Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: Molecule design for shoot branching

Plant Physiology

Volumn 159, Issue 4, 2012, Pages 1524-1544

  Boyer, François Didier ^a   Germain, Alexandre de Saint ^b   Pillot, Jean Paul ^b   Pouvreau, Jean Bernard ^c   Chen, Victor Xiao ^a   Ramos, Suzanne ^a   Stévenin, Arnaud ^a   Simier, Philippe ^c   Delavault, Philippe ^c   Beau, Jean Marie ^a   Rameau, Catherine ^b  

^a CNRS   (France)

^b INSTITUT JEAN PIERRE BOURGIN   (France)

^c Laboratoire d'Acoustique Environnementale   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARBUSCULAR; FUNGI; OROBANCHACEAE; OROBANCHE; PHELIPANCHE RAMOSA; PISUM SATIVUM; STRIGA; ZEA MAYS;

EID: 84864657658     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.195826     Document Type: Article

References (83)

1. Adam W, Bialas J, Hadjiarapoglou L (1991) A convenient preparation of acetone solutions of dimethyldioxirane. Chem Ber 124: 2377
2. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108: 20242-20247
3. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal sym-bionts and parasitic weeds in plant roots. Ann Bot (Lond) 97: 925-931
4. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824-827
5. 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
6. 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 β-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351
7. Antoniotti S, Duñach E (2008) Facile preparation of metallic triflates and triflimidates by oxidative dissolution of metal powders. Chem Commun (Camb) 44: 993-995
8. 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
9. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4: e226
10. Beveridge CA (2000) Long-distance signalling and a mutational analysis of branching in pea. Plant Growth Regul 32: 193-203
11. Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13: 34-39
12. Beveridge CA, Symons GM, Murfet IC, Ross JJ, Rameau C (1997) The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced root-sap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol 115: 1251-1258
13. 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
14. Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12: 224-230
15. Braun N, de Saint Germain A, Pillot JP, Boutet-Mercey S, Dalmais M, Antoniadi I, Li X, Maia-Grondard A, Le Signor C, Bouteiller N, et al (2012) The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol 158: 225-238
16. Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Stri-golactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150: 482-493
17. Canevet JC, Graff Y (1978) Friedel-Crafts reaction of aromatic derivatives with 1,4-dicarbonyl-2,3-ethylenic compounds. II. Alkylations by some 5-hydroxy or 5-chloro-2,5-dihydro-2-furannones: new method for synthesis of 1h-indene-1-carboxylic acids. Tetrahedron 34: 1935-1942
18. Chen VX, Boyer F-D, Rameau C, Retailleau P, Vors J-P, Beau J-M (2010) Stereochemistry, total synthesis, and biological evaluation of the new plant hormone solanacol. Chemistry 16: 13941-13945
19. Cook CE, Coggon P, McPhail AT, Wall ME, Whichard LP, Egley GH, Luhan PA (1972) Germination stimulants. 2. Structure of strigol-potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94: 6198-6199
20. 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
21. Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Müller D, Domagalska MA, Leyser O (2010) Strigo-lactones enhance competition between shoot branches by dampening auxin transport. Development 137: 2905-2913
22. Domagalska MA, Leyser O (2011) Signal integration in the control of shoot branching. Nat Rev Mol Cell Biol 12: 211-221
23. Dos Santos CV, Letousey P, Delavault P, Thalouarn P (2003) Defense gene expression analysis of Arabidopsis thaliana parasitized by Orobanche ramosa. Phytopathology 93: 451-457
24. Dun EA, de Saint Germain A, Rameau C, Beveridge CA (2012) Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol 158: 487-498
25. Fell SCM, Harbridge JB (1990) 2,5-Dimethoxy-2,5-dihydrofuran: a convenient synthon for a novel mono-protected glyoxal. Synthesis of 4-hydroxybutenolides. Tetrahedron Lett 31: 4227-4228
26. Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234: 1073-1081
27. Fox J (2005) The R commander: a basic-statistics graphical user interface to R. J Stat Softw 14: 1-41
28. Fukui K, Ito S, Ueno K, Yamaguchi S, Kyozuka J, Asami T (2011) New branching inhibitors and their potential as strigolactone mimics in rice. Bioorg Med Chem Lett 21: 4905-4908
29. Galloway WRJD, Hodgkinson JT, Bowden SD, Welch M, Spring DR (2011) Quorum sensing in gram-negative bacteria: small-molecule modulation of AHL and AI-2 quorum sensing pathways. Chem Rev 111: 28-67
30. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C, et al (2008) Strigo-lactone inhibition of shoot branching. Nature 455: 189-194
31. Gomez-Sanchez A, Moya PB, Bellanato J (1984) Protection of the amino group of amino-sugars by the acylvinyl group. Part I. Glycoside formation by the Fischer reaction. Carbohydr Res 135: 101-116
32. Gould KS, Cutter EG, Young JPW, Charlton WA (1987) Positional differences in size, morphology, and in vitro performance of pea axillary buds. Can J Bot 65: 406-411
33. Hoffmann HMR, Schmidt B, Wolff S (1989) Preparation of 5-bromotetronates [4-alkoxy-5-bromo-2(5h)-furanones] and a new concept for the synthesis of aflatoxins and related structure types: tributyltin hydride versus palladium-promoted intramolecular hydroarylation. Tetrahedron 45: 6113-6126
34. Johnson AW, Gowda G, Hassanali A, Knox J, Monaco S, Razavi Z, Rosebery G (1981) The preparation of synthetic analogs of strigol. J Chem Soc Perkin Trans 1981: 1734-1743
35. Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species: genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142: 1014-1026
36. Just G, Chung BY, Kim S, Rosebery G, Rossy P (1976) Reactions of oxygen and sulfur anions with oxazolidine and thiazolidine derivatives of 2-mesyloxymethylglyceraldehyde acetonide. Can J Chem 54: 2089-2093
37. Kapulnik Y, Delaux P-M, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Séjalon-Delmas N, Combier J-P, Bécard G, Belausov E, et al (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233: 209-216
38. Kim HI, Xie XN, Kim HS, Chun JC, Yoneyama K, Nomura T, Takeuchi Y (2010) Structure-activity relationship of naturally occurring strigolactones in Orobanche minor seed germination stimulation. J Pestic Sci 35: 344-347
39. Limberg G, Thiem J (1995) [beta]-Elimination of protected aldono-1,4-lactones as a general approach to the synthesis of 2-keto-3-deoxyaldonic acids containing four to six carbon atoms. Carbohydr Res 275: 107-115
40. Macalpine GA, Raphael RA, Shaw A, Taylor AW, Wild HJ (1976) Synthesis of germination stimulant (+/-)-strigol. J Chem Soc Perkin Trans 1 410-416
41. Malik H, Kohlen W, Jamil M, Rutjes FPJT, Zwanenburg B (2011) Aromatic A-ring analogues of orobanchol, new germination stimulants for seeds of parasitic weeds. Org Biomol Chem 9: 2286-2293
42. Malik H, Rutjes F, Zwanenburg B (2010) A new efficient synthesis of GR24 and dimethyl A-ring analogues, germinating agents for seeds of the parasitic weeds Striga and Orobanche spp. Tetrahedron 66: 7198-7203
43. 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
44. Mangnus EM, Zwanenburg B (1992) Tentative molecular mechanism for germination stimulation of Striga and Orobanche seeds by strigol and its synthetic analogs. J Agric Food Chem 40: 1066-1070
45. 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 carote-noid pathway. Plant Physiol 139: 920-934
46. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root en-dosymbioses. Nat Rev Microbiol 6: 763-775
47. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45
48. Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto I (2011) New potent fluorescent analogues of strigo-lactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur J Org Chem 2011: 3781-3793
49. Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau C (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138: 1531-1539
50. Rameau C, Bodelin C, Cadier D, Grandjean O, Miard F, Murfet IC (1997) New ramosus mutants at loci Rms1, Rms3 and Rms4 resulting from the mutation breeding program at Versailles. Pisum Genet 29: 7-12
51. Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigo-lactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46: 617-626
52. Reizelman A, Wigchert SCM, del-Bianco C, Zwanenburg B (2003) Synthesis and bioactivity of labelled germination stimulants for the isolation and identification of the strigolactone receptor. Org Biomol Chem 1: 950-959
53. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155: 721-734
54. Sato D, Awad AA, Takeuchi Y, Yoneyama K (2005) Confirmation and quantification of strigolactones, germination stimulants for root parasitic plants Striga and Orobanche, produced by cotton. Biosci Biotechnol Biochem 69: 98-102
55. 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
56. Schachtschabel D, Boland W (2007) Efficient generation of a trisporoid library by combination of synthesis and biotransformation. J Org Chem 72: 1366-1372
57. Schreiber J, Wermuth CG (1965) Etude de la condensation de l'acide pyruvique avec les aldéhydes aliphatiques non substitués en alpha. I. Produits de condensation dont la chaine carbonée est ramifiée-semial-déhydes méthyl-alcoyl maliques et semialdéhydes méthyl-alcoyl mal-éiques. Bull Soc Chim Fr 2242-2249
58. Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363: 67-69
59. Sorefan K, Booker J, Haurogné K, Goussot M, Bainbridge K, Foo E, Chatfield S, Ward S, Beveridge C, Rameau C, et al (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17: 1469-1474
60. Soto MJ, Fernandez-Aparicio M, Castellanos-Morales V, Garcia-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Med-icago sativa). Soil Biol Biochem 42: 383-385
61. Stévenin A, Boyer F-D, Beau J-M (2012) Highly selective formation of β-glycosides of N-acetylglucosamine using catalytic iron(III) triflate. Eur J Org Chem 2012: 1699-1702
62. Surmont R, Verniest G, De Kimpe N (2010) Short synthesis of the seed germination inhibitor 3,4,5-trimethyl-2(5H)-furanone. J Org Chem 75: 5750-5753
63. Thuring J, Keltjens R, Nefkens GHL, Zwanenburg B (1997) Synthesis and biological evaluation of potential substrates for the isolation of the strigol receptor. J Chem Soc Perkin Trans 1 759-765
64. Tsuchiya Y, McCourt P (2012) Strigolactones as small molecule communicators. Mol Biosyst 8: 464-469
65. Tumlinson JH, Klein MG, Doolittle RE, Ladd TL, Proveaux AT (1977) Identification of the female Japanese beetle sex pheromone: inhibition of male response by an enantiomer. Science 197: 789-792
66. Turnbull CGN, Booker JP, Leyser HMO (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32: 255-262
67. Ueno K, Fujiwara M, Nomura S, Mizutani M, Sasaki M, Takikawa H, Sugimoto Y (2011a) Structural requirements of strigolactones for germination induction of Striga gesnerioides seeds. J Agric Food Chem 59: 9226-9231
68. Ueno K, Nomura S, Muranaka S, Mizutani M, Takikawa H, Sugimoto Y (2011b) Ent-29-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
69. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200
70. 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
71. Wolff S, Hoffmann HMR (1988) Aflatoxins revisited: convergent synthesis of the ABC moiety. Synthesis 760-763
72. Xie X, Kusumoto D, Takeuchi Y, Yoneyama K, Yamada Y, Yoneyama K (2007) 29-Epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. J Agric Food Chem 55: 8067-8072
73. Xie X, Yoneyama K, Kusumoto D, Yamada Y, Yokota T, Takeuchi Y, Yoneyama K (2008) Isolation and identification of alectrol as (+)-or-obanchyl acetate, a germination stimulant for root parasitic plants. Phytochemistry 69: 427-431
74. Xie XN, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopa-thol 48: 93-117
75. Xie XN, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y, Yoneyama K (2009) Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum. Phytochemistry 70: 211-215
76. Yamaguchi S, Umehara M, Akiyama K, inventors. December 2, 2010. Plant branching inhibitor, method for producing same, and plant branching inhibitory composition. Japan Patent Application No. WO/2010/137662
77. Yoneyama K, Awad AA, Xie XN, Yoneyama K, Takeuchi Y (2010) Stri-golactones as germination stimulants for root parasitic plants. Plant Cell Physiol 51: 1095-1103
78. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235: 1197-1207
79. Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones: structures and biological activities. Pest Manag Sci 65: 467-470
80. Yoneyama K, Xie XN, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227: 125-132
81. Zanatta N, Barichello R, Pauletto MM, Bonacorso HG, Martins MAP (2003) Convenient synthesis of 3-aminomethylenedihydrofuran-2-ones. Tetrahedron Lett 44: 961-964
82. Zwanenburg B, Mwakaboko AS (2011) Strigolactone analogues and mimics derived from phthalimide, saccharine, p-tolylmalondialdehyde, benzoic and salicylic acid as scaffolds. Bioorg Med Chem 19: 7394-7400
83. Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65: 478-491