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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1168985/full |
| _version_ | 1797831701710241792 |
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| author | Xiaoxiang Fu Xiaoxiang Fu Xiaoxiang Fu Yu Jin Matthew J. Paul Minxuan Yuan Xingwei Liang Ruqiang Cui Yingjin Huang Wenwen Peng Wenwen Peng Xiaogui Liang Xiaogui Liang Xiaogui Liang |
| author_facet | Xiaoxiang Fu Xiaoxiang Fu Xiaoxiang Fu Yu Jin Matthew J. Paul Minxuan Yuan Xingwei Liang Ruqiang Cui Yingjin Huang Wenwen Peng Wenwen Peng Xiaogui Liang Xiaogui Liang Xiaogui Liang |
| author_sort | Xiaoxiang Fu |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-09T13:57:02Z |
| format | Article |
| id | doaj.art-aceec7e880e34ca196e8e5795b79c0cb |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-09T13:57:02Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-aceec7e880e34ca196e8e5795b79c0cb2023-05-08T04:35:39ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-05-011410.3389/fpls.2023.11689851168985Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilizationXiaoxiang Fu0Xiaoxiang Fu1Xiaoxiang Fu2Yu Jin3Matthew J. Paul4Minxuan Yuan5Xingwei Liang6Ruqiang Cui7Yingjin Huang8Wenwen Peng9Wenwen Peng10Xiaogui Liang11Xiaogui Liang12Xiaogui Liang13The Laboratory for Phytochemistry and Botanical Pesticides, College of Agriculture, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaCollege of Agronomy and Biotechnology, China Agricultural University, Beijing, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaPlant Sciences, Rothamsted Research, Harpenden, United KingdomThe Laboratory for Phytochemistry and Botanical Pesticides, College of Agriculture, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaThe Laboratory for Phytochemistry and Botanical Pesticides, College of Agriculture, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaThe Laboratory for Phytochemistry and Botanical Pesticides, College of Agriculture, Jiangxi Agricultural University, Nanchang, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang, ChinaCollege of Agronomy and Biotechnology, China Agricultural University, Beijing, ChinaUstiloxins 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.https://www.frontiersin.org/articles/10.3389/fpls.2023.1168985/fullseed germinationcarbon metabolismustiloxinsrice false smutsugar transport |
| spellingShingle | Xiaoxiang Fu Xiaoxiang Fu Xiaoxiang Fu Yu Jin Matthew J. Paul Minxuan Yuan Xingwei Liang Ruqiang Cui Yingjin Huang Wenwen Peng Wenwen Peng Xiaogui Liang Xiaogui Liang Xiaogui Liang Inhibition of rice germination by ustiloxin A involves alteration in carbon metabolism and amino acid utilization Frontiers in Plant Science seed germination carbon metabolism ustiloxins rice false smut sugar transport |
| 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 | seed germination carbon metabolism ustiloxins rice false smut sugar transport |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1168985/full |
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