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Science China Life Sciences

, Volume 61, Issue 3, pp 277–284 | Cite as

Recent advances in molecular basis for strigolactone action

  • Ruifeng Yao
  • Jiayang Li
  • Daoxin XieEmail author
Review

Abstract

Strigolactones (SLs) are a very special class of plant hormones, which act as endogenous signals to regulate shoot branching in plants, and also serve as rhizosphere signals to regulate interactions of host plants with heterologous organisms such as symbiotic arbuscular mycorrhizal fungi and parasitic weeds. In this short review, we give a brief description of novel discoveries in SL biosynthesis pathway, and mainly summarize the recent advances in SL perception and signal transduction.

Keywords

plant hormone strigolactone shoot branching perception receptor signal transduction repressor transcription factor 

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Notes

Acknowledgements

The work was supported by the National Key R&D Program of China (2016YFA0500501, 2016YFD0101800), the National Natural Science Foundation of China (31630085, 91635301) and the grant from the China Association for Science and Technology.

References

  1. Abe, S., Sado, A., Tanaka, K., Kisugi, T., Asami, K., Ota, S., Kim, H.I., Yoneyama, K., Xie, X., Ohnishi, T., Seto, Y., Yamaguchi, S., Akiyama, K., Yoneyama, K., and 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.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aguilar-Martínez, J.A., Poza-Carrión, C., and Cubas, P. (2007). Arabidopsis BRANCHED1 acts as an integrator of branching signals within axillary buds. Plant Cell 19, 458–472.CrossRefPubMedPubMedCentralGoogle Scholar
  3. Agusti, J., Herold, S., Schwarz, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Sieberer, T., Sehr, E.M., and Greb, T. (2011). Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108, 20242–20247.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Akiyama, K., Matsuzaki, K.I., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827.CrossRefPubMedGoogle Scholar
  5. Al-Babili, S., and Bouwmeester, H.J. (2015). Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66, 161–186.CrossRefPubMedGoogle Scholar
  6. 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 beta-carotene to carlactone, a strigolactone-like plant hormone. Science 335, 1348–1351.CrossRefPubMedGoogle Scholar
  7. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H., and Kyozuka, J. (2007). DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51, 1019–1029.CrossRefPubMedGoogle Scholar
  8. Arite, T., Umehara, M., Ishikawa, S., Hanada, A., Maekawa, M., Yamaguchi, S., and Kyozuka, J. (2009). d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50, 1416–1424.CrossRefPubMedGoogle Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. Brewer, P.B., Yoneyama, K., Filardo, F., Meyers, E., Scaffidi, A., Frickey, T., Akiyama, K., Seto, Y., Dun, E.A., Cremer, J.E., Kerr, S.C., Waters, M.T., Flematti, G.R., Mason, M.G., Weiller, G., Yamaguchi, S., Nomura, T., Smith, S.M., Yoneyama, K., and Beveridge, C.A. (2016). LATERAL BRANCHING OXIDOREDUCTASE acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 113, 6301–6306.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bu, Q., Lv, T., Shen, H., Luong, P., Wang, J., Wang, Z., Huang, Z., Xiao, L., Engineer, C., Kim, T.H., Schroeder, J.I., and Huq, E. (2014). Regulation of drought tolerance by the F-Box protein MAX2 in Arabidopsis. Plant Physiol 164, 424–439.CrossRefPubMedGoogle Scholar
  12. Cardoso, C., Zhang, Y., Jamil, M., Hepworth, J., Charnikhova, T., Dimkpa, S.O.N., Meharg, C., Wright, M.H., Liu, J., Meng, X., Wang, Y., Li, J., McCouch, S.R., Leyser, O., Price, A.H., Bouwmeester, H.J., and Ruyter-Spira, C. (2014). Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA 111, 2379–2384.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chevalier, F., Nieminen, K., Sánchez-Ferrero, J.C., Rodríguez, M.L., Chagoyen, M., Hardtke, C.S., and Cubas, P. (2014). Strigolactone promotes degradation of DWARF14, an alpha/beta hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26, 1134–1150.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Conn, C.E., Bythell-Douglas, R., Neumann, D., Yoshida, S., Whittington, B., Westwood, J.H., Shirasu, K., Bond, C.S., Dyer, K.A., and Nelson, D.C. (2015). Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349, 540–543.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. de Saint Germain, A., Clavé, G., Badet-Denisot, M.A., Pillot, J.P., Cornu, D., Le Caer, J.P., Burger, M., Pelissier, F., Retailleau, P., Turnbull, C., Bonhomme, S., Chory, J., Rameau, C., and Boyer, F.D. (2016). An histidine covalent receptor and butenolide complex mediates strigolactone perception. Nat Chem Biol 12, 787–794.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Decker, E.L., Alder, A., Hunn, S., Ferguson, J., Lehtonen, M.T., Scheler, B., Kerres, K.L., Wiedemann, G., Safavi-Rizi, V., Nordzieke, S., Balakrishna, A., Baz, L., Avalos, J., Valkonen, J.P.T., Reski, R., and Al-Babili, S. (2017). Strigolactone biosynthesis is evolutionarily conserved, regulated by phosphate starvation and contributes to resistance against phytopathogenic fungi in a moss, Physcomitrella patens. New Phytol 216, 455–468.CrossRefPubMedGoogle Scholar
  18. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005). The F-box protein TIR1 is an auxin receptor. Nature 435, 441–445.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. Fang, X., and Chen, X.Y. (2017). Branching out. Sci China Life Sci 60, 108–110.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gao, Z., Qian, Q., Liu, X., Yan, M., Feng, Q., Dong, G., Liu, J., and Han, B. (2009). Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71, 265–276.CrossRefPubMedGoogle Scholar
  23. Gobena, D., Shimels, M., Rich, P.J., Ruyter-Spira, C., Bouwmeester, H., Kanuganti, S., Mengiste, T., and Ejeta, G. (2017). Mutation in sorghum LOW GERMINATION STIMULANT 1 alters strigolactones and causes Striga resistance. Proc Natl Acad Sci USA 114, 4471–4476.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pagès, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., Bouwmeester, H., Bécard, G., Beveridge, C.A., Rameau, C., and Rochange, S.F. (2008). Strigolactone inhibition of shoot branching. Nature 455, 189–194.CrossRefPubMedGoogle Scholar
  25. González-Grandío, E., Poza-Carrión, C., Sorzano, C.O.S., and Cubas, P. (2013). BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 25, 834–850.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Guo, S., Xu, Y., Liu, H., Mao, Z., Zhang, C., Ma, Y., Zhang, Q., Meng, Z., and Chong, K. (2013). The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat Commun 4, 1566.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gutjahr, C., Gobbato, E., Choi, J., Riemann, M., Johnston, M.G., Summers, W., Carbonnel, S., Mansfield, C., Yang, S.Y., Nadal, M., Acosta, I., Takano, M., Jiao, W.B., Schneeberger, K., Kelly, K.A., and Paszkowski, U. (2015). Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350, 1521–1524.CrossRefPubMedGoogle Scholar
  28. Ha, C.V., Leyva-González, M.A., Osakabe, Y., Tran, U.T., Nishiyama, R., Watanabe, Y., Tanaka, M., Seki, M., Yamaguchi, S., Dong, N.V., Yamaguchi-Shinozaki, K., Shinozaki, K., Herrera-Estrella, L., and Tran, L.S.P. (2014). Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci USA 111, 851–856.CrossRefPubMedGoogle Scholar
  29. 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 α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22, 2032–2036.CrossRefPubMedGoogle Scholar
  30. Huang, K., Wang, D., Duan, P., Zhang, B., Xu, R., Li, N., and Li, Y. (2017). WIDE AND THICK GRAIN 1, which encodes an otubain-like protease with deubiquitination activity, influences grain size and shape in rice. Plant J 91, 849–860.CrossRefPubMedGoogle Scholar
  31. Huang, X., Qian, Q., Liu, Z., Sun, H., He, S., Luo, D., Xia, G., Chu, C., Li, J., and Fu, X. (2009). Natural variation at the DEP1 locus enhances grain yield in rice. Nat Genet 41, 494–497.CrossRefPubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. Janssen, B.J., Drummond, R.S.M., and Snowden, K.C. (2014). Regulation of axillary shoot development. Curr Opin Plant Biol 17, 28–35.CrossRefPubMedGoogle Scholar
  34. Jeong, D.H., Park, S., Zhai, J., Gurazada, S.G.R., De Paoli, E., Meyers, B.C., and Green, P.J. (2011). Massive analysis of rice small RNAs: mechanistic implications of regulated micrornas and variants for differential target RNA cleavage. Plant Cell 23, 4185–4207.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., Yi, W., Zhao, L., Ma, H., He, Y., Wu, Z., Melcher, K., Qian, Q., Xu, H.E., Wang, Y., and Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504, 401–405.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., Dong, G., Zeng, D., Lu, Z., Zhu, X., Qian, Q., and Li, J. (2010). Regulation of Os-SPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42, 541–544.CrossRefPubMedGoogle Scholar
  37. Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurogné, 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.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. Kameoka, H., Dun, E.A., Lopez-Obando, M., Brewer, P.B., de Saint Germain, A., Rameau, C., Beveridge, C.A., and Kyozuka, J. (2016). Phloem transport of the receptor DWARF14 protein is required for full function of strigolactones. Plant Physiol 172, 1844–1852.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kapulnik, Y., Delaux, P.M., Resnick, N., Mayzlish-Gati, E., Wininger, S., Bhattacharya, C., Séjalon-Delmas, N., Combier, J.P., Bécard, G., Belausov, E., Beeckman, T., Dor, E., Hershenhorn, J., and Koltai, H. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233, 209–216.CrossRefPubMedGoogle Scholar
  41. Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435, 446–451.CrossRefPubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. Kretzschmar, T., Kohlen, W., Sasse, J., Borghi, L., Schlegel, M., Bachelier, J.B., Reinhardt, D., Bours, R., Bouwmeester, H.J., and Martinoia, E. (2012). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483, 341–344.CrossRefPubMedGoogle Scholar
  44. Li, S., Chen, L., Li, Y., Yao, R., Wang, F., Yang, M., Gu, M., Nan, F., Xie, D., and Yan, J. (2016). Effect of GR24 stereoisomers on plant development in Arabidopsis. Mol Plant 9, 1432–1435.CrossRefPubMedGoogle Scholar
  45. Liang, Y., Ward, S., Li, P., Bennett, T., and Leyser, O. (2016). SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms. Plant Cell 28, 1581–1601.PubMedPubMedCentralGoogle Scholar
  46. Lin, H., Wang, R., Qian, Q., Yan, M., Meng, X., Fu, Z., Yan, C., Jiang, B., Su, Z., Li, J., and Wang, Y. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21, 1512–1525.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Liu, J., Cheng, X., Liu, P., and Sun, J. (2017). miR156-targeted SBP-Box transcription factors interact with DWARF53 to regulate TEOSINTE BRANCHED1 and BARREN STALK1 expression in bread wheat. Plant Physiol 174, 1931–1948.CrossRefPubMedGoogle Scholar
  48. Liu, W., Wu, C., Fu, Y., Hu, G., Si, H., Zhu, L., Luan, W., He, Z., and Sun, Z. (2009). Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230, 649–658.CrossRefPubMedGoogle Scholar
  49. Lu, Z., Yu, H., Xiong, G., Wang, J., Jiao, Y., Liu, G., Jing, Y., Meng, X., Hu, X., Qian, Q., Fu, X., Wang, Y., and Li, J. (2013). Genome-wide binding analysis of the transcription activator IDEAL PLANT ARCHITECTURE1 reveals a complex network regulating rice plant architecture. Plant Cell 25, 3743–3759.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Lumba, S., Holbrook-Smith, D., and McCourt, P. (2017a). The perception of strigolactones in vascular plants. Nat Chem Biol 13, 599–606.CrossRefPubMedGoogle Scholar
  51. Lumba, S., Subha, A., and McCourt, P. (2017b). Found in translation: applying lessons from model systems to strigolactone signaling in parasitic plants. Trends Biochem Sci 42, 556–565.CrossRefPubMedGoogle Scholar
  52. Ma, H., Duan, J., Ke, J., He, Y., Gu, X., Xu, T.H., Yu, H., Wang, Y., Brunzelle, J.S., Jiang, Y., Rothbart, S.B., Xu, H.E., Li, J., and Melcher, K. (2017). A D53 repression motif induces oligomerization of TOPLESS corepressors and promotes assembly of a corepressor-nucleosome complex. Sci Adv 3, e1601217.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., Cromer, L., Giraudet, D., Formey, D., Niebel, A., Martinez, E.A., Driguez, H., Bécard, G., and Dénarié, J. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63.CrossRefPubMedGoogle Scholar
  54. Minakuchi, K., Kameoka, H., Yasuno, N., Umehara, M., Luo, L., Kobayashi, K., Hanada, A., Ueno, K., Asami, T., Yamaguchi, S., and Kyozuka, J. (2010). FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51, 1127–1135.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Miura, K., Ikeda, M., Matsubara, A., Song, X.J., Ito, M., Asano, K., Matsuoka, M., Kitano, H., and Ashikari, M. (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42, 545–549.CrossRefPubMedGoogle Scholar
  56. Nakamura, H., Xue, Y.L., Miyakawa, T., Hou, F., Qin, H.M., Fukui, K., Shi, X., Ito, E., Ito, S., Park, S.H., Miyauchi, Y., Asano, A., Totsuka, N., Ueda, T., Tanokura, M., and Asami, T. (2013). Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4, 2613.PubMedGoogle Scholar
  57. Niwa, M., Daimon, Y., Kurotani, K., Higo, A., Pruneda-Paz, J.L., Breton, G., Mitsuda, N., Kay, S.A., Ohme-Takagi, M., Endo, M., and Araki, T. (2013). BRANCHED1 interacts with FLOWERING LOCUS T to repress the floral transition of the axillary meristems in Arabidopsis. Plant Cell 25, 1228–1242.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Rasmussen, A., Mason, M.G., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D., Greb, T., Goormachtig, S., Beeckman, T., and Beveridge, C.A. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158, 1976–1987.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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., Verstappen, F., and Bouwmeester, H. (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.CrossRefPubMedGoogle Scholar
  60. Schwartz, S.H., Qin, X., and Loewen, M.C. (2004). The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279, 46940–46945.CrossRefPubMedGoogle Scholar
  61. Shan, X., Yan, J., and Xie, D. (2012). Comparison of phytohormone signaling mechanisms. Curr Opin Plant Biol 15, 84–91.CrossRefPubMedGoogle Scholar
  62. Shinohara, N., Taylor, C., and Leyser, O. (2013). Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol 11, e1001474.CrossRefPubMedPubMedCentralGoogle Scholar
  63. Simons, J.L., Napoli, C.A., Janssen, B.J., Plummer, K.M., and Snowden, K.C. (2007). Analysis of the DECREASED APICAL DOMINANCE genes of petunia in the control of axillary branching. Plant Physiol 143, 697–706.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Smith, S.M., and Li, J. (2014). Signalling and responses to strigolactones and karrikins. Curr Opin Plant Biol 21, 23–29.CrossRefPubMedGoogle Scholar
  65. Snowden, K.C., and Janssen, B.J. (2016). Structural biology: signal locked in. Nature 536, 402–404.CrossRefPubMedGoogle Scholar
  66. Snowden, K.C., Simkin, A.J., Janssen, B.J., Templeton, K.R., Loucas, H.M., Simons, J.L., Karunairetnam, S., Gleave, A.P., Clark, D.G., and Klee, H.J. (2005). The decreased apical dominance1/petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17, 746–759.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Song, X., Lu, Z., Yu, H., Shao, G., Xiong, J., Meng, X., Jing, Y., Liu, G., Xiong, G., Duan, J., Yao, X.F., Liu, C.M., Li, H., Wang, Y., and Li, J. (2017). IPA1 functions as a downstream transcription factor repressed by D53 in strigolactone signaling in rice. Cell Res 27, 1128–1141.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sorefan, K., Booker, J., Haurogné, K., Goussot, M., Bainbridge, K., Foo, E., Chatfield, S., Ward, S., Beveridge, C., Rameau, C., and Leyser, O. (2003). MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. Genes Dev 17, 1469–1474.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Soundappan, I., Bennett, T., Morffy, N., Liang, Y., Stanga, J.P., Abbas, A., Leyser, O., and Nelson, D.C. (2015). SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell 27, 3143–3159.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Stirnberg, P., Furner, I.J., and Ottoline Leyser, H.M. (2007). MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50, 80–94.CrossRefPubMedGoogle Scholar
  72. Takeda, T., Suwa, Y., Suzuki, M., Kitano, H., Ueguchi-Tanaka, M., Ashikari, M., Matsuoka, M., and Ueguchi, C. (2003). The OsTB1 gene negatively regulates lateral branching in rice. Plant J 33, 513–520.CrossRefPubMedGoogle Scholar
  73. Toh, S., Holbrook-Smith, D., Stogios, P.J., Onopriyenko, O., Lumba, S., Tsuchiya, Y., Savchenko, A., and McCourt, P. (2015). Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350, 203–207.CrossRefPubMedGoogle Scholar
  74. Tsuchiya, Y., Yoshimura, M., Sato, Y., Kuwata, K., Toh, S., Holbrook-Smith, D., Zhang, H., McCourt, P., Itami, K., Kinoshita, T., and Hagihara, S. (2015). Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349, 864–868.CrossRefPubMedGoogle Scholar
  75. Ueda, H., and Kusaba, M. (2015). Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169, 138–147.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., Chow, T.Y., Hsing, Y.I.C., Kitano, H., Yamaguchi, I., and Matsuoka, M. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437, 693–698.CrossRefPubMedGoogle Scholar
  77. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu, K., Yoneyama, K., Kyozuka, J., and Yamaguchi, S. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195–200.CrossRefPubMedGoogle Scholar
  79. VanHook, A.M. (2016). A lock that cuts its own key. Sci Signal 9, ec196–ec196.CrossRefGoogle Scholar
  80. Wang, J., Yu, H., Xiong, G., Lu, Z., Jiao, Y., Meng, X., Liu, G., Chen, X., Wang, Y., and Li, J. (2017a). Tissue-specific ubiquitination by IPA1 INTERACTING PROTEIN1 modulates IPA1 protein levels to regulate plant architecture in rice. Plant Cell 29, 697–707.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wang, L., and Smith, S.M. (2016). Strigolactones redefine plant hormones. Sci China Life Sci 59, 1083–1085.CrossRefPubMedGoogle Scholar
  82. Wang, L., Wang, B., Jiang, L., Liu, X., Li, X., Lu, Z., Meng, X., Wang, Y., Smith, S.M., and Li, J. (2015). Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation. Plant Cell 27, 3128–3142.CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wang, S., Wu, K., Qian, Q., Liu, Q., Li, Q., Pan, Y., Ye, Y., Liu, X., Wang, J., Zhang, J., Li, S., Wu, Y., and Fu, X. (2017b). Non-canonical regulation of SPL transcription factors by a human OTUB1-like deubiquitinase defines a new plant type rice associated with higher grain yield. Cell Res 27, 1142–1156.CrossRefPubMedPubMedCentralGoogle Scholar
  84. Wang, Y., Sun, S., Zhu, W., Jia, K., Yang, H., and Wang, X. (2013). Strigolactone/ MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27, 681–688.CrossRefPubMedGoogle Scholar
  85. Waters, M.T., Gutjahr, C., Bennett, T., and Nelson, D.C. (2017). Strigolactone signaling and evolution. Annu Rev Plant Biol 68, 291–322.CrossRefPubMedGoogle Scholar
  86. Waters, M.T., Nelson, D.C., Scaffidi, A., Flematti, G.R., Sun, Y.K., Dixon, K.W., and Smith, S.M. (2012). Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139, 1285–1295.CrossRefPubMedGoogle Scholar
  87. Waters, M.T., and Smith, S.M. (2013). KAI2- and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol Plant 6, 63–75.CrossRefPubMedGoogle Scholar
  88. Woo, H.R., Kim, J.H., Nam, H.G., and Lim, P.O. (2004). The delayed leaf senescence mutants of Arabidopsis, ore1, ore3, and ore9 are tolerant to oxidative stress. Plant Cell Physiol 45, 923–932.CrossRefPubMedGoogle Scholar
  89. Xie, X., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Annu Rev Phytopathol 48, 93–117.CrossRefPubMedGoogle Scholar
  90. Xiong, G., Wang, Y., and Li, J. (2014). Action of strigolactones in plants. Enzymes 35, 57–84.CrossRefPubMedGoogle Scholar
  91. Yamada, Y., Furusawa, S., Nagasaka, S., Shimomura, K., Yamaguchi, S., and Umehara, M. (2014). Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240, 399–408.CrossRefPubMedGoogle Scholar
  92. Yan, J., Zhang, C., Gu, M., Bai, Z., Zhang, W., Qi, T., Cheng, Z., Peng, W., Luo, H., Nan, F., Wang, Z., and Xie, D. (2009). The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220–2236.CrossRefPubMedPubMedCentralGoogle Scholar
  93. Yao, R., Ming, Z., Yan, L., Li, S., Wang, F., Ma, S., Yu, C., Yang, M., Chen, L., Chen, L., Li, Y., Yan, C., Miao, D., Sun, Z., Yan, J., Sun, Y., Wang, L., Chu, J., Fan, S., He, W., Deng, H., Nan, F., Li, J., Rao, Z., Lou, Z., and Xie, D. (2016). DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536, 469–473.CrossRefPubMedGoogle Scholar
  94. Yao, R., Wang, F., Ming, Z., Du, X., Chen, L., Wang, Y., Zhang, W., Deng, H., and Xie, D. (2017). ShHTL7 is a non-canonical receptor for strigolactones in root parasitic weeds. Cell Res 27, 838–841.CrossRefPubMedGoogle Scholar
  95. Zhang, L., Yu, H., Ma, B., Liu, G., Wang, J., Wang, J., Gao, R., Li, J., Liu, J., Xu, J., Zhang, Y., Li, Q., Huang, X., Xu, J., Li, J., Qian, Q., Han, B., He, Z., and Li, J. (2017). A natural tandem array alleviates epigenetic repression of IPA1 and leads to superior yielding rice. Nat Commun 8, 14789.CrossRefPubMedPubMedCentralGoogle Scholar
  96. Zhang, Y., van Dijk, A.D.J., Scaffidi, A., Flematti, G.R., Hofmann, M., Charnikhova, T., Verstappen, F., Hepworth, J., van der Krol, S., Leyser, O., Smith, S.M., Zwanenburg, B., Al-Babili, S., Ruyter-Spira, C., and Bouwmeester, H.J. (2014). Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10, 1028–1033.CrossRefPubMedGoogle Scholar
  97. Zhao, L.H., Zhou, X.E., Yi, W., Wu, Z., Liu, Y., Kang, Y., Hou, L., de Waal, P.W., Li, S., Jiang, Y., Scaffidi, A., Flematti, G.R., Smith, S.M., Lam, V.Q., Griffin, P.R., Wang, Y., Li, J., Melcher, K., and Xu, H.E. (2015). Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res 25, 1219–1236.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 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., Kang, Y., Hou, L., He, Y., Xie, C., Song, W., Zhong, D., Xu, Y., Wang, Y., Li, J., Zhang, C., Melcher, K., and Xu, H.E. (2013). Crystal structures of two phytohormone signal-transducing α/β hydrolases: karrikin-signaling KAI2 and strigolactone-signaling DWARF14. Cell Res 23, 436–439.CrossRefPubMedPubMedCentralGoogle Scholar
  99. Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., Wu, F., Mao, H., Dong, W., Gan, L., Ma, W., Gao, H., Chen, J., Yang, C., Wang, D., Tan, J., Zhang, X., Guo, X., Wang, J., Jiang, L., Liu, X., Chen, W., Chu, J., Yan, C., Ueno, K., Ito, S., Asami, T., Cheng, Z., Wang, J., Lei, C., Zhai, H., Wu, C., Wang, H., Zheng, N., and Wan, J. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504, 406–410.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Tsinghua-Peking Joint Center for Life Sciences, and MOE Key Laboratory of Bioinformatics, School of Life SciencesTsinghua UniversityBeijingChina
  2. 2.Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina
  3. 3.University of Chinese Academy of SciencesBeijingChina

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