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Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization

Ustiloxins are the main mycotoxin in rice false smut, a devastating disease caused by Ustilaginoidea virens. A typical phytotoxicity of ustiloxins is strong inhibition of seed germination, but the physiological mechanism is not clear. Here, we show that the inhibition of rice germination by ustiloxi...

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Autores principales: Fu, Xiaoxiang, Jin, Yu, Paul, Matthew J., Yuan, Minxuan, Liang, Xingwei, Cui, Ruqiang, Huang, Yingjin, Peng, Wenwen, Liang, Xiaogui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10200953/
https://www.ncbi.nlm.nih.gov/pubmed/37223794
http://dx.doi.org/10.3389/fpls.2023.1168985
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author Fu, Xiaoxiang
Jin, Yu
Paul, Matthew J.
Yuan, Minxuan
Liang, Xingwei
Cui, Ruqiang
Huang, Yingjin
Peng, Wenwen
Liang, Xiaogui
author_facet Fu, Xiaoxiang
Jin, Yu
Paul, Matthew J.
Yuan, Minxuan
Liang, Xingwei
Cui, Ruqiang
Huang, Yingjin
Peng, Wenwen
Liang, Xiaogui
author_sort Fu, Xiaoxiang
collection PubMed
description Ustiloxins are the main mycotoxin in rice false smut, a devastating disease caused by Ustilaginoidea virens. A typical phytotoxicity of ustiloxins is strong inhibition of seed germination, but the physiological mechanism is not clear. Here, we show that the inhibition of rice germination by ustiloxin A (UA) is dose-dependent. The sugar availability in UA-treated embryo was lower while the starch residue in endosperm was higher. The transcripts and metabolites responsive to typical UA treatment were investigated. The expression of several SWEET genes responsible for sugar transport in embryo was down-regulated by UA. Glycolysis and pentose phosphate processes in embryo were transcriptionally repressed. Most of the amino acids detected in endosperm and embryo were variously decreased. Ribosomal RNAs for growth were inhibited while the secondary metabolite salicylic acid was also decreased under UA. Hence, we propose that the inhibition of seed germination by UA involves the block of sugar transport from endosperm to embryo, leading to altered carbon metabolism and amino acid utilization in rice plants. Our analysis provides a framework for understanding of the molecular mechanisms of ustiloxins on rice growth and in pathogen infection.
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spelling pubmed-102009532023-05-23 Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization Fu, Xiaoxiang Jin, Yu Paul, Matthew J. Yuan, Minxuan Liang, Xingwei Cui, Ruqiang Huang, Yingjin Peng, Wenwen Liang, Xiaogui Front Plant Sci Plant Science Ustiloxins are the main mycotoxin in rice false smut, a devastating disease caused by Ustilaginoidea virens. A typical phytotoxicity of ustiloxins is strong inhibition of seed germination, but the physiological mechanism is not clear. Here, we show that the inhibition of rice germination by ustiloxin A (UA) is dose-dependent. The sugar availability in UA-treated embryo was lower while the starch residue in endosperm was higher. The transcripts and metabolites responsive to typical UA treatment were investigated. The expression of several SWEET genes responsible for sugar transport in embryo was down-regulated by UA. Glycolysis and pentose phosphate processes in embryo were transcriptionally repressed. Most of the amino acids detected in endosperm and embryo were variously decreased. Ribosomal RNAs for growth were inhibited while the secondary metabolite salicylic acid was also decreased under UA. Hence, we propose that the inhibition of seed germination by UA involves the block of sugar transport from endosperm to embryo, leading to altered carbon metabolism and amino acid utilization in rice plants. Our analysis provides a framework for understanding of the molecular mechanisms of ustiloxins on rice growth and in pathogen infection. Frontiers Media S.A. 2023-05-08 /pmc/articles/PMC10200953/ /pubmed/37223794 http://dx.doi.org/10.3389/fpls.2023.1168985 Text en Copyright © 2023 Fu, Jin, Paul, Yuan, Liang, Cui, Huang, Peng and Liang https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Fu, Xiaoxiang
Jin, Yu
Paul, Matthew J.
Yuan, Minxuan
Liang, Xingwei
Cui, Ruqiang
Huang, Yingjin
Peng, Wenwen
Liang, Xiaogui
Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title_full Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title_fullStr Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title_full_unstemmed Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title_short Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization
title_sort inhibition of rice germination by ustiloxin a involves alteration in carbon metabolism and amino acid utilization
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10200953/
https://www.ncbi.nlm.nih.gov/pubmed/37223794
http://dx.doi.org/10.3389/fpls.2023.1168985
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