The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser.

Elin Claesson,Eriko Nango,Keith Moffat,Joachim Kübel,Melissa Carrillo,Gerrit Groenhof,Robert Bosman,So Iwata,Leticia Castillon,Weixiao Yuan Wahlgren,Valentyna Kuznetsova,Léocadie Henry,Marius Schmidt,Linnéa Isaksson,Andrea Cellini,Rahul Nanekar,Michał Maj,Suraj Pandey,Dmitry Morozov,Heikki Takala,Shigeki Owada,Amke Nimmrich,Moona Kurttila,Rie Tanaka,Luo Fangjia,Sebastian Westenhoff,Tomoyuki Tanaka,Emina A Stojković ,Matthijs R Panman ,Janne A Ihalainen

doi:10.7554/elife.53514

Abstract

Phytochrome proteins control the growth, reproduction, and photosynthesis of plants, fungi, and bacteria. Light is detected by a bilin cofactor, but it remains elusive how this leads to activation of the protein through structural changes. We present serial femtosecond X-ray crystallographic data of the chromophore-binding domains of a bacterial phytochrome at delay times of 1 ps and 10 ps after photoexcitation. The data reveal a twist of the D-ring, which leads to partial detachment of the chromophore from the protein. Unexpectedly, the conserved so-called pyrrole water is photodissociated from the chromophore, concomitant with movement of the A-ring and a key signaling aspartate. The changes are wired together by ultrafast backbone and water movements around the chromophore, channeling them into signal transduction towards the output domains. We suggest that the observed collective changes are important for the phytochrome photoresponse, explaining the earliest steps of how plants, fungi and bacteria sense red light.

Highlights

Phytochrome photosensor proteins are crucial for the optimal development of all vegetation on Earth (Butler et al, 1959; Gan et al, 2014; Quail et al, 1995)
Phytochrome proteins change shape when they are exposed to red light, and this change alters the behaviour of the cell
The red light is absorbed by a molecule known as chromophore, which is connected to a region of the phytochrome called the PHY-tongue

Summary

Introduction

Phytochrome photosensor proteins are crucial for the optimal development of all vegetation on Earth (Butler et al, 1959; Gan et al, 2014; Quail et al, 1995). Prototypical phytochromes can exist in two photochemical states with differential cellular signaling activity, called red light-absorbing (Pr) and far-red light-absorbing (Pfr) state (Figure 1—figure supplement 1). To detect the level of light, plant cells use proteins called phytochromes, which are found in some bacteria and fungi. Phytochrome proteins change shape when they are exposed to red light, and this change alters the behaviour of the cell. The red light is absorbed by a molecule known as chromophore, which is connected to a region of the phytochrome called the PHY-tongue. This region undergoes one of the key structural changes that occur when the phytochrome protein absorbs light, turning from a flat sheet into a helix

Methods

Results

Conclusion