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Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2

BACKGROUND: Our previous transcriptomic analysis revealed that downregulation of nitrogen and carbon metabolism in the basal portions of the shoots inhibited cytosolic glutamine synthetase1;2 (GS1;2), which severely reduced rice tiller number. In the present study, we used rice mutants lacking GS1;2...

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Autores principales: Ohashi, Miwa, Ishiyama, Keiki, Kusano, Miyako, Fukushima, Atsushi, Kojima, Soichi, Hayakawa, Toshihiko, Yamaya, Tomoyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer US 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303225/
https://www.ncbi.nlm.nih.gov/pubmed/30578468
http://dx.doi.org/10.1186/s12284-018-0261-y
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author Ohashi, Miwa
Ishiyama, Keiki
Kusano, Miyako
Fukushima, Atsushi
Kojima, Soichi
Hayakawa, Toshihiko
Yamaya, Tomoyuki
author_facet Ohashi, Miwa
Ishiyama, Keiki
Kusano, Miyako
Fukushima, Atsushi
Kojima, Soichi
Hayakawa, Toshihiko
Yamaya, Tomoyuki
author_sort Ohashi, Miwa
collection PubMed
description BACKGROUND: Our previous transcriptomic analysis revealed that downregulation of nitrogen and carbon metabolism in the basal portions of the shoots inhibited cytosolic glutamine synthetase1;2 (GS1;2), which severely reduced rice tiller number. In the present study, we used rice mutants lacking GS1;2 (gs1;2 mutants) to determine the contribution of carbon metabolism to tiller growth. RESULTS: Metabolomic analysis indicated the effects of carbon metabolism disorder such as reductions in the levels of sugar metabolites (e.g., sucrose and glucose 6-phosphate) in the shoot basal portions of the gs1;2 mutant seedlings. Decrease in sucrose caused by the lack of GS1;2 was successfully restored to the wild-type levels by introducing OsGS1;2 cDNA into the mutants. In the basal portions of the shoots, the lack of GS1;2 caused low expression of cytosolic fructose 1,6-bisphosphatase2 (OscFBP2), which is a key cytosolic sucrose synthesis enzyme; it is especially important in the phloem companion cells of the nodal vascular anastomoses. NH(4)(+) supply upregulated OscFBP2 expression in the shoot basal portions of the wild type but not in those of the gs1;2 mutants. Rice mutants lacking cFBPase2 presented with ~ 30% reduction in total cFBPase activity in the basal portions of their shoots. These mutants displayed reductions in sucrose levels of the basal portions of their shoots but not in their leaf blades. They also had relatively lower tiller numbers at the early growth stage. CONCLUSIONS: Metabolomic analysis revealed that the lack of GS1;2 reduced sucrose metabolism in the basal portions of the shoots. Our results indicated that sucrose reduction was caused by the downregulation of OscFBP2 expression in the basal portions of the gs1;2 mutant shoots. The reduction in sucrose content caused by the lack of cFBPase2 resulted in lower tiller number at the early growth stage. Therefore, adequate sucrose supply via cFBPase2 may be necessary for tiller growth in the basal portions of rice shoots. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12284-018-0261-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-63032252019-01-04 Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2 Ohashi, Miwa Ishiyama, Keiki Kusano, Miyako Fukushima, Atsushi Kojima, Soichi Hayakawa, Toshihiko Yamaya, Tomoyuki Rice (N Y) Original Article BACKGROUND: Our previous transcriptomic analysis revealed that downregulation of nitrogen and carbon metabolism in the basal portions of the shoots inhibited cytosolic glutamine synthetase1;2 (GS1;2), which severely reduced rice tiller number. In the present study, we used rice mutants lacking GS1;2 (gs1;2 mutants) to determine the contribution of carbon metabolism to tiller growth. RESULTS: Metabolomic analysis indicated the effects of carbon metabolism disorder such as reductions in the levels of sugar metabolites (e.g., sucrose and glucose 6-phosphate) in the shoot basal portions of the gs1;2 mutant seedlings. Decrease in sucrose caused by the lack of GS1;2 was successfully restored to the wild-type levels by introducing OsGS1;2 cDNA into the mutants. In the basal portions of the shoots, the lack of GS1;2 caused low expression of cytosolic fructose 1,6-bisphosphatase2 (OscFBP2), which is a key cytosolic sucrose synthesis enzyme; it is especially important in the phloem companion cells of the nodal vascular anastomoses. NH(4)(+) supply upregulated OscFBP2 expression in the shoot basal portions of the wild type but not in those of the gs1;2 mutants. Rice mutants lacking cFBPase2 presented with ~ 30% reduction in total cFBPase activity in the basal portions of their shoots. These mutants displayed reductions in sucrose levels of the basal portions of their shoots but not in their leaf blades. They also had relatively lower tiller numbers at the early growth stage. CONCLUSIONS: Metabolomic analysis revealed that the lack of GS1;2 reduced sucrose metabolism in the basal portions of the shoots. Our results indicated that sucrose reduction was caused by the downregulation of OscFBP2 expression in the basal portions of the gs1;2 mutant shoots. The reduction in sucrose content caused by the lack of cFBPase2 resulted in lower tiller number at the early growth stage. Therefore, adequate sucrose supply via cFBPase2 may be necessary for tiller growth in the basal portions of rice shoots. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12284-018-0261-y) contains supplementary material, which is available to authorized users. Springer US 2018-12-22 /pmc/articles/PMC6303225/ /pubmed/30578468 http://dx.doi.org/10.1186/s12284-018-0261-y Text en © The Author(s). 2018 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.
spellingShingle Original Article
Ohashi, Miwa
Ishiyama, Keiki
Kusano, Miyako
Fukushima, Atsushi
Kojima, Soichi
Hayakawa, Toshihiko
Yamaya, Tomoyuki
Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title_full Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title_fullStr Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title_full_unstemmed Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title_short Reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
title_sort reduction in sucrose contents by downregulation of fructose-1,6-bisphosphatase 2 causes tiller outgrowth cessation in rice mutants lacking glutamine synthetase1;2
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6303225/
https://www.ncbi.nlm.nih.gov/pubmed/30578468
http://dx.doi.org/10.1186/s12284-018-0261-y
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