Structural and functional properties of class 1 plant hemoglobins

Department of Biology, Memorial University of Newfoundland, St. John's, NL, Canada.
International Union of Biochemistry and Molecular Biology Life (Impact Factor: 3.14). 03/2011; 63(3):146-52. DOI: 10.1002/iub.439
Source: PubMed


Nonsymbiotic class 1 plant hemoglobins are induced under hypoxia. Structurally they are protein dimers consisting of two identical subunits, each containing heme iron in a weak hexacoordinate state. The weak hexacoordination of heme-iron binding to the distal histidine results in an extremely high avidity to oxygen, with a dissociation constant in the nanomolar range. This low dissociation constant is due to rapid oxygen binding resulting in protein conformational changes that slow dissociation from the heme site. Class 1 hemoglobins are characterized by an increased rate of Fe³(+) reduction which is likely mediated by cysteine residue. This cysteine can form a reversible covalent bond between two monomers as shown by mass spectrometry analysis and, in addition to its structural role, prevents the molecule from autoxidation. The structural properties of class 1 hemoglobins allow them to serve as soluble electron transport proteins in the enzymatic system scavenging nitric oxide produced in low oxygen via reduction of nitrite. During oxygenation of nitric oxide to nitrate, oxidized ferric hemoglobin is formed (methemoglobin), which can be reduced by an associated reductase. The identified candidate for this reduction is monodehydroascorbate reductase. It is suggested that hemoglobin functions as a terminal electron acceptor during the hypoxic turnover of nitrogen, the process aided by its extremely high affinity for oxygen.

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Available from: Abir U Igamberdiev,
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    • "Later, this NO-scavenging function has also been attributed to non-symbiotic class 1 Hbs (nsHb1) in Lotus japonicus (Shimoda et al., 2009) and more recently the three types of Hb were found to be expressed in nodules of Lotus japonicus, suggesting complementary roles of the different types of Hb for root nodule formation and/or functioning (Bustos-Sanmamed et al., 2011). Because class 1 nsHbs have an extreme affinity for O2, it is unlikely that they function as O2 transporters, stores, or sensors, therefore they have been supposed to play the role of NO scavenger in NO detoxifying pathways (Gupta et al., 2011b; Igamberdiev et al., 2011). These proteins are induced upon symbiotic infection, accumulate in nitrogen fixing nodules and their overexpression enhances symbiotic N2 fixation, further supporting a role in NO quenching in root nodules (Shimoda et al., 2009). "
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    ABSTRACT: Nitric oxide (NO) is emerging as an important regulatory player in the Rhizobium-legume symbiosis. The occurrence of NO during several steps of the symbiotic interaction suggests an important, but yet unknown, signaling role of this molecule for root nodule formation and functioning. The identification of the molecular targets of NO is key for the assembly of the signal transduction cascade that will ultimately help to unravel NO function. We have recently shown that the key nitrogen assimilatory enzyme glutamine synthetase (GS) is a molecular target of NO in root nodules of Medicago truncatula, being post-translationally regulated by tyrosine nitration in relation to nitrogen fixation. In functional nodules of M. truncatula NO formation has been located in the bacteroid containing cells of the fixation zone, where the ammonium generated by bacterial nitrogenase is released to the plant cytosol and assimilated into the organic pools by plant GS. We propose that the NO-mediated GS post-translational inactivation is connected to nitrogenase inhibition induced by NO and is related to metabolite channeling to boost the nodule antioxidant defenses. Glutamate, a substrate for GS activity is also the precursor for the synthesis of glutathione (GSH), which is highly abundant in root nodules of several plant species and known to play a major role in the antioxidant defense participating in the ascorbate/GSH cycle. Existing evidence suggests that upon NO-mediated GS inhibition, glutamate could be channeled for the synthesis of GSH. According to this hypothesis, GS would be involved in the NO-signaling responses in root nodules and the NO-signaling events would meet the nodule metabolic pathways to provide an adaptive response to the inhibition of symbiotic nitrogen fixation by reactive nitrogen species.
    Frontiers in Plant Science 09/2013; 4:372. DOI:10.3389/fpls.2013.00372 · 3.95 Impact Factor
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    • "Over the past decade, extensive work has shown that, in plants, oxygenated class 1 nsHbs can be oxidized by NO, resulting in nitrate production [32–34]. This NO scavenging reaction is now accepted as a general mechanism modulating NO bioavailability, participating in the regulation and detoxification of NO in plants [2,29–31,35]. Some studies also reported similar processes for class-2 symbiotic hemoglobins (sHb) that are able to interact with NO and to scavenge it [36–39]. "
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    ABSTRACT: Nitric oxide (NO) has been demonstrated as an essential regulator of several physiological processes in plants. The understanding of the molecular mechanism underlying its critical role constitutes a major field of research. NO can exert its biological function through different ways, such as the modulation of gene expression, the mobilization of second messengers, or interplays with protein kinases. Besides this signaling events, NO can be responsible of the posttranslational modifications (PTM) of target proteins. Several modifications have been identified so far, whereas metal nitrosylation, the tyrosine nitration and the S-nitrosylation can be considered as the main ones. Recent data demonstrate that these PTM are involved in the control of a wide range of physiological processes in plants, such as the plant immune system. However, a great deal of effort is still necessary to pinpoint the role of each PTM in plant physiology. Taken together, these new advances in proteomic research provide a better comprehension of the role of NO in plant signaling.
    International Journal of Molecular Sciences 12/2012; 13(11):15193-208. DOI:10.3390/ijms131115193 · 2.86 Impact Factor
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    • "autoxidation [27]. While the direct reduction of heme iron can be facilitated by ascorbate, the additional mechanism mediating this reduction and keeping the molecule in the ferrous state involves a cysteine residue and controlled by sulfhydryl reagents such as reduced glutathione [28]. The structural properties of class 1 hemoglobins allow them to serve as soluble electron transport proteins in the enzymatic system scavenging nitric oxide (NO) produced in low oxygen conditions primarily via reduction of nitrite in plants [29] (Fig. 3). "
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    ABSTRACT: Plant hemoglobins constitute a diverse group of hemeproteins and evolutionarily belong to three different classes. Class 1 hemoglobins possess an extremely high affinity to oxygen and their main function consists in scavenging of nitric oxide (NO) at very low oxygen levels. Class 2 hemoglobins have a lower oxygen affinity and they facilitate oxygen supply to developing tissues. Symbiotic hemoglobins in nodules have mostly evolved from class 2 hemoglobins. Class 3 hemoglobins are truncated and represent a clade with a very low similarity to class 1 and 2 hemoglobins. They may regulate oxygen delivery at high O(2) concentrations. Depending on their physical properties, hemoglobins belong either to hexacoordinate non-symbiotic or pentacoordinate symbiotic groups. Plant hemoglobins are plausible targets for improving resistance to multiple stresses.
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