Cargando…
The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane
Since membranes play essential roles in all living beings, all cells have developed mechanisms for efficient and fast repair of membrane damage. In Escherichia coli, the Phage shock stress A (PspA) protein is involved in the maintenance of the integrity of its inner membrane in response to the damag...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2020
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7479267/ https://www.ncbi.nlm.nih.gov/pubmed/32983195 http://dx.doi.org/10.3389/fpls.2020.01305 |
_version_ | 1783580235087740928 |
---|---|
author | Micol-Ponce, Rosa García-Alcázar, Manuel Capel, Carmen Yuste-Lisbona, Fernando Juan Pineda, Benito Atarés, Alejandro García-Sogo, Begoña Capel, Juan Moreno, Vicente Lozano, Rafael |
author_facet | Micol-Ponce, Rosa García-Alcázar, Manuel Capel, Carmen Yuste-Lisbona, Fernando Juan Pineda, Benito Atarés, Alejandro García-Sogo, Begoña Capel, Juan Moreno, Vicente Lozano, Rafael |
author_sort | Micol-Ponce, Rosa |
collection | PubMed |
description | Since membranes play essential roles in all living beings, all cells have developed mechanisms for efficient and fast repair of membrane damage. In Escherichia coli, the Phage shock stress A (PspA) protein is involved in the maintenance of the integrity of its inner membrane in response to the damage produced by exposure to stress conditions. A role in thylakoid membrane maintenance and reorganization has been proposed for Vesicle Inducing Protein in Plastid 1 (VIPP1), the putative PspA ortholog in Arabidopsis thaliana. While some membranes of plant cells have been extensively studied, the biosynthesis and maintenance of chloroplast thylakoid membrane remains poorly known. Here, we report the cloning and functional characterization of the tomato (Solanum lycopersicum L.) ortholog of Escherichia coli PspA and Arabidopsis thaliana VIPP1, which we dubbed SlVIPP1. Our genetic and molecular characterization of slvipp1, an insertional mutant, allowed us to conclude that the tomato SlVIPP1 gene is needed for development, as Arabidopsis VIPP1, but not Escherichia coli PspA. Homozygous slvipp1 tomato plants are albino and exhibit early lethality and highly aberrant chloroplast development with almost complete absence of thylakoids. The phenotype of tomato RNAi lines and that of additional slvipp1 alleles generated by CRISPR/Cas9 gene editing technology confirmed that the morphological and histological aberrations shown by slvipp1 homozygotes are caused by VIPP1 lack of function. We also found that tomato SlVIPP1 overexpression does not cause any visible effect on plant morphology and viability. Our work with slvipp1 plants evidences that SlVIPP1 is an essential gene required for tomato survival, since its function is crucial for the proper formation and/or maintenance of thylakoid membranes. |
format | Online Article Text |
id | pubmed-7479267 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-74792672020-09-26 The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane Micol-Ponce, Rosa García-Alcázar, Manuel Capel, Carmen Yuste-Lisbona, Fernando Juan Pineda, Benito Atarés, Alejandro García-Sogo, Begoña Capel, Juan Moreno, Vicente Lozano, Rafael Front Plant Sci Plant Science Since membranes play essential roles in all living beings, all cells have developed mechanisms for efficient and fast repair of membrane damage. In Escherichia coli, the Phage shock stress A (PspA) protein is involved in the maintenance of the integrity of its inner membrane in response to the damage produced by exposure to stress conditions. A role in thylakoid membrane maintenance and reorganization has been proposed for Vesicle Inducing Protein in Plastid 1 (VIPP1), the putative PspA ortholog in Arabidopsis thaliana. While some membranes of plant cells have been extensively studied, the biosynthesis and maintenance of chloroplast thylakoid membrane remains poorly known. Here, we report the cloning and functional characterization of the tomato (Solanum lycopersicum L.) ortholog of Escherichia coli PspA and Arabidopsis thaliana VIPP1, which we dubbed SlVIPP1. Our genetic and molecular characterization of slvipp1, an insertional mutant, allowed us to conclude that the tomato SlVIPP1 gene is needed for development, as Arabidopsis VIPP1, but not Escherichia coli PspA. Homozygous slvipp1 tomato plants are albino and exhibit early lethality and highly aberrant chloroplast development with almost complete absence of thylakoids. The phenotype of tomato RNAi lines and that of additional slvipp1 alleles generated by CRISPR/Cas9 gene editing technology confirmed that the morphological and histological aberrations shown by slvipp1 homozygotes are caused by VIPP1 lack of function. We also found that tomato SlVIPP1 overexpression does not cause any visible effect on plant morphology and viability. Our work with slvipp1 plants evidences that SlVIPP1 is an essential gene required for tomato survival, since its function is crucial for the proper formation and/or maintenance of thylakoid membranes. Frontiers Media S.A. 2020-08-26 /pmc/articles/PMC7479267/ /pubmed/32983195 http://dx.doi.org/10.3389/fpls.2020.01305 Text en Copyright © 2020 Micol-Ponce, García-Alcázar, Capel, Yuste-Lisbona, Pineda, Atarés, García-Sogo, Capel, Moreno and Lozano http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Plant Science Micol-Ponce, Rosa García-Alcázar, Manuel Capel, Carmen Yuste-Lisbona, Fernando Juan Pineda, Benito Atarés, Alejandro García-Sogo, Begoña Capel, Juan Moreno, Vicente Lozano, Rafael The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title | The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title_full | The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title_fullStr | The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title_full_unstemmed | The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title_short | The Tomato SlVIPP1 Gene Is Required for Plant Survival Through the Proper Development of Chloroplast Thylakoid Membrane |
title_sort | tomato slvipp1 gene is required for plant survival through the proper development of chloroplast thylakoid membrane |
topic | Plant Science |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7479267/ https://www.ncbi.nlm.nih.gov/pubmed/32983195 http://dx.doi.org/10.3389/fpls.2020.01305 |
work_keys_str_mv | AT micolponcerosa thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT garciaalcazarmanuel thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT capelcarmen thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT yustelisbonafernandojuan thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT pinedabenito thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT ataresalejandro thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT garciasogobegona thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT capeljuan thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT morenovicente thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT lozanorafael thetomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT micolponcerosa tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT garciaalcazarmanuel tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT capelcarmen tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT yustelisbonafernandojuan tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT pinedabenito tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT ataresalejandro tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT garciasogobegona tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT capeljuan tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT morenovicente tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane AT lozanorafael tomatoslvipp1geneisrequiredforplantsurvivalthroughtheproperdevelopmentofchloroplastthylakoidmembrane |