New strigolactone analogs as plant hormones with low activities in the rhizosphere

Molecular Plant

Volumn 7, Issue 4, 2014, Pages 675-690

  Boyer, François Didier ^a,b   De Saint Germain, Alexandre ^a   Pouvreau, Jean Bernard ^c   Clavé, Guillaume ^b   Pillot, Jean Paul ^a   Roux, Amélie ^b   Rasmussen, Amanda ^d,e   Depuydt, Stephen ^d,f   Lauressergues, Dominique ^g   Frei Dit Frey, Nicolas ^g   Heugebaert, Thomas S A ^d   Stevens, Christian V ^d   Geelen, Danny ^d   Goormachtig, Sofie ^d,f   Rameau, Catherine ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d GHENT UNIVERSITY   (Belgium)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Arabidopsis; Gigaspora rosea; Pisum sativum; plant growth regulator; root parasitic plants; strigolactones; synthetic analogs

Indexed keywords

LACTONE; PHYTOHORMONE;

ARABIDOPSIS; GENE EXPRESSION REGULATION; GLOMEROMYCOTA; METABOLISM; RHIZOSPHERE;

ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; GLOMEROMYCOTA; LACTONES; PLANT GROWTH REGULATORS; RHIZOSPHERE;

EID: 84898761615     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sst163     Document Type: Article

References (71)

1. Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Sieberer, T., Sehr, E.M., et al. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl Acad. Sci. U S A. 108, 20242-20247.
2. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 435, 824-827.
3. Akiyama, K., Ogasawara, S., Ito, S., and Hayashi, H. (2010). Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 51, 1104-1117.
4. Alder, A., Jamil, M., Marzorati, M., Bruno, M., Vermathen, M., Bigler, P., Ghisla, S., Bouwmeester, H., Beyer, P., and Al-Babili, S. (2012). The path from ?-carotene to carlactone, a strigolactone- like plant hormone. Science. 335, 1348-1351.
5. Becard, G., and Fortin, J.A. (1988). Early events of vesicular arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211-218.
6. Benharrat, H., Boulet, C., Theodet, C., and Thalouarn, P. (2005). Virulence diversity among branched broomrape (O ramosa L.) populations in France. Agron. Sustainable Dev. 25, 123-128.
7. Besserer, A., Puech-Pages, V., Kiefer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., Portais, J.C., Roux, C., Becard, G., and Sejalon-Delmas, N. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4, 1239-1247.
8. Beveridge, C.A., Symons, G.M., Murfet, I.C., Ross, J.J., and 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.
9. Boyer, F.-D., de Saint Germain, A., Pillot, J.-P., Pouvreau, J.-B., Chen, V.X., Ramos, S., Stévenin, A., Simier, P., Delavault, P., Beau, J.-M., et al. (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.
10. Braun, N., de Saint Germain, A., Pillot, J.P., 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.
11. Brewer, P.B., Koltai, H., and Beveridge, C.A. (2013). Diverse roles of strigolactones in plant development. Mol. Plant. 6, 18-28.
12. Buee, M., Rossignol, M., Jauneau, A., Ranjeva, R., and Becard, G. (2000). The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant-Microbe Interact. 13, 693-698.
13. Canevet, J.C., and Graff, Y. (1978). Friedel-crafts reaction of aromatic derivatives with 1, 4-dicarbonyl-2, 3-ethylenic compounds. 2. 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.
14. Chen, V.X., Boyer, F.-D., Rameau, C., Pillot, J.-P., Vors, J.-P., and Beau, J.-M. (2013). New synthesis of A-ring aromatic strigolactone analogues and their evaluation as plant hormones in pea (Pisum sativum). Chem. Eur. J. 19, 4849-4857.
15. Chen, V.X., Boyer, F.-D., Rameau, C., Retailleau, P., Vors, J.-P., and Beau, J.-M. (2010). Stereochemistry, total synthesis, and biological evaluation of the new plant hormone solanacol. Chem. Eur. J. 16, 13941-13945.
16. Cohen, M., Prandi, C., Occhiato, E.G., Tabasso, S., Wininger, S., Resnick, N., Steinberger, Y., Koltai, H., and Kapulnik, Y. (2013). Structure-function relations of strigolactone analogs: activity as plant hormones and plant interactions. Mol. Plant. 6, 141-152.
17. Cook, C.E., Whichard, L.P., Turner, B., and Wall, M.E. (1966). Germination of witchweed (Striga lutea lour): isolation and properties of a potent stimulant. Science. 154, 1189-1190.
18. de Saint Germain, A., Bonhomme, S., Boyer, F.-D., and Rameau, C. (2013a). Novel insights into strigolactone distribution and signalling. Curr. Opin. Plant Biol. 16, 583-589.
19. de Saint Germain, A., Ligerot, Y., Dun, E.A., Pillot, J.-P., Ross, J.J., Beveridge, C.A., and Rameau, C. (2013b). Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol. 163, 1012-1025.
20. Dor, E., Joel, D.M., Kapulnik, Y., Koltai, H., and Hershenhorn, J. (2011). The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta. 234, 419-427.
21. Dos Santos, C.V., Letousey, P., Delavault, P., and Thalouarn, P. (2003). Defense gene expression analysis of Arabidopsis thaliana parasitized by Orobanche ramosa. Phytopathology. 93, 451-457.
22. Foo, E., and Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta. 234, 1073-1081.
23. Fox, J. (2005). The R commander: a basic-statistics graphical user interface to R. J. Stat. Softw. 14, 1-42.
24. Fukui, K., Ito, S., and Asami, T. (2013). Selective mimics of strigolactone actions and their potential use for controlling damage caused by root parasitic weeds. Mol. Plant. 6, 88-99.
25. Fukui, K., Ito, S., Ueno, K., Yamaguchi, S., Kyozuka, J., and Asami, T. (2011). New branching inhibitors and their potential as strigolactone mimics in rice. Bioorg. Med. Chem. Lett. 21, 4905-4908.
26. Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., Fournier, J., Rochange, S., Bécard, G., Bonfante, P., et al. (2013). Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198, 190-202.
27. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.-P., Letisse, F., Matusova, R., Danoun, S., Portais, J.-C., et al. (2008). Strigolactone inhibition of shoot branching. Nature. 455, 189-194.
28. Hamiaux, C., Drummond, R.S.M., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D., and Snowden, K.C. (2012). DAD2 is an alpha/beta hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22, 2032-2036.
29. Humphrey, A.J., Galster, A.M., and Beale, M.H. (2006). Strigolactones in chemical ecology: waste products or vital allelochemicals? Nat. Prod. Rep. 23, 592-614.
30. Johnson, A.W., Gowda, G., Hassanali, A., Knox, J., Monaco, S., Razavi, Z., and Rosebery, G. (1981). The preparation of synthetic analogs of strigol. J. Chem. Soc., Perkin Trans. 1, 1734-1743.
31. Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogne, K., Beveridge, C.A., and 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.
32. Kagiyama, M., Hirano, Y., Mori, T., Kim, S.Y., Kyozuka, J., Seto, Y., Yamaguchi, S., and Hakoshima, T. (2013). Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells. 18, 147-160.
33. Kapulnik, Y., Delaux, P.-M., Resnick, N., Mayzlish-Gati, E., Wininger, S., Bhattacharya, C., Sejalon-Delmas, N., Combier, J.-P., Becard, G., Belausov, E., et al. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta. 233, 209-216.
34. Kgosi, R.L., Zwanenburg, B., Mwakaboko, A.S., and Murdoch, A.J. (2012). Strigolactone analogues induce suicidal seed germination of Striga spp. in soil. Weed Research. 52, 197-203.
35. Kim, H.I., Xie, X.N., Kim, H.S., Chun, J.C., Yoneyama, K., Nomura, T., and Takeuchi, Y. (2010). Structure-activity relationship of naturally occurring strigolactones in Orobanche minor seed germination stimulation. J. Pestic. Sci. 35, 344-347.
36. Kitahara, S., Tashiro, T., Sugimoto, Y., Sasaki, M., and Takikawa, H. (2011). First synthesis of (±)-sorgomol, the germination stimulant for root parasitic weeds isolated from Sorghum bicolor. Tetrahedron Lett. 52, 724-726.
37. Kohlen, W., Charnikhova, T., Lammers, M., Pollina, T., Toth, P., Haider, I., Pozo, M.J., de Maagd, R.A., Ruyter-Spira, C., Bouwmeester, H.J., et al. (2012). The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytologist. 196, 535-547.
38. Kohlen, W., Charnikhova, T., Liu, Q., Bours, R., Domagalska, M.A., Beguerie, S., Verstappen, F., Leyser, O., Bouwmeester, H., and 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.
39. Lechat, M.-M., Pouvreau, J.-B., Péron, T., Gauthier, M., Montiel, G., Véronési, C., Todoroki, Y., Le Bizec, B., Monteau, F., Macherel, D., et al. (2012). PrCYP707A1, an ABA catabolic gene, is a key component of Phelipanche ramosa seed germination in response to the strigolactone analogue GR24. J. Exp. Bot. 63, 5311-5322.
40. Maillet, F., Poinsot, V., Andre, O., Puech-Pages, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in Arbuscular mycorrhiza. Nature. 469, 58-63.
41. Malik, H., Kohlen, W., Jamil, M., Rutjes, F.P.J.T., and Zwanenburg, B. (2011). Aromatic A-ring analogues of orobanchol, new germination stimulants for seeds of parasitic weeds. Org. Biomol. Chem. 9, 2286-2293.
42. Mangnus, E.M., Dommerholt, F.J., Dejong, R.L.P., and 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.
43. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation anc cyto-toxicity assays. J. Immunol. Methods. 65, 55-63.
44. Murfet, I.C., and Reid, J.B. (1993). Developmental mutants. In Peas: Genetics, Molecular Biology and Biotechnology, Casey, R., and Davies, D.R., eds (Wallingford: CAB INTERNATIONAL), pp. 165-216.
45. Nadal, M., and Paszkowski, U. (2013). Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 16, 473-479.
46. Nair, V., Vietti, D.E., and Cooper, C.S. (1981). Degenerative chemistry of malondialdehyde: structure, stereochemistry, and kinetics of formation of enaminals from reaction with amino-acids. J. Am. Chem. Soc. 103, 3030-3036.
47. Nefkens, G.H.L., Thuring, J.W.J.F., Beenakkers, M.F.M., and Zwanenburg, B. (1997). Synthesis of a phthaloylglycinederived strigol analogue and its germination stimulatory activity toward seeds of the parasitic weeds Striga hermonthica and Orobanche crenata. J. Agric. Food Chem. 45, 2273-2277.
48. Pouvreau, J.B., Gaudin, Z., Auger, B., Lechat, M.M., Gauthier, M., Delavault, P., and Simier, P. (2013). A high-throughput seed germination assay for root parasitic plants. Plant Methods. 9, 32.
49. Prandi, C., Occhiato, E.G., Tabasso, S., Bonfante, P., Novero, M., Scarpi, D., Bova, M.E., and Miletto, I. (2011). New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur. J. Org. Chem. 2011, 3781-3793.
50. Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogue, F., and Rameau, C. (2011). Strigolactones regulate protonema branching and act as a quorum sensinglike signal in the moss Physcomitrella patens. Development. 138, 1531-1539.
51. Rameau, C., Bodelin, C., Cadier, D., Grandjean, O., Miard, F., and Murfet, I.C. (1997). New ramosus mutants at loci rms1, rms3 and rms4 resulting from the mutation breeding program at Versailles. Pisum Genetics. 29, 7-12.
52. Rasmussen, A., Heugebaert, T., Matthys, C., Van Deun, R., Boyer, F.-D., Goormachtig, S., Stevens, C., and Geelen, D. (2013). A fluorescent alternative to the synthetic strigolactone GR24. Mol. Plant. 6, 100-112.
53. Rasmussen, A., Mason, M.G., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D., Greb, T., Goormachtig, S., Beeckman, T., et al. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158, 1976-1987.
54. Reinhardt D. (2007). Programming good relations: development of the arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 10, 98-105.
55. Ross, J.J., Weston, D.E., Davidson, S.E., and Reid, J.B. (2011). Plant hormone interactions: how complex are they? Physiol. Plant. 141, 299-309.
56. Ruyter-Spira, C., Kohlen, W., Charnikhova, T., van Zeijl, A., van Bezouwen, L., de Ruijter, N., Cardoso, C., Lopez-Raez, J.A., 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.
57. Scaffidi, A., Waters, M.T., Bond, C.S., Dixon, K.W., Smith, S.M., Ghisalberti, E.L., and Flematti, G.R. (2012). Exploring the molecular mechanism of karrikins and strigolactones. Bioorg. Med. Chem. Lett. 22, 3743-3746.
58. Scaffidi, A., Waters, M.T., Ghisalberti, E.L., Dixon, K.W., Flematti, G.R., and Smith, S.M. (2013). Carlactone-independent seedling morphogenesis in Arabidopsis. Plant J. 76, 1-9.
59. Shoji, M., Suzuki, E., and Ueda, M. (2009). Total synthesis of (±)-5-deoxystrigol via reductive carbon-carbon bond formation. J. Org. Chem. 74, 3966-3969.
60. Sorefan, K., Booker, J., Haurogne, 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.
61. Soto, M.J., Fernandez-Aparicio, M., Castellanos-Morales, V., Garcia-Garrido, J.M., Ocampo, J.A., Delgado, M.J., and Vierheilig, H. (2010). First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol. Biochem. 42, 383-385.
62. Toh, S., Kamiya, Y., Kawakami, N., Nambara, E., McCourt, P., and Tsuchiya, Y. (2012). Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol. 53, 107-117.
63. 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.
64. Xie, X., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Annu. Rev. Phytopathol. 48, 93-117.
65. Xie, X., Yoneyama, K., Kisugi, T., Uchida, K., Ito, S., Akiyama, K., Hayashi, H., Yokota, T., Nomura, T., and Yoneyama, K. (2013). Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant. 6, 153-163.
66. Yoneyama, K., Xie, X., Kim, H.I., Kisugi, T., Nomura, T., Sekimoto, H., and Yokota, T. (2012). How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta. 235, 1197-1207.
67. Yoneyama, K., Xie, X., Yoneyama, K., and Takeuchi, Y. (2009). Strigolactones: structures and biological activities. Pest Manage. Sci. 65, 467-470.
68. Yoneyama, K., Yoneyama, K., Takeuchi, Y., and Sekimoto, H. (2007). Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta. 225, 1031-1038.
69. Zhao, L.H., Zhou, X.E., Wu, Z.S., Yi, W., Xu, Y., Li, S., Xu, T.H., Liu, Y., Chen, R.Z., Kovach, A., et al. (2013). Crystal structures of two phytohormone signal-transducing alpha/beta hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res. 23, 436-439.
70. Zwanenburg, B., and Pospisil, T. (2013). Structure and activity of strigolactones: new plant hormones with a rich future. Mol. Plant. 6, 38-62.
71. Zwanenburg, B., Nayak, S.K., Charnikhova, T.V., and Bouwmeester, H.J. (2013). New strigolactone mimics: structure-activity relationship and mode of action as germinating stimulants for parasitic weeds. Bioorg. Med. Chem. Lett. 23, 5182-5186.