Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Plant and animal stem cells: similar yet different

Key Points

  • Plant stem cells, as in animals, are maintained in specialized microenvironments, which are known as stem cell niches, where local signals from organizer cells act to prevent stem cell differentiation. Interestingly, committed stem cell progeny in plants also provide versatile feedback signals to their stem cell progenitors, thus becoming an indispensable component of the niche.

  • Plant stem cell niches are positioned within an organized group of dividing cells that are known as the meristem. In the model plant Arabidopsis thaliana, the shoot apical meristem and the root meristem are responsible for almost all the growth that occurs post-embryonically.

  • Despite their similar organization, the RB protein is the only known protein involved in stem cell function that is conserved between the animal and plant kingdoms. Control of stem cell differentiation in plants involves a conserved module of peptide–receptor signalling that counteracts homeodomain transcription factor activity from the organizer cells.

  • Both in plants and animals the position of a functional stem cell niche needs to be maintained within a dynamic structure. Also in plants, in which the position of a stem cell niche can be observed with cellular resolution from early embryonic stages onwards, several positional cues have been identified that involve crosstalk between hormone signalling, microRNAs and transcription factors.

  • The root and shoot stem cell niche organizers not only control the activity of surrounding stem cells but also regulate differentiation of distant transit-amplifying cells that sustain coherent organ growth. As observed in several animal stem cell niches the plant organizers have the ability to replace (damaged) stem cells.

  • The A. thaliana shoot organizing cells consist of a constantly changing pool of cells that are apically replenished by stem cell progeny, while shedding cells towards differentiation basally. The root organizing cells can act as long-term stem cells by replacing damaged stem cells, which ensures stem cell niche longevity.

Abstract

The astonishingly long lives of plants and their regeneration capacity depend on the activity of plant stem cells. As in animals, stem cells reside in stem cell niches, which produce signals that regulate the balance between self-renewal and the generation of daughter cells that differentiate into new tissues. Plant stem cell niches are located within the meristems, which are organized structures that are responsible for most post-embryonic development. The continuous organ production that is characteristic of plant growth requires a robust regulatory network to keep the balance between pluripotent stem cells and differentiating progeny. Components of this network have now been elucidated and provide a unique opportunity for comparing strategies that were developed in the animal and plant kingdoms, which underlie the logic of stem cell behaviour.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Comparing stem cell niches in animals and plants.
Figure 2: Organization of the shoot and root stem cell niches.
Figure 3: Maintenance of the stem cell niche.
Figure 4: Positioning the stem cell niche.

References

  1. 1

    Laux, T. The stem cell concept in plants: a matter of debate. Cell 113, 281–283 (2003).

    CAS  PubMed  Google Scholar 

  2. 2

    Sablowski, R. Plant and animal stem cells: conceptually similar, molecularly distinct? Trends Cell Biol. 14, 605–611 (2004).

    CAS  PubMed  Google Scholar 

  3. 3

    Scheres, B. Stem-cell niches: nursery rhymes across kingdoms. Nature Rev. Mol. Cell Biol. 8, 345–354 (2007).

    CAS  Google Scholar 

  4. 4

    Barker, N. Adult intestinal stem cells: critical drivers of epithelial homeostasis and regeneration. Nature Rev. Mol. Cell Biol. 15, 19–33 (2014).

    CAS  Google Scholar 

  5. 5

    Spradling, A., Drummond-Barbosa, D. & Kai, T. Stem cells find their niche. Nature 414, 98–104 (2001).

    CAS  PubMed  Google Scholar 

  6. 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).

    Google Scholar 

  7. 7

    Meyerowitz, E. M. Genetic control of cell division patterns in developing plants. Cell 88, 299–308 (1997).

    CAS  PubMed  Google Scholar 

  8. 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).

    CAS  PubMed  Google Scholar 

  9. 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).

    CAS  PubMed  Google Scholar 

  10. 10

    Papagiannouli, F. & Lohmann, I. Shaping the niche: Lessons from the Drosophila testis and other model systems. Biotechnol. J. 7, 723–736 (2012).

    CAS  PubMed  Google Scholar 

  11. 11

    Sage, J. The retinoblastoma tumor suppressor and stem cell biology. Genes Dev. 26, 1409–1420 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 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).

    CAS  PubMed  Google Scholar 

  13. 13

    Wildwater, M. et al. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123, 1337–1349 (2005).

    CAS  PubMed  Google Scholar 

  14. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 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).

    CAS  PubMed  Google Scholar 

  17. 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).

    CAS  PubMed  Google Scholar 

  18. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 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).

    CAS  PubMed  Google Scholar 

  20. 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). Shows that the shoot meristem has properties of a self-regulatory system in which WUS–CLV interactions establish a feedback loop between the stem cells and the underlying organizing centre.

    CAS  PubMed  Google Scholar 

  21. 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).

    CAS  PubMed  Google Scholar 

  22. 22

    Yadav, R. K. et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev. 25, 2025–2030 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. 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).

    CAS  PubMed  Google Scholar 

  24. 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).

    CAS  Google Scholar 

  25. 25

    Kayes, J. M. & Clark, S. E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125, 3843–3851 (1998).

    CAS  PubMed  Google Scholar 

  26. 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).

    CAS  PubMed  Google Scholar 

  27. 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).

    CAS  PubMed  Google Scholar 

  28. 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).

    CAS  PubMed  Google Scholar 

  29. 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).

    CAS  PubMed  Google Scholar 

  30. 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).

    CAS  Google Scholar 

  31. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    Ogawa, M., Shinohara, H., Sakagami, Y. & Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319, 294 (2008).

    CAS  PubMed  Google Scholar 

  33. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 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).

    CAS  PubMed  Google Scholar 

  35. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 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).

    Google Scholar 

  37. 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).

    CAS  PubMed  Google Scholar 

  38. 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).

    CAS  PubMed  Google Scholar 

  39. 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. 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).

    CAS  PubMed  Google Scholar 

  41. 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).

    CAS  PubMed  Google Scholar 

  42. 42

    Lohmann, J. U. et al. A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105, 793–803 (2001).

    CAS  PubMed  Google Scholar 

  43. 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).

    PubMed  PubMed Central  Google Scholar 

  44. 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).

    CAS  PubMed  Google Scholar 

  45. 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).

    CAS  PubMed  Google Scholar 

  46. 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). Suggests that apically derived cytokinin and CLV signalling act together as positional cues for patterning the WUS domain within the stem cell niche, using a developed computational model that illustrates a growing shoot apical meristem.

    CAS  PubMed  Google Scholar 

  47. 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).

    CAS  PubMed  Google Scholar 

  48. 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). Identifies WOX5 as an essential factor for root stem cell maintenance and as a conserved factor of what turned out to be a larger conserved module that regulates plant stem cell maintenance in general.

    CAS  PubMed  Google Scholar 

  49. 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).

    CAS  PubMed  Google Scholar 

  50. 50

    Stahl, Y. et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23, 362–371 (2013).

    CAS  PubMed  Google Scholar 

  51. 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).

    CAS  PubMed  Google Scholar 

  52. 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).

    CAS  PubMed  Google Scholar 

  53. 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).

    CAS  PubMed  Google Scholar 

  54. 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).

    CAS  Google Scholar 

  55. 55

    Mondal, B. C. et al. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 147, 1589–1600 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. 57

    Ding, Z. & Friml, J. Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc. Natl Acad. Sci. USA 107, 12046–12051 (2010).

    CAS  PubMed  Google Scholar 

  58. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. 59

    Moubayidin, L. et al. Spatial coordination between stem cell activity and cell differentiation in the root meristem. Dev. Cell 26, 405–415 (2013). Provides evidence that a single gene, SCR , acts from the root stem cell organizer to control activities of the surrounding stem cells and their differentiating progeny at the distance.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. 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).

    CAS  PubMed  Google Scholar 

  61. 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). Proposes a mechanism in which an interaction network of auxin and stem cell fate determinants (PLT genes) control patterning and growth of the root primordium.

    CAS  PubMed  Google Scholar 

  62. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 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).

    CAS  PubMed  Google Scholar 

  64. 64

    Brunoud, G. et al. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103–106 (2012).

    CAS  PubMed  Google Scholar 

  65. 65

    Brady, S. M. et al. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318, 801–806 (2007).

    CAS  PubMed  Google Scholar 

  66. 66

    Ikeda, Y. et al. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nature Cell Biol. 11, 731–738 (2009).

    CAS  PubMed  Google Scholar 

  67. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68

    Friml, J. et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108, 661–673 (2002).

    CAS  PubMed  Google Scholar 

  69. 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).

    PubMed  Google Scholar 

  70. 70

    Galweiler, L. et al. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282, 2226–2230 (1998).

    CAS  PubMed  Google Scholar 

  71. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. 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).

    CAS  PubMed  Google Scholar 

  73. 73

    Cheng, J. et al. Centrosome misorientation reduces stem cell division during ageing. Nature 456, 599–604 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. 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).

    CAS  PubMed  Google Scholar 

  75. 75

    Tulina, N. & Matunis, E. Control of Stem Cell Self-Renewal in Drosophila Spermatogenesis by JAK-STAT Signaling. Science 294, 2546–2549 (2001).

    CAS  PubMed  Google Scholar 

  76. 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).

    CAS  PubMed  Google Scholar 

  77. 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).

    CAS  PubMed  Google Scholar 

  78. 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).

    CAS  PubMed  Google Scholar 

  79. 79

    Benková, E. et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602 (2003).

    PubMed  Google Scholar 

  80. 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).

    CAS  PubMed  Google Scholar 

  81. 81

    Reinhardt, D. et al. Regulation of phyllotaxis by polar auxin transport. Nature 426, 255–260 (2003).

    CAS  PubMed  Google Scholar 

  82. 82

    Byrne, M. E., Simorowski, J. & Martienssen, R. A. ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129, 1957–1965 (2002).

    CAS  PubMed  Google Scholar 

  83. 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).

    CAS  PubMed  Google Scholar 

  84. 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).

    CAS  PubMed  Google Scholar 

  85. 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).

    CAS  PubMed  Google Scholar 

  86. 86

    Yanai, O., Shani, E., Dolezal, K., Tarkowski, P. & Sablowski, R. Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566–1571 (2005).

    CAS  PubMed  Google Scholar 

  87. 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).

    CAS  PubMed  Google Scholar 

  88. 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).

    CAS  PubMed  Google Scholar 

  89. 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).

    CAS  PubMed  Google Scholar 

  90. 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).

    CAS  PubMed  Google Scholar 

  91. 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).

    CAS  PubMed  Google Scholar 

  92. 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).

    CAS  Google Scholar 

  93. 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).

    CAS  PubMed  Google Scholar 

  94. 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). Describes a mechanism whereby the epidermis acts as a source of information to maintain the position of the shoot stem cell niche within the constantly changing cell population of the meristem.

    CAS  PubMed  Google Scholar 

  95. 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).

    CAS  PubMed  Google Scholar 

  96. 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).

    CAS  PubMed  Google Scholar 

  97. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. 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).

    CAS  PubMed  Google Scholar 

  99. 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).

    CAS  PubMed  Google Scholar 

  100. 100

    Chitwood, D. H. & Timmermans, M. C. Small RNAs are on the move. Nature 467, 415–419 (2010).

    CAS  PubMed  Google Scholar 

  101. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. 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).

    CAS  PubMed  Google Scholar 

  104. 104

    Smith, M. R. et al. Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc. Natl Acad. Sci. 106, 5424–5429 (2009).

    CAS  PubMed  Google Scholar 

  105. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. 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).

    CAS  PubMed  Google Scholar 

  107. 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). Identifies the PLT genes as key effectors for the establishment of the root stem cell niche during embryonic pattern formation.

    CAS  PubMed  Google Scholar 

  108. 108

    Hofhuis, H. et al. Phyllotaxis and Rhizotaxis in Arabidopsis are modified by three PLETHORA Transcription Factors. Curr. Biol. 23, 956–962 (2013).

    CAS  PubMed  Google Scholar 

  109. 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).

    CAS  PubMed  Google Scholar 

  110. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  111. 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).

    CAS  PubMed  Google Scholar 

  112. 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).

    CAS  PubMed  Google Scholar 

  113. 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).

    CAS  PubMed  Google Scholar 

  114. 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).

    CAS  PubMed  Google Scholar 

  115. 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). Describes the interaction between RBR and SCR as a mechanism to maintain organizer quiescence and thereby provide protection against DNA damage that enables the organizer to act as long-term stem cells.

    PubMed  PubMed Central  Google Scholar 

  116. 116

    Dolan, L. et al. Cellular organisation of the Arabidopsis thaliana root. Development 119, 71–84 (1993).

    CAS  PubMed  Google Scholar 

  117. 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).

    CAS  PubMed  Google Scholar 

  118. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  119. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 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).

    PubMed  PubMed Central  Google Scholar 

  121. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  122. 122

    Weimer, A. K. et al. RETINOBLASTOMA RELATED1 Regulates Asymmetric Cell Divisions in Arabidopsis. Plant Cell Online 24, 4083–4095 (2012).

    CAS  Google Scholar 

  123. 123

    Barlow, P. Regeneration of the cap of primary roots of zea mays. New Phytol. 73, 937–954 (1974).

    CAS  Google Scholar 

  124. 124

    Heyman, J. et al. ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342, 860–863 (2013). Describes how organizer mitotic quiescence correlates with insensitivity to stress conditions and functions to replace damaged stem cells, thereby acting as a pool of reserve stem cells and contributing to stem cell niche longevity.

    CAS  PubMed  Google Scholar 

  125. 125

    Fulcher, N. & Sablowski, R. Hypersensitivity to DNA damage in plant stem cell niches. Proc. Natl Acad. Sci. USA 106, 20984–20988 (2009).

    CAS  PubMed  Google Scholar 

  126. 126

    Peters, J.-M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nature Rev. Mol. Cell Biol. 7, 644–656 (2006).

    CAS  Google Scholar 

  127. 127

    Vanstraelen, M. et al. APC/CCCS52A complexes control meristem maintenance in the Arabidopsis root. Proc. Natl Acad. Sci. 106, 11806–11811 (2009).

    CAS  PubMed  Google Scholar 

  128. 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).

    CAS  PubMed  Google Scholar 

  129. 129

    Li, L. & Clevers, H. Coexistence of Quiescent and Active Adult Stem Cells in Mammals. Science 327, 542–545 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 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).

    CAS  PubMed  Google Scholar 

  132. 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).

    Google Scholar 

  133. 133

    Furner, I. J. & Pumfrey, J. E. Cell fate in the shoot apical meristem of arabidopsis-thaliana. Development 115, 755–764 (1992).

    Google Scholar 

  134. 134

    Irish, V. F. & Sussex, I. M. A fate map of the arabidopsis embryonic shoot apical meristem. Development 115, 745–753 (1992).

    Google Scholar 

  135. 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).

    Google Scholar 

  136. 136

    Raven, J. A. & Edwards, D. Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52, 381–401 (2001).

    CAS  PubMed  Google Scholar 

  137. 137

    Meyerowitz, E. M. Plants compared to animals: the broadest comparative study of development. Science 295, 1482–1485 (2002).

    CAS  PubMed  Google Scholar 

  138. 138

    Sato, T. et al. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469, 415–418 (2011).

    CAS  PubMed  Google Scholar 

  139. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  140. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. 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).

    PubMed  PubMed Central  Google Scholar 

  142. 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).

    CAS  PubMed  Google Scholar 

  143. 143

    Prusinkiewicz, P. & Runions, A. Computational models of plant development and form. New Phytol. 193, 549–569 (2012).

    CAS  PubMed  Google Scholar 

  144. 144

    Oliva, M., Farcot, E. & Vernoux, T. Plant hormone signaling during development: insights from computational models. Curr. Opin. Plant Biol. 16, 19–24 (2013).

    CAS  PubMed  Google Scholar 

  145. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. 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).

    PubMed  PubMed Central  Google Scholar 

  147. 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).

    CAS  PubMed  Google Scholar 

  148. 148

    Bozorg, B., Krupinski, P. & Jonsson, H. Stress and strain provide positional and directional cues in development. PLoS Comput. Biol. 10, e1003410 (2014).

    PubMed  PubMed Central  Google Scholar 

  149. 149

    Jurgens, G. & Mayer, U. in Arabidopsis (ed. Bard, J. B. L.) 7–21 (Wolfe Publishing, 1994).

    Google Scholar 

  150. 150

    Bayer, M. et al. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323, 1485–1488 (2009).

    CAS  PubMed  Google Scholar 

  151. 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).

    CAS  PubMed  Google Scholar 

  152. 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).

    CAS  PubMed  Google Scholar 

  153. 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).

    CAS  PubMed  Google Scholar 

  154. 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).

    PubMed  PubMed Central  Google Scholar 

  155. 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).

    CAS  PubMed  Google Scholar 

  156. 156

    Friml, J. et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 (2003).

    CAS  PubMed  Google Scholar 

  157. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  158. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. 159

    Smith, Z. R. & Long, J. A. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464, 423–426 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  160. 160

    Palovaara, J., Saiga, S. & Weijers, D. Transcriptomics approaches in the early Arabidopsis embryo. Trends Plant Sci. 18, 514–521 (2013).

    CAS  PubMed  Google Scholar 

  161. 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).

    CAS  PubMed  Google Scholar 

  162. 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).

    CAS  PubMed  Google Scholar 

  163. 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).

    CAS  PubMed  Google Scholar 

  164. 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).

    CAS  PubMed  Google Scholar 

  165. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  166. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  168. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  169. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  170. 170

    Gifford, Casey, A. et al. Transcriptional and epigenetic dynamics during specification of human embryonic stem cells. Cell 153, 1149–1163 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. 171

    Xie, W. et al. Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153, 1134–1148 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  172. 172

    Zhu, J. et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642–654 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  173. 173

    Apostolou, E. & Hochedlinger, K. Chromatin dynamics during cellular reprogramming. Nature 502, 462–471 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  174. 174

    Boutilier, K. et al. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14, 1737–1749 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  175. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  176. 176

    Birnbaum, K. et al. A gene expression map of the Arabidopsis Root. Science 302, 1956–1960 (2003).

    CAS  PubMed  Google Scholar 

  177. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  178. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  179. 179

    Clark, S. E. Cell signalling at the shoot meristem. Nature Rev. Mol. Cell Biol. 2, 276–284 (2001).

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank B. Scheres, M. Tsiantis and P. Costantino for their valuable comments on the manuscript. This work was supported by The European Research Council (to S.S.) and the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research (to R.H.).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sabrina Sabatini.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Glossary

Anticlinally dividing cells

Cells in which the division plane is perpendicular to the surface of the organ, thus maintaining a single cell layer.

Stele

In vascular plants, the stele is the central part of the root or stem that contains the vascular tissues.

Columella

Specialized root cells that are involved in gravity-sensing mechanisms.

Hub cell

Specialized cell of the Drosophila melanogaster testes that is necessary to maintain the adjacent stem cell.

Paneth cell

Specialized cell of the intestinal epithelium, which secretes factors that sustain the self-renewal capacity of the contacting stem cell.

E2F transcription factor

Member of a family of transcription factors that, by interacting with other proteins, control cell cycle progression.

Plasmodesmata

Microscopic channels that traverse the cell wall of plant cells, which enables transport and communication between them.

Integrin

Transmembrane protein that mediates attachment between an animal cell and its surroundings, such as cells or the extracellular matrix.

APC/C

(Anaphase-promoting complex; also known as the cyclosome). An E3 ubiquitin ligase protein complex that targets cell cycle proteins for degradation by the 26S proteasome, thus enabling cell cycle progression.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Heidstra, R., Sabatini, S. Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15, 301–312 (2014). https://doi.org/10.1038/nrm3790

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing