Plant and animal stem cells: Similar yet different

Nature Reviews Molecular Cell Biology

Volumn 15, Issue 5, 2014, Pages 301-312

  Heidstra, Renze ^a   Sabatini, Sabrina ^b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DAUGHTER CELL; EMBRYO DEVELOPMENT; HUMAN; MERISTEM; NONHUMAN; PLANT; PLANT REGENERATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROGENY; REVIEW;

ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MERISTEM; PLANT CELLS; PLURIPOTENT STEM CELLS; REGENERATION; SIGNAL TRANSDUCTION; STEM CELL NICHE; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 84899494165     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3790     Document Type: Review

References (179)

1. Laux, T. The stem cell concept in plants: a matter of debate. Cell 113, 281-283 (2003).
2. Sablowski, R. Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol. 14, 605-611 (2004).
3. Scheres, B. Stem-cell niches: nursery rhymes across kingdoms. Nature Rev. Mol. Cell Biol. 8, 345-354 (2007).
4. Barker, N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nature Rev. Mol. Cell Biol. 15, 19-33 (2014).
5. Spradling, A., Drummond-Barbosa, D. & Kai, T. Stem cells find their niche. Nature 414, 98-104 (2001).
6. Satina, S., Blakeslee, A. F. & Avery, A. G. Demonstration of the three germ layers in the shoot apex of datura by means of induced polyploidy in periclinal chimeras. Am. J. Bot. 27, 895-905 (1940).
7. Meyerowitz, E. M. Genetic control of cell division patterns in developing plants. Cell 88, 299-308 (1997).
8. van den Berg, C., Willemsen, V., Hage, W., Weisbeek, P. & Scheres, B. Cell fate in the Arabidopsis root meristem determined by directional signalling. Nature 378, 62-65 (1995).
9. van den Berg, C., Willemsen, V., Hendriks, G., Weisbeek, P. & Scheres, B. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390, 287-289 (1997).
10. Papagiannouli, F. & Lohmann, I. Shaping the niche: Lessons from the Drosophila testis and other model systems. Biotechnol. J. 7, 723-736 (2012).
11. Sage, J. The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 26, 1409-1420 (2012).
12. Gutzat, R., Borghi, L. & Gruissem, W. Emerging roles of RETINOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci. 17, 139-148 (2012).
13. Wildwater, M. et al. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337-1349 (2005).
14. Wyrzykowska, J., Schorderet, M., Pien, S., Gruissem, W. & Fleming, A. J. Induction of differentiation in the shoot apical meristem by transient overexpression of a retinoblastoma-related protein. Plant Physiol. 141, 1338-1348 (2006).
15. Borghi, L. et al. Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22, 1792-1811 (2010).
16. Laux, T., Mayer, K. F., Berger, J. & Jurgens, G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96 (1996).
17. Mayer, K. F. X. et al. Role of WUSCHEL in Regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95, 805-815 (1998).
18. Brand, U., Grunewald, M., Hobe, M. & Simon, R. Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiol. 129, 565-575 (2002).
19. Lenhard, M., Jürgens, G. & Laux, T. The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129, 3195-3206 (2002).
20. Schoof, H. et al. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100, 635-644 (2000).
21. 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 137, 3581-3589 (2010).
22. Yadav, R. K. et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25, 2025-2030 (2011).
23. Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 119, 397-418 (1993).
24. Clark, S. E., Running, M. P. & Meyerowitz, E. M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121, 2057-2067 (1995).
25. Kayes, J. M. & Clark, S. E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125, 3843-3851 (1998).
26. 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 289, 617-619 (2000).
27. Lenhard, M. & Laux, T. Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development 130, 3163-3173 (2003).
28. 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 283, 1911-1914 (1999).
29. Ito, Y., Nakanomyo, I., Motose, H., Iwamoto, K. & Sawa, S. Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842-845 (2006).
30. Ohyama, K., Shinohara, H., Ogawa-Ohnishi, M. & Matsubayashi, Y. A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nature Chem. Biol. 5, 578-580 (2009).
31. Ni, J. & Clark, S. E. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol. 140, 726-733 (2006).
32. Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294 (2008).
33. Guo, Y., Han, L., Hymes, M., Denver, R. & Clark, S. E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 63, 889-890 (2010).
34. Kinoshita, A., Betsuyaku, S., Osakabe, Y., Mizuno, S. & Nagawa, S. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911-3920 (2010).
35. Nimchuk, Z. L., Tarr, P. T. & Meyerowitz, E. M. An evolutionarily conserved pseudokinase mediates stem cell production in plants. Plant Cell 23, 851-854 (2011).
36. Müller, R., Bleckmann, A. & Simon, R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell Online 20, 934-946 (2008).
37. Clark, S. E., Williams, R. W. & Meyerowitz, E. M. The CLAVATA1Gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 89, 575-585 (1997).
38. Song, S.-K., Lee, M. M. & Clark, S. E. POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells. Development 133, 4691-4698 (2006).
39. Yadav, R. K. et al. Plant stem cell maintenance involves direct transcriptional repression of differentiation program. Mol. Syst. Biol. http://dx.doi.org/10.1038/msb.2013.8 (2013).
40. Busch, W., Miotk, A., Ariel, F. D., Zhao, Z. & Forner, J. Transcriptional control of a plant stem cell niche. Dev. Cell 18, 849-861 (2010).
41. Yadav, R. K., Girke, T., Pasala, S., Xie, M. & Reddy, G. V. Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl Acad. Sci. USA 106, 4941-4946 (2009).
42. Lohmann, J. U. et al. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793-803 (2001).
43. Muller, R., Borghi, L., Kwiatkowska, D., Laufs, P. & Simon, R. Dynamic and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signaling. Plant Cell 18, 1188-1198 (2006).
44. 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. USA 106, 16529-16534 (2009).
45. Uchida, N., Shimada, M. & Tasaka, M. ERECTA-Family receptor kinases regulate stem cell homeostasis via buffering its cytokinin responsiveness in the shoot apical meristem. Plant Cell Physiol. 54, 343-351 (2013).
46. 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. 109, 4002-4007 (2012).
47. Schuster, C. et al. A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals. Dev. Cell 28, 438-449 (2014).
48. Sarkar, A., Luijten, M., Miyashima, S., Lenhard, M. & Hashimoto, T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446, 811-814 (2007).
49. Stahl, Y., Wink, R. H., Ingram, G. C. & Simon, R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909-914 (2009).
50. Stahl, Y. et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23, 362-371 (2013).
51. De Smet, I., Vassileva, V., De Rybel, B., Levesque, M. P. & Grunewald, W. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322, 594-597 (2008).
52. Stahl, Y. & Simon, R. Gated communities: apoplastic and symplastic signals converge at plasmodesmata to control cell fates. J. Exp. Bot. 64, 5237-5241 (2013).
53. Hobe, M., Muller, R., Grunewald, M., Brand, U. & Simon, R. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol. 213, 371-381 (2003).
54. Hsu, Y. C. & Fuchs, E. A family business: stem cell progeny join the niche to regulate homeostasis. Nature Rev. Mol. Cell Biol. 13, 103-114 (2012).
55. Mondal, B. C. et al. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147, 1589-1600 (2011).
56. Wang, J. W. et al. Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17, 2204-2216 (2005).
57. Ding, Z. & Friml, J. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl Acad. Sci. USA 107, 12046-12051 (2010).
58. Sabatini, S., Heidstra, R., Wildwater, M. & Scheres, B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev. 17, 354-358 (2003).
59. Moubayidin, L. et al. Spatial coordination between stem cell activity and cell differentiation in the root meristem. Dev. Cell 26, 405-415 (2013).
60. Dello Ioio, R. et al. A genetic framework for the control of cell division and differentiation in the root meristem. Science 322, 1380-1384 (2008).
61. Blilou, I., Xu, J., Wildwater, M., Willemsen, V. & Paponov, I. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39-44 (2005).
62. Petersson, S. V., Johansson, A. I., Kowalczyk, M., Makoveychuk, A. & Wang, J. Y. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21, 1659-1668 (2009).
63. Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J. & Guilfoyle, T. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463-472 (1999).
64. Brunoud, G. et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103-106 (2012).
65. Brady, S. M. et al. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801-806 (2007).
66. Ikeda, Y. et al. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biol. 11, 731-738 (2009).
67. Stepanova, A. N., Hoyt, J. M., Hamilton, A. A. & Alonso, J. M. A. Link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell 17, 2230-2242 (2005).
68. Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661-673 (2002).
69. Friml, J., Wisniewska, J., Benkova, E., Mendgen, K. & Palme, K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415, 806-809 (2002).
70. Galweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226-2230 (1998).
71. Sheng, X. R. & Matunis, E. Live imaging of the Drosophila spermatogonial stem cell niche reveals novel mechanisms regulating germline stem cell output. Development 138, 3367-3376 (2011).
72. Reddy, G. V. & Meyerowitz, E. M. Stem-cell homeostasis and growth dynamics can be uncoupled in the Arabidopsis shoot apex. Science 310, 663-667 (2005).
73. Cheng, J. et al. Centrosome misorientation reduces stem cell division during ageing. Nature 456, 599-604 (2008).
74. Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. & Fuller, M. T. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542-2545 (2001).
75. Tulina, N. & Matunis, E. Control of Stem Cell Self-Renewal in Drosophila Spermatogenesis by JAK-STAT Signaling. Science 294, 2546-2549 (2001).
76. Kitadate, Y., Shigenobu, S., Arita, K. & Kobayashi, S. Boss/sev signaling from germline to soma restricts germline-stem-cell-niche formation in the anterior region of Drosophila male gonads. Dev. Cell 13, 151-159 (2007).
77. Tanentzapf, G., Devenport, D., Godt, D. & Brown, N. H. Integrin-dependent anchoring of a stem-cell niche. Nature Cell Biol. 9, 1413-1418 (2007).
78. Long, J. A., Moan, E. I., Medford, J. I. & Barton, M. K. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379, 66-69 (1996).
79. Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591-602 (2003).
80. Byrne, M. E., Barley, R., Curtis, M., Arroyo, J. M. & Dunham, M. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967-971 (2000).
81. Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255-260 (2003).
82. Byrne, M. E., Simorowski, J. & Martienssen, R. A. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129, 1957-1965 (2002).
83. Hay, A., Barkoulas, M. & Tsiantis, M. ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133, 3955-3961 (2006).
84. Scofield, S., Dewitte, W., Nieuwland, J. & Murray, J. A. H. The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. Plant J. 75, 53-66 (2013).
85. Jasinski, S., Piazza, P., Craft, J., Hay, A. & Woolley, L. KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15, 1560-1565 (2005).
86. Yanai, O., Shani, E., Dolezal, K., Tarkowski, P. & Sablowski, R. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566-1571 (2005).
87. Chen, H., Banerjee, A. K. & Hannapel, D. J. The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J. 38, 276-284 (2004).
88. Hay, A. et al. The gibberellin pathway mediates KNOTTED1-Type homeobox function in plants with different body plans. Curr. Biol. 12, 1557-1565 (2002).
89. Kurakawa, T., Ueda, N., Maekawa, M., Kobayashi, K. & Kojima, M. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445, 652-655 (2007).
90. Jacqmard, A., Detry, N., Dewitte, W., Van Onckelen, H. & Bernier, G. In situ localisation of cytokinins in the shoot apical meristem of Sinapis alba at floral transition. Planta 214, 970-973 (2002).
91. Leibfried, A., To, J. P., Busch, W., Stehling, S. & Kehle, A. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172-1175 (2005).
92. Bartrina, I., Otto, E., Strnad, M., Werner, T. & Schmülling, T. Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and thus seed yield in Arabidopsis thaliana. Plant Cell Online 23, 69-80 (2011).
93. Zhao, Z., Andersen, S. U., Ljung, K., Dolezal, K. & Miotk, A. Hormonal control of the shoot stem-cell niche. Nature 465, 1089-1092 (2010).
94. Knauer, S. et al. A Protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev. Cell 24, 125-132 (2013).
95. Song, J. B., Huang, S. Q., Dalmay, T. & Yang, Z. M. Regulation of leaf morphology by microRNA394 & its target LEAF CURLING RESPONSIVENESS. Plant Cell Physiol. 53, 1283-1294 (2012).
96. Losick, V. P., Morris, L. X., Fox, D. T. & Spradling, A. Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev. Cell 21, 159-171 (2011).
97. Zhang, L., Stokes, N., Polak, L. & Fuchs, E. Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment. Cell Stem Cell 8, 294-308 (2011).
98. Zhou, G.-K., Kubo, M., Zhong, R., Demura, T. & Ye, Z.-H. Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol. 48, 391-404 (2007).
99. Liu, Q. et al. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and leaf polarity establishment by repressing miR165/166 in Arabidopsis. Plant J. 58, 27-40 (2009).
100. Chitwood, D. H. & Timmermans, M. C. Small RNAs are on the move. Nature 467, 415-419 (2010).
101. Zhu, H., Hu, F., Wang, R., Zhou, X. & Sze, S. H. Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145, 242-256 (2011).
102. Prigge, M. J. et al. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17, 61-76 (2005).
103. Emery, J. F., Floyd, S. K., Alvarez, J., Eshed, Y. & Hawker, N. P. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13, 1768-1774 (2003).
104. Smith, M. R. et al. Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc. Natl Acad. Sci. 106, 5424-5429 (2009).
105. Tucker, M. et al. Accession-specific modifiers act with ZWILLE/ARGONAUTE10 to maintain shoot meristem stem cells during embryogenesis in Arabidopsis. BMC Genomics 14, 809 (2013).
106. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V. & Blilou, I. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449, 1053-1057 (2007).
107. Aida, M., Beis, D., Heidstra, R., Willemsen, V. & Blilou, I. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109-120 (2004).
108. Hofhuis, H. et al. Phyllotaxis and Rhizotaxis in Arabidopsis are modified by three PLETHORA Transcription Factors. Curr. Biol. 23, 956-962 (2013).
109. Matsuzaki, Y., Ogawa-Ohnishi, M., Mori, A. & Matsubayashi, Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 329, 1065-1067 (2010).
110. Zhou, W., Wei, L., Xu, J., Zhai, Q. & Jiang, H. Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22, 3692-3709 (2010).
111. Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K. & Jung, J. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555-567 (2000).
112. Nakajima, K., Sena, G., Nawy, T. & Benfey, P. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413, 307-311 (2001).
113. Cui, H. et al. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421-425 (2007).
114. Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W. & Paquette, A. J. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421-425 (2007).
115. Cruz-Ramírez, A. et al. A SCARECROW-RETINOBLASTOMA Protein network controls protective quiescence in the Arabidopsis root stem cell organizer. PLoS Biol. 11, e1001724 (2013).
116. Dolan, L. et al. Cellular organisation of the Arabidopsis thaliana root. Development 119, 71-84 (1993).
117. Kidner, C., Sundaresan, V., Roberts, K. & Dolan, L. Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate. Planta 211, 191-199 (2000).
118. Wachsman, G., Heidstra, R. & Scheres, B. Distinct cell-autonomous functions of RETINOBLASTOMA-RELATED in Arabidopsis stem cells revealed by the Brother of Brainbow clonal analysis system. Plant Cell 23, 2581-2591 (2011).
119. Chen, T.-T. & Wang, J. Y. J. Establishment of irreversible growth arrest in myogenic differentiation requires the RB LXCXE-Binding function. Mol. Cell. Biol. 20, 5571-5580 (2000).
120. Cruz-Ramírez, A. et al. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150, 1002-1015 (2012).
121. Sozzani, R., Cui, H., Moreno-Risueno, M. A., Busch, W. & Van Norman, J. M. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466, 128-132 (2010).
122. Weimer, A. K. et al. RETINOBLASTOMA RELATEDI Regulates Asymmetric Cell Divisions in Arabidopsis. Plant Cell Online 24, 4083-4095 (2012).
123. Barlow, P. Regeneration of the cap of primary roots of zea mays. New Phytol. 73, 937-954 (1974).
124. Heyman, J. et al. ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342, 860-863 (2013).
125. Fulcher, N. & Sablowski, R. Hypersensitivity to DNA damage in plant stem cell niches. Proc. Natl Acad. Sci. USA 106, 20984-20988 (2009).
126. Peters, J.-M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nature Rev. Mol. Cell Biol. 7, 644-656 (2006).
127. Vanstraelen, M. et al. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl Acad. Sci. 106, 11806-11811 (2009).
128. Licausi, F., Ohme-Takagi, M. & Perata, P. APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol. 199, 639-649 (2013).
129. Li, L. & Clevers, H. Coexistence of Quiescent and Active Adult Stem Cells in Mammals. Science 327, 542-545 (2010).
130. Liu, Y. et al. CCS52A2/FZR1, a cell cycle regulator, is an essential factor for shoot apical meristem maintenance in Arabidopsis thaliana. BMC Plant Biol. 12, 135 (2012).
131. 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 130, 4073-4083 (2003).
132. Stewart, R. N. & Dermen, H. Determination of Number and Mitotic Activity of Shoot Apical Initial Cells by Analysis of Mericlinal Chimeras. Am. J. Bot. 57, 816-826 (1970).
133. Furner, I. J. & Pumfrey, J. E. Cell fate in the shoot apical meristem of arabidopsis-thaliana. Development 115, 755-764 (1992).
134. Irish, V. F. & Sussex, I. M. A fate map of the arabidopsis embryonic shoot apical meristem. Development 115, 745-753 (1992).
135. Satina, S., Blakeslee, A. F. & Avery, A. Demonstration of three germ layers in the shoot apex of Datura by means of induced polyploidy in periclinal chimeras. Am. J. Bot. 27, 895-905 (1940).
136. Raven, J. A. & Edwards, D. Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52, 381-401 (2001).
137. Meyerowitz, E. M. Plants compared to animals: the broadest comparative study of development. Science 295, 1482-1485 (2002).
138. Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415-418 (2011).
139. Izhaki, A. & Bowman, J. L. KANADI and class III HD-Zip gene families regulate embryo patterning and modulate auxin flow during embryogenesis in Arabidopsis. Plant Cell 19, 495-508 (2007).
140. Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676 (2006).
141. Nakagawa, M. et al. A novel efficient feeder-free culture system for the derivation of human induced pluripotent stem cells. Sci. Rep. 4, 3594 (2014).
142. Sirakov, M., Skah, S., Nadjar, J. & Plateroti, M. Thyroid hormone's action on progenitor/stem cell biology: new challenge for a classic hormone? Biochim. Biophys. Acta 1830, 3917-3927 (2013).
143. Prusinkiewicz, P. & Runions, A. Computational models of plant development and form. New Phytol. 193, 549-569 (2012).
144. Oliva, M., Farcot, E. & Vernoux, T. Plant hormone signaling during development: insights from computational models. Curr. Opin. Plant Biol. 16, 19-24 (2013).
145. Middleton, A. M., Farcot, E., Owen, M. R. & Vernoux, T. Modeling regulatory networks to understand plant development: small is beautiful. Plant Cell 24, 3876-3891 (2012).
146. Azpeitia, E., Weinstein, N., Benitez, M., Mendoza, L. & Alvarez-Buylla, E. R. Finding missing interactions of the Arabidopsis thaliana root stem cell niche gene regulatory network. Front. Plant Sci. 4, 110 (2013).
147. Schmidt, T. et al. The iRoCS Toolbox - 3D analysis of the plant root apical meristem at cellular resolution. Plant J. 77, 806-814 (2014).
148. Bozorg, B., Krupinski, P. & Jonsson, H. Stress and strain provide positional and directional cues in development. PLoS Comput. Biol. 10, e1003410 (2014).
149. Jurgens, G. & Mayer, U. in Arabidopsis (ed. Bard, J. B. L.) 7-21 (Wolfe Publishing, 1994).
150. Bayer, M. et al. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323, 1485-1488 (2009).
151. Jeong, S., Palmer, T. M. & Lukowitz, W. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr. Biol. 21, 1268-1276 (2011).
152. Lukowitz, W., Roeder, A., Parmenter, D. & Somerville, C. A. MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116, 109-119 (2004).
153. Waki, T., Hiki, T., Watanabe, R., Hashimoto, T. & Nakajima, K. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr. Biol. 21, 1277-1281 (2011).
154. Wang, H., Ngwenyama, N., Liu, Y., Walker, J. C. & Zhang, S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19, 63-73 (2007).
155. Breuninger, H., Rikirsch, E., Hermann, M., Ueda, M. & Laux, T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev. Cell 14, 867-876 (2008).
156. Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147-153 (2003).
157. Hamann, T., Benkova, E., Baurle, I., Kientz, M. & Jurgens, G. The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev. 16, 1610-1615 (2002).
158. Mallory, A. C. et al. MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region. EMBO J. 23, 3356-3364 (2004).
159. Smith, Z. R. & Long, J. A. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464, 423-426 (2010).
160. Palovaara, J., Saiga, S. & Weijers, D. Transcriptomics approaches in the early Arabidopsis embryo. Trends Plant Sci. 18, 514-521 (2013).
161. Llavata-Peris, C., Lokerse, A., Moller, B., De Rybel, B. & Weijers, D. Imaging of phenotypes, gene expression, and protein localization during embryonic root formation in Arabidopsis. Methods Mol. Biol. 959, 137-148 (2013).
162. Miyashima, S. et al. A comprehensive expression analysis of the Arabidopsis MICRORNA165/6 gene family during embryogenesis reveals a conserved role in meristem specification and a non-cell-autonomous function. Plant Cell Physiol. 54, 375-384 (2013).
163. Kaya, H. et al. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 104, 131-142 (2001).
164. Bertrand, C., Bergounioux, C., Domenichini, S., Delarue, M. & Zhou, D. X. Arabidopsis histone acetyltransferase AtGCN5 regulates the floral meristem activity through the WUSCHEL/AGAMOUS pathway. J. Biol. Chem. 278, 28246-28251 (2003).
165. Kwon, C. S., Chen, C. & Wagner, D. WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes Dev. 19, 992-1003 (2005).
166. Carles, C. C. & Fletcher, J. C. The SAND domain protein ULTRAPETALA1 acts as a trithorax group factor to regulate cell fate in plants. Genes Dev. 23, 2723-2728 (2009).
167. Kornet, N. & Scheres, B. Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21, 1070-1079 (2009).
168. Graf, P. et al. MGOUN1 encodes an Arabidopsis type IB DNA topoisomerase required in stem cell regulation and to maintain developmentally regulated gene silencing. Plant Cell 22, 716-728 (2010).
169. Aichinger, E., Villar, C. B., Di Mambro, R., Sabatini, S. & Kohler, C. The CHD3 chromatin remodeler PICKLE and Polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23, 1047-1060 (2011).
170. Gifford, Casey, A. et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 153, 1149-1163 (2013).
171. Xie, W. et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153, 1134-1148 (2013).
172. Zhu, J. et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642-654 (2013).
173. Apostolou, E. & Hochedlinger, K. Chromatin dynamics during cellular reprogramming. Nature 502, 462-471 (2013).
174. Boutilier, K. et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14, 1737-1749 (2002).
175. 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. 18, 375-380 (2004).
176. Birnbaum, K. et al. A gene expression map of the Arabidopsis Root. Science 302, 1956-1960 (2003).
177. Zhang, C., Barthelson, R. A., Lambert, G. M. & Galbraith, D. W. Global characterization of cell-specific gene expression through fluorescence-activated sorting of nuclei. Plant Physiol. 147, 30-40 (2008).
178. Deal, R. B. & Henikoff, S. A. Simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev. Cell 18, 1030-1040 (2010).
179. Clark, S. E. Cell signalling at the shoot meristem. Nature Rev. Mol. Cell Biol. 2, 276-284 (2001).