Manganese (Mn) is an important micronutrient for plant growth and development and sustains metabolic roles within different plant cell compartments. The metal is an essential cofactor for the oxygen-evolving complex (OEC) of the photosynthetic machinery, catalyzing the water-splitting reaction in photosystem II (PSII). Despite the importance of Mn for photosynthesis and other processes, the physiological relevance of Mn uptake and compartmentation in plants has been underrated. The subcellular Mn homeostasis to maintain compartmented Mn-dependent metabolic processes like glycosylation, ROS scavenging, and photosynthesis is mediated by a multitude of transport proteins from diverse gene families. However, Mn homeostasis may be disturbed under suboptimal or excessive Mn availability. Mn deficiency is a serious, widespread plant nutritional disorder in dry, well-aerated and calcareous soils, as well as in soils containing high amounts of organic matter, where bio-availability of Mn can decrease far below the level that is required for normal plant growth. By contrast, Mn toxicity occurs on poorly drained and acidic soils in which high amounts of Mn are rendered available. Consequently, plants have evolved mechanisms to tightly regulate Mn uptake, trafficking, and storage. This review provides a comprehensive overview, with a focus on recent advances, on the multiple functions of transporters involved in Mn homeostasis, as well as their regulatory mechanisms in the plant's response to different conditions of Mn availability.

/pdf/manganese-in-plants-from-acquisition-to-subcellular-1vn9c3muvz.pdf

Manganese in Plants: From Acquisition to Subcellular Allocation.

Metal homeostasis is critical for plant growth, development and adaptation to environmental stresses and largely governed by a variety of metal transporters. The plant ZIP (Zn-regulated transporter, Iron-regulated transporter-like Protein) family proteins belong to the integral membrane transporters responsible for uptake and allocation of essential and non-essential metals. However, whether the ZIP family members mediate metal efflux and its regulatory mechanism remains unknown. In this report, we provided evidence that OsZIP1 is a metal-detoxified transporter through preventing excess Zn, Cu and Cd accumulation in rice. OsZIP1 is abundantly expressed in roots throughout the life span and sufficiently induced by excess Zn, Cu and Cd but not by Mn and Fe at transcriptional and translational levels. Expression of OsZIP-GFP fusion in rice protoplasts and tobacco leaves shows that OsZIP1 resides in the endoplasmic reticulum (ER) and plasma membrane (PM). The yeast (Saccharomyces cerevisiae) complementation test shows that expression of OsZIP1 reduced Zn accumulation. Transgenic rice overexpressing OsZIP1 grew better under excess metal stress but accumulated less of the metals in plants. In contrast, both oszip1 mutant and RNA interference (RNAi) lines accumulated more metal in roots and contributed to metal sensitive phenotypes. These results suggest OsZIP1 is able to function as a metal exporter in rice when Zn, Cu and Cd are excess in environment. We further identified the DNA methylation of histone H3K9me2 of OsZIP1 and found that OsZIP1 locus, whose transcribed regions imbed a 242 bp sequence, is demethylated, suggesting that epigenetic modification is likely associated with OsZIP1 function under Cd stress. OsZIP1 is a transporter that is required for detoxification of excess Zn, Cu and Cd in rice.

/pdf/oszip1-functions-as-a-metal-efflux-transporter-limiting-5bqjynoz8l.pdf

OsZIP1 functions as a metal efflux transporter limiting excess zinc, copper and cadmium accumulation in rice

Rice is a major dietary source of the toxic metal, cadmium (Cd). Previous studies reported that the rice transporter, OsNRAMP1, (Natural resistance-associated macrophage protein 1) could transport iron (Fe), Cd and arsenic (As) in heterologous yeast assays. However, the in planta function of OsNRAMP1 remains unknown. Here, we showed that OsNRAMP1 was able to transport Cd and manganese (Mn) when expressed in yeast, but did not transport Fe or As. OsNRAMP1 was mainly expressed in roots and leaves and encoded a plasma membrane-localized protein. OsNRAMP1 expression was induced by Cd treatment and Fe deficiency. Immunostaining showed that OsNRAMP1 was localized in all root cells, except the central vasculature, and in leaf mesophyll cells. The knockout of OsNRAMP1 resulted in significant decreases in root uptake of Cd and Mn and their accumulation in rice shoots and grains, and increased sensitivity to Mn deficiency. The knockout of OsNRAMP1 had smaller effects on Cd and Mn uptake than knockout of OsNRAMP5, while knockout of both genes resulted in large decreases in the uptake of the two metals. Taken together, OsNRAMP1 contributes significantly to the uptake of Mn and Cd in rice, and the functions of OsNRAMP1 and OsNRAMP5 are similar but not redundant.

OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice

Cadmium (Cd) is one of the most toxic metals in the environment, and has noxious effects on plant growth and production. Cd-accumulating plants showed reduced growth and productivity. Therefore, remediation of this non-essential and toxic pollutant is a prerequisite. Plant-based phytoremediation methodology is considered as one a secure, environmentally friendly, and cost-effective approach for toxic metal remediation. Phytoremediating plants transport and accumulate Cd inside their roots, shoots, leaves, and vacuoles. Phytoremediation of Cd-contaminated sites through hyperaccumulator plants proves a ground-breaking and profitable choice to combat the contaminants. Moreover, the efficiency of Cd phytoremediation and Cd bioavailability can be improved by using plant growth-promoting bacteria (PGPB). Emerging modern molecular technologies have augmented our insight into the metabolic processes involved in Cd tolerance in regular cultivated crops and hyperaccumulator plants. Plants’ development via genetic engineering tools, like enhanced metal uptake, metal transport, Cd accumulation, and the overall Cd tolerance, unlocks new directions for phytoremediation. In this review, we outline the physiological, biochemical, and molecular mechanisms involved in Cd phytoremediation. Further, a focus on the potential of omics and genetic engineering strategies has been documented for the efficient remediation of a Cd-contaminated environment.

Phytoremediation of Cadmium: Physiological, Biochemical, and Molecular Mechanisms

Plants require trace levels of manganese (Mn) for survival, as it is an essential cofactor in oxygen metabolism, especially O2 production via photosynthesis and the disposal of superoxide radicals. These processes occur in specialized organelles, requiring membrane-bound intracellular transporters to partition Mn between cell compartments. We identified an Arabidopsis thaliana member of the NRAMP family of divalent metal transporters, NRAMP2, which functions in the intracellular distribution of Mn. Two knockdown alleles of NRAMP2 showed decreased activity of photosystem II and increased oxidative stress under Mn-deficient conditions, yet total Mn content remained unchanged. At the subcellular level, these phenotypes were associated with a loss of Mn content in vacuoles and chloroplasts. NRAMP2 was able to rescue the mitochondrial yeast mutant mtm1∆ In plants, NRAMP2 is a resident protein of the trans-Golgi network. NRAMP2 may act indirectly on downstream organelles by building up a cytosolic pool that is used to feed target compartments. Moreover, not only does the nramp2 mutant accumulate superoxide ions, but NRAMP2 can functionally replace cytosolic superoxide dismutase in yeast, indicating that the pool of Mn displaced by NRAMP2 is required for the detoxification of reactive oxygen species.

https://hal.archives-ouvertes.fr/hal-01695892/document

Intracellular Distribution of Manganese by the Trans-Golgi Network Transporter NRAMP2 Is Critical for Photosynthesis and Cellular Redox Homeostasis

To 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 (H2 O2 ) 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 H2 O2 is partially responsible for the root growth inhibition and NRAMP2 is involved in remobilization of Mn in Golgi for root growth.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.14783

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

OsMTP11, a trans-Golgi network localized transporter, is involved in manganese tolerance in rice.

Natural resistance-associated macrophage proteins (NRAMPs) have been shown to transport a wide range of divalent metal ions, such as manganese (Mn), cadmium (Cd), and Iron (Fe). Iron is an essential micronutrient for plants and Fe deficiency can lead to chlorosis or decreased biomass. AtNRAMP6 has demonstrated the capability to transport Cd, but its physiological function is currently unclear. This study demonstrates that AtNRAMP6 is localized to the Golgi/trans-Golgi network and plays an important role in intracellular Fe homeostasis in the flowering plant genus Arabidopsis. GUS tissue-specific expression revealed that AtNRAMP6 is highly expressed in the lateral roots and young leaves (three to four top leaves) of Arabidopsis. Moreover, knocking out AtNRAMP6 was shown to impair lateral root growth without having a differential effect on the main root under Fe-deficient conditions. Lastly, the expression of AtNRAMP6 was found to exacerbate the sensitivity of the yeast mutant Δccc1 to an excessive amount of Fe. These findings indicate that AtNRAMP6 plays an important role in the growth of Arabidopsis in Fe-deficient conditions.

/pdf/the-intracellular-transporter-atnramp6-is-involved-in-fe-w0rtsu3t0f.pdf

The Intracellular Transporter AtNRAMP6 Is Involved in Fe Homeostasis in Arabidopsis.

Metal tolerance proteins (MTPs) play important roles in heavy metal homeostasis and tolerance in plants. As a part of the MTP family, manganese-cation diffusion facilitator (Mn-CDF) subfamily members transport Mn and iron (Fe) in plants. However, the role of these Mn-CDFs in pear is not well established. In this study, seven members of the Mn-CDF subgroup were identified in Chinese white pear (Pyrus bretschneideri Rehd.), based on recently released draft genome of pear. These members were predicted to encode proteins ranging from 394 to 416 amino acids, including 6 putative transmembrane domains (TMDs), and predicted to localize in the Golgi or vacuole membrane. Furthermore, all the members contained a highly conserved signature sequence in TMD-II and TMD-V. Yeast functional complementation assays demonstrated that the expression of PbMTP8.1, PbMTP8.2, PbMTP9, and PbMTP10 in particular conferred Mn and Fe tolerance, while PbMTP11.1 and PbMTP11.2 only transport Mn, and PbMTP11.3 transports neither Mn nor any other ion that was used in the study. Quantitative real-time PCR analysis indicated that these genes were widely expressed in the root, stem, and leaf tissues of the pear seedlings, but the expression levels differed among the different tissues. The results provide us with systematic information about the Mn-CDF subgroup genes and their possible roles in the distribution and homeostasis of Mn and Fe in pear.

Phylogenetic and Expression Analysis of Mn-CDF Transporters in Pear (Pyrus bretschneideri Rehd.)

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

OsMTP11, a trans-Golgi network localized transporter, is involved in manganese tolerance in rice.

The Intracellular Transporter AtNRAMP6 Is Involved in Fe Homeostasis in Arabidopsis.

Phylogenetic and Expression Analysis of Mn-CDF Transporters in Pear (Pyrus bretschneideri Rehd.)