On the substrate specificity of the rice strigolactone biosynthesis enzyme DWARF27

Planta

Volumn 243, Issue 6, 2016, Pages 1429-1440

  Bruno, Mark ^b   Al Babili, Salim ^a,b  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Apocarotenoids; Carlactone; Carotene isomerase; Carotenoid cleavage dioxygenase; Carotenoids; Strigolactones

Indexed keywords

CAROTENOID; ISOMERASE; LACTONE; PHYTOHORMONE; PLANT PROTEIN;

BIOSYNTHESIS; CHEMISTRY; ENZYME SPECIFICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; ORYZA; PHYSIOLOGY;

BIOSYNTHETIC PATHWAYS; CAROTENOIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ISOMERASES; LACTONES; ORYZA; PLANT GROWTH REGULATORS; PLANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84960097079     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-016-2487-5     Document Type: Article

References (55)

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 111:18084–18089
2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827
3. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186
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 416:289–296
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 335:1348–1351
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 53:9512–9518
7. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9:315–321
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 26:2524–2537
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 14:1232–1238
10. Bouvier F, Isner JC, Dogbo O, Camara B (2005) Oxidative tailoring of carotenoids: a prospect towards novel functions in plants. Trends Plant Sci 10:187–194
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 220:785–793
12. Britton G (1995) Carotenoids, vol 1b: Spectroscopy. Birkhäuser Verlag, Basel
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 588:1802–1807
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 572:126–133
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 154:1189–1190
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 328:130–138
17. de Saint Germain A, Bonhomme S, Boyer FD, Rameau C (2013) Novel insights into strigolactone distribution and signalling. Curr Opin Plant Biol 16:583–589
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 719:333–343
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 45:1497–1505
20. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43:228–265
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 111:12246–12251
22. Giuliano G, Al-Babili S, Von Lintig J (2003) Carotenoid oxygenases: cleave it or leave it. Trends Plant Sci 8:145–149
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 455:189–194
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 282:3986–4000
25. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4:210–218
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 276:736–747
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 4:584–593
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 136:4246–4255
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 46:79–86
30. Jensen NH, Nielsen AB, Wilbrandt R (1982) Chlorophyll a-sensitized trans-cis photoisomerization of all-trans-beta-carotene. J Am Chem Soc 104:6117–6119
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 109:19021–19026
32. Kapulnik Y, Koltai H (2014) Strigolactone involvement in root development, response to abiotic stress, and interactions with the biotic soil environment. Plant Physiol 166:560–569
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 21:1512–1525
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 139:920–934
35. Medina HR, Cerda-Olmedo E, Al-Babili S (2011) Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 82:199–208
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 138:1341–1350
37. Moise AR, von Lintig J, Palczewski K (2005) Related enzymes solve evolutionarily recurrent problems in the metabolism of carotenoids. Trends Plant Sci 10:178–186
38. Moise AR, Al-Babili S, Wurtzel ET (2014) Mechanistic aspects of carotenoid biosynthesis. Chem Rev 114:164–193
39. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8:68–82
40. Park H (2002) Identification of the carotenoid isomerase provides insight into carotenoid biosynthesis, prolamellar body formation, and photomorphogenesis. Plant Cell 14:321–332
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 64:448–460
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 6:650–657
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:e0158
45. Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874
46. Seto Y, Yamaguchi S (2014) Strigolactone biosynthesis and perception. Curr Opin Plant Biol 21C:1–6
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 108:122–128
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 455:195–200
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–E1309
50. von Lintig J (2012) Metabolism of carotenoids and retinoids related to vision. J Biol Chem 287:1627–1634
51. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622
52. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692
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 159:1073–1085
54. Xie X, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117
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 10:1028–1033