Shade-induced nuclear localization of PIF7 is regulated by phosphorylation and 14-3-3 proteins in Arabidopsis

Xu Huang,Qianyue Wang,Chuanwei Yang,Qian Zhang,Lin Li,Yupei Jiang

doi:10.7554/elife.31636

Abstract

Shade avoidance syndrome enables shaded plants to grow and compete effectively against their neighbors. In Arabidopsis, the shade-induced de-phosphorylation of the transcription factor PIF7 (PHYTOCHROME-INTERACTING FACTOR 7) is the key event linking light perception to stem elongation. However, the mechanism through which phosphorylation regulates the activity of PIF7 is unclear. Here, we show that shade light induces the de-phosphorylation and nuclear accumulation of PIF7. Phosphorylation-resistant site mutations in PIF7 result in increased nuclear localization and shade-induced gene expression, and consequently augment hypocotyl elongation. PIF7 interacts with 14-3-3 proteins. Blocking the interaction between PIF7 and 14-3-3 proteins or reducing the expression of 14-3-3 proteins accelerates shade-induced nuclear localization and de-phosphorylation of PIF7, and enhances the shade phenotype. By contrast, the 14-3-3 overexpressing line displays an attenuated shade phenotype. These studies demonstrate a phosphorylation-dependent translocation of PIF7 when plants are in shade and a novel mechanism involving 14-3-3 proteins, mediated by the retention of PIF7 in the cytoplasm that suppresses the shade response.

Highlights

Because chlorophyll preferentially absorbs light in the red and blue ranges but not in the far-red range of the light spectrum, a perceived decrease in the ratio of red/far-red (R/FR) radiation, and in photosynthetically active radiation (PAR) of between 400 and 700 nm, provides a signal that shading by other plants is imminent
In an open environment under sunlight, most of the phytochrome B (phyB) is in the far-red-absorbing (Pfr) active form and moves to the nucleus, where it interacts with basic helix-loop-helix proteins known as PHYTOCHROME-INTERACTING FACTORS (PIFs) (Duek and Fankhauser, 2005; Leivar and Quail, 2011)
Shade treatment resulted in an increase of PIF7 in the nucleus and a decrease of PIF7 in the non-nuclear fraction, indicating that the increased nuclear fraction of PIF7 was probably translocated from the cytoplasmic compartment

Summary

Introduction

Because chlorophyll preferentially absorbs light in the red and blue ranges but not in the far-red range of the light spectrum, a perceived decrease in the ratio of red/far-red (R/FR) radiation, and in photosynthetically active radiation (PAR) of between 400 and 700 nm, provides a signal that shading by other plants is imminent. In the SAS, energy resources are reallocated from storage organs to stem-like organs, including hypocotyls and petioles, thereby enabling plants to initiate a rapid growth response (Cole et al, 2011; Casal, 2012). In an open environment under sunlight (where the ratio of R/FR is about 1.2–1.5), most of the phyB is in the far-red-absorbing (Pfr) active form and moves to the nucleus, where it interacts with basic helix-loop-helix (bHLH) proteins known as PHYTOCHROME-INTERACTING FACTORS (PIFs) (Duek and Fankhauser, 2005; Leivar and Quail, 2011). When plants are in the shade, phyB is mostly in the inactive red-

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