Abstract
The NRAMP (natural resistance-associated macrophage protein) family of genes has been widely characterized in organisms ranging from bacteria to yeast, plants, mice, and humans. This gene family plays vital roles in divalent metal ion transport across cellular membranes. As yet, comprehensive analysis of NRAMP family genes has not been reported for soybean. In this study, bioinformatics analysis was conducted to identify 13 soybean NRAMP genes, along with their gene structures, phylogenetic relationships, and transmembrane domains. Expression analysis suggests that GmNRAMP genes function in numerous tissues and development stages. Moreover, soybean NRAMP genes were differentially regulated by deficiencies of N, P, K, Fe, and S, along with toxicities of Fe, Cu, Cd, and Mn. These results indicate that GmNRAMP genes function in many nutrient stress pathways, and might be involved in crosstalk among nutrient stress pathways. Subcellular localization analysis in Arabidopsis protoplasts confirmed the tonoplast or plasma membrane localization of selected soybean NRMAP proteins. Protein-protein interaction analysis found that the networks of three GmNRAMP proteins which putatively interact with nodulin-like proteins, almost distinct from the network that is common to the other 10 soybean NRAMP proteins. Subsequent qRT-PCR results confirmed that these three GmNRMAP genes exhibited enhanced expression in soybean nodules, suggesting potential functions in the transport of Fe or other metal ions in soybean nodules. Overall, the systematic analysis of the GmNRAMP gene family reported herein provides valuable information for further studies on the biological roles of GmNRAMPs in divalent metal ion transport in various soybean tissues under numerous nutrient stresses and soybean-rhizobia symbiosis.
Highlights
Iron (Fe) is an essential element for plant development and growth, with functions in several basic cellular processes, including photosynthesis, respiration, and chlorophyll biosynthesis (Kobayashi and Nishizawa, 2012)
All identified GmNRAMPs were named based on phylogenetic relationships among soybean NRAMP family members (Figure 1A and Table 1), with the tree being comprised of two main branches (Figure 1A)
From the phylogenetic tree of soybean NRAMP proteins, we noticed that all but GmNRAMP7 appeared in pairs, implying possible gene duplication occurred during evolution of NRAMP gene family, synteny analysis performed to determine the potential gene duplication with soybean NRAMP family
Summary
Iron (Fe) is an essential element for plant development and growth, with functions in several basic cellular processes, including photosynthesis, respiration, and chlorophyll biosynthesis (Kobayashi and Nishizawa, 2012). Fe is a vital component in heme, the Fe-sulfur (S) cluster, and other Fe-binding sites (Kobayashi and Nishizawa, 2012) Given these requirements and Fe deficiency is common in soils, plants have evolved highly efficient systems to acquire. Strategy I, which is found in non-graminaceous plants, utilizes IRT1 as the primary transporter responsible for uptake of Fe from soil into roots (Eide et al, 1996; Hell and Stephan, 2003; Walker and Connolly, 2008). YSL is the main transporter responsible for uptake of Fe from siderophore-Fe complexes into Strategy II graminaceous plants (Curie et al, 2001; Inoue et al, 2009; Thomine and Vert, 2013). Beyond these Strategy I and II transporters, the NRAMP family represents another transporter family associated with Fe uptake and transport (Thomine and Vert, 2013)
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