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  • Review Article
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Survival of the flexible: hormonal growth control and adaptation in plant development

Nature Reviews Genetics volume 10, pages 305–317 (2009)Cite this article

Key Points

  • Indeterminate growth is a unique feature of plant development that is subject to intrinsic controls and modulated by environmental cues.

  • Growth control is mediated by hormonal responses that rapidly alter gene expression programmes by inducing or preventing degradation of transcriptional regulators by the ubiquitin–proteasome system.

  • Developmental targets of hormones are the meristems (stem cells and their transit amplifying daughter cells), lateral organ founder cells and the developing organ primordia.

  • Plant development is modulated by the well-known classic hormones, such as auxin, cytokinin and gibberellin, and by newly identified growth regulators, such as peptides, strigolactone and fatty acid-related molecules. Numerous growth regulators are yet to be discovered.

  • Hormones do not act in isolation but are interrelated by synergistic or antagonistic crosstalk so that the hormones modulate each other's biosynthesis or response.

  • Hormones stimulate or terminate cell proliferation and thus regulate meristem or organ size, depending on the spatial distribution of their receptors and transcriptional regulators, as well as the relative concentrations of antagonistically acting hormones such as auxin and cytokinin.

  • Environmental cues, such as light or stress, elicit stimulatory or inhibitory growth changes by altering local hormone biosynthesis or response.

  • Despite tremendous recent progress, important aspects of hormone action in development are yet to be analysed, including hormone-regulated cell fate and tissue-specific hormone responses.

Abstract

Plant development is subject to hormonal growth control and adapts to environmental cues such as light or stress. Recently, significant progress has been made in elucidating hormone synthesis, signalling and degradation pathways, and in resolving spatial and temporal aspects of hormone responses. Here we review how hormones control maintenance of stem cell systems, influence developmental transitions of stem cell daughters and define developmental compartments in Arabidopsis thaliana. We also discuss how environmental cues change plant growth by modulating hormone levels and response. Future analysis of hormone crosstalk and of hormone action at both single cell and organ levels will substantially improve our understanding of how plant development adapts to changes in intrinsic and environmental conditions.

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Figure 1: Embryo and meristem organization.
Figure 2: Models for hormone crosstalk in different developmental contexts.
Figure 3: Model for hormonal input into cell cycle regulation.
Figure 4: Environmental influence on growth.

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Acknowledgements

We would like to thank C. Kägi for help with the figures and for critical reading of the manuscript.

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Authors and Affiliations

  1. ZMBP, Entwicklungsgenetik, Universität Tübingen, Auf der Morgenstelle 3, 72076, Tübingen, Germany

    Hanno Wolters & Gerd Jürgens

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  1. Hanno Wolters
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Correspondence to Gerd Jürgens.

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Glossary

F-box receptor

The component of an SCF E3 ubiquitin ligase that acts as a hormone receptor and that recognizes repressor proteins as substrates to be targeted for degradation.

Meristem

A plant stem cell system comprising the niche, the pluripotent stem cells and their highly proliferating daughter cells.

Determinate organ

Plant organ that does not have unlimited growth potential but that differentiates once the final size is reached, for example, a leaf.

Quiescent centre

A group of cells located in the centre of the root meristem and required to keep the surrounding stem cells from differentiating.

Histone acetyltransferase

An enzyme that adds acetyl groups to lysine residues in the DNA-binding histone group of proteins and thereby modulates the transcriptional activity of genes.

Chromatin remodelling

Transient changes in chromatin accessibility.

Cotyledon

The leaves of a seedling that are formed during embryonic development.

Indeterminate

Refers to a pattern of growth and development that is open ended. In meristems, this is associated with the continuous ability to produce determinate lateral organs, such as leaves. By contrast, determinate refers to growth and development that is restricted in time or space.

Organizing centre

A group of cells that is located in the centre of the shoot meristem and is required to prevent the surrounding stem cells from differentiating.

Transit amplifying cells

Stem cell daughters that divide for a definite number of times before they leave the meristem to undergo terminal differentiation.

Transition zone

Boundary between the meristematic zone (which is proliferative) and the differentiation zones; it is easily recognized by the onset of cell elongation in the root.

DELLA proteins

DELLA domain-containing gibberellin signalling repressors, which are named after a conserved stretch of amino acids that are required for their degradation by the 26S proteasome.

CLE family

Family of CLV3-related peptide ligands that bind to receptor kinases that contain leucine-rich repeats, such as CLV1.

Hormonal regime

Describes a situation in which the hormone concentration or the concentration ratio of different hormones mediates cell- or compartment-specific responses.

Callus

A disorganized group of proliferating or undifferentiated cells.

Lateral organ

An organ that is produced from the shoot apical meristem. Includes leaves and putatively homologous organs such as cotyledons (embryonic leaves), bracts (modified leaves that subtend reproductive structures) and floral organs.

Signalosome

A multifunctional protein complex essential for development and possibly involved in the regulation of protein degradation.

Proteasome

A large intracellular protein complex that degrades soluble proteins that have been modified by ubiquitylation.

Photomorphogenesis

A light-dependent developmental process, such as seed germination or seedling growth.

Phytochrome

One of three classes of known plant photoreceptors. Phytochromes are composed of a protein moiety covalently associated with a tetrapyrrole chromophore; they are synthesized in a red-light-absorbing form and are converted by red light to a far-red-light-absorbing isoforms, which bind to nuclear-localized transcription factors of the PIF class.

Hypocotyl

The stem of a seedling.

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Wolters, H., Jürgens, G. Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10, 305–317 (2009). https://doi.org/10.1038/nrg2558

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