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 -