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  • Review Article
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Regulation of transcription in plants: mechanisms controlling developmental switches

Nature Reviews Genetics volume 11, pages 830–842 (2010)Cite this article

Subjects

Key Points

  • Developmental phase switches and identity changes need global changes in gene expression patterns.

  • Genome-wide chromatin immunoprecipitation approaches have provided insights into the transcriptional networks and topology of the networks that underlie phase changes and identity specification.

  • Phase switches involve suppression of the preceding developmental programme by negative feedback regulation and activation of the next developmental programme by positive (autoregulatory) regulation mechanisms.

  • Combinatorial interaction among transcription factors determines regulatory specificity and defines the set of target genes.

  • Key regulators are transcription factors and chromatin modifiers

  • These key regulators form protein complexes and the transcription factors may recruit the chromatin modifiers to specific loci.

Abstract

Unlike animals, plants produce new organs throughout their life cycle using pools of stem cells that are organized in meristems. Although many key regulators of meristem and organ identities have been identified, it is still not well understood how they function at the molecular level and how they can switch an entire developmental programme in which thousands of genes are involved. Recent advances in the genome-wide identification of target genes controlled by key plant transcriptional regulators and their interactions with epigenetic factors provide new insights into general transcriptional regulatory mechanisms that control switches of developmental programmes and cell fates in complex organisms.

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Figure 1: Phase changes in plant development.
Figure 2: Evolving models of the action of developmental master regulators.
Figure 3: A regulatory network of the transition to flowering.

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Acknowledgements

We thank R. de Maagd, J. M. Muino, R. Karlova, J. Wellink and R. Immink for useful comments on the manuscript. We wish to apologize to all authors whose publications we could not cite due to space constraints.

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Authors and Affiliations

  1. Laboratory of Molecular Biology, Wageningen University, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Kerstin Kaufmann & Alice Pajoro

  2. Bioscience, Plant Research International, Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Alice Pajoro & Gerco C. Angenent

  3. Centre for BioSystems Genomics (CBSG), Droevendaalsesteeg 1, 6708 PB, Wageningen, The Netherlands

    Gerco C. Angenent

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  1. Kerstin Kaufmann
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  2. Alice Pajoro
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Correspondence to Kerstin Kaufmann.

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Supplementary information

Supplementary information S1 (table)

Examples of genome-wide target gene studies of transcription factors controlling development in Arabidopsis thaliana. (PDF 343 kb)

Supplementary information S2 (table)

Examples of chromatin modifying and remodeling complexes with roles in developmental switches in plants (PDF 364 kb)

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FURTHER INFORMATION

Chromatin Database

Glossary

Pluripotent cell

An undifferentiated cell that has the potential to adopt different identities. In plants, pluripotent cells are found in meristems and there are stem cell-like populations in shoots, roots and leaves.

Meristem

A tissue in plants consisting of pluripotent cells. In apical meristems, cell-to-cell signalling establishes and maintains a zone that contains the stem cells, which is separated from the peripheral zone in which differentiation is eventually initiated. Other types of meristems give rise to the vasaculture and epidermis, or enable secondary growth.

Shoot apical meristem

The meristem that forms all major above-ground plant organs. It is established during embryogenesis. During plant development, it changes from a juvenile to a vegetative state, and then to inflorescence and floral identity.

Inflorescence meristem

A type of shoot apical meristem that gives rise to floral meristems at its flanks.

Floral meristem

A meristem that gives rise to the floral organs: sepals, petals, stamens and carpels.

Histone-modifying enzyme

An enzyme that can modify specific sites in histones, for example, by adding or removing a chemical group. Common modifications are methylation, acetylation, ubiquitylation, sumoylation, phosphorylation and proline isomerization.

Nucleosome-remodelling enzyme

An enzyme that can establish, remove, or change the positions of nucleosomes on the DNA.

MADS-box family

A family of transcription factors that is present in all major groups of eukaryotes. The family is named after the founding members MCM1 from Saccharomyces cerevisiae, AGAMOUS from Arabidopsis thaliana, DEFICIENS from Antirrhinum majus and SRF from humans.

ChIP–seq

(Chromatin immunoprecipitation followed by next-generation sequencing). A technique that is used to identify the in vivo DNA-binding sites of proteins. After crosslinking of proteins to DNA, isolation and fragmentation of the chromatin, genomic regions that are bound by the protein of interest are isolated using specific antibodies. The immunoprecipitated DNA is then sequenced.

ChIP–chip

(Chromatin immunoprecipitation followed by microarray). DNA associated with a protein of interest, isolated by chromatin immunoprecipitation, is hybridized to genomic-tiling arrays to identify DNA-binding sites of the protein.

Direct target gene

A gene whose expression is controlled by a particular transcription factor through direct binding of the factor to cis-regulatory elements of that gene.

Autoregulation

A mechanism in which a molecule (such as a transcription factor) regulates its own production. This process can involve interactions with other molecules.

Floral pathway integrator

A protein that can integrate the inputs of the different environmental and internal floral induction pathways and transmit the information to their downstream targets, such as floral meristem identity genes, at the shoot apex. Their combined action controls flowering time. The transcriptional regulators SOC1, LFY, FT and FD are 'classical' floral pathway integrators.

Perianth

The sterile organs in the outer whorls of a flower. Many flowering plant species such as Arabidopsis, Petunia and Antirrhinum have a perianth that is differentiated into sepals and petals.

Trichome

An epidermal outgrowth (hair) that can have different structures and functions. In Arabidopsis thaliana, trichomes are unicellular.

Stoma

A pore found in the epidermis of leaves and in several other above-ground plant organs. Stomata are surrounded by pairs of specialized epidermal cells called guard cells.

Homeotic mutant

A mutant in which one organ type is replaced by a different organ type.

Stele

The central part of the root, mainly consisting of the vasculature and the surrounding pericycle.

Floral reversion

The reversion of a meristem from a reproductive state back to a vegetative state, caused by mutations in regulatory genes. A floral meristem can revert to an inflorescence meristem or an inflorescence meristem can revert to a vegetative meristem. Reversion leads to the formation of shoots instead of flowers and 'aerial' rosettes instead of shoots.

(CHD)-type nucleosome remodeller

An ATP-dependent chromatin-remodelling factor of the chromodomain/helicase/DNA-binding domain (CHD) subfamily. These remodellers usually function as part of multisubunit complexes. In mammals and flies, they are involved in transcriptional repression by nucleosome remodelling and histone deacetylation. They have also been shown to be involved in transcriptional activation.

Vernalization

The induction of the transition from vegetative to reproductive plant growth by a prolonged period of cold (winter).

Sequential ChIP

The identification of DNA-binding sites that are common to two proteins (for example, two types of modified histones or transcription factors). It involves two rounds of immunoprecipitation using separate antibodies against the proteins of interest.

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Kaufmann, K., Pajoro, A. & Angenent, G. Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11, 830–842 (2010). https://doi.org/10.1038/nrg2885

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