Keywords
Algae, angiosperms, bryophytes, gymnosperms, legumes, nonsymbiotic, truncated
This article is included in the Oxygen-binding and sensing proteins collection.
This article is included in the Iowa State University collection.
Algae, angiosperms, bryophytes, gymnosperms, legumes, nonsymbiotic, truncated
Hemoglobin (Hb) is a heme-containing protein found in the red blood cells of vertebrates1. Hemoglobin-like proteins are also found in other tissues of vertebrates where they are given tissue-specific names that help to identify their locations and distinguish them from red blood cell Hb2,3. For many years, the only known Hb-like molecule in plants was leghemoglobin (Lb), a protein induced as a result of the symbiotic relationship between legume plants and nitrogen-fixing bacteria4. The discovery that other Hb-like proteins existed in plants not capable of symbiotic relationships led to the term “nonsymbiotic Hbs (nsHbs)” to differentiate them from the Lbs5. While this terminology was adequate in the early stages of research on the protein, the complexity of the research in this area necessitates a change in the definition of these proteins to delineate them from red blood cell Hb, in keeping with the terminology for other Hb-like proteins, such as myoglobin in muscle, neuroglobin in neuron tissue and cytoglobin in vertebrate cell cytoplasm2,3. In 2001 Hunt et al.6 classified plant Hbs as globin (GLB)0, GLB1, GLB2, GLb3 and GLBS corresponding to undetermined (mostly liverwort and moss) nsHbs, angiosperm nsHbs class/type 1 and nsHbs class/type 2, truncated Hbs and symbiotic Hbs (which included Lbs), respectively. However, an epithet for plant Hbs was absent in this nomenclature and distinctive characteristics for each category were not fully defined resulting in an incomplete classification system.
At the 2014 XVIII Conference on Oxygen-Binding and Sensing Proteins, the group devoted to the study of heme-containing proteins, the above issue was discussed and a consensus was reached on a proposed name change. Phytoglobin (phyto, plant; globin, heme-containing protein folding structurally similar to the sperm whale myoglobin structure whose heme-Fe is invariably coordinated at the proximal site by His F8), abbreviated as Phytogb, was proposed as a logical, descriptive name to describe a heme-containing (Hb-like) protein found in plants. It will be readily recognized by the research community without a prolonged explanation of the origin of the term, as is the case for ‘nonsymbiotic hemoglobin’. The classification system that has been established can essentially remain unchanged substituting Phytogb in place of nsHb. A guide to the new nomenclature, with reference to the existing terminology, is given in Table 1. A more detailed phylogenetic scheme, placing the known Phytogbs in the new nomenclature, is shown in Figure 1. Also, we propose that acronym for the species-specific Phytogbs corresponds to the first three binomial (i.e. genus and species) letters followed by the Phytogb type and phytogb number of copy. For example, the acronym for rice (Oryza sativa) Phytogb1.1 (see Table 1) corresponds to OrysatPhytogb1.1.
Former plant globin name and abbreviation (in parenthesis) | New nomenclaturea | Plant origin | Distinctive characteristicsb |
---|---|---|---|
Nonsymbiotic hemoglobin (nsHb) | Phytogb0 | Algaec+bryophytes+ gymnosperms | Heme-Fe either penta- or hexacoordinate. Moderate to high affinity for O2. Localized in any plant organ. |
Class/type 1 nonsymbiotic hemoglobin (nsHb-1) | Phytogb1 | Angiosperms | Heme-Fe predominantly hexacoordinated by a distal amino acid. Extremely high affinity for O2 mostly due to a very low O2-dissociation rate constant (koff). Localized in any plant organ. |
Class/type 2 nonsymbiotic hemoglobin (nsHb-2) | Phytogb2 | Angiosperms | Heme-Fe predominantly pentacoordinated. Moderate to high affinity for O2. Localized in any plant organ. |
Symbiotic hemoglobin (symHb) | SymPhytogb | Non-legume N2-fixing plantsd | Heme-Fe predominantly pentacoordinated. Moderate to high affinity for O2. Specifically localized in N2-fixing nodules of actinorhizal plants or any other non-legume land plant |
Leghemoglobin (Lb) | Lb | N2-fixing legumesd | Heme-Fe predominantly pentacoordinate. Moderate to high affinity for O2. Specifically localized in legume N2-fixing nodules. |
Class/type 3 nonsymbiotic hemoglobin/ Truncated hemoglobin (tHb) | Phytogb3 | Algaec+land plants | Globin-domain amino acid sequence and structure (i.e. folding into the 2/2-fold) similar to those of bacterial tHbs. Heme-Fe either penta- or hexacoordinate. Moderate to high affinity for O2. Localized in any plant organ. |
aNumerical classification corresponds to that previously proposed by Hunt et al.6. Proteins coded by multiple phytogb gene copy numbers within the same plant species should be indicated as the number of copy after the Phytogb numerical classification. For example, rice (Oryza sativa) Phytogbs 1 and 2 (corresponding to the former nsHbs-1) should be indicated as rice Phytogb1.1 and Phytogb1.2, respectively (see text for a description on the species-specific Phytogbs acronym).
bHeme-Fe coordination and affinity for O2 correspond to those from moss Phytogb07–9, barley10, rice11 and Arabidopsis12 Phytogb1, Arabidopsis Phytogb212, Casuarina SymPhytogb13, soybean Lb14,15 and Arabidopsis Phytogb316 representative of Phytogb0, Phytogb1, Phytogb2, SymPhytogb, Lb and Phytogb3, respectively.
cAmino acid sequence of algal globins analyzed so far17–19 is similar to that of land plant Phytogb0 and Phytogb3, hence algal globins can be classified as Phytogb0 or Phytogb3, respectively.
dSome SymPhytogbs and Lbs (such as the Parasponia20 and Casuarina21 and Chamaecrista22 globins, respectively) are intermediate between Phytogbs1 and Phytogbs2 and SymPhytogbs and Lbs22,23 because they exhibit amino acid sequence similarity to Phytogbs1 and Phytogbs2 (Figure 1) and are localized in non-legume an legume nodules and apparently play a role in symbiotic N2-fixation.
Note that Parasponia, Casuarina, Alnus and Myrica SymPhytogbs are intermediate between SymPhytogbs and Phytogbs1 and Phytogbs2 (see Table 1 for explanation). Figure modified from Garrocho-Villegas et al.23 (reprinted with permission).
RDH conceived the proposal. RDH, MSH and RAP discussed and proposed the novel nomenclature, prepared the first draft of the manuscript, revised the draft manuscript and have agreed to the final content.
Authors wish to express their gratitude to Itzel Rojas Sánchez, Gisselle A. Fuentes and Gustavo Rodríguez-Alonso for evaluating the Phytoglobins nomenclature presented here and providing useful comments.
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Competing Interests: No competing interests were disclosed.
References
1. VIRTANEN AI, LAINE T: Red, brown and green pigment in leguminous root nodules.Nature. 1946; 157: 25 PubMed AbstractCompeting Interests: No competing interests were disclosed.
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