Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability

Grain filling ability is mainly affected by the translocation of carbohydrates generated from temporarily stored stem starch in most field crops including rice (Oryza sativa L.). The partitioning of non-structural stem carbohydrates has been recognized as an important trait for raising the yield cei...

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Autores principales: Wada, H., Masumoto-Kubo, C., Tsutsumi, K., Nonami, H., Tanaka, F., Okada, H., Erra-Balsells, R., Hiraoka, K., Nakashima, T., Hakata, M., Morita, S.
Formato: JOUR
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Acceso en línea:http://hdl.handle.net/20.500.12110/paper_19326203_v12_n7_p_Wada
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id todo:paper_19326203_v12_n7_p_Wada
record_format dspace
institution Universidad de Buenos Aires
institution_str I-28
repository_str R-134
collection Biblioteca Digital - Facultad de Ciencias Exactas y Naturales (UBA)
topic carbohydrate
carbon 13
starch
plant protein
starch
water
AMY2A gene
Article
BAM2 gene
bioaccumulation
biodegradation
biological model
carbohydrate metabolism
controlled study
cultivar
gene expression profiling
gene expression regulation
grain filling ability
grain weight
GWD1 gene
isotope labeling
mass spectrometry
mean panicle number
metabolic regulation
nonhuman
nonstructural stem carbohydrate partitioning
number of spikelets per panicle
panicle weight
percentage of ripened grain
phosphorylation
plant gene
plant parameters
plant stem
plant yield
plant yield component
reference value
rice
species difference
species diversity
starch degradation
starch phosphorylation
transcription regulation
turgor pressure
water content
genetics
growth, development and aging
metabolism
Oryza
phosphorylation
physiology
plant stem
Gene Expression Profiling
Oryza
Phosphorylation
Plant Proteins
Plant Stems
Starch
Water
spellingShingle carbohydrate
carbon 13
starch
plant protein
starch
water
AMY2A gene
Article
BAM2 gene
bioaccumulation
biodegradation
biological model
carbohydrate metabolism
controlled study
cultivar
gene expression profiling
gene expression regulation
grain filling ability
grain weight
GWD1 gene
isotope labeling
mass spectrometry
mean panicle number
metabolic regulation
nonhuman
nonstructural stem carbohydrate partitioning
number of spikelets per panicle
panicle weight
percentage of ripened grain
phosphorylation
plant gene
plant parameters
plant stem
plant yield
plant yield component
reference value
rice
species difference
species diversity
starch degradation
starch phosphorylation
transcription regulation
turgor pressure
water content
genetics
growth, development and aging
metabolism
Oryza
phosphorylation
physiology
plant stem
Gene Expression Profiling
Oryza
Phosphorylation
Plant Proteins
Plant Stems
Starch
Water
Wada, H.
Masumoto-Kubo, C.
Tsutsumi, K.
Nonami, H.
Tanaka, F.
Okada, H.
Erra-Balsells, R.
Hiraoka, K.
Nakashima, T.
Hakata, M.
Morita, S.
Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
topic_facet carbohydrate
carbon 13
starch
plant protein
starch
water
AMY2A gene
Article
BAM2 gene
bioaccumulation
biodegradation
biological model
carbohydrate metabolism
controlled study
cultivar
gene expression profiling
gene expression regulation
grain filling ability
grain weight
GWD1 gene
isotope labeling
mass spectrometry
mean panicle number
metabolic regulation
nonhuman
nonstructural stem carbohydrate partitioning
number of spikelets per panicle
panicle weight
percentage of ripened grain
phosphorylation
plant gene
plant parameters
plant stem
plant yield
plant yield component
reference value
rice
species difference
species diversity
starch degradation
starch phosphorylation
transcription regulation
turgor pressure
water content
genetics
growth, development and aging
metabolism
Oryza
phosphorylation
physiology
plant stem
Gene Expression Profiling
Oryza
Phosphorylation
Plant Proteins
Plant Stems
Starch
Water
description Grain filling ability is mainly affected by the translocation of carbohydrates generated from temporarily stored stem starch in most field crops including rice (Oryza sativa L.). The partitioning of non-structural stem carbohydrates has been recognized as an important trait for raising the yield ceiling, yet we still do not fully understand how carbohydrate partitioning occurs in the stems. In this study, two rice subspecies that exhibit different patterns of nonstructural stem carbohydrates partitioning, a japonica-dominant cultivar, Momiroman, and an indica-dominant cultivar, Hokuriku 193, were used as the model system to study the relationship between turgor pressure and metabolic regulation of non-structural stem carbohydrates, by combining the water status measurement with gene expression analysis and a dynamic prefixed 13 C tracer analysis using a mass spectrometer. Here, we report a clear varietal difference in turgor-associated starch phosphorylation occurred at the initiation of non-structural carbohydrate partitioning. The data indicated that starch degradation in Hokuriku 193 stems occurred at full-heading, 5 days earlier than in Momiroman, contributing to greater sink filling. Gene expression analysis revealed that expression pattern of the gene encoding α-glucan, water dikinase (GWD1) was similar between two varieties, and the maximum expression level in Hokuriku 193, reached at full heading (4 DAH), was greater than in Momiroman, leading to an earlier increase in a series of amylase-related gene expression in Hokuriku 193. In both varieties, peaks in turgor pressure preceded the increases in GWD1 expression, and changes in GWD1 expression was correlated with turgor pressure. Additionally, a threshold is likely to exist for GWD1 expression to facilitate starch degradation. Taken together, these results raise the possibility that turgor-associated starch phosphorylation in cells is responsible for the metabolism that leads to starch degradation. Because the two cultivars exhibited remarkable varietal differences in the pattern of non-structural carbohydrate partitioning, our findings propose that the observed difference in grain-filling ability originated from turgor-associated regulation of starch phosphorylation in stem parenchyma cells. Further understanding of the molecular mechanism of turgor-regulation may provide a new selection criterion for breaking the yield barriers in crop production. © 2017 Wada et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
format JOUR
author Wada, H.
Masumoto-Kubo, C.
Tsutsumi, K.
Nonami, H.
Tanaka, F.
Okada, H.
Erra-Balsells, R.
Hiraoka, K.
Nakashima, T.
Hakata, M.
Morita, S.
author_facet Wada, H.
Masumoto-Kubo, C.
Tsutsumi, K.
Nonami, H.
Tanaka, F.
Okada, H.
Erra-Balsells, R.
Hiraoka, K.
Nakashima, T.
Hakata, M.
Morita, S.
author_sort Wada, H.
title Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
title_short Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
title_full Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
title_fullStr Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
title_full_unstemmed Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability
title_sort turgor-responsive starch phosphorylation in oryza sativa stems: a primary event of starch degradation associated with grain-filling ability
url http://hdl.handle.net/20.500.12110/paper_19326203_v12_n7_p_Wada
work_keys_str_mv AT wadah turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT masumotokuboc turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT tsutsumik turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT nonamih turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT tanakaf turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT okadah turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT errabalsellsr turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT hiraokak turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
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AT hakatam turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
AT moritas turgorresponsivestarchphosphorylationinoryzasativastemsaprimaryeventofstarchdegradationassociatedwithgrainfillingability
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spelling todo:paper_19326203_v12_n7_p_Wada2023-10-03T16:34:51Z Turgor-responsive starch phosphorylation in Oryza sativa stems: A primary event of starch degradation associated with grain-filling ability Wada, H. Masumoto-Kubo, C. Tsutsumi, K. Nonami, H. Tanaka, F. Okada, H. Erra-Balsells, R. Hiraoka, K. Nakashima, T. Hakata, M. Morita, S. carbohydrate carbon 13 starch plant protein starch water AMY2A gene Article BAM2 gene bioaccumulation biodegradation biological model carbohydrate metabolism controlled study cultivar gene expression profiling gene expression regulation grain filling ability grain weight GWD1 gene isotope labeling mass spectrometry mean panicle number metabolic regulation nonhuman nonstructural stem carbohydrate partitioning number of spikelets per panicle panicle weight percentage of ripened grain phosphorylation plant gene plant parameters plant stem plant yield plant yield component reference value rice species difference species diversity starch degradation starch phosphorylation transcription regulation turgor pressure water content genetics growth, development and aging metabolism Oryza phosphorylation physiology plant stem Gene Expression Profiling Oryza Phosphorylation Plant Proteins Plant Stems Starch Water Grain filling ability is mainly affected by the translocation of carbohydrates generated from temporarily stored stem starch in most field crops including rice (Oryza sativa L.). The partitioning of non-structural stem carbohydrates has been recognized as an important trait for raising the yield ceiling, yet we still do not fully understand how carbohydrate partitioning occurs in the stems. In this study, two rice subspecies that exhibit different patterns of nonstructural stem carbohydrates partitioning, a japonica-dominant cultivar, Momiroman, and an indica-dominant cultivar, Hokuriku 193, were used as the model system to study the relationship between turgor pressure and metabolic regulation of non-structural stem carbohydrates, by combining the water status measurement with gene expression analysis and a dynamic prefixed 13 C tracer analysis using a mass spectrometer. Here, we report a clear varietal difference in turgor-associated starch phosphorylation occurred at the initiation of non-structural carbohydrate partitioning. The data indicated that starch degradation in Hokuriku 193 stems occurred at full-heading, 5 days earlier than in Momiroman, contributing to greater sink filling. Gene expression analysis revealed that expression pattern of the gene encoding α-glucan, water dikinase (GWD1) was similar between two varieties, and the maximum expression level in Hokuriku 193, reached at full heading (4 DAH), was greater than in Momiroman, leading to an earlier increase in a series of amylase-related gene expression in Hokuriku 193. In both varieties, peaks in turgor pressure preceded the increases in GWD1 expression, and changes in GWD1 expression was correlated with turgor pressure. Additionally, a threshold is likely to exist for GWD1 expression to facilitate starch degradation. Taken together, these results raise the possibility that turgor-associated starch phosphorylation in cells is responsible for the metabolism that leads to starch degradation. Because the two cultivars exhibited remarkable varietal differences in the pattern of non-structural carbohydrate partitioning, our findings propose that the observed difference in grain-filling ability originated from turgor-associated regulation of starch phosphorylation in stem parenchyma cells. Further understanding of the molecular mechanism of turgor-regulation may provide a new selection criterion for breaking the yield barriers in crop production. © 2017 Wada et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. JOUR info:eu-repo/semantics/openAccess http://creativecommons.org/licenses/by/2.5/ar http://hdl.handle.net/20.500.12110/paper_19326203_v12_n7_p_Wada