TY - JOUR

T1 - Curvature thylakoid 1 proteins modulate prolamellar body morphology and promote organized thylakoid biogenesis in Arabidopsis thaliana

AU - Sandoval-Ibáñez, Omar

AU - Sharma, Anurag

AU - Bykowski, Michał

AU - Borràs-Gas, Guillem

AU - Behrendorff, James B.Y.H.

AU - Mellor, Silas

AU - Qvortrup, Klaus

AU - Verdonk, Julian C.

AU - Bock, Ralph

AU - Kowalewska, Łucja

AU - Pribil, Mathias

N1 - Funding Information: M.P. acknowledges funding from the Novo Nordisk Foundation (NNF15OC0016586), the Danish Council for Independent Research (7017-00122A), and the Copenhagen Plant Science Centre, University of Copenhagen. ?.K. acknowledges funding from the National Science Centre, Poland, under Grant No. 2019/35/D/NZ3/03904. R.B. acknowledges financial support from the Deutsche Forschungsgemeinschaft (FOR 2092; BO 1482/17-2). A.S. was the recipient of a postdoctoral fellowship from the Carlsberg Foundation. We thank the Center for Advanced Bioimaging at the University of Copenhagen for providing facilities for TEM sample preparation and microscopy and the Core Facility for Integrated Microscopy in the Panum Institute (University of Copenhagen) for assistance with immunogold labeling and microscopy. Funding Information: ACKNOWLEDGMENTS. M.P. acknowledges funding from the Novo Nordisk Foundation (NNF15OC0016586), the Danish Council for Independent Research (7017-00122A), and the Copenhagen Plant Science Centre, University of Copenhagen. Ł.K. acknowledges funding from the National Science Centre, Poland, under Grant No. 2019/35/D/NZ3/03904. R.B. acknowledges financial support from the Deutsche Forschungsgemeinschaft (FOR 2092; BO 1482/ 17-2). A.S. was the recipient of a postdoctoral fellowship from the Carlsberg Foundation. We thank the Center for Advanced Bioimaging at the University of Copenhagen for providing facilities for TEM sample preparation and microscopy and the Core Facility for Integrated Microscopy in the Panum Institute (University of Copenhagen) for assistance with immunogold labeling and microscopy. Publisher Copyright: © 2021 National Academy of Sciences. All rights reserved.

PY - 2021

Y1 - 2021

N2 - 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.

AB - 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.

KW - Chloroplast biogenesis

KW - CURT1

KW - De-etiolation

KW - Photosynthesis

KW - Prolamellar bodies

U2 - 10.1073/pnas.2113934118

DO - 10.1073/pnas.2113934118

M3 - Journal article

C2 - 34654749

AN - SCOPUS:85117262895

VL - 118

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 42

M1 - e2113934118

ER -