Abstract
Thylakoid membranes isolated from leaves of two plant species, the chilling tolerant (CT) pea and chilling sensitive (CS) runner bean, were assessed for the composition of lipids, carotenoids as well as for the arrangement of photosynthetic complexes. The response to stress conditions was investigated in dark-chilled and subsequently photo-activated detached leaves of pea and bean. Thylakoids of both species have a similar level of monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), but different sulfoquinovosyldiacylglycerol to phosphatidylglycerol (PG) ratio. In pea thylakoid fraction, the MGDG, DGDG and PG, have a higher double bond index (DBI), whereas bean thylakoids contain higher levels of high melting point PG. Furthermore, the lutein to the β-carotene ratio is higher in bean thylakoids. Smaller protein/lipid ratio in pea than in bean thylakoids suggests different lipid-protein interactions in both species. The differences between species are also reflected by the course of temperature-dependent plots of chlorophyll fluorescence pointing various temperatures of the lipid phase transitions of pea and bean thylakoids. Our results showed higher fluidity of the thylakoid membrane network in pea than in bean in optimal temperature conditions. Dark-chilling decreases the photochemical activity and induces significant degradation of MGDG in bean but not in pea leaves. Similarly, substantial changes in the arrangement of photosynthetic complexes with increase in LHCII phosphorylation and disturbances of the thylakoid structure take place in bean thylakoids only. Changes in the physical properties of bean thylakoids are manifested by the conversion of a three-phase temperature-dependent plot to a one-phase plot. Subsequent photo-activation of chilled bean leaves caused a partial restoration of the photochemistry and of membrane physical properties, but not of the photosynthetic complexes arrangement nor the thylakoid network structure. Summarizing, the composition of the thylakoid lipid matrix of CT pea allows retaining the optimal fluidity of its chloroplast membranes under low temperatures. In contrast, the fluidity of CS bean thylakoids is drastically changed, leading to the reorganization of the supramolecular structure of the photosynthetic complexes and finally results in structural remodeling of the CS bean thylakoid network.
Highlights
Thylakoid membranes in chloroplasts of higher plants are assemblies of chlorophyll-protein (CP) complexes and lipids, organized into two distinct domains: stacked membranes called grana and unstacked stroma thylakoids (Ruban and Johnson, 2015)
The fast fluorescence induction curves (Figures 1B,C) showed that in pea there was some decrease of fluorescence intensity after dark-chilling comparing to control leaves, subsequent photo-activation led to almost complete recovery (Figure 1B)
Our results showed that the supramolecular organization of CP complexes, lipid composition and double-bond index (DBI) index, lutein/β-carotene and protein/lipid ratios differ between CT pea and chilling-sensitive plants (CS) bean, indicating higher fluidity of the thylakoid membrane network in pea in optimal temperature conditions
Summary
Thylakoid membranes in chloroplasts of higher plants are assemblies of chlorophyll-protein (CP) complexes and lipids, organized into two distinct domains: stacked membranes called grana and unstacked stroma thylakoids (Ruban and Johnson, 2015). The lipid phase of thylakoids is formed by monogalactosyldiacylglycerol (MGDG) that accounts for about 50% of the total lipid content, digalactosyldiacylglycerol (DGDG) (∼30%), sulfoquinovosyldiacylglycerol (SQDG) (∼5–12%), and phosphatidylglycerol (PG) (∼5–12%) (Pali et al, 2003). The MGDG, the lipid forming inverted hexagonal phase, is linked with the dynamic polymorphism of lipids in thylakoid membranes, where the main bilayer phase coexists with minor non-bilayer domains (Garab et al, 2017). The ratio of lipids to proteins in thylakoids is estimated to be roughly 0.3 (Koochak et al, 2019); the membrane dynamics might be substantially modulated by lipid-protein interactions (Pali et al, 2003)
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