VIPP2 interacts with VIPP1 and HSP22E/F at chloroplast membranes and modulates a retrograde signal for HSP22E/F gene expression

Abstract

VIPP proteins aid thylakoid biogenesis and membrane maintenance in cyanobacteria, algae, and plants. Some members of the Chlorophyceae contain two VIPP paralogs termed VIPP1 and VIPP2, which originate from an early gene duplication event during the evolution of green algae. VIPP2 is barely expressed under nonstress conditions but accumulates in cells exposed to high light intensities or H 2 O 2 , during recovery from heat stress, and in mutants with defective integration (alb3.1) or translocation (secA) of thylakoid membrane proteins. Recombinant VIPP2 forms rod-like structures in vitro and shows a strong affinity for phosphatidylinositol phosphate.Under stress conditions, >70% of VIPP2 is present in membrane fractions and localizes to chloroplast membranes. A vipp2 knock-out mutant displays no growth phenotypes and no defects in the biogenesis or repair of photosystem II. However, after exposure to high light intensities, the vipp2 mutant accumulates less HSP22E/F and more LHCSR3 protein and transcript. This suggests that VIPP2 modulates a retrograde signal for the expression of nuclear genes HSP22E/F and LHCSR3. Immunoprecipitation of VIPP2 from solubilized cells and membrane-enriched fractions revealed major interactions with VIPP1 and minor interactions with HSP22E/F. Our data support a distinct role of VIPP2 in sensing and coping with chloroplast membrane stress.

Acclimation in plants – the Green Hub consortium

“…Stressed Arabidopsis chloroplasts can also signal to the nucleus via the endoplasmic reticulum (ER) through the unfolded protein response (UPR) (Walley et al ., 2015), or the UPR‐like response, during which chloroplast proteins engaged in protein quality control accumulate (Dogra et al ., 2019). We have recently unravelled a chloroplast unfolded membrane protein response in C. reinhardtii which involves chloroplast vesicle‐inducing protein in plastids 1 (VIPP1) and VIPP2, together with the small heat shock proteins HSP22E and F (Theis et al ., 2020). In chloroplasts challenged with high light or H 2 O 2 , VIPP2, VIPP1 (Table 2) and HSP22E/F bind to chloroplast membranes presumably suffering from lipid packing stress caused by accumulation of misfolded proteins (Figure 3).…”

PspA adopts an ESCRT-III-like fold and remodels bacterial membranes

“…EcoPspA was found to form large, homo-oligomeric rings in solution with outer diameters of ~20 nm and a molecular mass of about 1 MDa (Hankamer et al, 2004), as well as higher-order rod structures (Male et al, 2014). Similarly, the PspA homologous proteins LiaH and IM30 form rings (Aseeva et al, 2004;Fuhrmann et al, 2009;Saur et al, 2017;Wolf et al, 2010), while IM30 also forms rod structures (Fuhrmann et al, 2009;Theis et al, 2019Theis et al, , 2020Vothknecht et al, 2012). In addition to the shared property to form large homo-oligomeric structures, the predicted secondary structure and some sequence motifs of PspA/LiaH/IM30 are conserved (Bultema et al, 2010;Thurotte et al, 2017;Vothknecht et al, 2012).…”

Phosphoinositides regulate chloroplast processes

“…On the one hand, the work by Hertle et al (12) undoubtedly will launch a quest for PI-related effector proteins involved in chloroplast vesicle traffic. On the other hand, their work underpins the existence of PI signaling in chloroplasts, which was implied by the presence of 2 to 3% PtdIns in chloroplast envelope and thylakoid membranes (13) and the identification of chloroplast PIbinding proteins WKS1 (14), VIPP1 (15), and VIPP2 (16).…”

“…VIPP proteins can oligomerize into rings and rods (18,19) and bind to membranes via an N-terminal amphipathic α-helical domain (20). Chlamydomonas chloroplast VIPP1 and its paralog VIPP2 bind to PIs and VIPP1 rods can engulf PI-containing liposomes in vitro (15,16). Since cyanobacteria possess neither PtdIns (21) nor Sec14-like proteins (12), the adaptation of VIPP1 to PI signaling appears to have evolved during domestication of the cyanobacterial endosymbiont.…”

“…1). VIPP2 plays a role in the sensing and signaling of membrane packing stress induced by lipid peroxidation or misfolded/aggregated proteins (16) (Fig. 1).…”