Interdependency of Brassinosteroid and Auxin Signaling in Arabidopsis

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.

Inhibition of Brassinosteroid Biosynthesis by Either a dwarf4 Mutation or a Brassinosteroid Biosynthesis Inhibitor Rescues Defects in Tropic Responses of Hypocotyls in the Arabidopsis Mutant nonphototropic hypocotyl 4

“…YUCCA is overexpressed by the cauliflower mosaic virus 35S enhancer in the yucca mutant, in which an increase in the auxin level causes long hypocotyls in the light condition (Zhao et al, 2001). Hypocotyls of yucca bri1 double mutants are as short as those of bri1 in the light condition, showing that BR insensitivity is epistatic to auxin action (Nemhauser et al, 2004).…”

“…Genes responsive to both auxin and BL include those of early auxin-responsive gene families, such as AUX/IAA, SAUR, and GH3, and a putative transcriptional regulator for tropic responses, MSG2/IAA19 (Tatematsu et al, 2004), also responds to both auxin and BL (Nakamura et al, 2003a). The expression of several genes was found to be synergistically promoted by auxin and BL (Nakamura et al, 2003b;Nemhauser et al, 2004). Furthermore, the TGTCTC auxin response element is more enriched in the 5#-flanking region of genes up-regulated by both IAA and BL than those up-regulated specifically by auxin (Goda et al, 2004).…”

“…Seventeen to 25% of the auxin-induced genes are also activated by BL in microarray analyses (Goda et al, 2004;Nemhauser et al, 2004). Genes responsive to both auxin and BL include those of early auxin-responsive gene families, such as AUX/IAA, SAUR, and GH3, and a putative transcriptional regulator for tropic responses, MSG2/IAA19 (Tatematsu et al, 2004), also responds to both auxin and BL (Nakamura et al, 2003a).…”

The Arabidopsis transcription factor bZIP11 activates auxin-mediated transcription by recruiting the histone acetylation machinery

“…Several biased and unbiased bioinformatic approaches have revealed that GREs, which are preferred binding sites for plant bZIP TFs, are significantly enriched in auxin-responsive promoters and are preferentially located in close vicinity to AuxREs 35,52,53 . Although GREs by themselves are not sufficient to mediate auxin responsiveness, this work demonstrates that GREs cooperate with AuxREs and that they significantly enhance auxin-mediated transcription in an auxin concentrationdependent manner.…”

The brassinosteroid signal transduction pathway

“…In this case, BES1 was shown to interact with three homologous basic-helix-loop-helix (bHLH) transcription factors (BIM1-3) in yeast two-hybrid assays [45]. Gel shift assays demonstrated that BES1 could bind to the E-box (CANNTG) elements in the promoter of SAUR-AC1, a gene showing early induction by both BR and auxin [56,57]. The BIM1 protein was also shown to bind the same E-box, and synergism between BES1 and BIM1 was observed for both DNA binding in vitro and activation of SAUR-AC1 promoter in transient assays.…”