Production of nitric oxide and nitrosylleghemoglobin complexes in soybean nodules in response to flooding

Cristina Sánchez, Andrew J. Gates, Georgina E. Meakin, Toshiki Uchiumi, Lourdes Girard, David J. Richardson, Eulogio J. Bedmar, María J. Delgado

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    73 Citations (Scopus)

    Abstract

    Nitric oxide (NO) has gained interest as a major signaling molecule during plant development and in response to environmental cues. Formation of NO during symbiotic interactions has been reported, but the role and sources of NO in nodules remain unclear. In this work, the involvement of denitrification, performed by the symbiont Bradyrhizobium japonicum, in NO formation in soybean nodules in response to flooding conditions has been investigated by inoculating plants with napA-, nirK-, or norC-deficient mutants. Levels of nitrosylleghemoglobin (LbNO) in flooded nirK and norC nodules were significantly higher than those observed in wild-type nodules. In addition, nirK and norC nodules accumulated more nitrite and NO, respectively, than wild-type nodules. By contrast, levels of LbNO, nitrite, and NO in flooded napA nodules were lower than in wild-type nodules. These results suggest that LbNO formation in soybean nodules in response to flooding conditions is caused by nitrite and NO generated from periplasmic nitrate reductase (Nap) and also containing nitrite reductase (NirK) denitrification enzymes. Flooding caused a decrease of nifH expression and nitrogenase activity in wild-type and norC nodules but not in napA or nirK nodules. Incubation of wild-type and norC nodules with a NO scavenger counteracted the effect of flooding. Under free-living conditions, β-galactosidase activity from a nifD′-′lacZ fusion decreased in a norC mutant, which also accumulated NO in the medium. These results suggest that NO formed by Cu-containing nitrite reductase in soybean nodules in response to flooding has a negative effect on expression of nitrogenase. We propose that Lb has a major role in detoxifying NO and nitrite produced by bacteroidal denitrification in response to flooding conditions.

    Original languageEnglish
    Pages (from-to)702-711
    Number of pages10
    JournalMolecular Plant-Microbe Interactions
    Volume23
    Issue number5
    DOIs
    Publication statusPublished - 2010 May

    ASJC Scopus subject areas

    • Physiology
    • Agronomy and Crop Science

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