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The role of invertases in plant compensatory responses to simulated herbivory

BACKGROUND: The ability of a plant to overcome animal-induced damage is referred to as compensation or tolerance and ranges from undercompensation (decreased fitness when damaged) to overcompensation (increased fitness when damaged). Although it is clear that genetic variation for compensation exist...

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Autores principales: Siddappaji, Madhura H., Scholes, Daniel R., Krishnankutty, Sindhu M., Calla, Bernarda, Clough, Steven J., Zielinski, Raymond E., Paige, Ken N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4647499/
https://www.ncbi.nlm.nih.gov/pubmed/26572986
http://dx.doi.org/10.1186/s12870-015-0655-6
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author Siddappaji, Madhura H.
Scholes, Daniel R.
Krishnankutty, Sindhu M.
Calla, Bernarda
Clough, Steven J.
Zielinski, Raymond E.
Paige, Ken N.
author_facet Siddappaji, Madhura H.
Scholes, Daniel R.
Krishnankutty, Sindhu M.
Calla, Bernarda
Clough, Steven J.
Zielinski, Raymond E.
Paige, Ken N.
author_sort Siddappaji, Madhura H.
collection PubMed
description BACKGROUND: The ability of a plant to overcome animal-induced damage is referred to as compensation or tolerance and ranges from undercompensation (decreased fitness when damaged) to overcompensation (increased fitness when damaged). Although it is clear that genetic variation for compensation exists among plants, little is known about the specific genetic underpinnings leading to enhanced fitness. Our previous study identified the enzyme GLUCOSE-6-PHOSPHATE DEHYDROGENASE 1 (G6PD1) as a key regulator contributing to the phenomenon of overcompensation via its role in the oxidative pentose phosphate pathway (OPPP). Apart from G6PD1 we also identified an invertase gene which was up-regulated following damage and that potentially integrates with the OPPP. The invertase family of enzymes hydrolyze sucrose to glucose and fructose, whereby the glucose produced is shunted into the OPPP and presumably supports plant regrowth, development, and ultimately compensation. In the current study, we measured the relative expression of 12 invertase genes over the course of plant development in the Arabidopsis thaliana genotypes Columbia-4 and Landsberg erecta, which typically overcompensate and undercompensate, respectively, when damaged. We also compared the compensatory performances of a set of invertase knockout mutants to the Columbia-4 wild type. RESULTS: We report that Columbia-4 significantly up-regulated 9 of 12 invertase genes when damaged relative to when undamaged, and ultimately overcompensated for fruit production. Landsberg erecta, in contrast, down-regulated two invertase genes following damage and suffered reduced fitness. Knockout mutants of two invertase genes both exhibited significant undercompensation for fruit production, exhibiting a complete reversal of the wild type Col-4’s overcompensation. CONCLUSION: Collectively, these results confirm that invertases are essential for not only normal plant growth and development, but also plants’ abilities to regrow and ultimately compensate for fitness following apical damage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0655-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-46474992015-11-18 The role of invertases in plant compensatory responses to simulated herbivory Siddappaji, Madhura H. Scholes, Daniel R. Krishnankutty, Sindhu M. Calla, Bernarda Clough, Steven J. Zielinski, Raymond E. Paige, Ken N. BMC Plant Biol Research Article BACKGROUND: The ability of a plant to overcome animal-induced damage is referred to as compensation or tolerance and ranges from undercompensation (decreased fitness when damaged) to overcompensation (increased fitness when damaged). Although it is clear that genetic variation for compensation exists among plants, little is known about the specific genetic underpinnings leading to enhanced fitness. Our previous study identified the enzyme GLUCOSE-6-PHOSPHATE DEHYDROGENASE 1 (G6PD1) as a key regulator contributing to the phenomenon of overcompensation via its role in the oxidative pentose phosphate pathway (OPPP). Apart from G6PD1 we also identified an invertase gene which was up-regulated following damage and that potentially integrates with the OPPP. The invertase family of enzymes hydrolyze sucrose to glucose and fructose, whereby the glucose produced is shunted into the OPPP and presumably supports plant regrowth, development, and ultimately compensation. In the current study, we measured the relative expression of 12 invertase genes over the course of plant development in the Arabidopsis thaliana genotypes Columbia-4 and Landsberg erecta, which typically overcompensate and undercompensate, respectively, when damaged. We also compared the compensatory performances of a set of invertase knockout mutants to the Columbia-4 wild type. RESULTS: We report that Columbia-4 significantly up-regulated 9 of 12 invertase genes when damaged relative to when undamaged, and ultimately overcompensated for fruit production. Landsberg erecta, in contrast, down-regulated two invertase genes following damage and suffered reduced fitness. Knockout mutants of two invertase genes both exhibited significant undercompensation for fruit production, exhibiting a complete reversal of the wild type Col-4’s overcompensation. CONCLUSION: Collectively, these results confirm that invertases are essential for not only normal plant growth and development, but also plants’ abilities to regrow and ultimately compensate for fitness following apical damage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-015-0655-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-11-16 /pmc/articles/PMC4647499/ /pubmed/26572986 http://dx.doi.org/10.1186/s12870-015-0655-6 Text en © Siddappaji et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Siddappaji, Madhura H.
Scholes, Daniel R.
Krishnankutty, Sindhu M.
Calla, Bernarda
Clough, Steven J.
Zielinski, Raymond E.
Paige, Ken N.
The role of invertases in plant compensatory responses to simulated herbivory
title The role of invertases in plant compensatory responses to simulated herbivory
title_full The role of invertases in plant compensatory responses to simulated herbivory
title_fullStr The role of invertases in plant compensatory responses to simulated herbivory
title_full_unstemmed The role of invertases in plant compensatory responses to simulated herbivory
title_short The role of invertases in plant compensatory responses to simulated herbivory
title_sort role of invertases in plant compensatory responses to simulated herbivory
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4647499/
https://www.ncbi.nlm.nih.gov/pubmed/26572986
http://dx.doi.org/10.1186/s12870-015-0655-6
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