Abstract
Legumes express two major types of hemoglobins, namely symbiotic (leghemoglobins) and non-symbiotic (phytoglobins), with the latter being categorized into three classes according to phylogeny and biochemistry. Using knockout mutants, we show that all three phytoglobin classes are required for optimal vegetative and reproductive development of Lotus japonicus. The mutants of two class 1 phytoglobins showed different phenotypes: Ljglb1-1 plants were smaller and had relatively more pods, whereas Ljglb1-2 plants had no distinctive vegetative phenotype and produced relatively fewer pods. Non-nodulated plants lacking LjGlb2-1 showed delayed growth and alterations in the leaf metabolome linked to amino acid processing, fermentative and respiratory pathways, and hormonal balance. The leaves of mutant plants accumulated salicylic acid and contained relatively less methyl jasmonic acid, suggesting crosstalk between LjGlb2-1 and the signaling pathways of both hormones. Based on the expression of LjGlb2-1 in leaves, the alterations of flowering and fruiting of nodulated Ljglb2-1 plants, the developmental and biochemical phenotypes of the mutant fed on ammonium nitrate, and the heme coordination and reactivity of the protein toward nitric oxide, we conclude that LjGlb2-1 is not a leghemoglobin but an unusual class 2 phytoglobin. For comparison, we have also characterized a close relative of LjGlb2-1 in Medicago truncatula, MtLb3, and conclude that this is an atypical leghemoglobin.
Highlights
Legumes contain two major types of hemoglobins, namely symbiotic or leghemoglobins (Lbs) and non-symbiotic or phytoglobins (Glbs)
Based on the expression of LjGlb2-1 in leaves, the alterations of flowering and fruiting of nodulated Ljglb2-1 plants, the developmental and biochemical phenotypes of the mutant fed on ammonium nitrate, and the heme coordination and reactivity of the protein toward nitric oxide, we conclude that LjGlb2-1 is not a leghemoglobin but an unusual class 2 phytoglobin
The mutant lines for all four genes were phenotyped under nodulating conditions
Summary
Legumes contain two major types of hemoglobins, namely symbiotic or leghemoglobins (Lbs) and non-symbiotic or phytoglobins (Glbs). Class 1 Glbs have a very high O2 affinity and are unlikely to transport and deliver O2 for metabolic reactions.Among other functions, they are involved in plant responses and adaptations to hypoxia and in nitric oxide (NO) homeostasis (Igamberdiev and Hill, 2004). These Glbs are crucial for the onset and functioning of the legume–Rhizobium symbiosis by modulating NO levels (Shimoda et al, 2005; Fukudome et al, 2016; Berger et al, 2020). Class 3 Glbs share homology with the ‘truncated’ hemoglobins of prokaryotes and show low O2 affinity.They have unknown functions, roles in the suppression of plant defense responses during rhizobial and mycorrhizal symbioses and in protection from nitrosative stress have been suggested (Vieweg et al, 2005)
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