Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery

Moshe Kafri; Weronika Patena; Lance Martin; Lianyong Wang; Gillian Gomer; Sabrina L. Ergun; Arthur K. Sirkejyan; Audrey Goh; Alexandra T. Wilson; Sophia E. Gavrilenko; Michal Breker; Asael Roichman; Claire D. McWhite; Joshua D. Rabinowitz; Frederick R. Cross; Martin Wühr; Martin C. Jonikas

doi:10.1016/j.cell.2023.11.007

Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery

Moshe Kafri, Weronika Patena, Lance Martin, Lianyong Wang, Gillian Gomer, Sabrina L. Ergun, Arthur K. Sirkejyan, Audrey Goh, Alexandra T. Wilson, Sophia E. Gavrilenko, Michal Breker, Asael Roichman, Claire D. McWhite, Joshua D. Rabinowitz, Frederick R. Cross, Martin Wühr, Martin C. Jonikas

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

3 Scopus citations

Abstract

Photosynthesis is central to food production and the Earth's biogeochemistry, yet the molecular basis for its regulation remains poorly understood. Here, using high-throughput genetics in the model eukaryotic alga Chlamydomonas reinhardtii, we identify with high confidence (false discovery rate [FDR] < 0.11) 70 poorly characterized genes required for photosynthesis. We then enable the functional characterization of these genes by providing a resource of proteomes of mutant strains, each lacking one of these genes. The data allow assignment of 34 genes to the biogenesis or regulation of one or more specific photosynthetic complexes. Further analysis uncovers biogenesis/regulatory roles for at least seven proteins, including five photosystem I mRNA maturation factors, the chloroplast translation factor MTF1, and the master regulator PMR1, which regulates chloroplast genes via nuclear-expressed factors. Our work provides a rich resource identifying regulatory and functional genes and placing them into pathways, thereby opening the door to a system-level understanding of photosynthesis.

Original language	English (US)
Pages (from-to)	5638-5655.e25
Journal	Cell
Volume	186
Issue number	25
DOIs	https://doi.org/10.1016/j.cell.2023.11.007
State	Published - Dec 7 2023

All Science Journal Classification (ASJC) codes

General Biochemistry, Genetics and Molecular Biology

Keywords

RNA sequencing
genetics
methionyl-tRNA formyltransferase
photosynthesis
photosystem I maturation factors
protein localization
protein profiling
retrograde regulation

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10.1016/j.cell.2023.11.007

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Kafri, M., Patena, W., Martin, L., Wang, L., Gomer, G., Ergun, S. L., Sirkejyan, A. K., Goh, A., Wilson, A. T., Gavrilenko, S. E., Breker, M., Roichman, A., McWhite, C. D., Rabinowitz, J. D., Cross, F. R., Wühr, M., & Jonikas, M. C. (2023). Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery. Cell, 186(25), 5638-5655.e25. https://doi.org/10.1016/j.cell.2023.11.007

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title = "Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery",

abstract = "Photosynthesis is central to food production and the Earth's biogeochemistry, yet the molecular basis for its regulation remains poorly understood. Here, using high-throughput genetics in the model eukaryotic alga Chlamydomonas reinhardtii, we identify with high confidence (false discovery rate [FDR] < 0.11) 70 poorly characterized genes required for photosynthesis. We then enable the functional characterization of these genes by providing a resource of proteomes of mutant strains, each lacking one of these genes. The data allow assignment of 34 genes to the biogenesis or regulation of one or more specific photosynthetic complexes. Further analysis uncovers biogenesis/regulatory roles for at least seven proteins, including five photosystem I mRNA maturation factors, the chloroplast translation factor MTF1, and the master regulator PMR1, which regulates chloroplast genes via nuclear-expressed factors. Our work provides a rich resource identifying regulatory and functional genes and placing them into pathways, thereby opening the door to a system-level understanding of photosynthesis.",

keywords = "RNA sequencing, genetics, methionyl-tRNA formyltransferase, photosynthesis, photosystem I maturation factors, protein localization, protein profiling, retrograde regulation",

author = "Moshe Kafri and Weronika Patena and Lance Martin and Lianyong Wang and Gillian Gomer and Ergun, {Sabrina L.} and Sirkejyan, {Arthur K.} and Audrey Goh and Wilson, {Alexandra T.} and Gavrilenko, {Sophia E.} and Michal Breker and Asael Roichman and McWhite, {Claire D.} and Rabinowitz, {Joshua D.} and Cross, {Frederick R.} and Martin W{\"u}hr and Jonikas, {Martin C.}",

note = "Publisher Copyright: {\textcopyright} 2023 The Author(s)",

year = "2023",

month = dec,

day = "7",

doi = "10.1016/j.cell.2023.11.007",

language = "English (US)",

volume = "186",

pages = "5638--5655.e25",

journal = "Cell",

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Kafri, M, Patena, W, Martin, L, Wang, L, Gomer, G, Ergun, SL, Sirkejyan, AK, Goh, A, Wilson, AT, Gavrilenko, SE, Breker, M, Roichman, A, McWhite, CD, Rabinowitz, JD, Cross, FR, Wühr, M & Jonikas, MC 2023, 'Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery', Cell, vol. 186, no. 25, pp. 5638-5655.e25. https://doi.org/10.1016/j.cell.2023.11.007

TY - JOUR

T1 - Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery

AU - Kafri, Moshe

AU - Patena, Weronika

AU - Martin, Lance

AU - Wang, Lianyong

AU - Gomer, Gillian

AU - Ergun, Sabrina L.

AU - Sirkejyan, Arthur K.

AU - Goh, Audrey

AU - Wilson, Alexandra T.

AU - Gavrilenko, Sophia E.

AU - Breker, Michal

AU - Roichman, Asael

AU - McWhite, Claire D.

AU - Rabinowitz, Joshua D.

AU - Cross, Frederick R.

AU - Wühr, Martin

AU - Jonikas, Martin C.

PY - 2023/12/7

Y1 - 2023/12/7

N2 - Photosynthesis is central to food production and the Earth's biogeochemistry, yet the molecular basis for its regulation remains poorly understood. Here, using high-throughput genetics in the model eukaryotic alga Chlamydomonas reinhardtii, we identify with high confidence (false discovery rate [FDR] < 0.11) 70 poorly characterized genes required for photosynthesis. We then enable the functional characterization of these genes by providing a resource of proteomes of mutant strains, each lacking one of these genes. The data allow assignment of 34 genes to the biogenesis or regulation of one or more specific photosynthetic complexes. Further analysis uncovers biogenesis/regulatory roles for at least seven proteins, including five photosystem I mRNA maturation factors, the chloroplast translation factor MTF1, and the master regulator PMR1, which regulates chloroplast genes via nuclear-expressed factors. Our work provides a rich resource identifying regulatory and functional genes and placing them into pathways, thereby opening the door to a system-level understanding of photosynthesis.

AB - Photosynthesis is central to food production and the Earth's biogeochemistry, yet the molecular basis for its regulation remains poorly understood. Here, using high-throughput genetics in the model eukaryotic alga Chlamydomonas reinhardtii, we identify with high confidence (false discovery rate [FDR] < 0.11) 70 poorly characterized genes required for photosynthesis. We then enable the functional characterization of these genes by providing a resource of proteomes of mutant strains, each lacking one of these genes. The data allow assignment of 34 genes to the biogenesis or regulation of one or more specific photosynthetic complexes. Further analysis uncovers biogenesis/regulatory roles for at least seven proteins, including five photosystem I mRNA maturation factors, the chloroplast translation factor MTF1, and the master regulator PMR1, which regulates chloroplast genes via nuclear-expressed factors. Our work provides a rich resource identifying regulatory and functional genes and placing them into pathways, thereby opening the door to a system-level understanding of photosynthesis.

KW - RNA sequencing

KW - genetics

KW - methionyl-tRNA formyltransferase

KW - photosynthesis

KW - photosystem I maturation factors

KW - protein localization

KW - protein profiling

KW - retrograde regulation

UR - http://www.scopus.com/inward/record.url?scp=85178149852&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85178149852&partnerID=8YFLogxK

U2 - 10.1016/j.cell.2023.11.007

DO - 10.1016/j.cell.2023.11.007

M3 - Article

C2 - 38065083

AN - SCOPUS:85178149852

SN - 0092-8674

VL - 186

SP - 5638-5655.e25

JO - Cell

JF - Cell

IS - 25

ER -

Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery

Abstract

All Science Journal Classification (ASJC) codes

Keywords

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