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Title: Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas

Abstract

Plastid isoprenoid-derived carotenoids serve essential roles in chloroplast development and photosynthesis. Although nearly all enzymes that participate in the biosynthesis of carotenoids in plants have been identified, the complement of auxiliary proteins that regulate synthesis, transport, sequestration, and degradation of these molecules and their isoprenoid precursors have not been fully described. To identify such proteins that are necessary for the optimal functioning of oxygenic photosynthesis, we screened a large collection of nonphotosynthetic (acetate-requiring) DNA insertional mutants of Chlamydomonas reinhardtii and isolated cpsfl1. Thecpsfl1mutant is extremely light-sensitive and susceptible to photoinhibition and photobleaching. The CPSFL1gene encodes a CRAL-TRIO hydrophobic ligand-binding (Sec14) domain protein. Proteins containing this domain are limited to eukaryotes, but some may have been retargeted to function in organelles of endosymbiotic origin. The cpsfl1 mutant showed decreased accumulation of plastidial isoprenoid-derived pigments, especially carotenoids, and whole-cell focused ion-beam scanning-electron microscopy revealed a deficiency of carotenoid-rich chloroplast structures (e.g., eyespot and plastoglobules). The low carotenoid content resulted from impaired biosynthesis at a step prior to phytoene, the committed precursor to carotenoids. The CPSFL1 protein bound phytoene and β-carotene when expressed in Escherichia coli and phosphatidic acid in vitro. We suggest that CPSFL1 is involved in the regulation of phytoene synthesismore » and carotenoid transport and thereby modulates carotenoid accumulation in the chloroplast.« less

Authors:
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Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); National Science Foundation (NSF); National Institutes of Health (NIH)
OSTI Identifier:
1618498
Alternate Identifier(s):
OSTI ID: 1756331
Grant/Contract Number:  
FWP 449B; AC02-05CH11231; MCB-1515169; T32 GM110523
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 117 Journal Issue: 22; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

García-Cerdán, José G., Schmid, Eva M., Takeuchi, Tomomi, McRae, Ian, McDonald, Kent L., Yordduangjun, Nichakarn, Hassan, Ahmed M., Grob, Patricia, Xu, C. Shan, Hess, Harald F., Fletcher, Daniel A., Nogales, Eva, and Niyogi, Krishna K. Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas. United States: N. p., 2020. Web. doi:10.1073/pnas.1916948117.
García-Cerdán, José G., Schmid, Eva M., Takeuchi, Tomomi, McRae, Ian, McDonald, Kent L., Yordduangjun, Nichakarn, Hassan, Ahmed M., Grob, Patricia, Xu, C. Shan, Hess, Harald F., Fletcher, Daniel A., Nogales, Eva, & Niyogi, Krishna K. Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas. United States. doi:https://doi.org/10.1073/pnas.1916948117
García-Cerdán, José G., Schmid, Eva M., Takeuchi, Tomomi, McRae, Ian, McDonald, Kent L., Yordduangjun, Nichakarn, Hassan, Ahmed M., Grob, Patricia, Xu, C. Shan, Hess, Harald F., Fletcher, Daniel A., Nogales, Eva, and Niyogi, Krishna K. Wed . "Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas". United States. doi:https://doi.org/10.1073/pnas.1916948117.
@article{osti_1618498,
title = {Chloroplast Sec14-like 1 (CPSFL1) is essential for normal chloroplast development and affects carotenoid accumulation in Chlamydomonas},
author = {García-Cerdán, José G. and Schmid, Eva M. and Takeuchi, Tomomi and McRae, Ian and McDonald, Kent L. and Yordduangjun, Nichakarn and Hassan, Ahmed M. and Grob, Patricia and Xu, C. Shan and Hess, Harald F. and Fletcher, Daniel A. and Nogales, Eva and Niyogi, Krishna K.},
abstractNote = {Plastid isoprenoid-derived carotenoids serve essential roles in chloroplast development and photosynthesis. Although nearly all enzymes that participate in the biosynthesis of carotenoids in plants have been identified, the complement of auxiliary proteins that regulate synthesis, transport, sequestration, and degradation of these molecules and their isoprenoid precursors have not been fully described. To identify such proteins that are necessary for the optimal functioning of oxygenic photosynthesis, we screened a large collection of nonphotosynthetic (acetate-requiring) DNA insertional mutants of Chlamydomonas reinhardtii and isolated cpsfl1. Thecpsfl1mutant is extremely light-sensitive and susceptible to photoinhibition and photobleaching. The CPSFL1gene encodes a CRAL-TRIO hydrophobic ligand-binding (Sec14) domain protein. Proteins containing this domain are limited to eukaryotes, but some may have been retargeted to function in organelles of endosymbiotic origin. The cpsfl1 mutant showed decreased accumulation of plastidial isoprenoid-derived pigments, especially carotenoids, and whole-cell focused ion-beam scanning-electron microscopy revealed a deficiency of carotenoid-rich chloroplast structures (e.g., eyespot and plastoglobules). The low carotenoid content resulted from impaired biosynthesis at a step prior to phytoene, the committed precursor to carotenoids. The CPSFL1 protein bound phytoene and β-carotene when expressed in Escherichia coli and phosphatidic acid in vitro. We suggest that CPSFL1 is involved in the regulation of phytoene synthesis and carotenoid transport and thereby modulates carotenoid accumulation in the chloroplast.},
doi = {10.1073/pnas.1916948117},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 22,
volume = 117,
place = {United States},
year = {2020},
month = {5}
}

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DOI: https://doi.org/10.1073/pnas.1916948117

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