The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons

During a plant’s life cycle, plastids undergo several modifications, from undifferentiated pro-plastids to either photosynthetically-active chloroplasts, ezioplasts, chromoplasts or storage organelles, such as amyloplasts, elaioplasts and proteinoplasts. Plastid proteome rearrangements and protein h...

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Main Authors: Nicolaj Jeran, Lisa Rotasperti, Giorgia Frabetti, Anna Calabritto, Paolo Pesaresi, Luca Tadini
Format: Article
Language:English
Published: MDPI AG 2021-09-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/12/9/1387
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author Nicolaj Jeran
Lisa Rotasperti
Giorgia Frabetti
Anna Calabritto
Paolo Pesaresi
Luca Tadini
author_facet Nicolaj Jeran
Lisa Rotasperti
Giorgia Frabetti
Anna Calabritto
Paolo Pesaresi
Luca Tadini
author_sort Nicolaj Jeran
collection DOAJ
description During a plant’s life cycle, plastids undergo several modifications, from undifferentiated pro-plastids to either photosynthetically-active chloroplasts, ezioplasts, chromoplasts or storage organelles, such as amyloplasts, elaioplasts and proteinoplasts. Plastid proteome rearrangements and protein homeostasis, together with intracellular communication pathways, are key factors for correct plastid differentiation and functioning. When plastid development is affected, aberrant organelles are degraded and recycled in a process that involves plastid protein ubiquitination. In this study, we have analysed the Arabidopsis <i>gun1-102 ftsh5-3</i> double mutant, lacking both the plastid-located protein GUN1 (Genomes Uncoupled 1), involved in plastid-to-nucleus communication, and the chloroplast-located <i>FTSH</i>5 (Filamentous temperature-sensitive H5), a metalloprotease with a role in photosystem repair and chloroplast biogenesis. <i>gun1-102 ftsh5-3</i> seedlings show variegated cotyledons and true leaves that we attempted to suppress by introgressing second-site mutations in genes involved in: (i) plastid translation, (ii) plastid folding/import and (iii) cytosolic protein ubiquitination. Different phenotypic effects, ranging from seedling-lethality to partial or complete suppression of the variegated phenotype, were observed in the corresponding triple mutants. Our findings indicate that Plant U-Box 4 (PUB4) E3 ubiquitin ligase plays a major role in the target degradation of damaged chloroplasts and is the main contributor to the variegated phenotype observed in <i>gun1-102 ftsh5-3</i> seedlings.
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spelling doaj.art-421b516733af410699d497ab625d76502023-11-22T13:14:17ZengMDPI AGGenes2073-44252021-09-01129138710.3390/genes12091387The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis CotyledonsNicolaj Jeran0Lisa Rotasperti1Giorgia Frabetti2Anna Calabritto3Paolo Pesaresi4Luca Tadini5Dipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDipartimento di Bioscienze, Università degli Studi di Milano, 20133 Milano, ItalyDuring a plant’s life cycle, plastids undergo several modifications, from undifferentiated pro-plastids to either photosynthetically-active chloroplasts, ezioplasts, chromoplasts or storage organelles, such as amyloplasts, elaioplasts and proteinoplasts. Plastid proteome rearrangements and protein homeostasis, together with intracellular communication pathways, are key factors for correct plastid differentiation and functioning. When plastid development is affected, aberrant organelles are degraded and recycled in a process that involves plastid protein ubiquitination. In this study, we have analysed the Arabidopsis <i>gun1-102 ftsh5-3</i> double mutant, lacking both the plastid-located protein GUN1 (Genomes Uncoupled 1), involved in plastid-to-nucleus communication, and the chloroplast-located <i>FTSH</i>5 (Filamentous temperature-sensitive H5), a metalloprotease with a role in photosystem repair and chloroplast biogenesis. <i>gun1-102 ftsh5-3</i> seedlings show variegated cotyledons and true leaves that we attempted to suppress by introgressing second-site mutations in genes involved in: (i) plastid translation, (ii) plastid folding/import and (iii) cytosolic protein ubiquitination. Different phenotypic effects, ranging from seedling-lethality to partial or complete suppression of the variegated phenotype, were observed in the corresponding triple mutants. Our findings indicate that Plant U-Box 4 (PUB4) E3 ubiquitin ligase plays a major role in the target degradation of damaged chloroplasts and is the main contributor to the variegated phenotype observed in <i>gun1-102 ftsh5-3</i> seedlings.https://www.mdpi.com/2073-4425/12/9/1387chloroplastubiquitinationvariegated phenotypeprotein homeostasis
spellingShingle Nicolaj Jeran
Lisa Rotasperti
Giorgia Frabetti
Anna Calabritto
Paolo Pesaresi
Luca Tadini
The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
Genes
chloroplast
ubiquitination
variegated phenotype
protein homeostasis
title The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
title_full The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
title_fullStr The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
title_full_unstemmed The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
title_short The PUB4 E3 Ubiquitin Ligase Is Responsible for the Variegated Phenotype Observed upon Alteration of Chloroplast Protein Homeostasis in Arabidopsis Cotyledons
title_sort pub4 e3 ubiquitin ligase is responsible for the variegated phenotype observed upon alteration of chloroplast protein homeostasis in arabidopsis cotyledons
topic chloroplast
ubiquitination
variegated phenotype
protein homeostasis
url https://www.mdpi.com/2073-4425/12/9/1387
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