An actin nucleation factor in plants
Kong et al. explore how phototropins regulate actin filaments associated with chloroplasts and unveil CHUP1 as a type of actin nucleator.
https://doi.org/10.1093/plcell/koad320
Sam-Geun Kong
Kongju National University, Gongju Korea
Background: Chloroplasts dynamically adjust their intracellular positioning in response to the intensity and direction of light, mediating the accumulation response, which optimizes photosynthesis under weak light conditions, and the avoidance response, which mitigates photodamage under strong light conditions. The blue light photoreceptors, phototropin1 and 2, redundantly mediate these responses—both phot1 and phot2 contribute to the accumulation response, while phot2 alone governs the avoidance response. Specifically, short actin filaments associated with chloroplasts, referred to as cp-actin filaments, facilitate chloroplast movement through asymmetrical reorganizations at the front side of moving chloroplasts, specifically in the space between the chloroplast and plasma membrane. CHLOROPLAST UNUSUAL POSITIONING 1 (CHUP1) regulates the cp-actin filaments.
Question: How do phototropins regulate cp-actin filaments, and what role does CHUP1 play in the regulation of cp-actin filaments?
Findings: Using a comprehensive approach that includes cell biology, X-ray crystallography, biochemistry, electron microscopy, and plant physiology, our study reveals CHUP1 as a type of actin nucleator controlling chloroplast movement. Noteworthy discoveries include CHUP1’s pivotal role in polymerizing cp-actin filaments under weak light and depolymerizing them under strong light, in a blue light- and phototropin-dependent manner. Notably, the C-terminal half of CHUP1 (CHUP1-C) exhibits structural similarity to the formin FH-2 domain, despite lacking amino acid sequence homology. Furthermore, CHUP1-C’s ability to promote actin polymerization when complexed with profilin in vitro implies that CHUP1 evolved independently as a plant-specific actin nucleator for chloroplast movement.
Next steps: Our present model relies on actin polymerization as the motive force for chloroplast movements. The coordinated rearrangement of cp-actin filaments at the leading edge of moving chloroplasts is governed by the asymmetric distribution of CHUP1. However, the mechanism by which CHUP1 and cp-actin filaments are aligned in one direction and their collective contribution to the motive force of chloroplast relocation remain to be elucidated.
Reference:
Sam-Geun Kong, Yosuke Yamazaki, Atsushi Shimada, Saku T. Kijima, Keiko Hirose, Kaoru Katoh, Jeongsu Ahn, Hyun-Geun Song, Jae-Woo Han, Takeshi Higa, Akira Takano, Yuki Nakamura, Noriyuki Suetsugu, Daisuke Kohda, Taro Q. P. Uyeda, and Masamitsu Wada. (2024). CHLOROPLAST UNUSUAL POSITIONING 1 is a plant-specific actin polymerization factor regulating chloroplast movement. https://doi.org/10.1093/plcell/koad320
