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Stem-cell niches: nursery rhymes across kingdoms

Nature Reviews Molecular Cell Biology volume 8, pages 345–354 (2007)Cite this article

Key Points

  • Animal and plant stem-cell niches have conserved cellular organization. Both maintain stem cells by short-range signals that originate from organizing centres.

  • The positioning of two different types of plant stem-cell niches is determined by combinatorial codes of plant-specific transcription factors. Combinatorial coding is also important in animal stem cells.

  • Plant behaviour requires flexible developmental strategies. In line with this, stem-cell programming in plants is dynamic, and this is reflected in multiple feedback connections between stem-cell-maintenance factors and -differentiation factors.

  • New approaches are needed for dynamic studies on plant stem cells. Improved imaging techniques and computational modelling are important steps towards this goal.

  • The importance of epigenetic programming for the stem-cell state has been recognized for both animals and plants. The current challenge is to determine whether the epigenetic control mechanisms that are used are similar between animals and plants.

Abstract

Despite the large evolutionary distance between the plant and animal kingdoms, stem cells in both reside in specialized cellular contexts called stem-cell niches. Although stem-cell-specification factors have been recruited from plant-specific gene families, maintenance factors that repress stem-cell differentiation are conserved between plants and animals. Recent evidence indicates that stem cells in multicellular organisms can be specified by kingdom-specific patterning mechanisms that connect to a related core of epigenetic stem-cell factors.

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Figure 1: Stem cells in the plant kingdom.
Figure 2: Stem-cell-niche organization in animals and plants.
Figure 3: Stem-cell specification in the root apex.
Figure 4: Stem-cell specification in the shoot apex.
Figure 5: Secondary stem-cell niches for plant architecture.
Figure 6: Stem cells and chromatin modification.

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Acknowledgements

Many thanks to M. Aida and P. Doerner for providing images and to my laboratory members, and especially to B. Horvath and M. Laskowski, for critical reading of the manuscript. I am grateful to K. Scheres for 'vette' Photoshop drawings. Finally, I apologize to colleagues for not citing other relevant work owing to space constraints.

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  1. Department of Biology, Molecular Genetics Group, Utrecht University, Padualaan 8, Utrecht, 3584 CH, the Netherlands

    Ben Scheres

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Tair

WUS

PLT1

PLT2

SHR

SCR

STM

PIN1

ZLL

LHP1

RBR

FURTHER INFORMATION

Ben Scheres's homepage

Glossary

Stem-cell niche

The cellular microenvironment that provides the signals and physical support to maintain stem cells.

Asymmetrical divisions

Mitotic divisions that generate distinct fates in the two daughter cells; in the case of stem cells, one daughter preserves the stem-cell state.

Transit-amplifying cells

Dividing stem-cell daughters that are fated for differentiation and that can retain the ability to divide.

Totipotent

Cells that can produce progeny that can form an entire organism.

Multipotent

Cells that can produce progeny that can form all cell types of a tissue.

Homeodomain

Conserved DNA-binding domain in both plant and animal transcription factors.

Pluripotent

Cells that can produce progeny that can form all cell lineages.

Auxin

Plant hormone that is implicated in a range of developmental processes, including cell-fate specification, cell division and cell expansion. In most plants, indole-3-acetic acid is the main active form.

PIN family

Transmembrane proteins that mediate auxin efflux, named after the founding member, PIN-FORMED1.

AP2 domain

A plant specific DNA-binding domain that was first found in the floral homeotic protein APETALA2. Members of a distinctive subclade of the AP2-domain family, which includes both APETALA2 and the PLETHORA genes, contain two AP2 domains.

GRAS family

A plant-specific transcription-factor family named after the first three members cloned: GIBBERELLIN-INSENSITIVE, RGA and SCARECROW.

GATA

Transcription-factor family in both plants and animals with zinc-finger DNA-binding domains.

NAC domain

A plant-specific DNA-binding domain first found in Petunia NO APICAL MERISTEM and Arabidopsis ATAF1 and CUP-SHAPED COTYLEDON2.

RNA-induced silencing complex

A complex that binds double-stranded RNA and targets it to homologous sequences to induce silencing.

Arabidopsis response regulators

(ARR). Transcription factors that are activated by phosphorelay in cytokinin signal transduction.

Cytokinin

Purine derivates that function as a plant hormone. Cytokinin is implicated in the control of cell division, but also in the determination of shoot identity.

Polycomb group

A class of genes and proteins that was originally identified in D. melanogaster through mutations that are unable to maintain the repression of homeotic genes.

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Scheres, B. Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8, 345–354 (2007). https://doi.org/10.1038/nrm2164

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