The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity

Development (Cambridge)

Volumn 141, Issue 4, 2014, Pages 830-841

  Mandel, Tali ^a   Moreau, Fanny ^b   Kutsher, Yaarit ^a   Fletcher, Jennifer C ^c   Carles, Cristel C ^b   Williams, Leor Eshed ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b CNRS   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AGAMOUS (AG); Cell fate; WUSCHEL (WUS)

Indexed keywords

ERECTA RECEPTOR KINASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

APICAL MERISTEM; ARABIDOPSIS; ARTICLE; CARPEL; FRAMESHIFT MUTATION; GENE INTERACTION; HOMEOBOX; INFLORESCENCE; MISSENSE MUTATION; MULTIGENE FAMILY; NONHUMAN; PLANT DEVELOPMENT; PLURIPOTENT STEM CELL; POINT MUTATION; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; SHOOT APICAL MERISTEM; WILD TYPE;

AGAMOUS (AG); CELL FATE; WUSCHEL (WUS);

AGAMOUS PROTEIN, ARABIDOPSIS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; COMPUTATIONAL BIOLOGY; DNA PRIMERS; GENE EXPRESSION REGULATION, PLANT; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MERISTEM; MICROSCOPY, ELECTRON, SCANNING; MUTAGENESIS; PLANT SHOOTS; PLANTS, GENETICALLY MODIFIED; PLURIPOTENT STEM CELLS; PROTEIN-SERINE-THREONINE KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION;

EID: 84893300503     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.104687     Document Type: Article

References (82)

1. Alvarez-Buylla, E. R., Benitez, M., Corvera-Poire, A., Chaos Cador, A., de Folter, S., Gamboa de Buen, A., Garay-Arroyo, A., Garcia-Ponce, B., Jaimes-Miranda, F., Perez-Ruiz, R. V., et al. (2010). Flower development. Arabidopsis Book 8, e0127.
2. 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.
3. Becker, A. and Theissen, G. (2003). The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464-489.
4. Bemis, S. M., Lee, J. S., Shpak, E. D. and Torii, K. U. (2013). Regulation of floral patterning and organ identity by Arabidopsis ERECTA-family receptor kinase genes. J. Exp. Bot. [Epub ahead of print] doi:10.1093/jxb/ert270.
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. Berleth, T., Scarpella, E. and Prusinkiewicz, P. (2007). Towards the systems biology of auxin-transport-mediated patterning. Trends Plant Sci. 12, 151-159.
7. Bowman, J. L., Smyth, D. R. and Meyerowitz, E. M. (1989). Genes directing flower development in Arabidopsis. Plant Cell 1, 37-52.
8. Bowman, J. L., Smyth, D. R. and Meyerowitz, E. M. (2012). The ABC model of flower development: then and now. Development 139, 4095-4098.
9. Brand, U., Fletcher, J. C., Hobe, M., Meyerowitz, E. M. and Simon, R. (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289, 617-619.
10. Busch, M. A., Bomblies, K. and Weigel, D. (1999). Activation of a floral homeotic gene in Arabidopsis. Science 285, 585-587.
11. Carles, C. C. and Fletcher, J. C. (2003). Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci. 8, 394-401.
12. Carles, C. C., Lertpiriyapong, K., Reville, K. and Fletcher, J. C. (2004). The ULTRAPETALA1 gene functions early in Arabidopsis development to restrict shoot apical meristem activity and acts through WUSCHEL to regulate floral meristem determinacy. Genetics 167, 1893-1903.
13. Clark, S. E., Running, M. P. and Meyerowitz, E. M. (1993). CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119, 397-418.
14. Clark, S. E., Williams, R. W. and Meyerowitz, E. M. (1997). The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585.
15. 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.
16. Coen, E. S. and Meyerowitz, E. M. (1991). The war of the whorls: genetic interactions controlling flower development. Nature 353, 31-37.
17. Colombo, M., Brambilla, V., Marcheselli, R., Caporali, E., Kater, M. M. and Colombo, L. (2010). A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Dev. Biol. 337, 294-302.
18. DeYoung, B. J., Bickle, K. L., Schrage, K. J., Muskett, P., Patel, K. and Clark, S. E. (2006). The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 45, 1-16.
19. Diévart, A., Dalal, M., Tax, F. E., Lacey, A. D., Huttly, A., Li, J. and Clark, S. E. (2003). CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. Plant Cell15, 1198-1211.
20. Drews, G. N., Bowman, J. L. and Meyerowitz, E. M. (1991). Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65, 991-1002.
21. Durbak, A. R. and Tax, F. E. (2011). CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristems. Genetics 189, 177-194.
22. Efroni, I., Blum, E., Goldshmidt, A. and Eshed, Y. (2008). A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20, 2293-2306.
23. Fletcher, J. C. (2001). The ULTRAPETALA gene controls shoot and floral meristem size in Arabidopsis. Development 128, 1323-1333.
24. Furner, I. J. and Pumfrey, J. E. (1992). Cell fate in the shoot apical meristem of Arabidopsis-thaliana. Development 115, 755-764.
25. Giulini, A., Wang, J. and Jackson, D. (2004). Control of phyllotaxy by the cytokinininducible response regulator homologue ABPHYL1. Nature 430, 1031-1034.
26. Golz, J. F. and Hudson, A. (2002). Signalling in plant lateral organ development. Plant Cell 14 Suppl., S277-S288.
27. Gómez-Mena, C., de Folter, S., Costa, M. M., Angenent, G. C. and Sablowski, R. (2005). Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132, 429-438.
28. Goodrich, J., Puangsomlee, P., Martin, M., Long, D., Meyerowitz, E. M. and Coupland, G. (1997). A Polycomb-group gene regulates homeotic gene expression in Arabidopsis. Nature 386, 44-51.
29. Hall, M. C., Dworkin, I., Ungerer, M. C. and Purugganan, M. (2007). Genetics of microenvironmental canalization in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA104, 13717-13722.
30. 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.
31. Hong, R. L., Hamaguchi, L., Busch, M. A. and Weigel, D. (2003). Regulatory elements of the floral homeotic gene AGAMOUS identified by phylogenetic footprinting and shadowing. Plant Cell 15, 1296-1309.
32. Ito, T., Wellmer, F., Yu, H., Das, P., Ito, N., Alves-Ferreira, M., Riechmann, J. L. and Meyerowitz, E. M. (2004). The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430, 356-360.
33. Ito, T., Ng, K. H., Lim, T. S., Yu, H. and Meyerowitz, E. M. (2007). The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell 19, 3516-3529.
34. Jander, G., Baerson, S. R., Hudak, J. A., Gonzalez, K. A., Gruys, K. J. and Last, R. L. (2003). Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol. 131, 139-146.
35. Jönsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M. and Mjolsness, E. (2006). An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. USA 103, 1633-1638.
36. Kaya, H., Shibahara, K. I., Taoka, K. I., Iwabuchi, M., Stillman, B. and Araki, T. (2001). FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142.
37. Kirch, T., Simon, R., Grünewald, M. and Werr, W. (2003). The DORNROSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem ccll fate and lateral organ development. Plant Cell 15, 694-705.
38. Krizek, B. A. and Fletcher, J. C. (2005). Molecular mechanisms of flower development: an armchair guide. Nat. Rev. Genet. 6, 688-698.
39. Kwiatkowska, D. (2006). Flower primordium formation at the Arabidopsis shoot apex: quantitative analysis of surface geometry and growth. J. Exp. Bot. 57, 571-580.
40. Laufs, P., Dockx, J., Kronenberger, J. and Traas, J. (1998a). MGOUN1 and MGOUN2: two genes required for primordium initiation at the shoot apical and floral meristems in Arabidopsis thaliana. Development 125, 1253-1260.
41. Laufs, P., Grandjean, O., Jonak, C., Kiêu, K. and Traas, J. (1998b). Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 10, 1375-1390.
42. Laux, T., Mayer, K. F., Berger, J. and Jürgens, G. (1996). The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
43. Lease, K. A., Lau, N. Y., Schuster, R. A., Torii, K. U. and Walker, J. C. (2001). Receptor serine/threonine protein kinases in signalling: analysis of the erecta receptor-like kinase of Arabidopsis thaliana. New Phytolog, 151, 133-143.
44. Lenhard, M., Bohnert, A., Jürgens, G. and Laux, T. (2001). Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105, 805-814.
45. Leyser, H. M. O. and Furner, I. J. (1992). Characterisation of three shoot apical meristem mutants of Arabidopsis thaliana. Development 116, 397-403.
46. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) Method. Methods 25, 402-408.
47. Lohmann, D., Stacey, N., Breuninger, H., Jikumaru, Y., Müller, D., Sicard, A., Leyser, O., Yamaguchi, S. and Lenhard, M. (2010). SLOW MOTION is required for within-plant auxin homeostasis and normal timing of lateral organ initiation at the shoot meristem in Arabidopsis. Plant Cell 22, 335-348.
48. Long, J. A. and Barton, M. K. (1998). The development of apical embryonic pattern in Arabidopsis. Development 125, 3027-3035.
49. Long, J. A., Moan, E. I., Medford, J. I. and Barton, M. K. (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69.
50. Mallory, A. C., Bartel, D. P. and Bartel, B. (2005). MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17, 1360-1375.
51. Mayer, K. F., 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.
52. Medford, J. I., Behringer, F. J., Callos, J. D. and Feldmann, K. A. (1992). Normal and abnormal development in the arabidopsis vegetative shoot apex. Plant Cell 4, 631-643.
53. Mizukami, Y. and Ma, H. (1992). Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity. Cell 71, 119-131.
54. Mizukami, Y. and Ma, H. (1995). Separation of AG function in floral meristem determinacy from that in reproductive organ identity by expressing antisense AG RNA. Plant Mol. Biol. 28, 767-784.
55. Perales, M. and Reddy, G. V. (2012). Stem cell maintenance in shoot apical meristems. Curr. Opin. Plant Biol. 15, 10-16.
56. Pinyopich, A., Ditta, G. S., Savidge, B., Liljegren, S. J., Baumann, E., Wisman, E. and Yanofsky, M. F. (2003). Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature 424, 85-88.
57. 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.
58. Roeder, A. H. and Yanofsky, M. F. (2006). Fruit development in Arabidopsis. Arabidopsis Book 4, e0075.
59. Sablowski, R. (2004). Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol. 14, 605-611.
60. Schoof, H., Lenhard, M., Haecker, A., Mayer, K. F., Jürgens, G. and Laux, T. (2000). The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644.
61. Seidlová, F. (1980). The rate of cell-division in the shoot apical meristem during photoperiodic induction and transition to flowering. Biol. Plant. 22, 428-433.
62. Shpak, E. D., Lakeman, M. B. and Torii, K. U. (2003). Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA Leucine-rich repeat receptor-like kinase signaling pathway that regulates organ shape. Plant Cell 15, 1095-1110.
63. Shpak, E. D., Berthiaume, C. T., Hill, E. J. and Torii, K. U. (2004). Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131, 1491-1501.
64. Smith, R. S., Guyomarc'h, S., Mandel, T., Reinhardt, D., Kuhlemeier, C. and Prusinkiewicz, P. (2006). A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA 103, 1301-1306.
65. Smyth, D. R., Bowman, J. L. and Meyerowitz, E. M. (1990). Early flower development in Arabidopsis. Plant Cell 2, 755-767.
66. Sussex, I. (1998). Themes in plant development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, xiii-xxii.
67. Takahashi, T., Matsuhara, S., Abe, M. and Komeda, Y. (2002). Disruption of a DNA topoisomerase I gene affects morphogenesis in Arabidopsis. Plant Cell 14, 2085-2093.
68. Torii, K. U., Mitsukawa, N., Oosumi, T., Matsuura, Y., Yokoyama, R., Whittier, R. F. and Komeda, Y. (1996). The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8, 735-746.
69. Traas, J. (2013). Phyllotaxis. Development 140, 249-253.
70. Uchida, N., Igari, K., Bogenschutz, N. L., Torii, K. U. and Tasaka, M. (2011). Arabidopsis ERECTA-family receptor kinases mediate morphological alterations stimulated by activation of NB-LRR-type UNI proteins. Plant Cell Physiol. 52, 804-814.
71. Uchida, N., Shimada, M. and Tasaka, M. (2012). Modulation of the balance between stem cell proliferation and consumption by ERECTA-family genes. Plant Signal. Behav. 7, 1506-1508.
72. Uchida, N., Shimada, M. and Tasaka, M. (2013). ERECTA-family receptor kinases regulate stem cell homeostasis via buffering its cytokinin responsiveness in the shoot apical meristem. Plant Cell Physiol. 54, 343-351.
73. Vanneste, S. and Friml, J. (2009). Auxin: a trigger for change in plant development. Cell 136, 1005-1016.
74. Vidaurre, D. P., Ploense, S., Krogan, N. T. and Berleth, T. (2007). AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134, 2561-2567.
75. Vieten, A., Sauer, M., Brewer, P. B. and Friml, J. (2007). Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 12, 160-168.
76. Wahl, V., Brand, L. H., Guo, Y. L. and Schmid, M. (2010). The FANTASTIC FOUR proteins influence shoot meristem size in Arabidopsis thaliana. BMC Plant Biol. 10, 285.
77. Williams, L. and Fletcher, J. C. (2005). Stem cell regulation in the Arabidopsis shoot apical meristem. Curr. Opin. Plant Biol. 8, 582-586.
78. Williams, L., Grigg, S. P., Xie, M., Christensen, S. and Fletcher, J. C. (2005). Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132, 3657-3668.
79. Wu, X., Dabi, T. and Weigel, D. (2005). Requirement of homeobox gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance. Curr. Biol. 15, 436-440.
80. Würschum, T., Gross-Hardt, R. and Laux, T. (2006). APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18, 295-307.
81. Yanofsky, M. F., Ma, H., Bowman, J. L., Drews, G. N., Feldmann, K. A. and Meyerowitz, E. M. (1990). The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346, 35-39.
82. Yokoyama, R., Takahashi, T., Kato, A., Torii, K. U. and Komeda, Y. (1998). The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. Plant J. 15, 301-310.