Date Published: September 24, 2004
Publisher: Public Library of Science
Author(s): Jennifer L Nemhauser, Todd C Mockler, Joanne Chory
Abstract: How growth regulators provoke context-specific signals is a fundamental question in developmental biology. In plants, both auxin and brassinosteroids (BRs) promote cell expansion, and it was thought that they activated this process through independent mechanisms. In this work, we describe a shared auxin:BR pathway required for seedling growth. Genetic, physiological, and genomic analyses demonstrate that response from one pathway requires the function of the other, and that this interdependence does not act at the level of hormone biosynthetic control. Increased auxin levels saturate the BR-stimulated growth response and greatly reduce BR effects on gene expression. Integration of these two pathways is downstream from BES1 and Aux/IAA proteins, the last known regulatory factors acting downstream of each hormone, and is likely to occur directly on the promoters of auxin:BR target genes. We have developed a new approach to identify potential regulatory elements acting in each hormone pathway, as well as in the shared auxin:BR pathway. We show that one element highly overrepresented in the promoters of auxin- and BR-induced genes is responsive to both hormones and requires BR biosynthesis for normal expression. This work fundamentally alters our view of BR and auxin signaling and describes a powerful new approach to identify regulatory elements required for response to specific stimuli.
Partial Text: The continuous shaping of plant form is a marvel of signal integration. In early seedling development this is particularly clear, as environmental cues, such as light, profoundly alter the innate morphogenetic program. How diverse pathways merge to determine a discrete cellular growth response is largely unknown. Auxin, the first plant hormone identified, has been implicated in patterning or growth of virtually every plant tissue from earliest embryo to developing fruit (Liscum and Reed 2002). Brassinosteroids (BRs), the polyhydroxylated steroid hormones of plants, have been linked to many of these same processes, including photomorphogenesis (Clouse 2002). The nature of the relationship between these hormones has remained largely undefined.
With the notable exception of auxin, most plant hormones are produced and perceived throughout the plant body. Modulation of hormone response stems from regulation of hormone levels and/or signal transduction components, as well as from interactions with other signaling pathways. There are many examples of cross-talk between hormones in plant biology. In addition to auxin and BRs, gibberellins (GAs), ethylene, ABA, and cytokinin have all been shown to affect hypocotyl elongation (reviewed in Nemhauser and Chory 2002). As mentioned previously, some of these hormones interact through biosynthetic regulation. For example, auxin, ABA, and cytokinin stimulate ethylene biosynthesis, particularly when supplied at high levels (Yang and Hoffman 1984; Vogel et al. 1998; Ghassemian et al. 2000). Physiological and genetic evidence suggests that auxin, GAs, and ethylene promote hypocotyl growth by largely independent means (Gray et al. 1998; Collett et al. 2000). Similarly, BRs and GAs interact additively in most cell elongation bioassays (Mandava et al. 1981), and analysis of bri1 mutants suggests that the two hormones independently and antagonistically regulate transcription of some target genes (Bouquin et al. 2001). In contrast, auxin and BRs interact synergistically and interdependently to promote hypocotyl cell elongation, making their relationship unique among plant growth regulators.