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Abstract
Photobody localization of Arabidopsis (Arabidopsis thaliana) phytochrome B (phyB) fused to green fluorescent protein (PBG) correlates closely with the photoinhibition of hypocotyl elongation. However, the amino-terminal half of phyB fused to green fluorescent protein (NGB) is hypersensitive to light despite its inability to localize to photobodies. Therefore, the significance of photobodies in regulating hypocotyl growth remains debatable. Accumulating evidence indicates that under diurnal conditions, photoactivated phyB persists into darkness to inhibit hypocotyl elongation. Here, we examine whether photobodies are involved in inhibiting hypocotyl growth in darkness by comparing the PBG and NGB lines after the red light-to-dark transition. Surprisingly, after the transition from 10 μmol m-2 s-1 red light to darkness, PBG inhibits hypocotyl elongation three times longer than NGB. The disassembly of photobodies in PBG hypocotyl nuclei correlates tightly with the accumulation of the growth-promoting transcription factor PHYTOCHROME-INTERACTING FACTOR3 (PIF3). Destabilizing photobodies by either decreasing the light intensity or adding monochromatic far-red light treatment before the light-to-dark transition leads to faster PIF3 accumulation and a dramatic reduction in the capacity for hypocotyl growth inhibition in PBG. In contrast, NGB is defective in PIF3 degradation, and its hypocotyl growth in the dark is nearly unresponsive to changes in light conditions. Together, our results support the model that photobodies are required for the prolonged, light-dependent inhibition of hypocotyl elongation in the dark by repressing PIF3 accumulation and by stabilizing the far-red light-absorbing form of phyB. Our study suggests that photobody localization patterns of phyB could serve as instructive cues that control light-dependent photomorphogenetic responses in the dark.
Highlights
Photobody localization of Arabidopsis (Arabidopsis thaliana) phytochrome B fused to green fluorescent protein (PBG) correlates closely with the photoinhibition of hypocotyl elongation
A growing body of evidence supports the biological importance of photobodies in the phytochromemediated photoinhibition of hypocotyl growth (Van Buskirk et al, 2012), comparisons between the photobodylocalized phyB fused to GFP (PBG) and nucleoplasm-localized NGB showed that, in the light, NGB is hyperactive in inhibiting hypocotyl growth, suggesting that photobodies are unnecessary and might even play a negative role in the light-dependent inhibition of hypocotyl elongation (Matsushita et al, 2003; Palágyi et al, 2010)
We developed an red light-to-dark (R-to-D) transition assay to examine the relationship between dynamic changes in photobody morphology, the molecular events of PHYTOCHROME-INTERACTING FACTOR3 (PIF3) accumulation, and the expression of phytochrome-interacting factors (PIFs) targets as well as the repression of hypocotyl growth between the PBG and NGB lines
Summary
Photobody localization of Arabidopsis (Arabidopsis thaliana) phytochrome B (phyB) fused to green fluorescent protein (PBG) correlates closely with the photoinhibition of hypocotyl elongation. Our results support the model that photobodies are required for the prolonged, light-dependent inhibition of hypocotyl elongation in the dark by repressing PIF3 accumulation and by stabilizing the far-red light-absorbing form of phyB. In dim R or in light with a low R-to-FR ratio, PBG is localized to many small photobodies or is evenly dispersed in the nucleoplasm, and seedlings are taller (Chen et al, 2003) Together, these results support the idea that the localization of phyB to photobodies correlates tightly with the degree of hypocotyl growth inhibition (Chen et al, 2003). In the extragenic hemera (hmr) mutant, PBG fails to localize to large photobodies and localizes to small photobodies instead; hmr mutants have correspondingly longer hypocotyls than the wild type in R (Chen et al, 2010)
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