Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii

Abstract An intact cell wall is critical for cellular interactions with the environment and protecting the cell from environmental challenges. Signaling mechanisms are necessary to monitor cell wall integrity and to regulate cell wall production and remodeling during growth and division cycles. The...

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Autores principales:	Evan Cronmiller, Deepak Toor, Nai Chun Shao, Thamali Kariyawasam, Ming Hsiu Wang, Jae-Hyeok Lee
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2019
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/7854728ef47b45d1b388938d9fbc5f3e
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spelling	oai:doaj.org-article:7854728ef47b45d1b388938d9fbc5f3e2021-12-02T15:09:41ZCell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii10.1038/s41598-019-48523-42045-2322https://doaj.org/article/7854728ef47b45d1b388938d9fbc5f3e2019-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-019-48523-4https://doaj.org/toc/2045-2322Abstract An intact cell wall is critical for cellular interactions with the environment and protecting the cell from environmental challenges. Signaling mechanisms are necessary to monitor cell wall integrity and to regulate cell wall production and remodeling during growth and division cycles. The green alga, Chlamydomonas, has a proteinaceous cell wall of defined structure that is readily removed by gametolysin (g-lysin), a metalloprotease released during sexual mating. Naked cells treated with g-lysin induce the mRNA accumulation of >100 cell wall-related genes within an hour, offering a system to study signaling and regulatory mechanisms for de novo cell wall assembly. Combining quantitative RT-PCR and luciferase reporter assays to probe transcript accumulation and promoter activity, we revealed that up to 500-fold upregulation of cell wall-related genes was driven at least partly by transcriptional activation upon g-lysin treatment. To investigate how naked cells trigger this rapid transcriptional activation, we tested whether osmotic stress and cell wall integrity are involved in this process. Under a constant hypotonic condition, comparable levels of cell wall-gene activation were observed by g-lysin treatment. In contrast, cells in an iso- or hypertonic condition showed up to 80% reduction in the g-lysin-induced gene activation, suggesting that osmotic stress is required for full-scale responses to g-lysin treatment. To test whether mechanical perturbation of cell walls is involved, we isolated and examined a new set of cell wall mutants with defective or little cell walls. All cell wall mutants examined showed a constitutive upregulation of cell wall-related genes at a level that is only achieved by treatment with g-lysin in wild-type cells. Our study suggests a cell wall integrity monitoring mechanism that senses both osmotic stress and mechanical defects of cell walls and regulates cell wall-gene expression in Chlamydomonas, which may relate to cell wall integrity signaling mechanisms in other organisms.Evan CronmillerDeepak ToorNai Chun ShaoThamali KariyawasamMing Hsiu WangJae-Hyeok LeeNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 9, Iss 1, Pp 1-14 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Evan Cronmiller Deepak Toor Nai Chun Shao Thamali Kariyawasam Ming Hsiu Wang Jae-Hyeok Lee Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
description	Abstract An intact cell wall is critical for cellular interactions with the environment and protecting the cell from environmental challenges. Signaling mechanisms are necessary to monitor cell wall integrity and to regulate cell wall production and remodeling during growth and division cycles. The green alga, Chlamydomonas, has a proteinaceous cell wall of defined structure that is readily removed by gametolysin (g-lysin), a metalloprotease released during sexual mating. Naked cells treated with g-lysin induce the mRNA accumulation of >100 cell wall-related genes within an hour, offering a system to study signaling and regulatory mechanisms for de novo cell wall assembly. Combining quantitative RT-PCR and luciferase reporter assays to probe transcript accumulation and promoter activity, we revealed that up to 500-fold upregulation of cell wall-related genes was driven at least partly by transcriptional activation upon g-lysin treatment. To investigate how naked cells trigger this rapid transcriptional activation, we tested whether osmotic stress and cell wall integrity are involved in this process. Under a constant hypotonic condition, comparable levels of cell wall-gene activation were observed by g-lysin treatment. In contrast, cells in an iso- or hypertonic condition showed up to 80% reduction in the g-lysin-induced gene activation, suggesting that osmotic stress is required for full-scale responses to g-lysin treatment. To test whether mechanical perturbation of cell walls is involved, we isolated and examined a new set of cell wall mutants with defective or little cell walls. All cell wall mutants examined showed a constitutive upregulation of cell wall-related genes at a level that is only achieved by treatment with g-lysin in wild-type cells. Our study suggests a cell wall integrity monitoring mechanism that senses both osmotic stress and mechanical defects of cell walls and regulates cell wall-gene expression in Chlamydomonas, which may relate to cell wall integrity signaling mechanisms in other organisms.
format	article
author	Evan Cronmiller Deepak Toor Nai Chun Shao Thamali Kariyawasam Ming Hsiu Wang Jae-Hyeok Lee
author_facet	Evan Cronmiller Deepak Toor Nai Chun Shao Thamali Kariyawasam Ming Hsiu Wang Jae-Hyeok Lee
author_sort	Evan Cronmiller
title	Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
title_short	Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
title_full	Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
title_fullStr	Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
title_full_unstemmed	Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii
title_sort	cell wall integrity signaling regulates cell wall-related gene expression in chlamydomonas reinhardtii
publisher	Nature Portfolio
publishDate	2019
url	https://doaj.org/article/7854728ef47b45d1b388938d9fbc5f3e
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Cell wall integrity signaling regulates cell wall-related gene expression in Chlamydomonas reinhardtii

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