Anionic lipids stabilize etioplast prolamellar bodies and facilitate thylakoid biogenesis during etioplast-to-chloroplast differentiation

Abstract

Etioplasts of dark-grown angiosperm seedlings contain prolamellar bodies (PLBs), lattice-like membranes that are quickly transformed into thylakoids upon illumination. Phosphatidylglycerol (PG) and sulfoquinovosyldiacylglycerol (SQDG) are major anionic lipids in these membranes, but their roles in etioplast-to-chloroplast differentiation remain unclear. We analyzed Arabidopsis thaliana mutants with reduced PG biosynthesis (pgp1-1), complete SQDG deficiency (sqd1), and the pgp1-1 sqd1 double mutant. Although pgp1-1 etioplasts showed a loosened PLB lattice when fixed under white light, they retained regular, wild-type-like lattices when fixed under infrared light, suggesting that their PLBs were more susceptible to light-induced disassembly. The rapid PLB disassembly in pgp1-1 upon illumination was accompanied by rapid conversion of dark-accumulated protochlorophyllide to chlorophyll and lamellar membrane formation, suggesting a link between membrane remodeling and chlorophyll formation. However, subsequent chlorophyll accumulation through de novo biosynthesis was retarded in illuminated pgp1-1 seedlings, whereas photosynthetic electron transport was quickly activated. Although sqd1 showed no obvious defects, pgp1-1 sqd1 exhibited more severe defects than pgp1-1, particularly in internal membrane formation, chlorophyll accumulation, photosynthetic activation, and photosynthetic gene expression. These findings suggest that PG is crucial for membrane-associated processes during etioplast-to-chloroplast differentiation, while SQDG may help maintain chloroplast development when PG availability is limited.