Auxin depletion from the leaf axil conditions competence for axillary meristem formation in Arabidopsis and tomato

Plant Cell

Volumn 26, Issue 5, 2014, Pages 2068-2079

  Wang, Quan ^a   Kohlen, Wouter ^a   Rossmann, Susanne ^a   Vernoux, Teva ^b   Theres, Klaus ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903587031     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.123059     Document Type: Article

References (62)

1. Aida, M., Ishida, T., Fukaki, H., Fujisawa, H., and Tasaka, M. (1997). Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9: 841-857.
2. Aida, M., Ishida, T., and Tasaka, M. (1999). Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development 126: 1563-1570.
3. Bainbridge, K., Guyomarc'h, S., Bayer, E., Swarup, R., Bennett, M., Mandel, T., and Kuhlemeier, C. (2008). Auxin influx carriers stabilize phyllotactic patterning. Genes Dev. 22: 810-823.
4. Bayer, E.M., Smith, R.S., Mandel, T., Nakayama, N., Sauer, M., Prusinkiewicz, P., and Kuhlemeier, C. (2009). Integration of transportbased models for phyllotaxis and midvein formation. Genes Dev. 23: 373-384.
5. Benková, E., Michniewicz, M., Sauer, M., Teichmann, T., Seifertová, D., Jürgens, G., and Friml, J. (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115: 591-602.
6. Bennett, S.R.M., Alvarez, J., Bossinger, G., and Smyth, D.R. (1995). Morphogenesis in pinoid mutants of Arabidopsis thaliana. Plant J. 8: 505-520.
7. Brunoud, G., Wells, D.M., Oliva, M., Larrieu, A., Mirabet, V., Burrow, A.H., Beeckman, T., Kepinski, S., Traas, J., Bennett, M.J., and Vernoux, T. (2012). A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482: 103-106.
8. Busch, B.L., Schmitz, G., Rossmann, S., Piron, F., Ding, J., Bendahmane, A., and Theres, K. (2011). Shoot branching and leaf dissection in tomato are regulated by homologous gene modules. Plant Cell 23: 3595-3609.
9. Christensen, S.K., Dagenais, N., Chory, J., and Weigel, D. (2000). Regulation of auxin response by the protein kinase PINOID. Cell 100: 469-478.
10. 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.
11. Coen, E.S., Romero, J.M., Doyle, S., Elliott, R., Murphy, G., and Carpenter, R. (1990). floricaula: a homeotic gene required for flower development in antirrhinum majus. Cell 63: 1311-1322.
12. Dharmasiri, N., Dharmasiri, S., and Estelle, M. (2005). The F-box protein TIR1 is an auxin receptor. Nature 435: 441-445.
13. Evans, M.W., and Grover, F.O. (1940). Developmental morphology of the growing point of the shoot and the inflorescence in grasses. J. Agric. Res. 61: 481-520.
14. Friml, J., et al. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306: 862-865.
15. Furutani, M., Vernoux, T., Traas, J., Kato, T., Tasaka, M., and Aida, M. (2004). PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development 131: 5021-5030.
16. Gallavotti, A., Yang, Y., Schmidt, R.J., and Jackson, D. (2008). The Relationship between auxin transport and maize branching. Plant Physiol. 147: 1913-1923.
17. Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226-2230.
18. Gomez-Roldan, V., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455: 189-194.
19. Grbić, V., and Bleecker, A.B. (2000). Axillary meristem development in Arabidopsis thaliana. Plant J. 21: 215-223.
20. Greb, T., Clarenz, O., Schäfer, E., Müller, D., Herrero, R., Schmitz, G., and Theres, K. (2003). Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev. 17: 1175-1187.
21. Hamann, T., Benkova, E., Bäurle, I., Kientz, M., and Jürgens, G. (2002). The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16: 1610-1615.
22. Hardtke, C.S., and Berleth, T. (1998). The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J. 17: 1405-1411.
23. Heisler, M.G., Ohno, C., Das, P., Sieber, P., Reddy, G.V., Long, J.A., and Meyerowitz, E.M. (2005). Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15: 1899-1911.
24. Hempel, F., and Feldman, L. (1994). Bi-directional inflorescence development in Arabidopsis thaliana: Acropetal initiation of flowers and basipetal initiation of paraclades. Planta 192: 276-286.
25. Hibara, K., Karim, M.R., Takada, S., Taoka, K., Furutani, M., Aida, M., and Tasaka, M. (2006). Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18: 2946-2957.
26. Kepinski, S., and Leyser, O. (2005). The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435: 446-451.
27. Koenig, D., Bayer, E., Kang, J., Kuhlemeier, C., and Sinha, N. (2009). Auxin patterns Solanum lycopersicum leaf morphogenesis. Development 136: 2997-3006.
28. Laux, T., and Jurgens, G. (1997). Embryogenesis: a new start in life. Plant Cell 9: 989-1000.
29. Leyser, H.M.O., Lincoln, C.A., Timpte, C., Lammer, D., Turner, J., and Estelle, M. (1993). Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364: 161-164.
30. Li, X., et al. (2003). Control of tillering in rice. Nature 422: 618-621.
31. Lincoln, C., Britton, J.H., and Estelle, M. (1990). Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2: 1071-1080.
32. Long, J., and Barton, M.K. (2000). Initiation of axillary and floral meristems in Arabidopsis. Dev. Biol. 218: 341-353.
33. Mayer, K.F.X., Schoof, H., Haecker, A., Lenhard, M., Jürgens, G., and Laux, T. (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
34. McSteen, P., and Hake, S. (2001). barren inflorescence2 regulates axillary meristem development in the maize inflorescence. Development 128: 2881-2891.
35. McSteen, P., Malcomber, S., Skirpan, A., Lunde, C., Wu, X., Kellogg, E., and Hake, S. (2007). barren inflorescence2 Encodes a co-ortholog of the PINOID serine/threonine kinase and is required for organogenesis during inflorescence and vegetative development in maize. Plant Physiol. 144: 1000-1011.
36. Michniewicz, M., et al. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130: 1044-1056.
37. Müller, D., Schmitz, G., and Theres, K. (2006). Blind homologous R2R3 Myb genes control the pattern of lateral meristem initiation in Arabidopsis. Plant Cell 18: 586-597.
38. Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677-684.
39. Paciorek, T., Sauer, M., Balla, J., Wiśniewska, J., and Friml, J. (2006). Immunocytochemical technique for protein localization in sections of plant tissues. Nat. Protoc. 1: 104-107.
40. Raman, S., Greb, T., Peaucelle, A., Blein, T., Laufs, P., and Theres, K. (2008). Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J. 55: 65-76.
41. Rast, M.I., and Simon, R. (2008). The meristem-to-organ boundary: more than an extremity of anything. Curr. Opin. Genet. Dev. 18: 287-294.
42. Reinhardt, D., Pesce, E.R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.
43. 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.
44. Schmitz, G., and Theres, K. (2005). Shoot and inflorescence branching. Curr. Opin. Plant Biol. 8: 506-511.
45. Schulze, S., Schäfer, B.N., Parizotto, E.A., Voinnet, O., and Theres, K. (2010). LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. Plant J. 64: 668-678.
46. Schumacher, K., Schmitt, T., Rossberg, M., Schmitz, G., and Theres, K. (1999). The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc. Natl. Acad. Sci. USA 96: 290-295.
47. Shani, E., Ben-Gera, H., Shleizer-Burko, S., Burko, Y., Weiss, D., and Ori, N. (2010). Cytokinin regulates compound leaf development in tomato. Plant Cell 22: 3206-3217.
48. Sorefan, K., Girin, T., Liljegren, S.J., Ljung, K., Robles, P., Galván-Ampudia, C.S., Offringa, R., Friml, J., Yanofsky, M.F., and Østergaard, L. (2009). A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583-586.
49. Stirnberg, P., Chatfield, S.P., and Leyser, H.M. (1999). AXR1 acts after lateral bud formation to inhibit lateral bud growth in Arabidopsis. Plant Physiol. 121: 839-847.
50. 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.
51. Takada, S., Hibara, K., Ishida, T., and Tasaka, M. (2001). The CUPSHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development 128: 1127-1135.
52. 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.
53. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/ IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
54. 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.
55. Vernoux, T., Besnard, F., and Traas, J. (2010). Auxin at the shoot apical meristem. Cold Spring Harb. Perspect. Biol. 2: a001487.
56. Vernoux, T., et al. (2011). The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7: 508.
57. Vroemen, C.W., Mordhorst, A.P., Albrecht, C., Kwaaitaal, M.A.C.J., and de Vries, S.C. (2003). The CUP-SHAPED COTYLEDON3 gene is required for boundary and shoot meristem formation in Arabidopsis. Plant Cell 15: 1563-1577.
58. Wardlaw, C.W. (1943). Experimental and analytical studies of Pteridophytes. I. Preliminary observations on the development of buds on the rhizome of the ostrich fern (Matteuccia struthiopteris Tod.). Ann. Bot. (Lond.) 26: 171-187.
59. Weijers, D., and Friml, J. (2009). SnapShot: auxin signaling and transport. Cell 136: 1172-1172.
60. Wu, X., and McSteen, P. (2007). The role of auxin transport during inflorescence development in maize (Zea mays, Poaceae). Am. J. Bot. 94: 1745-1755.
61. Yamada, T., Palm, C.J., Brooks, B., and Kosuge, T. (1985). Nucleotide sequences of the Pseudomonas savastanoi indoleacetic acid genes show homology with Agrobacterium tumefaciens T-DNA. Proc. Natl. Acad. Sci. USA 82: 6522-6526.
62. Yang, F., Wang, Q., Schmitz, G., Müller, D., and Theres, K. (2012). The bHLH protein ROX acts in concert with RAX1 and LAS to modulate axillary meristem formation in Arabidopsis. Plant J. 71: 61-70.