Iron: an essential micronutrient for the legume-rhizobium symbiosis

Abstract

Legumes, which develop a symbiosis with nitrogen-fixing bacteria, have an increased demand for iron. Iron is required for the synthesis of iron-containing proteins in the host, including the highly abundant leghemoglobin, and in bacteroids for nitrogenase and cytochromes of the electron transport chain. Deficiencies in iron can affect initiation and development of the nodule. Within root cells, iron is chelated with organic acids such as citrate and nicotianamine and distributed to other parts of the plant. Transport to the nitrogen-fixing bacteroids in infected cells of nodules is more complicated. Formation of the symbiosis results in bacteroids internalized within root cortical cells of the legume where they are surrounded by a plant-derived membrane termed the symbiosome membrane (SM). This membrane forms an interface that regulates nutrient supply to the bacteroid. Consequently, iron must cross this membrane before being supplied to the bacteroid. Iron is transported across the SM as both ferric and ferrous iron. However, uptake of Fe(II) by both the symbiosome and bacteroid is faster than Fe(III) uptake. Members of more than one protein family may be responsible for Fe(II) transport across the SM. The only Fe(II) transporter in nodules characterized to date is GmDMT1 (Glycine max divalent metal transporter 1), which is located on the SM in soybean. Like the root plasma membrane, the SM has ferric iron reductase activity. The protein responsible has not been identified but is predicted to reduce ferric iron accumulated in the symbiosome space prior to uptake by the bacteroid. With the recent publication of a number of legume genomes including Medicago truncatula and G. max, a large number of additional candidate transport proteins have been identified. Members of the NRAMP (natural resistance-associated macrophage protein), YSL (yellow stripe-like), VIT (vacuolar iron transporter), and ZIP (Zrt-, Irt-like protein) transport families show enhanced expression in nodules and are expected to play a role in the transport of iron and other metals across symbiotic membranes.

Proteomic Analysis of the Soybean Symbiosome Identifies New Symbiotic Proteins*

“…Glyma09g31910 and Glyma08g04830 are in a clade of the PLAC8 family, known as plant cadmium resistance (PCR) proteins and fruit weight 2.2-like (FWL). Of particular interest, given the requirement for metal transport into the symbiosome (132,133), is the reported role of two members of this clade from Arabidopsis, AtPCR1 and AtPCR2, that appear to be involved in the export of heavy metals from root cells (134,135). This would translate to an import of metal into the symbiosome and the presence of homologous proteins on the SM suggests a possible role in maintaining adequate nutrition for the isolated bacteroids through import of a variety of metal cations.…”

Transcriptional responses of tolerant and susceptible soybeans to soybean aphid (Aphis glycines Matsumura) herbivory

“…Two of these genes were of unknown function and one (Glyma10g31610) was a yellow stripelike (YSL) ortholog (Table 3). YSLs are membrane located transporters that are important to the intercellular transport of iron and other metals and contribute to the overall metal nutrition in plants (Brear et al 2013;Conte et al 2013). Although metal ion transporters have not been analyzed in detail in plant-aphid interactions, it is possible that they could be part of the cascade of changes that are elicited upon aphid feeding (Boyd 2006;Poschenrieder et al 2006).…”

Comparative analysis of iron deficiency chlorosis responses in soybean (Glycine max) and barrel medic (Medicago truncatula)

“…NRAMP3 and VIT1 have contrasting functions: while the first is responsible for the remobilization from the vacuole (Lanquar et al, 2005), the second is responsible for the Fe loading in the vacuole (Kim et al, 2006). Studies in A. thaliana demonstrate that NRAMP3 is an H + metal symporter responsible for Fe and Mn remobilization from the vacuole, a crucial step during early seedling development (Lanquar et al, 2010 (Brear et al, 2013). Studies in A. thaliana (Kim and Guerinot, 2007) demonstrated that AtNRAMP3 and AtVIT1 mutants present arrested seedling growth when grown on Fe deficient soils.…”

“…Fe 2+ is then transported into the plant by specific membrane transporters (Grotz and Guerinot, 2006), such as the Iron-Regulated Transporter 1 (IRT1) (Waters et al, 2002). A broad spectrum of transporters have been characterized, such as the Natural Resistance Associated Macrophage (NRAMP) proteins, involved in Fe import into the cytoplasm, the Vacuolar Iron Transporter (VIT), involved in the uptake of Fe 2+ into the vacuole for storage (Brear et al, 2013), and the Yellow Stripe 1-Like (YSL), involved in the transport of Fe 2+ -NA complexes (Kim et al, 2006). Free Fe is toxic since it facilitates the generation of highly reactive oxygen species (ROS).…”