NRAMP2, a trans‐Golgi network‐localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency

Abstract

SummaryTo cope with manganese (Mn) deficiency, plants have evolved an efficient transport system to uptake and redistribute Mn. However, the underlying molecular mechanisms remain to be demonstrated.We carried out a forward genetic screen in a root high-affinity Mn transporter nramp1 mutant background in Arabidopsis thaliana and identified an uncharacterized Mn transport NRAMP2. We investigated the effect of nramp2 mutation on root growth and reactive oxygen species (ROS) accumulation and we also examined the NRAMP2 expression pattern, and the subcellular localization and transport activity of NRAMP2.Mutation of NRAMP2 impaired plant growth, while overexpression of NRAMP2 improved plant growth under low Mn conditions. In the nramp2-1nramp1 double mutant, Mn deficiency inhibited root cell elongation and root hair development, which was associated with increased hydrogen peroxide (H 2 O 2 ) accumulation. NRAMP2 is preferentially localized to the trans-Golgi network. NRAMP2 has Mn influx transport activity in yeast, and mutation of NRAMP2 led to greater Mn retention in roots.Our results suggest that under Mn-deficient conditions, increased accumulation of H 2 O 2 is partially responsible for the root growth inhibition and NRAMP2 is involved in remobilization of Mn in Golgi for root growth.

Manganese in Plants: From Acquisition to Subcellular Allocation

“…Golgi/PVC Unaffected by +Mn - Delhaize et al, 2007;Peiter et al, 2007 ShMTP8 -Tonoplast -- Delhaize et al, 2003Delhaize et al, , 2007 Curie et al, 2000;Thomine et al, 2000;Cailliatte et al, 2010;Castaings et al, 2016 AtNRAMP2 Root (pericycle, root tip), leaf vasculature, flower, trichome TGN Up-regulated by -Mn down-regulated by -Fe - Curie et al, 2000;Alejandro et al, 2017;Gao et al, 2018 (Continued) (Henriques, 2004;Hebbern et al, 2009;Alejandro et al, 2017), as well as higher susceptibility to pathogen infections (Heckman et al, 2003;Heine et al, 2011), imbalance in plant water relations (Ohki, 1985;Hebbern et al, 2009), and decreased tolerance to low temperatures (Ihnatowicz et al, 2014;Stoltz and Wallenhammar, 2014). Mn deficiency leads to a reduced number of Mn-complexes in the PSII core, which causes the destabilization and disintegration of PSII complexes that lowers the net photosynthesis rate (Schmidt et al, 2016).…”

“…In Arabidopsis, AtNRAMP2 is located in the TGN ( Figure 3A) and was shown to be involved in the intracellular allocation of Mn (Alejandro et al, 2017;Gao et al, 2018). AtNRAMP2 is mainly expressed in the vasculature of roots and shoots and was barely induced upon Mn deficiency.…”

OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice

“…AtNRAMP1 is localized to the plasma membrane of roots cells, and mediates highaffinity Mn uptake into the roots under the conditions of low manganese (Mn) availability (Cailliatte, Schikora, Briat, Mari, & Curie, 2010), as well low-affinity uptake of ferrous iron [Fe(II)] (Castaings, Caquot, Loubet, & Curie, 2016). AtNRAMP2 encodes a resident protein in the trans-Golgi network and functions in the remobilization of Mn in the Golgi for root growth under Mn-deficient conditions (Alejandro et al, 2017;Gao et al, 2018). Both AtNRAMP3 and AtNRAMP4 proteins are localized at the tonoplast and play redundant roles in the remobilization of the vacuolar Fe stores to support early development under Fe-limiting conditions (Lanquar et al, 2005).…”

Sorting of Arabidopsis NRAMP3 and NRAMP4 depends on adaptor protein complex AP4 and a dileucine‐based motif

“…So does Arabidopsis NRAMP2, which was characterized very recently: NRAMP2‐GFP was found to co‐localize with SYP61‐mCherry at the TGN of transiently transformed mesophyll protoplasts, and, corresponding to that, NRAMP2‐YFP labeled small spherical compartments also in stably transformed plants. In yeast cells, however, the same YFP‐fusion was sorted to the vacuolar membrane . It would be interesting to determine how the N ‐terminal dileucine of NRAMP2 affects sorting in Arabidopsis and yeast (or in response to metal supply).…”

“…In yeast cells, however, the same YFP-fusion was sorted to the vacuolar membrane. 84 It would be interesting to determine how the N-terminal dileucine of NRAMP2 affects sorting in Arabidopsis and yeast (or in response to metal supply).…”