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Curvature thylakoid 1 proteins modulate prolamellar body morphology and promote organized thylakoid biogenesis in Arabidopsis thaliana
Saturday, 2021/10/23 | 07:15:36

Omar Sandoval-Ibáñez, Anurag Sharma, Michał Bykowski, Guillem Borràs-Gas, James B. Y. H. Behrendorff, Silas Mellor, Klaus Qvortrup, Julian C. Verdonk, Ralph Bock, Łucja Kowalewska, and Mathias Pribil

PNAS October 19, 2021 118 (42) e2113934118

Significance

Chloroplast biogenesis is a fundamental process occurring during seedling ontogenesis and leading to plant autotrophy. Which membrane components sterically organize the light-triggered transition of etioplast prolamellar bodies (PLBs) into chloroplast thylakoids, and thus mediate cubic–lamellar transformation, is poorly understood. Here, we used combined two- and three-dimensional electron microscopy, spectroscopy, and biochemical methods to determine the role of CURT1 proteins in the formation of etioplast cubic membranes and their transformation to photosynthetically active chloroplast thylakoids. CURT1 proteins were previously recognized as significant contributors to thylakoid membrane folding. We found that CURT1 proteins are integral proteins of etioplast membranes and act as factors modulating PLBs and prothylakoid nanomorphology. They are also required for concerted thylakoid maturation under de-etiolation.

Abstract

The term “de-etiolation” refers to the light-dependent differentiation of etioplasts to chloroplasts in angiosperms. The underlying process involves reorganization of prolamellar bodies (PLBs) and prothylakoids into thylakoids, with concurrent changes in protein, lipid, and pigment composition, which together lead to the assembly of active photosynthetic complexes. Despite the highly conserved structure of PLBs among land plants, the processes that mediate PLB maintenance and their disassembly during de-etiolation are poorly understood. Among chloroplast thylakoid membrane–localized proteins, to date, only Curvature thylakoid 1 (CURT1) proteins were shown to exhibit intrinsic membrane-bending capacity. Here, we show that CURT1 proteins, which play a critical role in grana margin architecture and thylakoid plasticity, also participate in de-etiolation and modulate PLB geometry and density. Lack of CURT1 proteins severely perturbs PLB organization and vesicle fusion, leading to reduced accumulation of the light-dependent enzyme protochlorophyllide oxidoreductase (LPOR) and a delay in the onset of photosynthesis. In contrast, overexpression of CURT1A induces excessive bending of PLB membranes, which upon illumination show retarded disassembly and concomitant overaccumulation of LPOR, though without affecting greening or the establishment of photosynthesis. We conclude that CURT1 proteins contribute to the maintenance of the paracrystalline PLB morphology and are necessary for efficient and organized thylakoid membrane maturation during de-etiolation.

 

See: https://www.pnas.org/content/118/42/e2113934118

 

Figure 1: CURT1 proteins are present in membrane fractions of cotyledons throughout de-etiolation. (A) Accumulation of CURT1A-C proteins in cotyledons and roots of 7-d-old Col-0 and Ler-0 seedlings grown under a 16/8 h light/dark cycle. ACTIN was used as the loading control. (B) Design of the de-etiolation assay. Seeds were stratified for 2 to 3 d and exposed to light for 1 h prior to dark acclimation for 1 wk. Seedlings were sampled at 0, 3, 6, 9, 12, 24, and 48 h after the onset of continuous light (dotted lines). (C) Immunoblotting analysis of CURT1A-C accumulation in total protein extracts from seedlings sampled at the times shown in B; 10 μg of protein was loaded in each lane. n = 3. (D) Membrane fractions (M. fractions) were prepared from cotyledons after 6 h of illumination. The accumulation of CURT1A-C proteins in mature thylakoids (T) and membrane fractions was analyzed in Col-0 and Ler-0. AtpB, a typical integral membrane protein, served as the loading control. n = 3. (E) Images of emerging cotyledons from Col-0, curt1abcd, Ler-0, and oeCURT1A at 0, 12, and 48 h after the onset of illumination. (Scale bar, 5 mm.) (F and G) Total chlorophyll content analyzed in (F) Col-0, curt1abcd, and (G) Ler-0 and oeCURT1A after 3, 6, 9, 12, 24, and 48 h of de-etiolation. The contributions of chlorophyll a (black columns) and chlorophyll b (white columns) to the total chlorophyll content are depicted. Error bars represent SDs of six biological replicates. Levels at 48 h were compared (by two-way ANOVA with Bonferroni posttest) between curt1abcd and Col-0 and between oeCURT1A and Ler-0. **P < 0.01; ***P < 0.001.

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