Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules

Kato, Kazuhisa; Kanahama, Koki; Kanayama, Yoshinori

doi:10.1016/j.jplph.2009.08.006

Cited by 76 publications

(74 citation statements)

References 29 publications

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“…However, despite decades of research (Vessey and Waterer 1992), the mechanism of nitrate's impact on the activity of existing nodules is not fully understood and remains controversial as there are several competing theories. The nitrate ion itself, nitrite, or nitric oxide has been implicated by either blocking leghemoglobin Kato et al, 2010) or by triggering a regulatory network at the gene expression level Wilson et al, 2008;Meilhoc et al, 2011). A further hypothesis is that the effect of nitrate on legume nodules is mediated by a closure of the oxygen diffusion barrier or a reduction in oxygen permeability facilitated by unspecified mechanisms (Vessey and Waterer, 1992;Minchin, 1997).…”

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confidence: 99%

An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula

et al. 2013

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The mechanism through which nitrate reduces the activity of legume nodules is controversial. The objective of the study was to follow Medicago truncatula nodule activity after nitrate provision continuously and to identify molecular mechanisms, which down-regulate the activity of the nodules. Nodule H 2 evolution started to decline after about 4 h of nitrate application. At that point in time, a strong shift in nodule gene expression (RNA sequencing) had occurred (1,120 differentially expressed genes). The most pronounced effect was the down-regulation of 127 genes for nodule-specific cysteine-rich peptides. Various other nodulins were also strongly down-regulated, in particular all the genes for leghemoglobins. In addition, shifts in the expression of genes involved in cellular iron allocation and mitochondrial ATP synthesis were observed. Furthermore, the expression of numerous genes for the formation of proteins and glycoproteins with no obvious function in nodules (e.g. germins, patatin, and thaumatin) was strongly increased. This occurred in conjunction with an up-regulation of genes for proteinase inhibitors, in particular those containing the Kunitz domain. The additionally formed proteins might possibly be involved in reducing nodule oxygen permeability. Between 4 and 28 h of nitrate exposure, a further reduction in nodule activity occurred, and the number of differentially expressed genes almost tripled. In particular, there was a differential expression of genes connected with emerging senescence. It is concluded that nitrate exerts rapid and manifold effects on nitrogenase activity. A certain degree of nitrate tolerance might be achieved when the down-regulatory effect on late nodulins can be alleviated.

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An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula

et al. 2013

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“…10,11 NO was shown to have a beneficial role during infection, nodule development and mature nodule functioning. 8,10 On the other hand NO was also shown to have inhibitory effects on nitrogenase, 12,13 and we have recently shown that NO could also be a signal triggering senescence of M. truncatula nodules.…”

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confidence: 96%

Control of NO level in rhizobium-legume root nodules

Meilhoc

Blanquet

Cam

et al. 2013

Plant Signaling & Behavior

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confidence: 99%

“…The involvement of NO in nitrogenase inactivation has been demonstrated in soybean (Glycine max) and Lotus after nitrate supply (Kanayama et al, 1990;Meakin et al, 2007;Kato et al, 2010). In Lotus japonicus, the artificial application of the NO donor sodium nitroprusside (SNP) decreased nitrogen fixation, whereas the application of a NO scavenger (2-4-carboxyphenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) enhanced nitrogen fixation (Shimoda et al, 2009;Kato et al, 2010). In spite of the inhibitory effect of NO on nitrogenase, it appears that NO production is required for nodule development and functioning, and the plant antioxidant systems appear to be crucial to maintain nodule functioning Keyster et al, 2010;Leach et al, 2010;Sanchez et al, 2011).…”

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confidence: 99%

“…In spite of the inhibitory effect of NO on nitrogenase, it appears that NO production is required for nodule development and functioning, and the plant antioxidant systems appear to be crucial to maintain nodule functioning Keyster et al, 2010;Leach et al, 2010;Sanchez et al, 2011). The levels of NO inside the nodule appear to be controlled by leghemoglobin, which is able to scavenge NO and in this way may protect nitrogenase from inactivation (Kanayama et al, 1990;Herold and Puppo, 2005;Meakin et al, 2007;Kato et al, 2010;Sanchez et al, 2011). Nitroso-leghemoglobin complexes have been detected in nodules of soybean and Lotus (Kanayama et al, 1990;Mathieu et al, 1998;Meakin et al, 2007;Sanchez et al, 2010).…”

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confidence: 99%

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Glutamine Synthetase Is a Molecular Target of Nitric Oxide in Root Nodules of Medicago truncatula and Is Regulated by Tyrosine Nitration

Melo

Silva²,

Ribeiro³

et al. 2011

Plant Physiology

119

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Nitric oxide (NO) is emerging as an important regulatory player in the Rhizobium-legume symbiosis, but its biological role in nodule functioning is still far from being understood. To unravel the signal transduction cascade and ultimately NO function, it is necessary to identify its molecular targets. This study provides evidence that glutamine synthetase (GS), a key enzyme for root nodule metabolism, is a molecular target of NO in root nodules of Medicago truncatula, being regulated by tyrosine (Tyr) nitration in relation to active nitrogen fixation. In vitro studies, using purified recombinant enzymes produced in Escherichia coli, demonstrated that the M. truncatula nodule GS isoenzyme (MtGS1a) is subjected to NO-mediated inactivation through Tyr nitration and identified Tyr-167 as the regulatory nitration site crucial for enzyme inactivation. Using a sandwich enzymelinked immunosorbent assay, it is shown that GS is nitrated in planta and that its nitration status changes in relation to active nitrogen fixation. In ineffective nodules and in nodules fed with nitrate, two conditions in which nitrogen fixation is impaired and GS activity is reduced, a significant increase in nodule GS nitration levels was observed. Furthermore, treatment of root nodules with the NO donor sodium nitroprusside resulted in increased in vivo GS nitration accompanied by a reduction in GS activity. Our results support a role of NO in the regulation of nitrogen metabolism in root nodules and places GS as an important player in the process. We propose that the NO-mediated GS posttranslational inactivation is related to metabolite channeling to boost the nodule antioxidant defenses in response to NO.

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Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules

Cited by 76 publications

References 29 publications

An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula

An RNA Sequencing Transcriptome Analysis Reveals Novel Insights into Molecular Aspects of the Nitrate Impact on the Nodule Activity of Medicago truncatula

Control of NO level in rhizobium-legume root nodules

Glutamine Synthetase Is a Molecular Target of Nitric Oxide in Root Nodules of Medicago truncatula and Is Regulated by Tyrosine Nitration

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