoid biosynthesis pathway in plants. Plant Physiol 136:4246–4255CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46:79–86CrossRefPubMedGoogle Scholar
  30. Jensen NH, Nielsen AB, Wilbrandt R (1982) Chlorophyll a-sensitized trans-cis photoisomerization of all-trans-beta-carotene. J Am Chem Soc 104:6117–6119CrossRefGoogle Scholar
  31. Kachanovsky DE, Filler S, Isaacson T, Hirschberg J (2012) Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc Natl Acad Sci USA 109:19021–19026CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kapulnik Y, Koltai H (2014) Strigolactone involvement in root development, response to abiotic stress, and interactions with the biotic soil environment. Plant Physiol 166:560–569CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525CrossRefPubMedPubMedCentralGoogle Scholar
  34. Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934CrossRefPubMedPubMedCentralGoogle Scholar
  35. Medina HR, Cerda-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82:199–208CrossRefPubMedGoogle Scholar
  36. Melendez-Martinez AJ, Stinco CM, Liu C, Wang XD (2013) A simple HPLC method for the comprehensive analysis of cis/trans (Z/E) geometrical isomers of carotenoids for nutritional studies. Food Chem 138:1341–1350CrossRefPubMedGoogle Scholar
  37. Moise AR, von Lintig J, Palczewski K (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci 10:178–186CrossRefPubMedGoogle Scholar
  38. Moise AR, Al-Babili S, Wurtzel ET (2014) Mechanistic aspects of carotenoid biosynthesis. Chem Rev 114:164–193CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82CrossRefPubMedGoogle Scholar
  40. Park H (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332CrossRefPubMedPubMedCentralGoogle Scholar
  41. Prado-Cabrero A, Estrada AF, Al-Babili S, Avalos J (2007a) Identification and biochemical characterization of a novel carotenoid oxygenase: elucidation of the cleavage step in the Fusarium carotenoid pathway. Mol Microbiol 64:448–460CrossRefPubMedGoogle Scholar
  42. Prado-Cabrero A, Scherzinger D, Avalos J, Al-Babili S (2007b) Retinal biosynthesis in fungi: characterization of the carotenoid oxygenase CarX from Fusarium fujikuroi. Eukaryot Cell 6:650–657CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ruch S, Beyer P, Ernst H, Al-Babili S (2005) Retinal biosynthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Mol Microbiol 55(4):1015–1024. doi: 10.1111/j.1365-2958.2004.04460.x
  44. Ruiz-Sola MA, Rodriguez-Concepcion M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10:e0158CrossRefPubMedPubMedCentralGoogle Scholar
  45. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874CrossRefPubMedGoogle Scholar
  46. Seto Y, Yamaguchi S (2014) Strigolactone biosynthesis and perception. Curr Opin Plant Biol 21C:1–6CrossRefGoogle Scholar
  47. Ueno K, Furumoto T, Umeda S, Mizutani M, Takikawa H, Batchvarova R, Sugimoto Y (2014) Heliolactone, a non-sesquiterpene lactone germination stimulant for root parasitic weeds from sunflower. Phytochemistry 108:122–128CrossRefPubMedGoogle Scholar
  48. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200CrossRefPubMedGoogle Scholar
  49. Van Norman JM, Zhang J, Cazzonelli CI, Pogson BJ, Harrison PJ, Bugg TD, Chan KX, Thompson AJ, Benfey PN (2014) Periodic root branching in Arabidopsis requires synthesis of an uncharacterized carotenoid derivative. Proc Natl Acad Sci USA 111:E1300–E1309CrossRefPubMedPubMedCentralGoogle Scholar
  50. von Lintig J (2012) Metabolism of carotenoids and retinoids related to vision. J Biol Chem 287:1627–1634CrossRefGoogle Scholar
  51. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622CrossRefPubMedGoogle Scholar
  52. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692CrossRefPubMedGoogle Scholar
  53. Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159:1073–1085CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117CrossRefPubMedGoogle Scholar
  55. Zhang Y, van DijK ADJ, Scaffidi A, Flematti GR, Hofmann M, Charnikhova T, Verstappen F, Hepworth J, van der Krol S, Leyser O, Smith SM, Zwanenburg B, Al-Babili S, Ruyter-Spira C, Bouwmeester H (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.BESE DivisionKing Abdullah University of Science and Technology (KAUST)ThuwalKingdom of Saudi Arabia
  2. 2.Faculty of BiologyAlbert-Ludwigs University of FreiburgFreiburgGermany

Personalised recommendations