A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways

Lianyong Wang; Weronika Patena; Kelly A. Van Baalen; Yihua Xie; Emily R. Singer; Sophia Gavrilenko; Michelle Warren-Williams; Linqu Han; Henry R. Harrigan; Linnea D. Hartz; Vivian Chen; Vinh T.N.P. Ton; Saw Kyin; Henry H. Shwe; Matthew H. Cahn; Alexandra T. Wilson; Masayuki Onishi; Jianping Hu; Danny J. Schnell; Claire D. McWhite; Martin C. Jonikas

doi:10.1016/j.cell.2023.06.008

A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways

Lianyong Wang, Weronika Patena, Kelly A. Van Baalen, Yihua Xie, Emily R. Singer, Sophia Gavrilenko, Michelle Warren-Williams, Linqu Han, Henry R. Harrigan, Linnea D. Hartz, Vivian Chen, Vinh T.N.P. Ton, Saw Kyin, Henry H. Shwe, Matthew H. Cahn, Alexandra T. Wilson, Masayuki Onishi, Jianping Hu, Danny J. Schnell, Claire D. McWhiteMartin C. Jonikas

Research output: Contribution to journal › Article › peer-review

26 Scopus citations

Abstract

Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition, function, and spatial organization remains limited. Here, we determined the localizations of 1,034 candidate chloroplast proteins using fluorescent protein tagging in the model alga Chlamydomonas reinhardtii. The localizations provide insights into the functions of poorly characterized proteins; identify novel components of nucleoids, plastoglobules, and the pyrenoid; and reveal widespread protein targeting to multiple compartments. We discovered and further characterized cellular organizational features, including eleven chloroplast punctate structures, cytosolic crescent structures, and unexpected spatial distributions of enzymes within the chloroplast. We also used machine learning to predict the localizations of other nuclear-encoded Chlamydomonas proteins. The strains and localization atlas developed here will serve as a resource to accelerate studies of chloroplast architecture and functions.

Original language	English (US)
Pages (from-to)	3499-3518.e14
Journal	Cell
Volume	186
Issue number	16
DOIs	https://doi.org/10.1016/j.cell.2023.06.008
State	Published - Aug 3 2023

All Science Journal Classification (ASJC) codes

General Biochemistry, Genetics and Molecular Biology

Keywords

Chlamydomonas reinhardtii
chloroplast
dual targeting
fluorescent tagging
nucleoid
plastoglobule
protein localization
protein localization prediction
protein-protein interaction
pyrenoid

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10.1016/j.cell.2023.06.008

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Wang, L., Patena, W., Van Baalen, K. A., Xie, Y., Singer, E. R., Gavrilenko, S., Warren-Williams, M., Han, L., Harrigan, H. R., Hartz, L. D., Chen, V., Ton, V. T. N. P., Kyin, S., Shwe, H. H., Cahn, M. H., Wilson, A. T., Onishi, M., Hu, J., Schnell, D. J., ... Jonikas, M. C. (2023). A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways. Cell, 186(16), 3499-3518.e14. https://doi.org/10.1016/j.cell.2023.06.008

@article{fb45fafe038c43c0be1993583183d528,

title = "A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways",

abstract = "Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition, function, and spatial organization remains limited. Here, we determined the localizations of 1,034 candidate chloroplast proteins using fluorescent protein tagging in the model alga Chlamydomonas reinhardtii. The localizations provide insights into the functions of poorly characterized proteins; identify novel components of nucleoids, plastoglobules, and the pyrenoid; and reveal widespread protein targeting to multiple compartments. We discovered and further characterized cellular organizational features, including eleven chloroplast punctate structures, cytosolic crescent structures, and unexpected spatial distributions of enzymes within the chloroplast. We also used machine learning to predict the localizations of other nuclear-encoded Chlamydomonas proteins. The strains and localization atlas developed here will serve as a resource to accelerate studies of chloroplast architecture and functions.",

keywords = "Chlamydomonas reinhardtii, chloroplast, dual targeting, fluorescent tagging, nucleoid, plastoglobule, protein localization, protein localization prediction, protein-protein interaction, pyrenoid",

author = "Lianyong Wang and Weronika Patena and {Van Baalen}, {Kelly A.} and Yihua Xie and Singer, {Emily R.} and Sophia Gavrilenko and Michelle Warren-Williams and Linqu Han and Harrigan, {Henry R.} and Hartz, {Linnea D.} and Vivian Chen and Ton, {Vinh T.N.P.} and Saw Kyin and Shwe, {Henry H.} and Cahn, {Matthew H.} and Wilson, {Alexandra T.} and Masayuki Onishi and Jianping Hu and Schnell, {Danny J.} and McWhite, {Claire D.} and Jonikas, {Martin C.}",

note = "Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = aug,

day = "3",

doi = "10.1016/j.cell.2023.06.008",

language = "English (US)",

volume = "186",

pages = "3499--3518.e14",

journal = "Cell",

issn = "0092-8674",

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Wang, L, Patena, W, Van Baalen, KA, Xie, Y, Singer, ER, Gavrilenko, S, Warren-Williams, M, Han, L, Harrigan, HR, Hartz, LD, Chen, V, Ton, VTNP, Kyin, S, Shwe, HH, Cahn, MH, Wilson, AT, Onishi, M, Hu, J, Schnell, DJ, McWhite, CD & Jonikas, MC 2023, 'A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways', Cell, vol. 186, no. 16, pp. 3499-3518.e14. https://doi.org/10.1016/j.cell.2023.06.008

TY - JOUR

T1 - A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways

AU - Wang, Lianyong

AU - Patena, Weronika

AU - Van Baalen, Kelly A.

AU - Xie, Yihua

AU - Singer, Emily R.

AU - Gavrilenko, Sophia

AU - Warren-Williams, Michelle

AU - Han, Linqu

AU - Harrigan, Henry R.

AU - Hartz, Linnea D.

AU - Chen, Vivian

AU - Ton, Vinh T.N.P.

AU - Kyin, Saw

AU - Shwe, Henry H.

AU - Cahn, Matthew H.

AU - Wilson, Alexandra T.

AU - Onishi, Masayuki

AU - Hu, Jianping

AU - Schnell, Danny J.

AU - McWhite, Claire D.

AU - Jonikas, Martin C.

PY - 2023/8/3

Y1 - 2023/8/3

N2 - Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition, function, and spatial organization remains limited. Here, we determined the localizations of 1,034 candidate chloroplast proteins using fluorescent protein tagging in the model alga Chlamydomonas reinhardtii. The localizations provide insights into the functions of poorly characterized proteins; identify novel components of nucleoids, plastoglobules, and the pyrenoid; and reveal widespread protein targeting to multiple compartments. We discovered and further characterized cellular organizational features, including eleven chloroplast punctate structures, cytosolic crescent structures, and unexpected spatial distributions of enzymes within the chloroplast. We also used machine learning to predict the localizations of other nuclear-encoded Chlamydomonas proteins. The strains and localization atlas developed here will serve as a resource to accelerate studies of chloroplast architecture and functions.

AB - Chloroplasts are eukaryotic photosynthetic organelles that drive the global carbon cycle. Despite their importance, our understanding of their protein composition, function, and spatial organization remains limited. Here, we determined the localizations of 1,034 candidate chloroplast proteins using fluorescent protein tagging in the model alga Chlamydomonas reinhardtii. The localizations provide insights into the functions of poorly characterized proteins; identify novel components of nucleoids, plastoglobules, and the pyrenoid; and reveal widespread protein targeting to multiple compartments. We discovered and further characterized cellular organizational features, including eleven chloroplast punctate structures, cytosolic crescent structures, and unexpected spatial distributions of enzymes within the chloroplast. We also used machine learning to predict the localizations of other nuclear-encoded Chlamydomonas proteins. The strains and localization atlas developed here will serve as a resource to accelerate studies of chloroplast architecture and functions.

KW - Chlamydomonas reinhardtii

KW - chloroplast

KW - dual targeting

KW - fluorescent tagging

KW - nucleoid

KW - plastoglobule

KW - protein localization

KW - protein localization prediction

KW - protein-protein interaction

KW - pyrenoid

UR - http://www.scopus.com/inward/record.url?scp=85166674688&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85166674688&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2023.06.008

DO - 10.1016/j.cell.2023.06.008

M3 - Article

C2 - 37437571

AN - SCOPUS:85166674688

SN - 0092-8674

VL - 186

SP - 3499-3518.e14

JO - Cell

JF - Cell

IS - 16

ER -

A chloroplast protein atlas reveals punctate structures and spatial organization of biosynthetic pathways

Abstract

All Science Journal Classification (ASJC) codes

Keywords

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