A molecular framework for light and gibberellin control of cell elongation

Abstract

Cell elongation during seedling development is antagonistically regulated by light and gibberellins (GAs) 1,2 . Light induces photomorphogenesis, leading to inhibition of hypocotyl growth, whereas GAs promote etiolated growth, characterized by increased hypocotyl elongation. The mechanism underlying this antagonistic interaction remains unclear. Here we report on the central role of the Arabidopsis thaliana nuclear transcription factor PIF4 (encoded by PHYTOCHROME INTERACTING FACTOR 4) 3 in the positive control of genes mediating cell elongation and show that this factor is negatively regulated by the light photoreceptor phyB (ref. 4) and by DELLA proteins that have a key repressor function in GA signalling 5 . Our results demonstrate that PIF4 is destabilized by phyB in the light and that DELLAs block PIF4 transcriptional activity by binding the DNA-recognition domain of this factor. We show that GAs abrogate such repression by promoting DELLA destabilization, and therefore cause a concomitant accumulation of free PIF4 in the nucleus. Consistent with this model, intermediate hypocotyl lengths were observed in transgenic plants over-accumulating both DELLAs and PIF4. Destabilization of this factor by phyB, together with its inactivation by DELLAs, constitutes a protein interaction framework that explains how plants integrate both light and GA signals to optimize growth and development in response to changing environments.Seedlings undergo alternative developmental programmes depending on whether they are germinated in the dark or in the light. Dark-grown seedlings exhibit etiolated growth, characterized by long hypocotyls, small and closed cotyledons with undifferentiated chloroplasts, and the repression of light-regulated genes 1 . During photomorphogenesis, light inhibits hypocotyl growth and promotes cotyledon opening and expansion, chloroplast differentiation and the activation of light-regulated genes. phyB is the main photoreceptor mediating de-etiolation in red light 4,6 . Absorption of red light converts this photoreceptor into a Pfr active form that is translocated into the nucleus 7,8 ; Pfr interacts there with members of the bHLH family of phytochrome-interacting factors (PIFs), involved in modulation of light-regulated genes with a role in photomorphogenesis 1,4 . Gibberellins (GAs) exert an opposite effect to light on photomorphogenesis 2 . GAs promote etiolated growth, whereas GA-deficiency induces a partially de-etiolated phenotype in the dark, which is reverted by a lack of DELLA function 2,9 . DELLAs function as key repressors of GA-responsive growth, by inhibiting GA-regulated gene expression 5 . These repressors accumulate in the nucleus and are rapidly degraded in response to GA 10,11 . In Arabidopsis, RGA (encoded by repressor of ga1-3) and GAI (encoded by GA insensitive) are the main repressors controlling hypocotyl growth and stem elongation 12,13 . Mutations within the DELLA domain render these proteins resistant to degradation, and result in a GA-insensitive dwarf phenotype 12,14 . This ...

The Energy-Signaling Hub SnRK1 Is Important for Sucrose-Induced Hypocotyl Elongation

“…Auxin, GA, and brassinosteroids are reported to mediate Suc-induced hypocotyl elongation, with a role for auxin identified under light/dark cycles and roles for GA and brassinosteroids identified under extended darkness (de Lucas et al, 2008;Zhang et al, 2010Zhang et al, , 2015Zhang et al, , 2016Liu et al, 2011;Stewart et al, 2011;Lilley et al, 2012;). Consistent with this, our data indicate that auxin signaling has a major role in Suc-induced hypocotyl elongation under light/dark cycles (Fig.…”

The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROME-INTERACTING FACTORS

“…PIFs thus integrate light and GA signals to control developmental responses. The inhibitory role of DELLA proteins in the regulation of PIFs is particularly prominent in the dark, when phytochromes are inactive, and during the transition from skotomorphogenic to photomorphogenic seedling growth, when DELLA protein levels increase due to decreasing GA levels and reduced DELLA protein turnover (Alabadi et al 2008;de Lucas et al 2008;Feng et al 2008).…”

“…DELLA proteins repress GA responses, at least in part, by interfering with the DNA-binding activity of PHYTO-CHROME-INTERACTING FACTOR (PIF) basic helixloop-helix (bHLH) transcription factors (de Lucas et al 2008;Feng et al 2008). In Arabidopsis, PIFs constitute a multiprotein family with seven members, and the developmental roles of individual PIFs in isolation and in combination with other PIF family members have been elucidated in recent years; e.g., through the analysis of a pif1 pif3 pif4 pif5 quadruple mutant (Castillon et al 2007;Leivar et al 2008).…”

Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis

“…The GA effect on flowering is genetically mediated by five DELLA proteins, GIBBERELLIC ACID INSENSITIVE (GAI), REPRESSOR OF ga1-3 (RGA), RGA-LIKE1 (RGL1), RGL2 and RGL3, which are key GA signalling repressors whose degradation is triggered by GA 22,23 . As transcriptional regulators, DELLA proteins have been shown to exert their function by recruiting other transcription factors rather than directly binding to their target genes [24][25][26][27] .…”