VESICLE-INDUCING PROTEIN IN PLASTIDS 1 from thylakoid-lacking Gloeobacter promotes thylakoid formation in Arabidopsis

Abstract The thylakoid membrane (TM) is a specialized structure present in most oxygen-evolving photosynthetic cyanobacteria and chloroplasts. VESICLE-INDUCING PROTEINS IN PLASTIDS 1 (VIPP1) is a key protein involved in TM biogenesis, shaping, and maintenance. VIPP1 originated from PspA and over time has specialized to the TM, which likely coevolved with the emergence of the C-terminal tail (Vc) present in VIPP1 but not in PspA. To characterize Vc, we performed a bioinformatic analysis of the PspA/VIPP1 proteins. All Vc regions varied in length and exhibited intrinsically disordered characteristics. More importantly, Vc was shown to exist in Archaea and anoxygenic bacteria, as well as in cyanobacteria, indicating that Vc emerged from ancestral PspA multiple times during evolution. A detailed classification of Vc-containing bacteria suggested that Vc may have emerged in harsh environments to protect early bacteria thriving in their natural habitats. Subsequently, we focused on VIPP1 from Gloeobacter (GviVIPP1), a common ancestor cyanobacterium that performs oxygenic photosynthesis but lacks a TM. Heterologous complementation of the Arabidopsis (Arabidopsis thaliana) vipp1 mutant with chloroplast-targeted GviVIPP1 showed that GviVIPP1 has the capacity to construct a functional TM, a process that is Vc-dependent. Visualization of GviVIPP1-GFP showed that Vc regulates oligomer formation dynamics, similar to Arabidopsis VIPP1. Together, our results reinforce the important role of Vc in VIPP1, which involves negatively regulating VIPP1 complex assembly to assist TM formation.