Strigolactone signaling in Arabidopsis regulates shoot development by targeting D53-like SMXL repressor proteins for ubiquitination and degradation

Plant Cell

Volumn 27, Issue 11, 2015, Pages 3128-3142

  Wang, Lei ^a,b   Wang, Bing ^a   Jiang, Liang ^a,b   Liu, Xue ^a,b   Li, Xilong ^a   Lu, Zefu ^a,b   Meng, Xiangbing ^a   Wang, Yonghong ^a,b   Smith, Steven M ^a,c   Lia, Jiayang ^a,b  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; GREEN FLUORESCENT PROTEIN; LACTONE; PROTEIN BINDING; REPRESSOR PROTEIN;

ANATOMY AND HISTOLOGY; ARABIDOPSIS; DRUG EFFECTS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PLANT LEAF; PROTEIN DEGRADATION; SHOOT; SIGNAL TRANSDUCTION; UBIQUITINATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GREEN FLUORESCENT PROTEINS; LACTONES; MUTATION; PLANT LEAVES; PLANT SHOOTS; PROTEIN BINDING; PROTEOLYSIS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84949664392     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.15.00605     Document Type: Article

References (57)

1. Abe, 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. 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.
3. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827.
4. Al-Babili, S., and Bouwmeester, H.J. (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., and Al-Babili, S. (2012). The path from b-carotene to carlactone, a strigolactonelike plant hormone. Science 335: 1348–1351.
6. Bargmann, B.O., and Birnbaum, K.D. (2009). Positive fluorescent selection permits precise, rapid, and in-depth overexpression analysis in plant protoplasts. Plant Physiol. 149: 1231–1239.
7. Bennett, T., and Leyser, O. (2014). Strigolactone signalling: standing on the shoulders of DWARFs. Curr. Opin. Plant Biol. 22: 7–13.
8. 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.
9. Braun, N., et al. (2012). The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol. 158: 225–238.
10. Bythell-Douglas, R., Waters, M.T., Scaffidi, A., Flematti, G.R., Smith, S.M., and Bond, C.S. (2013). The structure of the karrikin-insensitive protein (KAI2) in Arabidopsis thaliana. PLoS One 8: e54758.
11. Causier, B., Ashworth, M., Guo, W., and Davies, B. (2012). The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol. 158: 423–438.
12. Chen, X., Zhou, X., Xi, L., Li, J., Zhao, R., Ma, N., and Zhao, L. (2013). Roles of DgBRC1 in regulation of lateral branching in chrysanthemum (Dendranthema 3 grandiflora cv. Jinba). PLoS One 8: e61717.
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 a/b hydrolase essential for strigolactone signaling in Arabidopsis. Plant Cell 26: 1134–1150.
14. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735–743.
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.
16. Dai, Y., Wang, H., Li, B., Huang, J., Liu, X., Zhou, Y., Mou, Z., and Li, J. (2006). Increased expression of MAP KINASE KINASE7 causes deficiency in polar auxin transport and leads to plant architectural abnormality in Arabidopsis. Plant Cell 18: 308–320.
17. Ding, Y.H., Liu, N.Y., Tang, Z.S., Liu, J., and Yang, W.C. (2006). Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18: 815–830.
18. Domagalska, M.A., and Leyser, O. (2011). Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12: 211–221.
19. Ferguson, B.J., and Beveridge, C.A. (2009). Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol. 149: 1929–1944.
20. Gomez-Roldan, V., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455: 189–194.
21. González-Grandío, E., Poza-Carrión, C., Sorzano, C.O., and Cubas, P. (2013). BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 25: 834–850.
22. Hamiaux, C., Drummond, R.S., Janssen, B.J., Ledger, S.E., Cooney, J.M., Newcomb, R.D., and Snowden, K.C. (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.
23. Jiang, L., et al. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504: 401–405.
24. 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.
25. 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.
26. Long, J.A., Ohno, C., Smith, Z.R., and Meyerowitz, E.M. (2006). TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312: 1520–1523.
27. Lu, Z., et al. (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.
28. Mashiguchi, K., Sasaki, E., Shimada, Y., Nagae, M., Ueno, K., Nakano, T., Yoneyama, K., Suzuki, Y., and Asami, T. (2009). Feedbackregulation of strigolactone biosynthetic genes and strigolactoneregulated genes in Arabidopsis. Biosci. Biotechnol. Biochem. 73: 2460–2465.
29. Nelson, D.C., Scaffidi, A., Dun, E.A., Waters, M.T., Flematti, G.R., Dixon, K.W., Beveridge, C.A., Ghisalberti, E.L., and Smith, S.M. (2011). F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 108: 8897–8902.
30. Pauwels, L., et al. (2010). NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788–791.
31. Ruyter-Spira, C., Al-Babili, S., van der Krol, S., and Bouwmeester, H. (2013). The biology of strigolactones. Trends Plant Sci. 18: 72–83.
32. Sang, D., et al. (2014). Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. USA 111: 11199–11204.
33. 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.
34. Scaffidi, A., Waters, M.T., Sun, Y.K., Skelton, B.W., Dixon, K.W., Ghisalberti, E.L., Flematti, G.R., and Smith, S.M. (2014). Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol. 165: 1221–1232.
35. Seto, Y., Sado, A., Asami, K., Hanada, A., Umehara, M., Akiyama, K., and Yamaguchi, S. (2014). Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc. Natl. Acad. Sci. USA 111: 1640–1645.
36. Shen, H., Luong, P., and Huq, E. (2007). The F-box protein MAX2 functions as a positive regulator of photomorphogenesis in Arabidopsis. Plant Physiol. 145: 1471–1483.
37. Smith, S.M., and Li, J. (2014). Signalling and responses to strigolactones and karrikins. Curr. Opin. Plant Biol. 21: 23–29.
38. Smith, S.M., and Waters, M.T. (2012). Strigolactones: destructiondependent perception? Curr. Biol. 22: R924–R927.
39. 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 dioxygenaselike genes that regulate shoot branching in Arabidopsis and pea. Genes Dev. 17: 1469–1474.
40. 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.
41. 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.
42. Stirnberg, P., van De Sande, K., and Leyser, H.M. (2002). MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129: 1131–1141.
43. Szemenyei, H., Hannon, M., and Long, J.A. (2008). TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319: 1384–1386.
44. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731–2739.
45. 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.
46. Waldie, T., McCulloch, H., and Leyser, O. (2014). Strigolactones and the control of plant development: lessons from shoot branching. Plant J. 79: 607–622.
47. Wang, Y., and Li, J. (2008). Molecular basis of plant architecture. Annu. Rev. Plant Biol. 59: 253–279.
48. 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.
49. Xie, X., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Annu. Rev. Phytopathol. 48: 93–117.
50. Xiong, G., Wang, Y., and Li, J. (2014). Action of strigolactones in plants. Enzymes 35: 57–84.
51. Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., Zhou, X., and Qi, Y. (2012). Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol. Cell 46: 859–870.
52. Yoo, S.D., Cho, Y.H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565–1572.
53. Zhang, Y., et al. (2014). Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 10: 1028–1033.
54. Zhao, J., Wang, T., Wang, M., Liu, Y., Yuan, S., Gao, Y., Yin, L., Sun, W., Peng, L., Zhang, W., Wan, J., and Li, X. (2014). DWARF3 participates in an SCF complex and associates with DWARF14 to suppress rice shoot branching. Plant Cell Physiol. 55: 1096–1109.
55. Zhao, L.H., 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.
56. Zhao, L.H., et al. (2015). Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3. Cell Res. 25: 1219–1236.
57. Zhou, F., et al. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504: 406–410.