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Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots

Plant roots depend on sucrose imported from leaves as the substrate for metabolism and growth. Sucrose and hexoses derived from it are also signalling molecules that modulate growth and development, but the importance for signalling of endogenous changes in sugar levels is poorly understood. We repo...

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Autores principales: Pignocchi, Cristina, Ivakov, Alexander, Feil, Regina, Trick, Martin, Pike, Marilyn, Wang, Trevor L, Lunn, John E, Smith, Alison M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7921298/
https://www.ncbi.nlm.nih.gov/pubmed/33378456
http://dx.doi.org/10.1093/jxb/eraa581
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author Pignocchi, Cristina
Ivakov, Alexander
Feil, Regina
Trick, Martin
Pike, Marilyn
Wang, Trevor L
Lunn, John E
Smith, Alison M
author_facet Pignocchi, Cristina
Ivakov, Alexander
Feil, Regina
Trick, Martin
Pike, Marilyn
Wang, Trevor L
Lunn, John E
Smith, Alison M
author_sort Pignocchi, Cristina
collection PubMed
description Plant roots depend on sucrose imported from leaves as the substrate for metabolism and growth. Sucrose and hexoses derived from it are also signalling molecules that modulate growth and development, but the importance for signalling of endogenous changes in sugar levels is poorly understood. We report that reduced activity of cytosolic invertase, which converts sucrose to hexoses, leads to pronounced metabolic, growth, and developmental defects in roots of Arabidopsis (Arabidopsis thaliana) seedlings. In addition to altered sugar and downstream metabolite levels, roots of cinv1 cinv2 mutants have reduced elongation rates, cell and meristem size, abnormal meristematic cell division patterns, and altered expression of thousands of genes of diverse functions. Provision of exogenous glucose to mutant roots repairs relatively few of the defects. The extensive transcriptional differences between mutant and wild-type roots have hallmarks of both high sucrose and low hexose signalling. We conclude that the mutant phenotype reflects both low carbon availability for metabolism and growth and complex sugar signals derived from elevated sucrose and depressed hexose levels in the cytosol of mutant roots. Such reciprocal changes in endogenous sucrose and hexose levels potentially provide rich information about sugar status that translates into flexible adjustments of growth and development.
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spelling pubmed-79212982021-03-05 Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots Pignocchi, Cristina Ivakov, Alexander Feil, Regina Trick, Martin Pike, Marilyn Wang, Trevor L Lunn, John E Smith, Alison M J Exp Bot Research Papers Plant roots depend on sucrose imported from leaves as the substrate for metabolism and growth. Sucrose and hexoses derived from it are also signalling molecules that modulate growth and development, but the importance for signalling of endogenous changes in sugar levels is poorly understood. We report that reduced activity of cytosolic invertase, which converts sucrose to hexoses, leads to pronounced metabolic, growth, and developmental defects in roots of Arabidopsis (Arabidopsis thaliana) seedlings. In addition to altered sugar and downstream metabolite levels, roots of cinv1 cinv2 mutants have reduced elongation rates, cell and meristem size, abnormal meristematic cell division patterns, and altered expression of thousands of genes of diverse functions. Provision of exogenous glucose to mutant roots repairs relatively few of the defects. The extensive transcriptional differences between mutant and wild-type roots have hallmarks of both high sucrose and low hexose signalling. We conclude that the mutant phenotype reflects both low carbon availability for metabolism and growth and complex sugar signals derived from elevated sucrose and depressed hexose levels in the cytosol of mutant roots. Such reciprocal changes in endogenous sucrose and hexose levels potentially provide rich information about sugar status that translates into flexible adjustments of growth and development. Oxford University Press 2020-12-30 /pmc/articles/PMC7921298/ /pubmed/33378456 http://dx.doi.org/10.1093/jxb/eraa581 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Experimental Biology. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Papers
Pignocchi, Cristina
Ivakov, Alexander
Feil, Regina
Trick, Martin
Pike, Marilyn
Wang, Trevor L
Lunn, John E
Smith, Alison M
Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title_full Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title_fullStr Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title_full_unstemmed Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title_short Restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in Arabidopsis roots
title_sort restriction of cytosolic sucrose hydrolysis profoundly alters development, metabolism, and gene expression in arabidopsis roots
topic Research Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7921298/
https://www.ncbi.nlm.nih.gov/pubmed/33378456
http://dx.doi.org/10.1093/jxb/eraa581
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