Nitric Oxide: A Multitask Player in Plant–Microorganism Symbioses

Hichri, Imène; Boscari, Alexandre; Meilhoc, Eliane; Catalá, Myriam; Barreno, Eva; Bruand, Claude; Lanfranco, Luisa; Brouquisse, Renaud

doi:10.1007/978-3-319-40713-5_12

Cited by 17 publications

(7 citation statements)

References 153 publications

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“…Similar results were observed in other Medicago species (Pii et al, 2007). In M. truncatula mature nodules, NO has been shown to accumulate particularly in the N 2 -fixing zone (Baudouin et al, 2006;Hichri et al, 2016), and at the onset of nodule senescence a NO production was reported at the junction of the N 2 -fixing and senescence zones (Cam et al, 2012). A recent study with M. truncatula showed that NO is produced throughout the whole symbiotic process, from infection with Sinorhizobium meliloti up to, at least, 8 weeks post-inoculation (wpi), exhibiting production peaks during the first hours of the symbiotic interaction, during early development of the nodule and when the nodule becomes mature (Berger et al, 2020).…”

Section: Introductionsupporting

confidence: 80%

“…During the first hours after inoculation with the symbiotic partner, NO was observed in the roots of Lotus japonicus, Medicago sativa, and Medicago truncatula (Nagata et al, 2008;Fukudome et al, 2016;Hichri et al, 2016). Its production was also detected during the infection process along the infection thread and in the dividing cells of the M. truncatula nodule primordium (del Giudice et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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Plant Nitrate Reductases Regulate Nitric Oxide Production and Nitrogen-Fixing Metabolism During the Medicago truncatula–Sinorhizobium meliloti Symbiosis

et al. 2020

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Nitrate reductase (NR) is the first enzyme of the nitrogen reduction pathway in plants, leading to the production of ammonia. However, in the nitrogen-fixing symbiosis between legumes and rhizobia, atmospheric nitrogen (N 2) is directly reduced to ammonia by the bacterial nitrogenase, which questions the role of NR in symbiosis. Next to that, NR is the best-characterized source of nitric oxide (NO) in plants, and NO is known to be produced during the symbiosis. In the present study, we first surveyed the three NR genes (MtNR1, MtNR2, and MtNR3) present in the Medicago truncatula genome and addressed their expression, activity, and potential involvement in NO production during the symbiosis between M. truncatula and Sinorhizobium meliloti. Our results show that MtNR1 and MtNR2 gene expression and activity are correlated with NO production throughout the symbiotic process and that MtNR1 is particularly involved in NO production in mature nodules. Moreover, NRs are involved together with the mitochondrial electron transfer chain in NO production throughout the symbiotic process and energy regeneration in N 2fixing nodules. Using an in vivo NMR spectrometric approach, we show that, in mature nodules, NRs participate also in the regulation of energy state, cytosolic pH, carbon and nitrogen metabolism under both normoxia and hypoxia. These data point to the importance of NR activity for the N 2-fixing symbiosis and provide a first explanation of its role in this process.

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Section: Introductionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 99%

Plant Nitrate Reductases Regulate Nitric Oxide Production and Nitrogen-Fixing Metabolism During the Medicago truncatula–Sinorhizobium meliloti Symbiosis

et al. 2020

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“…Hence, to maintain efficient infection and nitrogen fixation, the level of NO inside legume root nodules must be finely tuned. The NO level results from a balance between NO synthesis and consumption, two processes which rely on both partners (Hichri et al, 2016a). Indeed, both plant and bacterial hemoglobins have been shown to be involved in NO transformation or detoxification (Berger et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

The Nitrate Assimilatory Pathway in Sinorhizobium meliloti: Contribution to NO Production

et al. 2019

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The interaction between rhizobia and their legume host plants culminates in the formation of specialized root organs called nodules in which differentiated endosymbiotic bacteria (bacteroids) fix atmospheric nitrogen to the benefit of the plant. Interestingly, nitric oxide (NO) has been detected at various steps of the rhizobium-legume symbiosis where it has been shown to play multifaceted roles. It is recognized that both bacterial and plant partners of the Sinorhizobium meliloti – Medicago truncatula symbiosis are involved in NO synthesis in nodules. S. meliloti can also produce NO from nitrate when living as free cells in the soil. S. meliloti does not possess any NO synthase gene in its genome. Instead, the denitrification pathway is often described as the main driver of NO production with nitrate as substrate. This pathway includes the periplasmic nitrate reductase (Nap) which reduces nitrate into nitrite, and the nitrite reductase (Nir) which reduces nitrite into NO. However, additional genes encoding putative nitrate and nitrite reductases (called narB and nirB , respectively) have been identified in the S. meliloti genome. Here we examined the conditions where these genes are expressed, investigated their involvement in nitrate assimilation and NO synthesis in culture and their potential role in planta . We found that narB and nirB are expressed under aerobic conditions in absence of ammonium in the medium and most likely belong to the nitrate assimilatory pathway. Even though these genes are clearly expressed in the fixation zone of legume root nodule, they do not play a crucial role in symbiosis. Our results support the hypothesis that in S. meliloti , denitrification remains the main enzymatic way to produce NO while the assimilatory pathway involving NarB and NirB participates indirectly to NO synthesis by cooperating with the denitrification pathway.

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“…NO is revealing itself as a keystone in stress tolerance of symbiotic associations such as Symbiodinium —cnidarian (corals), plant— Rhizobium or mycorrhizae, critical in global geomorphology and nitrogen ecology [35]. Thus, it is of the utmost interest to elucidate the mechanisms that mediate its production in lichens, symbiotic organisms inhabiting almost every terrestrial habitat.…”

Section: Introductionmentioning

confidence: 99%

Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation

Expósito

Román

Barreno

et al. 2019

Plants

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Lichens are poikilohydrous symbiotic associations between a fungus, photosynthetic partners, and bacteria. They are tolerant to repeated desiccation/rehydration cycles and adapted to anhydrobiosis. Nitric oxide (NO) is a keystone for stress tolerance of lichens; during lichen rehydration, NO limits free radicals and lipid peroxidation but no data on the mechanisms of its synthesis exist. The aim of this work is to characterize the synthesis of NO in the lichen Ramalina farinacea using inhibitors of nitrate reductase (NR) and nitric oxide synthase (NOS), tungstate, and NG-nitro-L-arginine methyl ester (L-NAME), respectively. Tungstate suppressed the NO level in the lichen and caused an increase in malondialdehyde during rehydration in the hyphae of cortex and in phycobionts, suggesting that a plant-like NR is involved in the NO production. Specific activity of NR in R. farinacea was 91 μU/mg protein, a level comparable to those in the bryophyte Physcomitrella patens and Arabidopsis thaliana. L-NAME treatment did not suppress the NO level in the lichens. On the other hand, NADPH-diaphorase activity cytochemistry showed a possible presence of a NOS-like activity in the microalgae where it is associated with cytoplasmatic vesicles. These data provide initial evidence that NO synthesis in R. farinacea involves NR.

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Nitric Oxide: A Multitask Player in Plant–Microorganism Symbioses

Cited by 17 publications

References 153 publications

Plant Nitrate Reductases Regulate Nitric Oxide Production and Nitrogen-Fixing Metabolism During the Medicago truncatula–Sinorhizobium meliloti Symbiosis

Plant Nitrate Reductases Regulate Nitric Oxide Production and Nitrogen-Fixing Metabolism During the Medicago truncatula–Sinorhizobium meliloti Symbiosis

The Nitrate Assimilatory Pathway in Sinorhizobium meliloti: Contribution to NO Production

Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation

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