Trends in Cell Biology
ReviewPhytohormone collaboration: zooming in on auxin–brassinosteroid interactions
Introduction
In multicellular organisms, hormones transmit signals within the body, for instance to integrate physiological processes or trigger developmental decisions. Peptides, in addition to small organic molecules, have been identified as hormones in animals. In plants, the classic hormones are small organic compounds called phytohormones [1]. Notably, for most phytohormones, the separation between the tissues of hormone biosynthesis and hormone action typical for animal hormones is less sharp. Generally, phytohormones seem to function mainly in the growth and development of the tissue in which they are produced. Thus, phytohormones are often referred to as plant growth regulators, highlighting their ability to regulate growth through modulation of either cell size or cell division. For instance, gibberellic acid typically promotes cell elongation, whereas cytokinin is a crucial regulator of cell division. Here, we focus on two phytohormones, auxin and brassinosteroid (BR), which are essential for both cell elongation and cell proliferation. This similarity was a first hint towards possibly redundant or synergistic roles of auxin and BR in development, a notion which is increasingly supported by recent molecular genetic analyses, mainly in the model plant Arabidopsis thaliana. Here, we review the emerging evidence for direct molecular interactions between the two pathways.
Section snippets
The auxin and BR signal transduction pathways
A distinct feature that sets auxin apart from other phytohormones is the fact that it is highly mobile because it can be transported through the plant body by specialized molecular machinery. This regulated and directional transport is called polar auxin transport (PAT). Although other phytohormones, including BR, might well be mobile within a certain range from their site of production 2, 3, specialized transport systems for other phytohormones have not been found so far. The importance of PAT
Auxin–BR interaction in physiological assays of cell elongation
Although auxin was the first classical phytohormone to be discovered, BR is the most recently identified one. Early work on BR focused on the effects of external hormone application in different developmental contexts. These experiments quickly revealed a similarity in responses triggered by BR with those triggered by auxin [12] (Figure 2). This was particularly evident in physiological assays of cell elongation, which is promoted by application of low to moderate concentrations of either
Cellular responses to auxin and BR
A downstream effect of auxin and BR in modulating cell elongation might be rearrangement of the cytoskeleton. Plant cells are surrounded by a cell wall, whose elasticity limits their turgor-driven expansion. The ordered arrangement of cellulose fibrils is a central feature of the cell wall, which determines the direction of cell expansion. For instance, in hypocotyl cells, the fibrils are arranged in parallel circles perpendicular to the apical–basal axis of the cell, favoring elongation along
BR, auxin and cell proliferation
Although the effects of BR on cell elongation became evident soon after its discovery, its role in cell proliferation was more difficult to prove. For instance, analyses of BR biosynthesis mutants confirmed BR requirement for cell elongation but did not immediately support a role in cell proliferation 14, 20, 21. However, these studies focused on hypocotyl growth, in which the effects of BR on cell proliferation are possibly obscured by the fact that wild-type hypocotyls grow nearly exclusively
Conflicting data on auxin–BR physiology
In summary, although clear evidence for a synergistic auxin–BR interaction in cell proliferation is missing, a synergistic interaction in cell elongation has been observed in multiple assays and several species. However, although there is little doubt that both hormones are needed for cell elongation per se in hypocotyl and root 13, 14, 20, 21, 24, 27, 28, 29, 30, auxin–BR interaction in tropisms remains controversial. Some studies suggest synergistic action in this context 31, 32, 33, whereas
Auxin–BR interaction in modulating gene expression
The notion that auxin- and BR-induced gene expression changes might overlap dates back several years, when it was noticed that some transcriptional auxin targets are also BR inducible [13]. These targets, members of the SMALL AUXIN UP-REGULATED (SAUR) and AUX/IAA gene families 37, 38, typically react strongly to auxin and more weakly to BR. Isolation of BR signaling and biosynthesis mutants enabled expression analysis of those genes in mutant backgrounds, confirming that their correct
Possible auxin–BR connections in hormone biosynthesis
A straightforward route of hormone pathway interaction would be modulation of the biosynthesis of one hormone by the other, which has been observed repeatedly. For example, both auxin and BR promote ethylene biosynthesis [14]. In many instances, such as microtubule rearrangement or tropisms, ethylene can even largely replace auxin or BR [17]. Expression data suggest that ethylene levels are synergistically regulated by auxin and BR through transcriptional control of rate-limiting enzymes in
BR effects on polar auxin transport
Another connection between the auxin and BR pathways is suggested by reports of BR effects on PAT 32, 48. These observations correlate with the finding that the expression of PIN-FORMED (PIN) genes, which encode auxin efflux carriers that are crucial for the rate and direction of PAT, is partly controlled by BR 30, 32, 53. Moreover, BR modulates the localization of a PIN protein that is implicated in tropisms [32]. Collectively, these data suggest that PAT is enhanced by BR, although it remains
The calmodulin (CaM) connection – an upstream link between the auxin and BR pathways?
Interactions of a PAT modulator, the PINOID (PID) protein, point to a molecular link that could mediate communication between the auxin and BR pathways upstream of the TFs. PID activity regulates PAT direction by influencing the localization of PIN proteins [55]. Formally, PID can be considered as an auxin-signaling component because it is a serine/threonine kinase (S/T kinase) [56]. It seems possible, however, that PID directly modulates the PAT machinery because developmental defects
Conclusions
Recent years have witnessed increasing interest in auxin–BR pathway interactions, motivated by physiological observations that date back as far as 25 years. Using genomic tools combined with mutant analyses, the auxin–BR interaction has been substantiated at the molecular level, providing evidence for convergence of the two hormone pathways, at least at the level of common target gene promoters. Upstream connections between the two pathways also possibly exist – for instance, through
Acknowledgements
We thank the Swiss National Foundation and the Canton de Vaud for supporting the research in our laboratory. C.S.H. and K.S.O. also acknowledge support by a Marie-Curie post-doctoral fellowship awarded to K.S.O.
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