Nodule-specific Cu⁺-chaperone NCC1 is required for symbiotic nitrogen fixation inMedicago truncatularoot nodules

Abstract

Cu+-chaperones are a diverse group of proteins that allocate Cu+to specific copper-proteins, creating different copper pools targeted to specific physiological processes. Symbiotic nitrogen fixation carried out in legume root nodules requires relatively large amounts of copper, for which targeted copper deliver systems would be required. MtNCC1 is a nodule-specific Cu+-chaperone encoded in theMedicago truncatulagenome, with a N-terminus Atx1-like domain that can bind Cu+with picomolar affinities. This gene is expressed primarily from the late infection zone to the early fixation zone, and is located in the cytosol, associated to plasma and symbiosome membranes, and within nuclei. Consistent with its key role in nitrogen fixation,ncc1mutants have a severe reduction of nitrogenase activity, and a 50% reduction in copper-dependent cytochromecoxidase activity. A subset of the copper-proteome is also affected in the mutant nodules. Many of these proteins can be pulled-down when using a Cu+-loaded N-terminal MtNCC1 moiety as a bait, indicating a role in nodule copper homeostasis and in copper-dependent physiological processes. Overall, these data suggest a pleiotropic role of MtNCC1 in copper delivery for symbiotic nitrogen fixation.

Forging a symbiosis: transition metal delivery in symbiotic nitrogen fixation

“…Similar mechanisms are in place to control subcellular copper allocation in other bacterial and eukaryotic cells (O'Halloran & Culotta, 2000; Tottey et al ., 2002). Recent evidence indicates that nodules have specific Cu + ‐chaperones that are able to metallate a subset of the cell copper proteome (Navarro et al ., 2023). In addition to this metal pool, transition metals would also bind to NA, considering that NAS2 is highly expressed in all nodule cells (Escudero et al ., 2020a).…”