O Cell, Where Art Thou? The mechanisms of shoot meristem patterning

Current Opinion in Plant Biology

Volumn 23, Issue , 2015, Pages 91-97

  Gaillochet, Christophe ^a   Daum, Gabor ^a   Lohmann, Jan U ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CYTOLOGY; EMBRYOLOGY; MERISTEM; METABOLISM; MORPHOGENESIS; ORGANOGENESIS; PLANT CELL; STEM CELL;

BODY PATTERNING; CELL PROLIFERATION; MERISTEM; ORGANOGENESIS; PLANT CELLS; STEM CELLS;

EID: 84912055238     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2014.11.002     Document Type: Review

References (53)

1. Laux T., Mayer K.F., Berger J., Jurgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 1995, 122:87-96.
2. Mayer K.F., Schoof H., Haecker A., Lenhard M., Jurgens G., Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 1998, 95:805-815.
3. Fletcher J.C., Brand U., Running M.P., Simon R., Meyerowitz E.M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 1999, 283:1911-1914.
4. Reinhardt D., Frenz M., Mandel T., Kuhlemeier C. Microsurgical and laser ablation analysis of interactions between the zones and layers of the tomato shoot apical meristem. Development 2003, 130:4073-4083.
5. Gallois J-L., Nora F.R., Mizukami Y., Sablowski R. WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Genes Dev 2004, 18:375-380.
6. Yanai O., Shani E., Dolezal K., Tarkowski P., Sablowski R., Sandberg G., Samach A., Ori N. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr Biol 2005, 15:1566-1571.
7. Jasinski S., Piazza P., Craft J., Hay A., Woolley L., Rieu I., Phillips A., Hedden P., Tsiantis M. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 2005, 15:1560-1565.
8. Clark S.E., Running M.P., Meyerowitz E.M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 1993, 119:397-418.
9. Gordon S.P., Chickarmane V.S., Ohno C., Meyerowitz E.M. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. Proc Natl Acad Sci U S A 2009, 106:16529-16534.
10. Kuroha T., Tokunaga H., Kojima M., Ueda N., Ishida T., Nagawa S., Fukuda H., Sugimoto K., Sakakibara H. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 2009, 21:3152-3169.
11. Chickarmane V.S., Gordon S.P., Tarr P.T., Heisler M.G., Meyerowitz E.M. Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. Proc Natl Acad Sci U S A 2012, 109:4002-4007.
12. Leibfried A., To J.P.C., Busch W., Stehling S., Kehle A., Demar M., Kieber J.J., Lohmann J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 2005, 438:1172-1175.
13. Yadav R.K., Perales M., Gruel J., Girke T., Jönsson H., Reddy G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 2011, 25:2025-2030.
14. Daum G., Medzihradszky A., Suzaki T., Lohmann J.U. A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. Proc Natl Acad Sci U S A 2014, 111:14619-14624.
15. Brand U., Fletcher J.C., Hobe M., Meyerowitz E.M., Simon R. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 2000, 289:617-619.
16. Jeong S., Trotochaud A.E., Clark S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell 1999, 11:1925-1934.
17. Müller R., Bleckmann A., Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell 2008, 20:934-946.
18. Schoof H., Lenhard M., Haecker A., Mayer K.F., Jurgens G., Laux T. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100:635-644.
19. Bommert P., Je B.I., Goldshmidt A., Jackson D. The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size. Nature 2013, 502:555-558.
20. Knauer S., Holt A.L., Rubio-Somoza I., Tucker E.J., Hinze A., Pisch M., Javelle M., Timmermans M.C., Tucker M.R., Laux T. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 2013, 24:125-132.
21. Lucas W.J., Bouché-Pillon S., Jackson D.P., Nguyen L., Baker L., Ding B., Hake S. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 1995, 270:1980-1983.
22. Xu X.M., Wang J., Xuan Z., Goldshmidt A., Borrill P.G.M., Hariharan N., Kim J.Y., Jackson D. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 2011, 333:1141-1144.
23. Koizumi K., Wu S., MacRae-Crerar A., Gallagher K.L. An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 2011, 21:1559-1564.
24. Wu S., Gallagher K.L. Intact microtubules are required for the intercellular movement of the SHORT-ROOT transcription factor. Plant J 2013, 74:148-159.
25. Laufs P., Grandjean O., Jonak C., Kiêu K., Traas J. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell 1998, 10:1375-1390.
26. Reddy G.V., Heisler M.G., Ehrhardt D.W., Meyerowitz E.M. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 2004, 131:4225-4237.
27. Reddy G.V., Meyerowitz E.M. Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 2005, 310:663-667.
28. Yadav R.K., Tavakkoli M., Reddy G.V. WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors. Development 2010, 137:3581-3589.
29. Yadav R.K., Perales M., Gruel J., Ohno C., Heisler M., Girke T., Jönsson H., Reddy G.V. Plant stem cell maintenance involves direct transcriptional repression of differentiation program. Mol Syst Biol 2013, 9:1-13.
30. Busch W., Miotk A., Ariel F.D., Zhao Z., Forner J., Daum G., Suzaki T., Schuster C., Schultheiss S.J., Leibfried A., et al. Transcriptional control of a plant stem cell niche. Dev Cell 2010, 18:849-861.
31. Schuster C., Gaillochet C., Medzihradszky A., Busch W., Daum G., Krebs M., Kehle A., Lohmann J.U. A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals. Dev Cell 2014, 28:438-449.
32. Traas J. Phyllotaxis. Development 2013, 140:249-253.
33. Petrasek J., Friml J. Auxin transport routes in plant development. Development 2009, 136:2675-2688.
34. Reinhardt D., Pesce E.-R., Stieger P., Mandel T., Baltensperger K., Bennett M., Traas J., Friml J., Kuhlemeier C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426:255-260.
35. Heisler M.G., Ohno C., Das P., Sieber P., Reddy G.V., Long J.A., Meyerowitz E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol 2005, 15:1899-1911.
36. Smith R.S., Guyomarc'h S., Mandel T., Reinhardt D., Kuhlemeier C., Prusinkiewicz P. A plausible model of phyllotaxis. Proc Natl Acad Sci U S A 2006, 103:1301-1306.
37. Jönsson H., Heisler M.G., Shapiro B.E., Meyerowitz E.M., Mjolsness E. An auxin-driven polarized transport model for phyllotaxis. Proc Natl Acad Sci U S A 2006, 103:1633-1638.
38. de Reuille P.B., Bohn-Courseau I., Ljung K., Morin H., Carraro N., Godin C., Traas J. Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proc Natl Acad Sci U S A 2006, 103:1627-1632.
39. Gray W.M., Kepinski S., Rouse D., Leyser O., Estelle M. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature 2001, 414:271-276.
40. Vernoux T., Brunoud G.E.R., Farcot E., Morin V., Van den Daele H., Legrand J., Oliva M., Das P., Larrieu A., Wells D., et al. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 2011, 7:1-15.
41. Hardtke C.S., Berleth T. The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 1998, 17:1405-1411.
42. Vernoux T., Kronenberger J., Grandjean O., Laufs P., Traas J. PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. Development 2000, 127:5157-5165.
43. Besnard F., Refahi Y., Morin V., Marteaux B., Brunoud G., Chambrier P., Rozier F., Mirabet V., Legrand J., Lainé S., et al. Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 2014, 505:417-421.
44. Zhao Z., Andersen S.U., Ljung K., Dolezal K., Miotk A., Schultheiss S.J., Lohmann J.U. Hormonal control of the shoot stem-cell niche. Nature 2010, 465:1089-1092.
45. Yamaguchi N., Wu M.-F., Winter C.M., Berns M.C., Nole-Wilson S., Yamaguchi A., Coupland G., Krizek B.A., Wagner D. A molecular framework for auxin-mediated initiation of flower primordia. Dev Cell 2013, 24:271-282.
46. Yamaguchi N., Winter C.M., Wu M.F., Kanno Y., Yamaguchi A., Seo M., Wagner D. Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 2014, 344:638-641.
47. Weigel D., Alvarez J., Smyth D.R., Yanofsky M.F., Meyerowitz E.M. LEAFY controls floral meristem identity in Arabidopsis. Cell 1992, 69:843-859.
48. Elliott R.C., Betzner A.S., Huttner E., Oakes M.P., Tucker W.Q., Gerentes D., Perez P., Smyth D.R. AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 1996, 8:155-168.
49. Li W., Zhou Y., Liu X., Yu P., Cohen J.D., Meyerowitz E.M. LEAFY controls auxin response pathways in floral primordium formation. Sci Signal 2013, 6:ra23.
50. Breuil-Broyer S., Morel P., de Almeida-Engler J., Coustham V., Negrutiu I., Trehin C. High-resolution boundary analysis during Arabidopsis thaliana flower development. Plant J 2004, 38:182-192.
51. Gendron J.M., Liu J.-S., Fan M., Bai M.-Y., Wenkel S., Springer P.S., Barton M.K., Wang Z.-Y. Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc Natl Acad Sci U S A 2012, 109:21152-21157.
52. Bell E.M., Lin W.-C., Husbands A.Y., Yu L., Jaganatha V., Jablonska B., Mangeon A., Neff M.M., Girke T., Springer P.S. Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci U S A 2012, 109:21146-21151.
53. Yadav R.K., Tavakkoli M., Xie M., Girke T., Reddy G.V. A high-resolution gene expression map of the Arabidopsis shoot meristem stem cell niche. Development 2014, 141:2735-2744.