It seems that the epidermis is the cell layer through which growth-promoting plant hormones called brassinosteroids exert their effect on cell expansion — a finding that puts a new perspective on classical views of plant growth.
Brassinosteroids are growth-promoting plant hormones, and their absence, or the absence of their main transmembrane receptor protein, creates dwarfed plants. In the past few years, both the brassinosteroid biosynthetic pathway and the molecular signalling route from the brassinosteroid receptor to intracellular gene-transcription factors have been elucidated1,2. That information, and the ability to restore normal growth selectively in specific plant cell layers, has now allowed Savaldi-Goldstein and co-workers (page 199 of this issue)3 to clarify the pivotal role of a single cell layer — the outermost layer, known as the epidermis — in plant growth.
One of the main differences between animals and plants is that animal cells can move relative to each other, whereas plant cells are practically glued together by cell walls. Thus, whereas animals can build beautiful structures through the slipping and sliding of cell sheets across each other, plants must shape themselves solely by the coordinated division and expansion of individual cells. The intimate connectedness of plant cells through rigid walls creates a mechanical network that can be driven or constrained by individual cell layers — just as you can stretch bubble gum by blowing it up or by tearing it apart with your fingers. This notion that certain tissue layers can act as masters of plant growth, whereas others follow like slaves, has been around in plant biology for a long time, and it has been proposed that the epidermis drives growth 'from without'4,5 (Fig. 1a).
Savaldi-Goldstein and colleagues3 set out to study the contribution of the epidermis to shoot growth. They used a mutant of the flowering plant Arabidopsis thaliana (Fig. 1b) that lacks both copies of the CPD gene. This gene is involved in brassinosteroid biosynthesis and the plant is therefore dwarfed. The authors found that by supplying the epidermal layer of this mutant with an intact version of the CPD gene, tagged with a fluorescent 'reporter' molecule, dwarfism could be reversed. When this gene was expressed in the inner tissue layers, it was far less effective in overcoming the growth defect.
Furthermore, dwarfism in plants that had mutations in the bri1 gene, which encodes the brassinosteroid receptor BRI1, could be reversed by expressing this gene in the epidermal layer only. This confirmed that the receptor-binding ability of brassinosteroids in the epidermis is important for growth. Nonetheless, although growth recovered in these plants, certain aspects of inner-tissue differentiation that also require brassinosteroid signalling — more specifically, the organization of vascular tissues — did not. Moreover, expression of the bri1 gene only in the vascular layer could not overcome the growth defect.
In an experiment that combined reactivation both of brassinosteroid biosynthesis in the inner tissues and of its receptor-binding ability in the epidermis, the authors confirmed that the inner tissues made only a small contribution to growth. These data convinced Savaldi-Goldstein et al. that the brassinosteroid-mediated pathway in the epidermal tissue can drive growth. But they wondered whether the epidermis was also the tissue responsible for limiting general organ growth under normal conditions. They thus expressed in the various tissue layers a fluorescently tagged enzyme that breaks down brassinosteroids. Consistent with the idea that the epidermis is of major importance for growth, reduced plant stature was particularly obvious when the enzyme was restricted to the epidermis.
These experiments indicate that growth of the epidermal layer in a shoot is crucial for controlling total plant growth. This means that the epidermis must signal to the underlying tissues to keep their growth in step and prevent the plant from being torn apart. The authors therefore investigated how the epidermis might promote the growth of underlying tissues. Plant gene-transcription factors can move through intracellular channels called plasmodesmata. Growth-promoting gene-transcription factors downstream of brassinosteroid signalling have been identified6, and Savaldi-Golstein et al. showed that tagged versions of these factors could overcome the dwarfism associated with mutations in the bri1 gene when expressed in the epidermis. One of these transcription factors (BES1) was able to drive even greater growth than was seen in normal plants.
The authors' experiments using fluorescent tags revealed that these transcription factors relay their growth-promoting effect to the inner tissues without moving from the epidermis; thus, the nature of the growth-promoting signal between the epidermis and the inner layers remains unknown. Is the mobile signal chemical in nature? Or is it mechanical, with the epidermis pulling the inner tissues along? One way of addressing this issue is to elucidate the 'growth machinery' regulated by these hormones. Target-gene analysis of transcription factors such as BES1 should identify which candidates regulate cell expansion in the epidermis and whether these epidermal growth signals influence inner tissues.
Many other questions remain. Do the inner tissues respond only by modulating cell expansion? How does the brassinosteroid growth-control pathway fit in with other mechanisms of growth regulation, for example the regulation of growth repressors such as members of the DELLA family, by various plant growth substances7? Is the brassinosteroid response one pathway among several that affect epidermal growth, as is perhaps suggested by the limited overlap in target genes for the different growth-control pathways8,9? Do the various pathways target different layers? And finally, how does an essential role of the epidermis in growth, as observed by Savaldi-Goldstein and colleagues3, relate to genetic analyses in developing flowers, which suggest that the inner tissue layers dictate the identity and thus the development and growth of organs10,11,12? Perhaps the control of growth involves sequential communication pathways in which the dominance of a layer in one phase of development is followed by dominance of another layer at a later stage. The brassinosteroid pathway dissected by Savaldi-Goldstein et al., together with newly available molecular tools such as fluorescently tagged, functional signal-transduction components, are excellent means to address these questions, and to further our understanding of the integrated control of plant growth.
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Current Opinion in Plant Biology (2019)
Journal of Plant Growth Regulation (2011)
Trends in Plant Science (2010)
Journal of Experimental Botany (2010)
Trends in Plant Science (2008)