Phytochrome regulates translation of mRNA in the cytosol

Abstract

An array of photoreceptors including cryptochromes, phototropin, and phytochromes regulates various light responses in plants. Among these photoreceptors, phytochromes perceive red and far-red light by switching between two interconvertible spectral forms (Pr and Pfr). The Pfr form promotes light responses partly by destabilizing negatively acting, phytochrome-interacting basic helix-loop-helix transcription factors (PIFs), thus modulating transcription in the nucleus. The Pfr form is also present in the cytosol. However, the role of phytochromes in the cytosol is not well understood. Here we show that the Pfr form interacts with the cytosolic protein PENTA1 (PNT1) and inhibits the translation of protochlorophyllide reductase ( PORA ) mRNA. PNT1 possesses five C3H-type zinc finger domains and displays similarity to various RNA binding proteins including Tristetraprolin, which regulates stabilities of mRNAs such as TNF-α mRNA in humans. Consistent with its function as an RNA binding protein, PNT1 directly binds to mRNA of a key chlorophyll biosynthetic gene, protochlorophyllide reductase in vivo and inhibits the translation of PORA mRNA in the presence of phytochromes. The present results demonstrate that phytochromes transmit light signals to regulate not only transcription in the nucleus through PIFs, but also translation in the cytosol through PNT1.

Phytochrome controls alternative splicing to mediate light responses in Arabidopsis

“…Recently, it has been shown that phytochrome also regulates the translation of protochlorophyllide reductase mRNA by directly interacting with the RNA-binding protein PENTA1 in the cytosol (13). Therefore, phytochrome has emerged as a direct regulator of various aspects of gene expression that interacts with different partners in different subcellular locations.…”

“…Accumulating evidence suggests that light regulates not only transcription but also other aspects of gene expression, such as chromatin reorganization (12), translation (13,14), posttranslational modification (11,15), and pre-mRNA splicing (16)(17)(18). Pre-mRNA splicing is a posttranscriptional event that is carried out by a macromolecular complex called the spliceosome.…”

A Constitutively Active Allele of Phytochrome B Maintains Circadian Robustness in the Absence of Light

“…In the nucleus, YHB acts similarly to the P fr form of phyB by binding PHY-TOCHROME INTERACTING FACTOR (PIF) basic Helix-Loop-Helix (bHLH) transcription factors and targeting them for degradation (for review, see Bae and Choi, 2008). More recently, signaling roles for P fr in the cytoplasm have been reported (Paik et al, 2012;Hughes, 2013). To evaluate the contribution of cytoplasmic P fr signaling into the circadian system, we introduced the G767R mutation into the YHB allele (YHB-G767R).…”

PHYTOCHROME INTERACTING FACTOR1 Enhances the E3 Ligase Activity of CONSTITUTIVE PHOTOMORPHOGENIC1 to Synergistically Repress Photomorphogenesis in Arabidopsis

“…Within the nucleus, the activated Pfr physically interacts with multiple proteins, including a small group of basic helix-loop-helix (bHLH) transcription factors called Phytochrome Interacting Factors (PIFs; PIF1 and PIF3 to PIF8) (Quail, 2000;Quail, 2002, 2005;Huq et al, 2004;Duek and Fankhauser, 2005;M. Chen et al, 2010;Galvão et al, 2012;Paik et al, 2012). PIFs constitutively accumulate in the nucleus in the dark and inhibit photomorphogenesis (Castillon et al, 2007;Henriques et al, 2009;Leivar and Quail, 2011).…”