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Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis

Phosphoglucose isomerase (PGI) catalyzes the interconversion of fructose-6-phosphate and glucose-6-phosphate, which impacts cell carbon metabolic flow. Arabidopsis (Arabidopsis thaliana) contains two nuclear PGI genes respectively encoding plastidial PGI1 and cytosolic PGI (cPGI). The loss of PGI1 i...

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Autores principales: Liu, Hung-Chi, Chen, Hsiu-Chen, Huang, Tzu-Hsiang, Lue, Wei-Ling, Chen, Jychian, Suen, Der-Fen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9806618/
https://www.ncbi.nlm.nih.gov/pubmed/36271861
http://dx.doi.org/10.1093/plphys/kiac494
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author Liu, Hung-Chi
Chen, Hsiu-Chen
Huang, Tzu-Hsiang
Lue, Wei-Ling
Chen, Jychian
Suen, Der-Fen
author_facet Liu, Hung-Chi
Chen, Hsiu-Chen
Huang, Tzu-Hsiang
Lue, Wei-Ling
Chen, Jychian
Suen, Der-Fen
author_sort Liu, Hung-Chi
collection PubMed
description Phosphoglucose isomerase (PGI) catalyzes the interconversion of fructose-6-phosphate and glucose-6-phosphate, which impacts cell carbon metabolic flow. Arabidopsis (Arabidopsis thaliana) contains two nuclear PGI genes respectively encoding plastidial PGI1 and cytosolic PGI (cPGI). The loss of PGI1 impairs the conversion of F6P of the Calvin–Benson cycle to G6P for the synthesis of transitory starch in leaf chloroplasts. Since cpgi knockout mutants have not yet been obtained, they are thought to be lethal. The cpgi lethality can be rescued by expressing CaMV 35S promoter (p35S)-driven cPGI; however, the complemented line is completely sterile due to pollen degeneration. Here, we generated a cpgi mutant expressing p35S::cPGI-YFP in which YFP fluorescence in developing anthers was undetectable specifically in the tapetum and in pollen, which could be associated with male sterility. We also generated RNAi-cPGI knockdown lines with strong cPGI repression in floral buds that exhibited reduced male fertility due to the degeneration of most pollen. Histological analyses indicated that the synthesis of intersporal callose walls was impaired, causing microsporocytes to fail to separate haploid daughter nuclei to form tetrads, which might be responsible for subsequent pollen degeneration. We successfully isolated cpgi knockout mutants in the progeny of a heterozygous cpgi mutant floral-dipped with sugar solutions. The rescued cpgi mutants exhibited diminished young vegetative growth, reduced female fertility, and impaired intersporal callose wall formation in a meiocyte, and, thus, male sterility. Collectively, our data suggest that cPGI plays a vital role in carbohydrate partitioning, which is indispensable for microsporogenesis and early embryogenesis.
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spelling pubmed-98066182023-01-03 Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis Liu, Hung-Chi Chen, Hsiu-Chen Huang, Tzu-Hsiang Lue, Wei-Ling Chen, Jychian Suen, Der-Fen Plant Physiol Research Article Phosphoglucose isomerase (PGI) catalyzes the interconversion of fructose-6-phosphate and glucose-6-phosphate, which impacts cell carbon metabolic flow. Arabidopsis (Arabidopsis thaliana) contains two nuclear PGI genes respectively encoding plastidial PGI1 and cytosolic PGI (cPGI). The loss of PGI1 impairs the conversion of F6P of the Calvin–Benson cycle to G6P for the synthesis of transitory starch in leaf chloroplasts. Since cpgi knockout mutants have not yet been obtained, they are thought to be lethal. The cpgi lethality can be rescued by expressing CaMV 35S promoter (p35S)-driven cPGI; however, the complemented line is completely sterile due to pollen degeneration. Here, we generated a cpgi mutant expressing p35S::cPGI-YFP in which YFP fluorescence in developing anthers was undetectable specifically in the tapetum and in pollen, which could be associated with male sterility. We also generated RNAi-cPGI knockdown lines with strong cPGI repression in floral buds that exhibited reduced male fertility due to the degeneration of most pollen. Histological analyses indicated that the synthesis of intersporal callose walls was impaired, causing microsporocytes to fail to separate haploid daughter nuclei to form tetrads, which might be responsible for subsequent pollen degeneration. We successfully isolated cpgi knockout mutants in the progeny of a heterozygous cpgi mutant floral-dipped with sugar solutions. The rescued cpgi mutants exhibited diminished young vegetative growth, reduced female fertility, and impaired intersporal callose wall formation in a meiocyte, and, thus, male sterility. Collectively, our data suggest that cPGI plays a vital role in carbohydrate partitioning, which is indispensable for microsporogenesis and early embryogenesis. Oxford University Press 2022-10-22 /pmc/articles/PMC9806618/ /pubmed/36271861 http://dx.doi.org/10.1093/plphys/kiac494 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of American Society of Plant Biologists. https://creativecommons.org/licenses/by-nc-nd/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (https://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Research Article
Liu, Hung-Chi
Chen, Hsiu-Chen
Huang, Tzu-Hsiang
Lue, Wei-Ling
Chen, Jychian
Suen, Der-Fen
Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title_full Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title_fullStr Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title_full_unstemmed Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title_short Cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in Arabidopsis
title_sort cytosolic phosphoglucose isomerase is essential for microsporogenesis and embryogenesis in arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9806618/
https://www.ncbi.nlm.nih.gov/pubmed/36271861
http://dx.doi.org/10.1093/plphys/kiac494
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