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Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii
Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique re...
Autores principales: | , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9106746/ https://www.ncbi.nlm.nih.gov/pubmed/35562408 http://dx.doi.org/10.1038/s42003-022-03359-z |
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author | Zhang, Ningning Mattoon, Erin M. McHargue, Will Venn, Benedikt Zimmer, David Pecani, Kresti Jeong, Jooyeon Anderson, Cheyenne M. Chen, Chen Berry, Jeffrey C. Xia, Ming Tzeng, Shin-Cheng Becker, Eric Pazouki, Leila Evans, Bradley Cross, Fred Cheng, Jianlin Czymmek, Kirk J. Schroda, Michael Mühlhaus, Timo Zhang, Ru |
author_facet | Zhang, Ningning Mattoon, Erin M. McHargue, Will Venn, Benedikt Zimmer, David Pecani, Kresti Jeong, Jooyeon Anderson, Cheyenne M. Chen, Chen Berry, Jeffrey C. Xia, Ming Tzeng, Shin-Cheng Becker, Eric Pazouki, Leila Evans, Bradley Cross, Fred Cheng, Jianlin Czymmek, Kirk J. Schroda, Michael Mühlhaus, Timo Zhang, Ru |
author_sort | Zhang, Ningning |
collection | PubMed |
description | Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique responses to 24-hour moderate (35°C) and acute (40°C) high temperatures and subsequent recovery at 25°C. We identified previously overlooked unique elements in response to moderate high temperature. Heat at 35°C transiently arrested the cell cycle followed by partial synchronization, up-regulated transcripts/proteins involved in gluconeogenesis/glyoxylate-cycle for carbon uptake and promoted growth. But 40°C disrupted cell division and growth. Both high temperatures induced photoprotection, while 40°C distorted thylakoid/pyrenoid ultrastructure, affected the carbon concentrating mechanism, and decreased photosynthetic efficiency. We demonstrated increased transcript/protein correlation during both heat treatments and hypothesize reduced post-transcriptional regulation during heat may help efficiently coordinate thermotolerance mechanisms. During recovery after both heat treatments, especially 40°C, transcripts/proteins related to DNA synthesis increased while those involved in photosynthetic light reactions decreased. We propose down-regulating photosynthetic light reactions during DNA replication benefits cell cycle resumption by reducing ROS production. Our results provide potential targets to increase thermotolerance in algae and crops. |
format | Online Article Text |
id | pubmed-9106746 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-91067462022-05-15 Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii Zhang, Ningning Mattoon, Erin M. McHargue, Will Venn, Benedikt Zimmer, David Pecani, Kresti Jeong, Jooyeon Anderson, Cheyenne M. Chen, Chen Berry, Jeffrey C. Xia, Ming Tzeng, Shin-Cheng Becker, Eric Pazouki, Leila Evans, Bradley Cross, Fred Cheng, Jianlin Czymmek, Kirk J. Schroda, Michael Mühlhaus, Timo Zhang, Ru Commun Biol Article Different intensities of high temperatures affect the growth of photosynthetic cells in nature. To elucidate the underlying mechanisms, we cultivated the unicellular green alga Chlamydomonas reinhardtii under highly controlled photobioreactor conditions and revealed systems-wide shared and unique responses to 24-hour moderate (35°C) and acute (40°C) high temperatures and subsequent recovery at 25°C. We identified previously overlooked unique elements in response to moderate high temperature. Heat at 35°C transiently arrested the cell cycle followed by partial synchronization, up-regulated transcripts/proteins involved in gluconeogenesis/glyoxylate-cycle for carbon uptake and promoted growth. But 40°C disrupted cell division and growth. Both high temperatures induced photoprotection, while 40°C distorted thylakoid/pyrenoid ultrastructure, affected the carbon concentrating mechanism, and decreased photosynthetic efficiency. We demonstrated increased transcript/protein correlation during both heat treatments and hypothesize reduced post-transcriptional regulation during heat may help efficiently coordinate thermotolerance mechanisms. During recovery after both heat treatments, especially 40°C, transcripts/proteins related to DNA synthesis increased while those involved in photosynthetic light reactions decreased. We propose down-regulating photosynthetic light reactions during DNA replication benefits cell cycle resumption by reducing ROS production. Our results provide potential targets to increase thermotolerance in algae and crops. Nature Publishing Group UK 2022-05-13 /pmc/articles/PMC9106746/ /pubmed/35562408 http://dx.doi.org/10.1038/s42003-022-03359-z Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Zhang, Ningning Mattoon, Erin M. McHargue, Will Venn, Benedikt Zimmer, David Pecani, Kresti Jeong, Jooyeon Anderson, Cheyenne M. Chen, Chen Berry, Jeffrey C. Xia, Ming Tzeng, Shin-Cheng Becker, Eric Pazouki, Leila Evans, Bradley Cross, Fred Cheng, Jianlin Czymmek, Kirk J. Schroda, Michael Mühlhaus, Timo Zhang, Ru Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title | Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title_full | Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title_fullStr | Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title_full_unstemmed | Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title_short | Systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga Chlamydomonas reinhardtii |
title_sort | systems-wide analysis revealed shared and unique responses to moderate and acute high temperatures in the green alga chlamydomonas reinhardtii |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9106746/ https://www.ncbi.nlm.nih.gov/pubmed/35562408 http://dx.doi.org/10.1038/s42003-022-03359-z |
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