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Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake

Steve Slocombe, Tatiana Zúñiga-Burgos, Lili Chu, Payam Mehrshahi, Matthew P. Davey, Alison G. Smith, Miller Alonso Camargo-Valero, Alison Baker

Frontiers in Plant Science, Volume: 14

Swansea University Author: Steve Slocombe

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    © 2023 Slocombe, Zu´ ñiga-Burgos, Chu, Mehrshahi, Davey, Smith, Camargo-Valero and Baker. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY).

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DOI (Published version): 10.3389/fpls.2023.1208168

Abstract

Remediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription...

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Published in: Frontiers in Plant Science
ISSN: 1664-462X
Published: Frontiers Media SA 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa65453
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Manipulating a single gene (PSR1) drove uptake of both PO43- and a Mg2+ counter-ion leading to increased PolyP granule size, raising P levels 4-fold to 8% dry cell weight, and accelerated removal of PO43- from the medium. Examination of the gene expression profile showed that the P-starvation response was mimicked under P-replete conditions, switching on luxury uptake. Hyper-accumulation of P depended on a feed-forward mechanism, where a small set of ‘Class I’ P-transporter genes were activated despite abundant external PO43- levels. The transporters drove a reduction in external PO43- levels, permitting more genes to be expressed (Class II), leading to more P-uptake. Our data pointed toward a PSR1-independent mechanism for detection of external PO43- which suppressed Class II genes. This model provided a plausible mechanism for P-overplus where prior P-starvation elevates PSR1 and on P-resupply causes luxury P-uptake. 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spelling v2 65453 2024-01-17 Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake 4a1ea486a78ed357efdfa053a277ae40 Steve Slocombe Steve Slocombe true false 2024-01-17 SBI Remediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription factor: Phosphate Starvation Response 1) for over-expression in algae. Manipulating a single gene (PSR1) drove uptake of both PO43- and a Mg2+ counter-ion leading to increased PolyP granule size, raising P levels 4-fold to 8% dry cell weight, and accelerated removal of PO43- from the medium. Examination of the gene expression profile showed that the P-starvation response was mimicked under P-replete conditions, switching on luxury uptake. Hyper-accumulation of P depended on a feed-forward mechanism, where a small set of ‘Class I’ P-transporter genes were activated despite abundant external PO43- levels. The transporters drove a reduction in external PO43- levels, permitting more genes to be expressed (Class II), leading to more P-uptake. Our data pointed toward a PSR1-independent mechanism for detection of external PO43- which suppressed Class II genes. This model provided a plausible mechanism for P-overplus where prior P-starvation elevates PSR1 and on P-resupply causes luxury P-uptake. This is because the Class I genes, which include P-transporter genes, are not suppressed by the excess PO43-. Taken together, these discoveries facilitate a bio-circular approach of recycling nutrients from wastewater back to agriculture. Journal Article Frontiers in Plant Science 14 Frontiers Media SA 1664-462X biomass, micro-algae, polyphosphate, transcription factor, wastewater remediation 27 7 2023 2023-07-27 10.3389/fpls.2023.1208168 Data availability statement:The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found here: https://doi.org/10.5518/1217. COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University This work was supported by: UK Research and Innovation (UKRI)’s Biotechnology and Biological Sciences Research Council (BBSRC) (grant number BB/N016033/1) and Global Challenges Research Fund (GCRF) as part of the Water Security and Sustainable Development Hub (grant number ES/S008179/1). The confocal microscopes in the Bioimaging Facility at the University of Leeds were funded by Welcome Trust grant WT104918MA. 2024-03-21T10:26:19.8644126 2024-01-17T15:36:27.7330036 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Steve Slocombe 1 Tatiana Zúñiga-Burgos 2 Lili Chu 3 Payam Mehrshahi 4 Matthew P. Davey 5 Alison G. Smith 6 Miller Alonso Camargo-Valero 7 Alison Baker 8 65453__29774__8638d09bd8c24d17a6ca13147aef434c.pdf 65453_VoR.pdf 2024-03-21T10:25:01.8447263 Output 15340557 application/pdf Version of Record true © 2023 Slocombe, Zu´ ñiga-Burgos, Chu, Mehrshahi, Davey, Smith, Camargo-Valero and Baker. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). true eng http://creativecommons.org/licenses/by/4.0/
title Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
spellingShingle Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
Steve Slocombe
title_short Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_full Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_fullStr Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_full_unstemmed Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_sort Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
author_id_str_mv 4a1ea486a78ed357efdfa053a277ae40
author_id_fullname_str_mv 4a1ea486a78ed357efdfa053a277ae40_***_Steve Slocombe
author Steve Slocombe
author2 Steve Slocombe
Tatiana Zúñiga-Burgos
Lili Chu
Payam Mehrshahi
Matthew P. Davey
Alison G. Smith
Miller Alonso Camargo-Valero
Alison Baker
format Journal article
container_title Frontiers in Plant Science
container_volume 14
publishDate 2023
institution Swansea University
issn 1664-462X
doi_str_mv 10.3389/fpls.2023.1208168
publisher Frontiers Media SA
college_str Faculty of Science and Engineering
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hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
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description Remediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription factor: Phosphate Starvation Response 1) for over-expression in algae. Manipulating a single gene (PSR1) drove uptake of both PO43- and a Mg2+ counter-ion leading to increased PolyP granule size, raising P levels 4-fold to 8% dry cell weight, and accelerated removal of PO43- from the medium. Examination of the gene expression profile showed that the P-starvation response was mimicked under P-replete conditions, switching on luxury uptake. Hyper-accumulation of P depended on a feed-forward mechanism, where a small set of ‘Class I’ P-transporter genes were activated despite abundant external PO43- levels. The transporters drove a reduction in external PO43- levels, permitting more genes to be expressed (Class II), leading to more P-uptake. Our data pointed toward a PSR1-independent mechanism for detection of external PO43- which suppressed Class II genes. This model provided a plausible mechanism for P-overplus where prior P-starvation elevates PSR1 and on P-resupply causes luxury P-uptake. This is because the Class I genes, which include P-transporter genes, are not suppressed by the excess PO43-. Taken together, these discoveries facilitate a bio-circular approach of recycling nutrients from wastewater back to agriculture.
published_date 2023-07-27T10:26:17Z
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