Structural requirements of strigolactones for shoot branching inhibition in rice and arabidopsis

Plant and Cell Physiology

Volumn 56, Issue 6, 2015, Pages 1059-1072

  Umehara, Mikihisa ^a,b   Cao, Mengmeng ^c   Akiyama, Kohki ^d   Akatsu, Tomoki ^c   Seto, Yoshiya ^a,c   Hanada, Atsushi ^a,c   Li, Weiqiang ^a,e   Takeda Kamiya, Noriko ^a   Morimoto, Yu ^a,c   Yamaguchi, Shinjiro ^a,c  

^a RIKEN Center for Sustainable Resource Science   (Japan)

^b TOYO UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

^d Osaka Prefecture University   (Japan)

^e NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Arabidopsis thaliana; Oryza sativa; Stereoisomer; Strigolactone

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; FUNGI; ORYZA SATIVA;

CULTURE MEDIUM; ETHER; LACTONE;

ARABIDOPSIS; CHEMISTRY; CULTURE MEDIUM; DRUG EFFECTS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HYDROPONICS; HYPOCOTYL; ORYZA; PLANT SEED; SHOOT; STEREOISOMERISM; TWO HYBRID SYSTEM;

ARABIDOPSIS; CULTURE MEDIA; ETHER; GERMINATION; HYDROPONICS; HYPOCOTYL; LACTONES; ORYZA; PLANT SHOOTS; SEEDS; STEREOISOMERISM; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84930741399     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv028     Document Type: Article

References (58)

1. Abe, S., Sado, A., Tanaka, K., Kisugi, T., Asami, K., Ota, S. et al. (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. 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. et al. (2012) The path from b-carotene to carlactone, a strigolactone-like plant hormone. Science 335: 1348-1351.
5. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M. et al. (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J. 51: 1019-1029.
6. Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S. et al. (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 50: 1416-1424.
7. Booker, J., Auldridge, M., Wills, S., McCarty, D., Klee, H. And 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.
8. Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P. et al. (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branchinhibiting hormone. Dev. Cell 8: 443-449.
9. Boyer, F. D., de Saint Germain, A., Pillot, J. P., Pouvreau, J. B., Chen, V. X., Ramos, S. 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. Boyer, F. D., de Saint Germain, A., Pouvreau, J. B., Clave, G., Pillot, J. P., Roux, A. et al. (2014) New strigolactone analogs as plant hormones with low activities in the rhizosphere. Mol. Plant 7: 675-690.
11. Bradow, J. M., Connick, W. J. And Pepperman, A. B. (1988) Comparison of the seed germination effects of synthetic analogs of strigol, gibberellic acid, cytokinins and other plant growth regulators. J. Plant Growth Regul. 7: 227-239.
12. Bradow, J. M., Connick, W. J., Pepperman, A. B. And Wartelle, L. H. (1990) Germination stimulation in wild oats (Avena fatua L. ) by synthetic strigol analogues and gibberellic acid. J. Plant Growth Regul. 9: 35-41.
13. Cook, C. E., Whichard, L. P., Turner, B., Wall, M. E. And Egley, G. H. (1966) Germination of witchweed (Striga lutea Lour. ): isolation and properties of a potent stimulant. Science 154: 1189-1190.
14. Cook, C. E., Whichard, L. P., Wall, M. E., Egley, G. H., Coggon, P., Luhan, P. A. et al. (1972) Germination stimulants. 2. The structure of strigol-a potent seed germination stmulant for witchweed (Striga lutea Lour. ). J. Amer. Chem. Soc. 94: 6198-6199.
15. Foo, E., Bullier, E., Goussot, M., Foucher, F., Rameau, C. And Beveridge, C. A. (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17: 464-474.
16. 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.
17. 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.
18. Gomez-Roldan, V., Fermas, S., Brewer, P. B., Puech-Pages, V., Dun, E. A., Pillot, J. P. et al. (2008) Strigolactone inhibition of shoot branching. Nature 455: 189-194.
19. Guo, Y., Zheng, Z., La Clair, J. J., Chory, J. And Noel, J. P. (2013) Smoke-derived karrikin perception by the a/b-hydrolase KAI2 from Arabidopsis. Proc. Natl Acad. Sci. USA 110: 8284-8289.
20. Hamiaux, C., Drummond, R. S., Janssen, B. J., Ledger, S. E., Cooney, J. M., Newcomb, R. D. et al. (2012) DAD2 is an a/b hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22: 2032-2036.
21. Humphrey, A. J. And Beale, M. H. (2006) Strigol: biogenesis and physiological activity. Phytochemistry 67: 636-640.
22. Ishikawa, S., Maekawa, M., Arite, T., Onishi, K., Takamure, I. And Kyozuka, J. (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol. 46: 79-86.
23. Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L. et al. (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401-405.
24. Johnson, A. W., Rosebery, G. And Parker, C. (1976) Novel-approach to Striga and Orobanche control using synthetic germination stimulants. Weed Res. 16: 223-227.
25. Johnson, A. W., Gowda, G., Hassanali, A., Knox, J., Monaco, S., Razavi, Z. et al. (1981) The preparation of synthetic analogs of strigol. J. Chem. Soc. Perkin Trans. 1: 1734-1743.
26. Johnson, X., Brcich, T., Dun, E. A., Goussot, M., Haurogne, K., Beveridge, C. A. et al. (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.
27. Kagiyama, M., Hirano, Y., Mori, T., Kim, S. Y., Kyozuka, J., Seto, Y. et al. (2013) Structures of D14 and D14L in the strigolactone and karrikin signaling pathways. Genes Cells 18: 147-160.
28. Kamachi, K., Yamaya, T., Mae, T. And Ojima, K. (1991) A role for glutaminesynthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol. 96: 411-417.
29. Kohlen, W., Charnikhova, T., Liu, Q., Bours, R., Domagalska, M. A., Beguerie, S. et al. (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. Kondo, Y., Tadokoro, E., Matsuura, M., Iwasaki, K., Sugimoto, Y., Miyake, H. et al. (2007) Synthesis and seed germination stimulating activity of some imino analogs of strigolactones. Biosci. Biotechnol. Biochem. 71: 2781-2786.
31. Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z. et al. (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21: 1512-1525.
32. MacAlpine, G. A., Raphael, R. A., Shaw, A., Taylor, A. W. And Wild, H. J. (1976) Synthesis of the germination stimulant (±)-strigol. J. Chem. Soc. Perkin Trans. 1: 410-416.
33. Mangnus, E. M., Stommen, P. L. A. And Zwanenburg, B. (1992) A standardized bioassay for evaluation of potential germination stimulants for seeds of parasitic weeds. J. Plant Growth Regul. 11: 91-98.
34. Mangnus, E. M. And Zwanenburg, B. (1992a) Synthesis, structural characterization, and biological evaluation of all 4 enantiomers of strigol analog GR7. J. Agric. Food Chem. 40: 697-700.
35. Mangnus, E. M. And Zwanenburg, B. (1992b) Tentative molecular mechanism for germination stimulation of striga and orobanche seeds by strigol and its synthetic analogs. J. Agric. Food Chem. 40: 1066-1070.
36. Nakamura, H., Xue, Y. L., Miyakawa, T., Hou, F., Qin, H. M., Fukui, K. et al. (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat. Commun. 4: 2613.
37. Nelson, D. C., Scaffidi, A., Dun, E. A., Waters, M. T., Flematti, G. R., Dixon, K. W. et al. (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 108: 8897-8902.
38. Norén, H., Svensson, P. And Andersson, B. (2004) A convenient and versatile hydroponic cultivation system for Arabidopsis thaliana. Physiol. Plant. 121: 343-348.
39. Reizelman, A., Scheren, M., Nefkens, G. H. L. And Zwanenburg, B. (2000) Synthesis of all eight stereoisomers of the germination stimulant strigol. Synthesis 13: 1944-1951.
40. Scaffidi, A., Waters, M., Sun, Y. K., Skelton, B. W., Dixon, K. W., Ghisalberti, E. L. et al. (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 165: 1221-1232.
41. Seto, Y., Sado, A., Asami, K., Hanada, A., Umehara, M., Akiyama, K. et al. (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc. Natl Acad. Sci. USA 111: 1640-1645.
42. Sorefan, K., Booker, J., Haurogne, K., Goussot, M., Bainbridge, K., Foo, E. et al. (2003) MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev. 17: 1469-1474.
43. Stanga, J. P., Smith, S. M., Briggs, W. R. And Nelson, D. C. (2013) SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol. 163: 318-330.
44. Stirnberg, P., van De Sande, K. And Leyser, H. M. (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131-1141.
45. Sugimoto, Y., Wigchert, S. C. M., Thuring, J. And Zwanenburg, B. (1998) Synthesis of all eight stereoisomers of the germination stimulant sorgolactone. J. Org. Chem. 63: 1259-1267.
46. Sugimoto, Y. And Ueyama, T. (2008) Production of (+)-5-deoxystrigol by Lotus japonicus root culture. Phytochemistry 69: 212-217.
47. Sun, X. D. And Ni, M. (2011) HYPOSENSITIVE TO LIGHT, an a/b fold protein, acts downstream of ELONGATED HYPOCOTYL 5 to regulate seedling de-etiolation. Mol. Plant 4: 116-126.
48. Thuring, J., Nefkens, G. H. L. And Zwanenburg, B. (1997) Asymmetric synthesis of all stereoisomers of the strigol analogue GR24. Dependence of absolute configuration on stimulatory activity of Striga hermonthica and Orobanche crenata seed germination. J. Agric. Food Chem. 45: 2278-2283.
49. Ueno, K., Nomura, S., Muranaka, S., Mizutani, M., Takikawa, H. And Sugimoto, Y. (2011) Ent-20-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.
50. Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N. And Yamaguchi, S. (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol. 51: 1118-1126.
51. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N. et al. (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455: 195-200.
52. Waters, M. T., Nelson, D. C., Scaffidi, A., Flematti, G. R., Sun, Y. K., Dixon, K. W. et al. (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139: 1285-1295.
53. Xie, X., Yoneyama, K., Kisugi, T., Uchida, K., Ito, S., Akiyama, K. et al. (2013) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol. Plant 6: 153-163.
54. Xie, X., Yoneyama, K. And Yoneyama, K. (2010) The strigolactone story. Annu. Rev. Phytopathol. 48: 93-117.
55. Yoneyama, K., Xie, X., Yoneyama, K. And Takeuchi, Y. (2009) Structural diversity and distribution of strigolactones in the plant kingdom. J. Pestic. Sci. 34: 302-305.
56. Zhao, L. H., Zhou, X. E., Wu, Z. S., Yi, W., Xu, Y., Li, S. et al. (2013) Crystal structures of two phytohormone signal-transducing a/b hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res. 23: 436-439.
57. Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N. et al. (2013) D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406-410.
58. Zwanenburg, B., Mwakaboko, A. S., Reizelman, A., Anilkumar, G. And Sethumadhavan, D. (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag. Sci. 65: 478-491.