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Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum

BACKGROUND: Diatoms (Bacilliariophyceae) encode two light-dependent protochlorophyllide oxidoreductases (POR1 and POR2) that catalyze the penultimate step of chlorophyll biosynthesis in the light. Algae live in dynamic environments whose changing light levels induce photoacclimative metabolic shifts...

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Autores principales: Hunsperger, Heather M., Ford, Christopher J., Miller, James S., Cattolico, Rose Ann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4930169/
https://www.ncbi.nlm.nih.gov/pubmed/27367227
http://dx.doi.org/10.1371/journal.pone.0158614
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author Hunsperger, Heather M.
Ford, Christopher J.
Miller, James S.
Cattolico, Rose Ann
author_facet Hunsperger, Heather M.
Ford, Christopher J.
Miller, James S.
Cattolico, Rose Ann
author_sort Hunsperger, Heather M.
collection PubMed
description BACKGROUND: Diatoms (Bacilliariophyceae) encode two light-dependent protochlorophyllide oxidoreductases (POR1 and POR2) that catalyze the penultimate step of chlorophyll biosynthesis in the light. Algae live in dynamic environments whose changing light levels induce photoacclimative metabolic shifts, including altered cellular chlorophyll levels. We hypothesized that the two POR proteins may be differentially adaptive under varying light conditions. Using the diatom Phaeodactylum tricornutum as a test system, differences in POR protein abundance and por gene expression were examined when this organism was grown on an alternating light:dark cycles at different irradiances; exposed to continuous light; and challenged by a significant decrease in light availability. RESULTS: For cultures maintained on a 12h light: 12h dark photoperiod at 200μE m(−2) s(−1) ((200)L/D), both por genes were up-regulated during the light and down-regulated in the dark, though por1 transcript abundance rose and fell earlier than that of por2. Little concordance occurred between por1 mRNA and POR1 protein abundance. In contrast, por2 mRNA and POR2 protein abundances followed similar diurnal patterns. When (200)L/D P. tricornutum cultures were transferred to continuous light ((200)L/L), the diurnal regulatory pattern of por1 mRNA abundance but not of por2 was disrupted, and POR1 but not POR2 protein abundance dropped steeply. Under 1200μE m(−2) s(−1) ((1200)L/D), both por1 mRNA and POR1 protein abundance displayed diurnal oscillations. A compromised diel por2 mRNA response under (1200)L/D did not impact the oscillation in POR2 abundance. When cells grown at (1200)L/D were then shifted to 50μE m(−2) s(−1) ((50)L/D), por1 and por2 mRNA levels decreased swiftly but briefly upon light reduction. Thereafter, POR1 but not POR2 protein levels rose significantly in response to this light stepdown. CONCLUSION: Given the sensitivity of diatom por1/POR1 to real-time light cues and adherence of por2/POR2 regulation to the diurnal cycle, we suggest that POR1 supports photoacclimation, whereas POR2 is the workhorse for daily chlorophyll synthesis.
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spelling pubmed-49301692016-07-18 Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum Hunsperger, Heather M. Ford, Christopher J. Miller, James S. Cattolico, Rose Ann PLoS One Research Article BACKGROUND: Diatoms (Bacilliariophyceae) encode two light-dependent protochlorophyllide oxidoreductases (POR1 and POR2) that catalyze the penultimate step of chlorophyll biosynthesis in the light. Algae live in dynamic environments whose changing light levels induce photoacclimative metabolic shifts, including altered cellular chlorophyll levels. We hypothesized that the two POR proteins may be differentially adaptive under varying light conditions. Using the diatom Phaeodactylum tricornutum as a test system, differences in POR protein abundance and por gene expression were examined when this organism was grown on an alternating light:dark cycles at different irradiances; exposed to continuous light; and challenged by a significant decrease in light availability. RESULTS: For cultures maintained on a 12h light: 12h dark photoperiod at 200μE m(−2) s(−1) ((200)L/D), both por genes were up-regulated during the light and down-regulated in the dark, though por1 transcript abundance rose and fell earlier than that of por2. Little concordance occurred between por1 mRNA and POR1 protein abundance. In contrast, por2 mRNA and POR2 protein abundances followed similar diurnal patterns. When (200)L/D P. tricornutum cultures were transferred to continuous light ((200)L/L), the diurnal regulatory pattern of por1 mRNA abundance but not of por2 was disrupted, and POR1 but not POR2 protein abundance dropped steeply. Under 1200μE m(−2) s(−1) ((1200)L/D), both por1 mRNA and POR1 protein abundance displayed diurnal oscillations. A compromised diel por2 mRNA response under (1200)L/D did not impact the oscillation in POR2 abundance. When cells grown at (1200)L/D were then shifted to 50μE m(−2) s(−1) ((50)L/D), por1 and por2 mRNA levels decreased swiftly but briefly upon light reduction. Thereafter, POR1 but not POR2 protein levels rose significantly in response to this light stepdown. CONCLUSION: Given the sensitivity of diatom por1/POR1 to real-time light cues and adherence of por2/POR2 regulation to the diurnal cycle, we suggest that POR1 supports photoacclimation, whereas POR2 is the workhorse for daily chlorophyll synthesis. Public Library of Science 2016-07-01 /pmc/articles/PMC4930169/ /pubmed/27367227 http://dx.doi.org/10.1371/journal.pone.0158614 Text en © 2016 Hunsperger et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Hunsperger, Heather M.
Ford, Christopher J.
Miller, James S.
Cattolico, Rose Ann
Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title_full Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title_fullStr Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title_full_unstemmed Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title_short Differential Regulation of Duplicate Light-Dependent Protochlorophyllide Oxidoreductases in the Diatom Phaeodactylum tricornutum
title_sort differential regulation of duplicate light-dependent protochlorophyllide oxidoreductases in the diatom phaeodactylum tricornutum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4930169/
https://www.ncbi.nlm.nih.gov/pubmed/27367227
http://dx.doi.org/10.1371/journal.pone.0158614
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