Stereospecificity in strigolactone biosynthesis and perception

Planta

Volumn 243, Issue 6, 2016, Pages 1361-1373

  Flematti, Gavin R ^a   Scaffidi, Adrian ^a   Waters, Mark T ^a   Smith, Steven M ^b,c  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF TASMANIA   (Australia)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Carlactone; Carotenoid; Stereochemistry; Strigolactone; Fold hydrolase

Indexed keywords

LACTONE; PHYTOHORMONE;

BIOSYNTHESIS; CHEMISTRY; METABOLISM; MYCORRHIZA; PLANT DEVELOPMENT; STEREOISOMERISM; SYNTHESIS;

BIOSYNTHETIC PATHWAYS; LACTONES; MYCORRHIZAE; PLANT DEVELOPMENT; PLANT GROWTH REGULATORS; STEREOISOMERISM;

EID: 84964285768     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-016-2523-5     Document Type: Review

References (62)

1. Abe S, 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. Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117
4. Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186
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. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424
7. Artuso E, Ghibaudi E, Lace B, Marabello D, Vinciguerra D, Lombardi C, Koltai H, Kapulnik Y, Novero M, Occhiato EG, Scarpi D, Parisotto S, Deagostino A, Venturello P, Mayzlish-Gati E, Bier A, Prandi C (2015) Stereochemical assignment of strigolactone analogues confirms their selective biological activity. J Nat Prod 78:2624–2633
8. Bennett T, Leyser O (2014) Strigolactone signalling: standing on the shoulders of DWARFs. Curr Opin Plant Biol 22:7–13
9. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449
10. Boyer F-D, de Saint Germain A, Pillot J-P, Pouvreau J-B, Chen VX, Ramos S, Stévenin A, Simier P, Delavault P, Beau J-M, Rameau C (2012) Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol 159:1524–1544
11. Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28
12. Brooks DW, Bevinakatti HS, Powell DR (1985) The absolute structure of (+)-strigol. J Org Chem 50:3779–3781
13. Cavar S, Zwanenburg B, Tarkowski P (2015) Strigolactones: occurrence, structure, and biological activity in the rhizosphere. Phytochem Rev 14:691–711
14. Challis RJ, Hepworth J, Mouchel C, Waites R, Leyser O (2013) A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol 161:1885–1902
15. Chevalier F, Nieminen K, Sánchez-Ferrero JC, Rodríguez ML, Chagoyen M, Hardtke CS, Cubas P (2014) Strigolactone promotes degradation of DWARF14, an α/β hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26:1134–1150
16. Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B, Westwood JH, Shirasu K, Bond CS, Dyer KA, Nelson DC (2015) Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 49:540–543
17. 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
18. Cook CE, Whichard LP, Wall ME, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. II. The structure of strigol—a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199
19. Delaux P-M, Xie X, Timme RE, Puech-Pagès V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195:857–871
20. Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977
21. Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55:21–28
22. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194
23. Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22:2032–2036
24. Hirayama K, Mori K (1999) Synthesis of (+)-strigol and (+)-orobanchol, the germination stimulants, and their stereoisomers by employing lipase-catalyzed asymmetric acetylation as the key step. Eur J Org Chem 1999:2211–2217
25. Igbinnosa I, Okonkwo SNC (1992) Stimulation of germination of seeds of cowpea witchweed (Striga gesnerioides) by sodium hypochlorite and some growth regulators. Weed Sci 40:25–28
26. Johnson AW, Gowada G, Hassanali A, Knox J, Monaco S, Razavi Z, Roseberry G (1981) The preparation of synthetic analogues of strigol. J Chem Soc Perkin Trans 1:1734–1743
27. Kameoka H, Kyozuka J (2015) Downregulation of rice DWARF 14 LIKE suppress mesocotyl elongation via a strigolactone independent pathway in the dark. J Genet Genomics 42:119–124
28. Kim HI, Xie XN, Kim HS, Chun JC, Yoneyama K, Nomura T, Takeuchi Y, Yoneyama K (2010) Structure-activity relationship of naturally occurring strigolactones in Orobanche minor seed germination stimulation. J Pest Sci 35:344–347
29. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155:974–987
30. Mangnus EM, Dommerholt FJ, Dejong RLP, Zwanenburg B (1992) Improved synthesis of strigol analog GR24 and evaluation of the biological-activity of its diastereomers. J Agric Food Chem 40:1230–1235
31. Mori K, Matsui J, Yokota T, Sakai H, Bando M, Takeuchi Y (1999) Structure and synthesis of orobanchol, the germination stimulant for Orobanche minor. Tetrahedron Lett 40:943–946
32. Nakamura H, Xue YL, Miyakawa T, Hou F, Qin HM, Fukui K, Shi X, Ito E, Ito S, Park SH, Miyauchi Y, Asano A, Totsuka N, Ueda T, Tanokura M, Asami T (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613
33. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108:8897–8902
34. Nelson DC, Flematti GR, Ghisalberti EL, Dixon KW, Smith SM (2012) Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu Rev Plant Biol 63:107–130
35. Nomura S, Nakashima H, Mizutani M, Takikawa H, Sugimoto Y (2013) Structural requirements of strigolactones for germination induction and inhibition of Striga gesnerioides seeds. Plant Cell Rep 32:829–838
36. Ruyter-Spira C, Al-Babili S, van der Krol S, Bouwmeester H (2013) The biology of strigolactones. Trends Plant Sci 18:72–83
37. Scaffidi A, Waters MT, Bond CS, Dixon KW, Smith SM, Ghisalberti EL, Flematti GR (2012) Exploring the molecular mechanism of karrikins and strigolactones. Bioorg Med Chem Lett 22:3743–3746
38. Scaffidi A, Waters MT, Ghisalberti EL, Dixon KW, Flematti GR, Smith SM (2013) Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J 76:1–9
39. Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232
40. Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111:1640–1645
41. Smith SM, Li J (2014) Signalling and responses to strigolactones and karrikins. Curr Opin Plant Biol 21:23–29
42. Sun X-D, Ni M (2011) HYPOSENSITIVE TO LIGHT, an alpha/beta fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol Plant 4:116–126
43. Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenko O, Lumba S, Tsuchiya Y, Savchenko A, McCourt P (2015) Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350:203–207
44. Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S, Holbrook-Smith D, Zhang H, McCourt P, Itami K, Kinoshita T, Hagihara S (2015) Parasitic plants. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–868
45. Ueno K, Nomura S, Muranaka S, Mizutani M, Takikawa H, Sugimoto Y (2011) Ent-2 ‘-epi-orobanchol and its acetate, as germination stimulants for Striga gesnerioides seeds isolated from cowpea and red clover. J Agric Food Chem 59:10485–10490
46. Ueno K, Sugimoto Y, Zwanenburg B (2015) The genuine structure of alectrol: end of a long controversy. Phytochem Rev 14:835–847
47. 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
48. Umehara M, Cao M, Akiyama K, Akatsu T, Seto Y, Hanada A, Li W, Takeda-Kamiya N, Morimoto Y, Yamaguchi S (2015) Structural requirements of strigolactones for shoot branching inhibition in rice and Arabidopsis. Plant Cell Physiol 56:1059–1072
49. Vurro M, Yoneyama K (2012) Strigolactones—intriguing biologically active compounds: perspectives for deciphering their biological role and for proposing practical application. Pest Manag Sci 68:664–668
50. Waldie T, McCulloch H, Leyser O (2014) Strigolactones and the control of plant development: lessons from shoot branching. Plant J 79:607–622
51. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012a) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295
52. Waters MT, Scaffidi A, Flematti GR, Smith SM (2012b) Karrikins force a rethink of strigolactone mode of action. Plant Signal Behav 7:969–972
53. Waters MT, Scaffidi A, Flematti GR, Smith SM (2013) The origins and mechanisms of karrikin signalling. Curr Opin Plant Biol 16:667–673
54. Waters MT, Scaffidi A, Sun YK, Flematti GR, Smith SM (2014) The karrikin response system of Arabidopsis. Plant J 79:623–631
55. Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27:1925–1944
56. Xie XN, Yoneyama K, Kisugi T, Uchida K, Ito S, Akiyama K, Hayashi H, Yokota T, Nomura T, Yoneyama K (2013) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol Plant 6:153–163
57. Yokota T, Sakai H, Okuno K, Yoneyama K, Takeuchi Y (1998) Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochemistry 49:1967–1973
58. Zhang Y, van Dijk AD, 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 HJ (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033
59. Zhao LH, Zhou XE, Wu ZS, Yi W, Xu Y, Li S, Xu TH, Liu Y, Chen RZ, Kovach A, Kang Y, Hou L, He Y, Xie C, Song W, Zhong D, Xu Y, Wang Y, Li J, Zhang C, Melcher K, Xu HE (2013) Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23:436–439
60. Zhao LH, Zhou XE, Yi W, Wu Z, Liu Y, Kang Y, Hou L, de Waal PW, Li S, Jiang Y, Scaffidi A, Flematti GR, Smith SM, Lam VQ, Griffin PR, Wang Y, Li J, Melcher K, Xu HE (2015) Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res 25:1219–1236
61. Zwanenburg B, Pospisil T (2013) Structure and activity of strigolactones: new plant hormones with a rich future. Mol Plant 6:38–62
62. Zwanenburg B, Cavar Zeljkovic S, Pospisil T (2016) Synthesis of strigolactones, a strategic account. Pest Manag Sci 72:15–29