Abstract
Light is essential for plant organogenesis and development. Light-regulated shoot morphogenesis has been extensively studied; however, the mechanisms by which plant roots perceive and respond to aboveground light are largely unknown, particularly because the roots of most terrestrial plants are usually located underground in darkness. To mimic natural root growth conditions, we developed a root-covered system (RCS) in which the shoots were illuminated and the plant roots could be either exposed to light or cultivated in darkness. Using the RCS, we observed that root growth of wild-type plants was significantly promoted when the roots were in darkness, whereas it was inhibited by direct light exposure. This growth change seems to be regulated by ELONGATED HYPOCOTYL 5 (HY5), a master regulator of photomorphogenesis. Light was found to regulate HY5 expression in the roots, while a HY5 deficiency partially abolished the inhibition of growth in roots directly exposed to light, suggesting that HY5 expression is induced by direct light exposure and inhibits root growth. However, no differences in HY5 expression were observed between illuminated and dark-grown cop1 roots, indicating that HY5 may be regulated by COP1-mediated proteasome degradation. We confirmed the crucial role of HY5 in regulating root development in response to light under soil-grown conditions. A transcriptomic analysis revealed that light controls the expression of numerous genes involved in phytohormone signaling, stress adaptation, and metabolic processes in a HY5-dependent manner. In combination with the results of the flavonol quantification and exogenous quercetin application, these findings suggested that HY5 regulates the root response to light through a complex network that integrates flavonol biosynthesis and reactive oxygen species signaling. Collectively, our results indicate that HY5 is a master regulator of root photomorphogenesis.
Highlights
Root system architecture (RSA) is vital for plant fitness, crop performance, and plant productivity, and its development is regulated by both genetic components and environmental factors (Jansen et al, 2013; Rogers and Benfey, 2015; Li et al, 2018a; Xiao et al, 2018)
Plant biologists have been growing Arabidopsis seedlings on transparent Petri dishes with the roots exposed to light, an approach we designated as a traditional culture system (TCS)
Using a TCS, plant roots that would naturally grow in darkness were instead exposed to light (Figures S1A, B), which is controversial in the field of root research (Xu et al, 2013; Yokawa et al, 2013; Mo et al, 2015)
Summary
Root system architecture (RSA) is vital for plant fitness, crop performance, and plant productivity, and its development is regulated by both genetic components and environmental factors (Jansen et al, 2013; Rogers and Benfey, 2015; Li et al, 2018a; Xiao et al, 2018). The genes encoding photoreceptors are expressed in the roots, enabling them to detect ambient light and trigger downstream responses that mediate root tropism and elongation in the soil (Galen et al, 2007; Salisbury et al, 2007; Mo et al, 2015; Van Gelderen et al, 2018b). The RING E3 ubiquitin ligase CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1), a major integrator of light responses, ubiquitinates two downstream transcription factors, ELONGATED HYPOCOTYL 5 (HY5) and HY5 HOMOLOG (HYH), to mediate their degradation (Ang et al, 1998; Osterlund et al, 2000; Holm et al, 2002). The expression levels of HY5 and HYH are upregulated by light in the seedlings (Osterlund et al, 2000; Holm et al, 2002; Singh et al, 2012)
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