Role of isotropic lipid phase in the fusion of photosystem II membranes

• Published in: Photosynthesis research 2024-08, Vol.161 (1-2), p.127-140
• Main Authors: Böde, Kinga, Javornik, Uroš, Dlouhý, Ondřej, Zsíros, Ottó, Biswas, Avratanu, Domonkos, Ildikó, Šket, Primož, Karlický, Václav, Ughy, Bettina, Lambrev, Petar H., Špunda, Vladimír, Plavec, Janez, Garab, Győző
• Format: Article
• Language: English
• Subjects: Biochemistry; Biomedical and Life Sciences; Centrifugation; Functional morphology; Life Sciences; Linear dichroism; Lipids; Lipids - chemistry; Magnetic Resonance Spectroscopy; Membrane fusion; Membrane Fusion - physiology; Membranes; NMR; Nuclear magnetic resonance; Photosystem II; Photosystem II Protein Complex - metabolism; Plant Genetics and Genomics; Plant Physiology; Plant Sciences; Scanning electron microscopy; Spectrum analysis; Structure-function relationships; Sucrose; Thylakoid membranes; Thylakoids - metabolism
• ISSN: 0166-8595; 1573-5079; 1573-5079
• DOI: 10.1007/s11120-024-01097-3

It has been thoroughly documented, by using 31 P-NMR spectroscopy, that plant thylakoid membranes (TMs), in addition to the bilayer (or lamellar, L) phase, contain at least two isotropic (I) lipid phases and an inverted hexagonal (H II ) phase. However, our knowledge concerning the structural and functional roles of the non-bilayer phases is still rudimentary. The objective of the present study is to elucidate the origin of I phases which have been hypothesized to arise, in part, from the fusion of TMs (Garab et al. 2022 Progr Lipid Res 101,163). We take advantage of the selectivity of wheat germ lipase (WGL) in eliminating the I phases of TMs (Dlouhý et al. 2022 Cells 11: 2681), and the tendency of the so-called BBY particles, stacked photosystem II (PSII) enriched membrane pairs of 300–500 nm in diameter, to form large laterally fused sheets (Dunahay et al. 1984 BBA 764: 179). Our 31 P-NMR spectroscopy data show that BBY membranes contain L and I phases. Similar to TMs, WGL selectively eliminated the I phases, which at the same time exerted no effect on the molecular organization and functional activity of PSII membranes. As revealed by sucrose-density centrifugation, magnetic linear dichroism spectroscopy and scanning electron microscopy, WGL disassembled the large laterally fused sheets. These data provide direct experimental evidence on the involvement of I phase(s) in the fusion of stacked PSII membrane pairs, and strongly suggest the role of non-bilayer lipids in the self-assembly of the TM system.