Dynamics of strigolactone function and shoot branching responses in pisum sativum

Molecular Plant

Volumn 6, Issue 1, 2013, Pages 128-140

  Dun, Elizabeth A ^a   De Saint Germain, Alexandre ^b   Rameau, Catherine ^b   Beveridge, Christine A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b INSTITUT JEAN PIERRE BOURGIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PISUM SATIVUM;

GAMMA BUTYROLACTONE; GR24 COMPOUND; INDOLEACETIC ACID DERIVATIVE; LACTONE; VEGETABLE PROTEIN;

ANALOGS AND DERIVATIVES; BIOSYNTHESIS; DRUG EFFECTS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PEA; PLANT; PLANT GENE;

4-BUTYROLACTONE; BIOSYNTHETIC PATHWAYS; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; INDOLEACETIC ACIDS; LACTONES; PEAS; PLANT PROTEINS; PLANT SHOOTS;

EID: 84875750236     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1093/mp/sss131     Document Type: Article

References (78)

1. Aguilar-Martínez, J.A., Poza-Carrión, C., and Cubas, P. (2007). Arabidopsis Branched1 acts as an integrator of branching wignals within axillary buds. Plant Cell. 19, 458-472.
2. 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.
3. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 435, 824-827.
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 β-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., Sakakibara, H., and Kyozuka, J. (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., and Kyozuka, J. (2009). d14, a strigolactone insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol. 50, 1416-1424.
7. Bainbridge, K., Sorefan, K., Ward, S., and Leyser, O. (2005). Hormonally controlled expression of the Arabidopsis MAX4 shoot branching regulatory gene. Plant J. 44, 569-580.
8. Bangerth, F. (1994). Response of cytokinin concentration in the xylem exudate of bean (Phaseolus vulgaris L.) plants to decapitation and auxin treatment, and relationship to apical dominance. Planta. 194, 439-442.
9. Bennett, T., Sieberer, T., Willett, B., Booker, J., Luschnig, C., and Leyser, O. (2006). The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr. Biol. 16, 553-563.
10. Beveridge, C.A. (2000). Long-distance signalling and a mutational analysis of branching in pea. Plant Growth Regul. 32, 193-203.
11. Beveridge, C.A., and Kyozuka, J. (2010). New genes in the strigolactone- related shoot branching pathway. Curr. Opin. Plant Biol. 13, 34-39.
12. Beveridge, C.A., Dun, E.A., and Rameau, C. (2009). Pea has its tendrils in branching discoveries spanning a century from auxin to strigolactones. Plant Physiol. 151, 985-990.
13. Beveridge, C.A., Murfet, I.C., Kerhoas, L., Sotta, B., Miginiac, E., and Rameau, C. (1997a). The shoot controls zeatin riboside export from pea roots: evidence from the branching mutant rms4. Plant J. 11, 339-345.
14. Beveridge, C.A., Ross, J.J., and Murfet, I.C. (1996). Branching in pea: action of genes Rms3 and Rms4. Plant Physiol. 110, 859-865.
15. Beveridge, C.A., Symons, G.M., Murfet, I.C., Ross, J.J., and Rameau, C. (1997b). The rms1 mutant of pea has elevated indole-3-acetic acid levels and reduced rootsap zeatin riboside content but increased branching controlled by graft-transmissible signal(s). Plant Physiol. 115, 1251-1258.
16. 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.
17. Booker, J., Sieberer, T., Wright, W., Williamson, L., Willett, B., Stirnberg, P., Turnbull, C., Srinivasan, M., Goddard, P., and Leyser, O. (2005). MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev. Cell. 8, 443-449.
18. Braun, N., de Saint Germain, A., Pillot, J.-P., Xin, L., Dalmais, M., Le Signor, C., Bouteiller, N., Luo, D., Bendahmane, A., Turnbull, C., and Rameau, C. (2012). The pea TCP transcription factor PsBRC1 acts downstream of strigolactones to control shoot branching. Plant Physiol. 158, 225-238.
19. Brewer, P.B., Dun, E.A., Ferguson, B.J., Rameau, C., and Beveridge, C.A. (2009). Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol. 150, 482-493.
20. Brewer, P.B., Koltai, H., and Beveridge, C.A. (2013). Diverse roles of strigolactones in plant development. Mol. Plant. 6, 18-28.
21. Cook, C.E., Whichard, L.P., Wall, M.E., Egley, G.H., Coggon, P., Luhan, P.A., and McPhail, A.T. (1972). Germination stimulants. II. The structure of strigol-A potent seed germination stimulant for witchweed (Striga lutea Lour.). J. Am. Chem. Soc. 94, 6198-6199.
22. Crawford, S., Shinohara, N., Sieberer, T., Williamson, L., George, G., Hepworth, J., Müller, D., Domagalska, M.A., and Leyser, O. (2010). Strigolactones enhance competition between shoot branches by dampening auxin transport. Development. 137, 2905-2913.
23. Domagalska, M.A., and Leyser, O. (2011). Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Bio. 12, 211-221.
24. Drummond, R.S.M., Martínez-Sánchez, N.M., Janssen, B.J., Templeton, K.R., Simons, J.L., Quinn, B.D., Karunairetnam, S., and Snowden, K.C. (2009). Petunia hybrida carotenoid cleavage dioxygenase7 is involved in the production of negative and positive branching signals in petunia. Plant Physiol. 151, 1867-1877.
25. Dun, E.A., Brewer, P.B., and Beveridge, C.A. (2009a). Strigolactones: discovery of the elusive shoot branching hormone. Trends Plant Sci. 14, 364-372.
26. Dun, E.A., de Saint Germain, A., Rameau, C., and Beveridge, C.A. (2012). Antagonistic action of strigolactone and cytokinin in bud outgrowth control. Plant Physiol. 158, 487-498.
27. Dun, E.A., Hanan, J., and Beveridge, C.A. (2009b). Computational modeling and molecular physiology experiments reveal new insights into shoot branching in pea. Plant Cell. 21, 3459-3472.
28. Ferguson, B.J., and Beveridge, C.A. (2009). Roles for auxin, cytokinin, and strigolactone in regulating shoot branching. Plant Physiol. 149, 1929-1944.
29. Finlayson, S.A. (2007). Arabidopsis teosinte branched1-like 1 regulates axillary bud outgrowth and is homologous to monocot teosinte Branched1. Plant Cell Physiol. 48, 667-677.
30. Finlayson, S.A., Krishnareddy, S.R., Kebrom, T.H., and Casal, J.J. (2010). Phytochrome regulation of branching in Arabidopsis. Plant Physiol. 152, 1914-1927.
31. Foo, E., and Davies, N.W. (2011). Strigolactones promote nodulation in pea. Planta. 234, 1073-1081.
32. 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.
33. Foo, E., Morris, S.E., Parmenter, K., Young, N., Wang, H., Jones, A., Rameau, C., Turnbull, C.G.N., and Beveridge, C.A. (2007). Feedback regulation of xylem cytokinin content is conserved in pea and Arabidopsis. Plant Physiol. 143, 1418-1428.
34. 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.
35. 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., et al. (2008). Strigolactone inhibition of shoot branching. Nature. 455, 189-194.
36. 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 α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr. Biol. 22, 2032-2036.
37. Hayward, A., Stirnberg, P., Beveridge, C., and Leyser, O. (2009). Interactions between auxin and strigolactone in shoot branching control. Plant Physiol. 151, 400-412.
38. 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.
39. 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.
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., et al. (2011). Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta. 223, 209-216.
41. 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.
42. Koltai, H., LekKala, S.P., Bhattacharya, C., Mayzlish-Gati, E., Resnick, N., Wininger, S., Dor, E., Yoneyama, K., Yoneyama, K., Hershenhorn, J., et al. (2010). A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J. Exp. Bot. 61, 1739-1749.
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.
44. Leyser, O. (2009). The control of shoot branching: an example of plant information processing. Plant Cell Environ. 32, 694-703.
45. Liang, J., Zhao, L., Challis, R., and Leyser, O. (2010). Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum) J. Exp. Bot. 61, 3069-3078.
46. Lin, H., Wang, R.X., Qian, Q., Yan, M.X., Meng, X.B., Fu, Z.M., Yan, C.Y., Jiang, B., Su, Z., Li, J., et al. (2009). DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell. 21, 1512-1525.
47. 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.
48. Mashiguchi, K., Sasaki, E., Shimada, Y., Nagae, M., Ueno, K., Nakano, T., Yoneyama, K., Suzuki, Y., and Asami, T. (2009). Feedback-regulation of strigolactone biosynthetic genes and strigolactone-related genes in Arabidopsis. Biosci. Biotechnol. Biochem. 73, 2460-2465.
49. Mayzlish-Gati, E., LekKala, S.P., Resnick, N., Wininger, S., Bhattacharya, C., Lemcoff, J.H., Kapulnik, Y., and Koltai, H. (2010). Strigolactones are positive regulators of light-harvesting genes in tomato. J. Exp. Bot. 61, 3129-3136.
50. Morris, S.E., Cox, M.C.H., Ross, J.J., Krisantini, S., and Beveridge, C.A. (2005). Auxin dynamics after decapitation are not correlated with the initial growth of axillary buds. Plant Physiol. 138, 1665-1672.
51. Morris, S.E., Turnbull, C.G., Murfet, I.C., and Beveridge, C.A. (2001). Mutational analysis of branching in pea: evidence that Rms1 and Rms5 regulate the same novel signal. Plant Physiol. 126, 1205-1213.
52. Napoli, C.A. (1996). Highly branched phenotype of the petunia dad1-1 mutant is reversed by grafting. Plant Physiol. 111, 27-37.
53. 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. U S A. 108, 8897-8902.
54. Nordström, A., Tarkowski, P., Tarkowski, D., Norbaek, R., Åstot, C., Dolezal, K., and Sandberg, G. (2004). Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. Proc. Natl Acad. Sci. U S A. 101, 8039-8044.
55. Ongaro, V., Bainbridge, K., Williamson, L., and Leyser, O. (2008). Interactions between axillary branches of Arabidopsis. Mol. Plant. 1, 388-400.
56. Ozga, J.A., Yu, J., and Reinecke, D.M. (2003). Pollination-, development-, and auxin-specific regulation of gibberellin 3β-hydroxylase gene expression in pea fruit and seeds. Plant Physiol. 131, 1137-1146.
57. Prusinkiewicz, P., Crawford, S., Smith, R.S., Ljung, K., Bennett, T., Ongaro, V., and Leyser. O. (2009). Control of bud activation by an auxin transport switch. Proc. Natl Acad. Sci. U S A. 106, 17431-17436.
58. Rasmussen, A., Mason, M., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D.N.V., Greb, T., Goormachtig, S., Beeckman, T., and et al. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol. 158, 1976-1987.
59. Renton, M., Hanan, J., Ferguson, B.J., and Beveridge, C.A. (2012). Models of long-distance transport: how is carrier-dependent auxin transport regulated in the stem? New Phytol. 194, 704-715.
60. 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.
61. Sachs, T., and Thimann, K.V. (1967). The role of auxins and cytokinins in the release of buds from dominance. Am. J. Bot. 54, 136-144.
62. 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.
63. Shimizu-Sato, S., Tanaka, M., and Mori, H. (2009). Auxin-cytokinin interactions in the control of shoot branching. Plant Mol. Biol. 69, 429-435.
64. Snow, R. (1929). The transmission of inhibition through dead stretches of stem. Ann. Bot. 43, 261-267.
65. Snow, R. (1931). Experiments on growth and inhibition. Part I. New phenomena of inhibition. Proc. R. Soc. Lond. B Biol. Sci. 108, 305-316.
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.
67. 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.
68. Stirnberg, P., Furner, I.J., and Leyser, H.M.O. (2007). MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 50, 80-94.
69. Stirnberg, P., van de Sande, K., and Leyser, H.M.O. (2002). MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development. 129, 1131-1141.
70. Tanaka, M., Takei, K., Kojima, M., Sakakibara, H., and Mori, H. (2006). Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. Plant J. 45, 1028-1036.
71. Thimann, K.V., and Skoog, F. (1933). Studies on the growth hormone of plants. III. The inhibiting action of the growth substance on bud development. Proc. Natl Acad. Sci. U S A. 19, 714-716.
72. Thimann, K.V., and Skoog, F. (1934). On the inhibition of bud development and other functions of growth substance in Vicia faba. Proc. R. Soc. Lond. B Biol. Sci. 114, 317-339.
73. Turnbull, C.G.N., Booker, J.P., and Leyser, H.M.O. (2002). Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J. 32, 255-262.
74. 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.
75. Werner, T., Köllmer, I., Bartrina, I., Holst, K., and Schmülling, T. (2006). New insights into the biology of cytokinin degradation. Plant Biol. 8, 371-381.
76. Woo, H.E., Chung, K.M., Park, J., Oh, S.A., Ahn, T., Hong, S.H., Jang, S.K., and Nam, H.G. (2001). ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell. 13, 1779-1790.
77. Yan, H., Saika, H., Maekawa, M., Takamure, I., Tsutsumi, N., Kyozuka J., and Nakazono, M. (2007) Rice tillering dwarf mutant dwarf3 has increased lead longevity during darknessinduced senescence or hydrogen peroxide-induced cell death. Genes Genet. Syst. 82, 361-366.
78. Zou, J., Zhang, S., Zhang, W., Li, G., Chen, Z., Zhai, W., Zhao, X., Pan, X., Xie, Q., and Zhu, L. (2006). The rice high-tillering dwarf1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J. 48, 687-696.