The FRD3 Citrate Effluxer Promotes Iron Nutrition between Symplastically Disconnected Tissues throughout Arabidopsis Development

Abstract

We present data supporting a general role for FERRIC REDICTASE DEFECTIVE3 (FRD3), an efflux transporter of the efficient iron chelator citrate, in maintaining iron homeostasis throughout plant development. In addition to its well-known expression in root, we show that FRD3 is strongly expressed in Arabidopsis thaliana seed and flower. Consistently, frd3 lossof-function mutants are defective in early germination and are almost completely sterile, both defects being rescued by iron and/or citrate supply. The frd3 fertility defect is caused by pollen abortion and is associated with the male gametophytic expression of FRD3. Iron imaging shows the presence of important deposits of iron on the surface of aborted pollen grains. This points to a role for FRD3 and citrate in proper iron nutrition of embryo and pollen. Based on the findings that iron acquisition in embryo, leaf, and pollen depends on FRD3, we propose that FRD3 mediated-citrate release in the apoplastic space represents an important process by which efficient iron nutrition is achieved between adjacent tissues lacking symplastic connections. These results reveal a physiological role for citrate in the apoplastic transport of iron throughout development, and provide a general model for multicellular organisms in the cell-to-cell transport of iron involving extracellular circulation.

Nicotianamine Functions in the Phloem-Based Transport of Iron to Sink Organs, in Pollen Development and Pollen Tube Growth in Arabidopsis

“…We therefore propose that lateral transport may rely on citrate and FRD3 rather than on NA. Citrate is used to mobilize extracellular Fe from the apoplast throughout plant development, and this could also be important during lateral transport of Fe from the xylem to the leaf parenchyma (Roschzttardtz et al, 2011). This is supported by the finding that frd3 nas4x-2 leaves are strongly chlorotic and do not recover from the chlorosis with age, in contrast with nas4x-2.…”

“…The Perls Fe stain method was previously described (Green and Rogers, 2004;Roschzttardtz et al, 2011). Leaves and flowers were harvested freshly and were vacuum infiltrated with the fixative methacarn (methanol/ chloroform/pure acetic acid, 6:3:1) and incubated for 1 h at room temperature.…”

“…Translocation of Fe out of the xylem and into the phloem occurs irrespective of NA and therefore does not seem to involve Fe-NA transporters, as mentioned above. It was reported that citrate also chelates Fe in the apoplast of leaf cells (Roschzttardtz et al, 2011), and this complex may facilitate the transport of Fe out of the xylem into adjacent cells. Ferric reductase genes and divalent metal transport genes are expressed in leaves (Guerinot, 2000;Mukherjee et al, 2006).…”

Iron-Binding E3 Ligase Mediates Iron Response in Plants by Targeting Basic Helix-Loop-Helix Transcription Factors

“…The role of YSL (AtYSL1 and AtYSL3) and the oligopeptide transporter (AtOPT3) protein family in iron translocation to developing embryo and into the seed coat is critical for reproductive growth (Le Jean et al, 2005;Stacey et al, 2008;Chu et al, 2010;Mendoza-Cózatl et al, 2014;Zhai et al, 2014). Additionally, the role of Arabidopsis thaliana FERRIC REDICTASE DEFECTIVE3 (AtFRD3) in iron acquisition in reproductive tissues such as pollen grain and embryos suggests a complex mechanism of iron nutrition during embryogenesis (Roschzttardtz et al, 2011b). Examination of ysl, opt3, and frd3 mutations in combination with the bts mutant background could shed new light on the role of BTS during seed development.…”

Similarities and Differences in the Acquisition of Fe and P by Dicot Plants

“…The Arabidopsis frd3 mutant is impaired in the translocation of Fe through the xylem [84,85]. When grown under Fe-sufficient conditions it is chlorotic and with constitutive activation of Fe acquisition genes it accumulates a high Fe concentration in the roots [86].…”