Hydrogen Sulfide Promotes Nodulation and Nitrogen Fixation in Soybean–Rhizobia Symbiotic System
The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H 2 S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H 2 S has regulatory effect in this symbiotic system remains unknown. Herein, w...
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Published in | Molecular plant-microbe interactions Vol. 32; no. 8; pp. 972 - 985 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Phytopathological Society
01.08.2019
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Subjects | |
Online Access | Get full text |
ISSN | 0894-0282 1943-7706 |
DOI | 10.1094/MPMI-01-19-0003-R |
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Abstract | The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H
2
S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H
2
S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H
2
S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H
2
S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H
2
S may act as a positive signaling molecule in the soybean–rhizobia symbiotic system and enhance the system’s nitrogen fixation ability. |
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AbstractList | The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H
2
S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H
2
S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H
2
S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H
2
S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H
2
S may act as a positive signaling molecule in the soybean–rhizobia symbiotic system and enhance the system’s nitrogen fixation ability. The rhizobium-legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H2S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H2S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H2S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H2S may act as a positive signaling molecule in the soybean-rhizobia symbiotic system and enhance the system's nitrogen fixation ability.The rhizobium-legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H2S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H2S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H2S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H2S may act as a positive signaling molecule in the soybean-rhizobia symbiotic system and enhance the system's nitrogen fixation ability. The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H₂S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H₂S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H₂S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H₂S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H₂S may act as a positive signaling molecule in the soybean–rhizobia symbiotic system and enhance the system’s nitrogen fixation ability. The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H2S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H2S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H2S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H2S may act as a positive signaling molecule in the soybean–rhizobia symbiotic system and enhance the system's nitrogen fixation ability. The rhizobium-legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H S in the symbiosis between soybean ( ) and rhizobium ( ). Our results demonstrated that an exogenous H S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes , , and of . In addition, expression of soybean nodulation marker genes, including early nodulin 40 ( ), ERF required for nodulation ( ), nodulation signaling pathway 2b ( ), and nodulation inception genes ( , , and ), were upregulated. Moreover, the expressions of glutamate synthase ( ), asparagine synthase ( ), nitrite reductase ( ), ammonia transporter ( ), leghemoglobin ( ), and involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H S may act as a positive signaling molecule in the soybean-rhizobia symbiotic system and enhance the system's nitrogen fixation ability. |
Author | Zou, Hang Pan, Qing Wei, Ge-Hong Zhang, Jian-Hua Zhang, Ni-Na Chen, Juan |
Author_xml | – sequence: 1 givenname: Hang surname: Zou fullname: Zou, Hang organization: State Key Laboratory of Crop Stress Biology in Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, PR China, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, Yangling, Shaanxi 712100, PR China – sequence: 2 givenname: Ni-Na surname: Zhang fullname: Zhang, Ni-Na organization: State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China – sequence: 3 givenname: Qing surname: Pan fullname: Pan, Qing organization: State Key Laboratory of Crop Stress Biology in Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, PR China, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, Yangling, Shaanxi 712100, PR China – sequence: 4 givenname: Jian-Hua surname: Zhang fullname: Zhang, Jian-Hua organization: School of Life Sciences and State Key Laboratory of Agrobiotechnology, the Chinese University of Hong Kong, Hong Kong, Department of Biology, Hong Kong Baptist University, Hong Kong – sequence: 5 givenname: Juan orcidid: 0000-0001-8395-3314 surname: Chen fullname: Chen, Juan organization: State Key Laboratory of Crop Stress Biology in Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, PR China, State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Northwest A&F University, Yangling, Shaanxi 712100, P.R. China, School of Life Sciences and State Key Laboratory of Agrobiotechnology, the Chinese University of Hong Kong, Hong Kong – sequence: 6 givenname: Ge-Hong surname: Wei fullname: Wei, Ge-Hong organization: State Key Laboratory of Crop Stress Biology in Arid Areas, College of Life Sciences, Northwest A&F University, Yangling, Shaanxi 712100, PR China, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, Yangling, Shaanxi 712100, PR China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31204904$$D View this record in MEDLINE/PubMed |
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Keywords | hydrogen sulfide symbiosis nitrogenase activity molecular signaling nodulation nitrogen fixation gene expression rhizobium-legume symbiosis |
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Snippet | The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H
2
S), a gaseous signaling molecule, may... The rhizobium-legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H S), a gaseous signaling molecule, may regulate... The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate... The rhizobium-legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate... The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H₂S), a gaseous signaling molecule, may regulate... |
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SubjectTerms | Ammonia Asparagine Gasotransmitters - pharmacology Gene expression gene expression regulation Genes genetic markers glutamic acid Glycine max Glycine max - microbiology Hydrogen sulfide Hydrogen Sulfide - pharmacology leghemoglobin Legumes NifH gene Nitrite reductase Nitrogen Nitrogen cycle Nitrogen fixation Nitrogen Fixation - drug effects Nitrogen metabolism Nitrogenase Nitrogenation Nodulation Nodules Physiological effects Plant Root Nodulation - drug effects Polymerase chain reaction quantitative polymerase chain reaction Reductases Rhizobium Rhizobium - physiology Root nodules roots Signal transduction Signaling Sinorhizobium fredii Sodium Soybeans Symbiosis Symbiosis - drug effects Western blotting |
Title | Hydrogen Sulfide Promotes Nodulation and Nitrogen Fixation in Soybean–Rhizobia Symbiotic System |
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