Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas

Liat Adler; Chun Sing Lau; Kashif M. Shaikh; Kim A. van Maldegem; Alex L. Payne-Dwyer; Cecile Lefoulon; Philipp Girr; Nicky Atkinson; James Barrett; Tom Z. Emrich-Mills; Emilija Dukic; Michael R. Blatt; Mark C. Leake; Gilles Peltier; Cornelia Spetea; Adrien Burlacot; Alistair J. McCormick; Luke C.M. Mackinder; Charlotte E. Walker

doi:10.1093/plphys/kiae450

Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas

Liat Adler, Chun Sing Lau, Kashif M. Shaikh, Kim A. van Maldegem, Alex L. Payne-Dwyer, Cecile Lefoulon, Philipp Girr, Nicky Atkinson, James Barrett, Tom Z. Emrich-Mills, Emilija Dukic, Michael R. Blatt, Mark C. Leake, Gilles Peltier, Cornelia Spetea^*, Adrien Burlacot^*, Alistair J. McCormick^*, Luke C.M. Mackinder^*, Charlotte E. Walker^*

^*Corresponding author for this work

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

Abstract

In many eukaryotic algae, CO2 fixation by Rubisco is enhanced by a CO2-concentrating mechanism, which utilizes a Rubisco-rich organelle called the pyrenoid. The pyrenoid is traversed by a network of thylakoid membranes called pyrenoid tubules, which are proposed to deliver CO2. In the model alga Chlamydomonas (Chlamydomonas reinhardtii), the pyrenoid tubules have been proposed to be tethered to the Rubisco matrix by a bestrophin-like transmembrane protein, BST4. Here, we show that BST4 forms a complex that localizes to the pyrenoid tubules. A Chlamydomonas mutant impaired in the accumulation of BST4 (bst4) formed normal pyrenoid tubules, and heterologous expression of BST4 in Arabidopsis (Arabidopsis thaliana) did not lead to the incorporation of thylakoids into a reconstituted Rubisco condensate. Chlamydomonas bst4 mutants did not show impaired growth under continuous light at air level CO2 but were impaired in their growth under fluctuating light. By quantifying the non-photochemical quenching (NPQ) of chlorophyll fluorescence, we propose that bst4 has a transiently lower thylakoid lumenal pH during dark-to-light transition compared to control strains. We conclude that BST4 is not a tethering protein but is most likely a pyrenoid tubule ion channel involved in the ion homeostasis of the lumen with particular importance during light fluctuations.

Original language	English
Pages (from-to)	2374-2394
Number of pages	21
Journal	Plant Physiology
Volume	196
Issue number	4
Early online date	6 Sept 2024
DOIs	https://doi.org/10.1093/plphys/kiae450
Publication status	Published - 2 Dec 2024

Bibliographical note

Keywords

Photosynthesis
Light
Acclimatization
Chlamydomonas reinhardtii/genetics
Mutation/genetics
Thylakoids/metabolism
Arabidopsis/genetics
Ribulose-Bisphosphate Carboxylase/metabolism
Carbon Dioxide/metabolism
Plant Proteins/metabolism
Chlamydomonas/genetics
Hydrogen-Ion Concentration

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Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas
© The Author(s) 2024
Final published version, 29.9 MBLicence: CC BY

Cite this

Adler, L., Lau, C. S., Shaikh, K. M., van Maldegem, K. A., Payne-Dwyer, A. L., Lefoulon, C., Girr, P., Atkinson, N., Barrett, J., Emrich-Mills, T. Z., Dukic, E., Blatt, M. R., Leake, M. C., Peltier, G., Spetea, C., Burlacot, A., McCormick, A. J., Mackinder, L. C. M., & Walker, C. E. (2024). Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas. Plant Physiology, 196(4), 2374-2394. https://doi.org/10.1093/plphys/kiae450

@article{eedf9a170cfd4eee81ef7c833491dcb8,

title = "Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas",

abstract = "In many eukaryotic algae, CO2 fixation by Rubisco is enhanced by a CO2-concentrating mechanism, which utilizes a Rubisco-rich organelle called the pyrenoid. The pyrenoid is traversed by a network of thylakoid membranes called pyrenoid tubules, which are proposed to deliver CO2. In the model alga Chlamydomonas (Chlamydomonas reinhardtii), the pyrenoid tubules have been proposed to be tethered to the Rubisco matrix by a bestrophin-like transmembrane protein, BST4. Here, we show that BST4 forms a complex that localizes to the pyrenoid tubules. A Chlamydomonas mutant impaired in the accumulation of BST4 (bst4) formed normal pyrenoid tubules, and heterologous expression of BST4 in Arabidopsis (Arabidopsis thaliana) did not lead to the incorporation of thylakoids into a reconstituted Rubisco condensate. Chlamydomonas bst4 mutants did not show impaired growth under continuous light at air level CO2 but were impaired in their growth under fluctuating light. By quantifying the non-photochemical quenching (NPQ) of chlorophyll fluorescence, we propose that bst4 has a transiently lower thylakoid lumenal pH during dark-to-light transition compared to control strains. We conclude that BST4 is not a tethering protein but is most likely a pyrenoid tubule ion channel involved in the ion homeostasis of the lumen with particular importance during light fluctuations.",

keywords = "Photosynthesis, Light, Acclimatization, Chlamydomonas reinhardtii/genetics, Mutation/genetics, Thylakoids/metabolism, Arabidopsis/genetics, Ribulose-Bisphosphate Carboxylase/metabolism, Carbon Dioxide/metabolism, Plant Proteins/metabolism, Chlamydomonas/genetics, Hydrogen-Ion Concentration",

author = "Liat Adler and Lau, {Chun Sing} and Shaikh, {Kashif M.} and {van Maldegem}, {Kim A.} and Payne-Dwyer, {Alex L.} and Cecile Lefoulon and Philipp Girr and Nicky Atkinson and James Barrett and Emrich-Mills, {Tom Z.} and Emilija Dukic and Blatt, {Michael R.} and Leake, {Mark C.} and Gilles Peltier and Cornelia Spetea and Adrien Burlacot and McCormick, {Alistair J.} and Mackinder, {Luke C.M.} and Walker, {Charlotte E.}",

note = "{\textcopyright} The Author(s) 2024",

year = "2024",

month = dec,

day = "2",

doi = "10.1093/plphys/kiae450",

language = "English",

volume = "196",

pages = "2374--2394",

journal = "Plant Physiology",

issn = "0032-0889",

publisher = "American Society of Plant Biologists",

number = "4",

}

Adler, L , Lau, CS, Shaikh, KM, van Maldegem, KA, Payne-Dwyer, AL, Lefoulon, C, Girr, P, Atkinson, N, Barrett, J, Emrich-Mills, TZ, Dukic, E, Blatt, MR, Leake, MC, Peltier, G, Spetea, C, Burlacot, A, McCormick, AJ, Mackinder, LCM & Walker, CE 2024, 'Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas', Plant Physiology, vol. 196, no. 4, pp. 2374-2394. https://doi.org/10.1093/plphys/kiae450

TY - JOUR

T1 - Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas

AU - Adler, Liat

AU - Lau, Chun Sing

AU - Shaikh, Kashif M.

AU - van Maldegem, Kim A.

AU - Payne-Dwyer, Alex L.

AU - Lefoulon, Cecile

AU - Girr, Philipp

AU - Atkinson, Nicky

AU - Barrett, James

AU - Emrich-Mills, Tom Z.

AU - Dukic, Emilija

AU - Blatt, Michael R.

AU - Leake, Mark C.

AU - Peltier, Gilles

AU - Spetea, Cornelia

AU - Burlacot, Adrien

AU - McCormick, Alistair J.

AU - Mackinder, Luke C.M.

AU - Walker, Charlotte E.

N1 - © The Author(s) 2024

PY - 2024/12/2

Y1 - 2024/12/2

N2 - In many eukaryotic algae, CO2 fixation by Rubisco is enhanced by a CO2-concentrating mechanism, which utilizes a Rubisco-rich organelle called the pyrenoid. The pyrenoid is traversed by a network of thylakoid membranes called pyrenoid tubules, which are proposed to deliver CO2. In the model alga Chlamydomonas (Chlamydomonas reinhardtii), the pyrenoid tubules have been proposed to be tethered to the Rubisco matrix by a bestrophin-like transmembrane protein, BST4. Here, we show that BST4 forms a complex that localizes to the pyrenoid tubules. A Chlamydomonas mutant impaired in the accumulation of BST4 (bst4) formed normal pyrenoid tubules, and heterologous expression of BST4 in Arabidopsis (Arabidopsis thaliana) did not lead to the incorporation of thylakoids into a reconstituted Rubisco condensate. Chlamydomonas bst4 mutants did not show impaired growth under continuous light at air level CO2 but were impaired in their growth under fluctuating light. By quantifying the non-photochemical quenching (NPQ) of chlorophyll fluorescence, we propose that bst4 has a transiently lower thylakoid lumenal pH during dark-to-light transition compared to control strains. We conclude that BST4 is not a tethering protein but is most likely a pyrenoid tubule ion channel involved in the ion homeostasis of the lumen with particular importance during light fluctuations.

AB - In many eukaryotic algae, CO2 fixation by Rubisco is enhanced by a CO2-concentrating mechanism, which utilizes a Rubisco-rich organelle called the pyrenoid. The pyrenoid is traversed by a network of thylakoid membranes called pyrenoid tubules, which are proposed to deliver CO2. In the model alga Chlamydomonas (Chlamydomonas reinhardtii), the pyrenoid tubules have been proposed to be tethered to the Rubisco matrix by a bestrophin-like transmembrane protein, BST4. Here, we show that BST4 forms a complex that localizes to the pyrenoid tubules. A Chlamydomonas mutant impaired in the accumulation of BST4 (bst4) formed normal pyrenoid tubules, and heterologous expression of BST4 in Arabidopsis (Arabidopsis thaliana) did not lead to the incorporation of thylakoids into a reconstituted Rubisco condensate. Chlamydomonas bst4 mutants did not show impaired growth under continuous light at air level CO2 but were impaired in their growth under fluctuating light. By quantifying the non-photochemical quenching (NPQ) of chlorophyll fluorescence, we propose that bst4 has a transiently lower thylakoid lumenal pH during dark-to-light transition compared to control strains. We conclude that BST4 is not a tethering protein but is most likely a pyrenoid tubule ion channel involved in the ion homeostasis of the lumen with particular importance during light fluctuations.

KW - Photosynthesis

KW - Light

KW - Acclimatization

KW - Chlamydomonas reinhardtii/genetics

KW - Mutation/genetics

KW - Thylakoids/metabolism

KW - Arabidopsis/genetics

KW - Ribulose-Bisphosphate Carboxylase/metabolism

KW - Carbon Dioxide/metabolism

KW - Plant Proteins/metabolism

KW - Chlamydomonas/genetics

KW - Hydrogen-Ion Concentration

UR - http://www.scopus.com/inward/record.url?scp=85210961426&partnerID=8YFLogxK

U2 - 10.1093/plphys/kiae450

DO - 10.1093/plphys/kiae450

M3 - Article

C2 - 39240724

AN - SCOPUS:85210961426

SN - 0032-0889

VL - 196

SP - 2374

EP - 2394

JO - Plant Physiology

JF - Plant Physiology

IS - 4

ER -

Bestrophin-like protein 4 is involved in photosynthetic acclimation to light fluctuations in Chlamydomonas

Abstract

Bibliographical note

Keywords

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