The iron‐regulated transporter 1 plays an essential role in uptake, translocation and grain‐loading of manganese, but not iron, in barley

Abstract

Transporters involved in manganese (Mn) uptake and intracellular Mn homeostasis in Arabidopsis and rice are well characterized, while much less is known for barley, which is particularly prone to Mn deficiency. In this study we have investigated the role of the iron-regulated transporter 1 (IRT1) for Mn uptake and translocation in barley plants. We employed an RNAi approach to reduce HvIRT1 expression to 5% of the wild-type level. This enabled characterization of the functional role of HvIRT1 by use of advanced imaging and phenotyping techniques applied to plants growing in hydroponics or soils with different Mn availability. Our results highlight the importance of HvIRT1 for the transport of Mn across the root endodermis into the stele. In the hvirt1-RNAi lines, a chlorotic phenotype with reduced shoot Mn concentration and impaired photosynthetic functionality was observed, especially under conditions with low Mn availability. We also document that HvIRT1 controlled the Mn distribution within the barley grain. Surprisingly, unlike other IRT1 orthologues, HvIRT1 played no significant role in iron uptake. We conclude that the barley IRT1 orthologue has a novel function with respect to ensuring sufficient shoot Mn concentrations. The preference of IRT1 for Mn instead of Fe is discussed in an evolutionary context.

The Intensity of Manganese Deficiency Strongly Affects Root Endodermal Suberization and Ion Homeostasis

“…Such outwards leakage would also be important for elements recycled from the shoots to the roots via the phloem, particularly K (White, 1997). Another important consideration for this model is the observation that the localization of IRT1 may change under Mn deficiency, compared to under control conditions, as was observed by (Long et al, 2018). This would implicate that more Mn could be taken up in the epidermis in the control plants, which potentially would lead to more Mn following the symplastic pathway, which is unaffected by suberin.…”

“…In barley, HvNramp5 is localized to the plasma membrane of the epidermal cells in the first half centimeter of the root tip, but is also weakly expressed in the central cylinder (Wu et al, 2016). HvIRT1 is expressed in a larger part of the root tip (the first 2 cm), showing predominantly epidermal localization in Mn-sufficient roots, but shifting toward the stele during Mn deficiency (Long et al, 2018). Effects of reduced suberization in mildly Mn-deficient plants will therefore likely be more important for HvIRT1 than for HvNramp5, because the latter is expressed closer to the root tip.…”

“…Effects of reduced suberization in mildly Mn-deficient plants will therefore likely be more important for HvIRT1 than for HvNramp5, because the latter is expressed closer to the root tip. Upregulation of HvIRT1 expression in the stele rather than in the epidermis in response to Mn deficiency (Long et al, 2018) may under these conditions provide a more efficient Mn transport to the shoot, rather than promoting Mn compartmentalization in root vacuoles. As already stated, previous studies have observed that increased suberization is associated with a decrease in leaf Mn concentrations and vice versa (Baxter et al, 2009;Li et al, 2017).…”

Manganese in Plants: From Acquisition to Subcellular Allocation

“…Interestingly, in barley, the plasma membrane transporter HvIRT1 is implicated in the uptake and translocation of Mn 2+ , but not Fe 2+ (Long et al, 2018). HvIRT1 is constitutively expressed in cells of the epidermis and in pericycle funder cells ( Figure 1C), but under Mn deficiency, its expression is extended to the entire pericycle and the cortex.…”

Grain Mineral Accumulation Changes in Chinese Maize Cultivars Released in Different Decades and the Responses to Nitrogen Fertilizer

“…Using quantitative trait loci in wheat, a previous study identified a relationship between grain protein concentration and grain Fe, Cu, and Zn concentrations (Peleg et al, 2009). Additionally, it was discovered that an Fe-regulated transporter (IRT1) plays an important role in Mn loading of grains in barley (Long et al, 2018), suggesting that there may be a common physiological mechanism for the accumulation of nutrients in grains. Thus, the concentrations of several nutrients can be increased as a whole without affecting crop yield.…”