Opposite Root Growth Phenotypes of hy5 versus hy5 hyh Mutants Correlate with Increased Constitutive Auxin Signaling

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Abstract
The Arabidopsis transcription factor HY5 controls light-induced gene expression downstream of photoreceptors and plays an important role in the switch of seedling shoots from dark-adapted to light-adapted development. In addition, HY5 has been implicated in plant hormone signaling, accounting for the accelerated root system growth phenotype of hy5 mutants. Mutants in the close HY5 homolog HYH resemble wild-type, despite the largely similar expression patterns and levels of HY5 and HYH, and the functional equivalence of the respective proteins. Moreover, the relative contribution of HYH to the overall activity of the gene pair is increased by an alternative HYH transcript, which encodes a stabilized protein. Consistent with the enhanced root system growth observed in hy5 loss-of-function mutants, constitutively overexpressed alternative HYH inhibits root system growth. Paradoxically, however, in double mutants carrying hy5 and hyh null alleles, the hy5 root growth phenotype is suppressed rather than enhanced. Even more surprisingly, compared to wild-type, root system growth is diminished in hy5 hyh double mutants. In addition, the double mutants display novel shoot phenotypes that are absent from either single mutant. These include cotyledon fusions and defective vasculature, which are typical for mutants in genes involved in the transcriptional response to the plant hormone auxin. Indeed, many auxin-responsive and auxin signaling genes are misexpressed in hy5 mutants, and at a higher number and magnitude in hy5 hyh mutants. Therefore, auxin-induced transcription is constitutively activated at different levels in the two mutant backgrounds. Our data support the hypothesis that the opposite root system phenotypes of hy5 single and hy5 hyh double mutants represent the morphological response to a quantitative gradient in the same molecular process, that is gradually increased constitutive auxin signaling. The data also suggest that HY5 and HYH are important negative regulators of auxin signaling amplitude in embryogenesis and seedling development. Genetic redundancy is the total or partial compensation of inactivation of one gene by another, usually related gene. In Arabidopsis, HY5 and HYH are highly similar, principally exchangeable genes. However, only inactivation of HY5 results in morphological defects, indicating that HY5 plays a more important role in development than HYH. Nevertheless, if inactive versions of such partially redundant genes are combined in a double mutant, the defects observed in the single mutant often worsen. Paradoxically, however, combined inactivation of HY5 and HYH leads to a defect that is opposite to inactivation of HY5 alone: compared to controls, root system growth is decreased in the double mutant, rather than enhanced as in plants only lacking HY5 activity. Through careful analysis of the double mutant defects and scans of genome-wide gene expression levels, the authors determined that the opposite root system growth of hy5 single and hy5 hyh double mutants is a morphological response to a gradually increased quantitative disturbance in the same molecular process, the physiological response to the plant hormone auxin. This example suggests that inactivation of genes that quantitatively affect the balance of a physiological process in the same manner might manifest in very different morphological changes.