Dataset Information

Implications for Cation Selectivity and Evolution by a Novel Cation Diffusion Facilitator Family Member From the Moderate Halophile Planococcus dechangensis.

ABSTRACT: In the cation diffusion facilitator (CDF) family, the transported substrates are confined to divalent metal ions, such as Zn2+, Fe2+, and Mn2+. However, this study identifies a novel CDF member designated MceT from the moderate halophile Planococcus dechangensis. MceT functions as a Na+(Li+, K+)/H+ antiporter, together with its capability of facilitated Zn2+ diffusion into cells, which have not been reported in any identified CDF transporters as yet. MceT is proposed to represent a novel CDF group, Na-CDF, which shares significantly distant phylogenetic relationship with three known CDF groups including Mn-CDF, Fe/Zn-CDF, and Zn-CDF. Variation of key function-related residues to "Y44-S48-Q150" in two structural motifs explains a significant discrimination in cation selectivity between Na-CDF group and three major known CDF groups. Functional analysis via site-directed mutagenesis confirms that MceT employs Q150, S158, and D184 for the function of MceT as a Na+(Li+, K+)/H+ antiporter, and retains D41, D154, and D184 for its facilitated Zn2+ diffusion into cells. These presented findings imply that MceT has evolved from its native CDF family function to a Na+/H+ antiporter in an evolutionary strategy of the substitution of key conserved residues to "Q150-S158-D184" motif. More importantly, the discovery of MceT contributes to a typical transporter model of CDF family with the unique structural motifs, which will be utilized to explore the cation-selective mechanisms of secondary transporters.

SUBMITTER: Xu T

PROVIDER: S-EPMC6440370 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Implications for Cation Selectivity and Evolution by a Novel Cation Diffusion Facilitator Family Member From the Moderate Halophile Planococcus dechangensis.

Xu Tong T Chen Huiwen H Li Jincheng J Hong Shan S Shao Li L Zheng Xiutao X Zou Qiao Q Wang Yuting Y Guo Sijia S Jiang Juquan J

Frontiers in microbiology 20190322

In the cation diffusion facilitator (CDF) family, the transported substrates are confined to divalent metal ions, such as Zn2+, Fe2+, and Mn2+. However, this study identifies a novel CDF member designated MceT from the moderate halophile Planococcus dechangensis. MceT functions as a Na+(Li+, K+)/H+ antiporter, together with its capability of facilitated Zn2+ diffusion into cells, which have not been re ...[more]

PMID: 30967858

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Project description:BackgroundMembers of the cation diffusion facilitator (CDF) family are integral membrane divalent cation transporters that transport metal ions out of the cytoplasm either into the extracellular space or into internal compartments such as the vacuole. The spectrum of cations known to be transported by proteins of the CDF family include Zn, Fe, Co, Cd, and Mn. Members of this family have been identified in prokaryotes, eukaryotes, and archaea, and in sequenced plant genomes. CDF families range in size from nine members in Selaginella moellendorffii to 19 members in Populus trichocarpa. Phylogenetic analysis suggests that the CDF family has expanded within plants, but a definitive plant CDF family phylogeny has not been constructed.ResultsRepresentative CDF members were annotated from diverse genomes across the Viridiplantae and Rhodophyta lineages and used to identify phylogenetic relationships within the CDF family. Bayesian phylogenetic analysis of CDF amino acid sequence data supports organizing land plant CDF family sequences into 7 groups. The origin of the 7 groups predates the emergence of land plants. Among these, 5 of the 7 groups are likely to have originated at the base of the tree of life, and 2 of 7 groups appear to be derived from a duplication event prior to or coincident with land plant evolution. Within land plants, local expansion continues within select groups, while several groups are strictly maintained as one gene copy per genome.ConclusionsDefining the CDF gene family phylogeny contributes to our understanding of this family in several ways. First, when embarking upon functional studies of the members, defining primary groups improves the predictive power of functional assignment of orthologous/paralogous genes and aids in hypothesis generation. Second, defining groups will allow a group-specific sequence motif to be generated that will help define future CDF family sequences and aid in functional motif identification, which currently is lacking for this family in plants. Third, the plant-specific expansion resulting in Groups 8 and 9 evolved coincident to the early primary radiation of plants onto land, suggesting these families may have been important for early land colonization.

Project description:Salt stress is one of the major abiotic factors that affect the metabolism, growth and development of plants, and soybean [Glycine max (L.) Merr.] germination is sensitive to salt stress. Thus, to ensure the successful establishment and productivity of soybeans in saline soil, the genetic mechanisms of salt tolerance at the soybean germination stage need to be explored. In this study, a population of 184 recombinant inbred lines (RILs) was utilized to map quantitative trait loci (QTLs) related to salt tolerance. A major QTL related to salt tolerance at the soybean germination stage named qST-8 was closely linked with the marker Sat_162 and detected on chromosome 8. Interestingly, a genome-wide association study (GWAS) identified several single nucleotide polymorphisms (SNPs) significantly associated with salt tolerance in the same genetic region on chromosome 8. Resequencing, bioinformatics and gene expression analyses were implemented to identify the candidate gene Glyma.08g102000, which belongs to the cation diffusion facilitator (CDF) family and was named GmCDF1. Overexpression and RNA interference of GmCDF1 in soybean hairy roots resulted in increased sensitivity and tolerance to salt stress, respectively. This report provides the first demonstration that GmCDF1 negatively regulates salt tolerance by maintaining K+-Na+ homeostasis in soybean. In addition, GmCDF1 affected the expression of two ion homeostasis-associated genes, salt overly sensitive 1 (GmSOS1) and Na+/H+ exchanger 1 (GmNHX1), in transgenic hairy roots. Moreover, a haplotype analysis detected ten haplotypes of GmCDF1 in 31 soybean genotypes. A candidate-gene association analysis showed that two SNPs in GmCDF1 were significantly associated with salt tolerance and that Hap1 was more sensitive to salt stress than Hap2. The results demonstrated that the expression level of GmCDF1 was negatively correlated with salt tolerance in the 31 soybean accessions (r = -0.56, P < 0.01). Taken together, these results not only indicate that GmCDF1 plays a negative role in soybean salt tolerance but also help elucidate the molecular mechanisms of salt tolerance and accelerate the breeding of salt-tolerant soybean.

Project description:Cation diffusion facilitators (CDFs) are a large family of divalent metal transporters that collectively possess broad metal specificity and contribute to intracellular metal homeostasis and virulence in bacterial pathogens. Streptococcus pneumoniae expresses two homologous CDF efflux transporters, MntE and CzcD. Cells lacking mntE or czcD are sensitive to manganese (Mn) or zinc (Zn) toxicity, respectively, and specifically accumulate Mn or Zn, respectively, thus suggesting that MntE selectively transports Mn, while CzcD transports Zn. Here, we probe the origin of this metal specificity using a phenotypic growth analysis of pneumococcal variants. Structural homology to Escherichia coli YiiP predicts that both MntE and CzcD are dimeric and each protomer harbors four pairs of conserved metal-binding sites, termed the A site, the B site, and the C1/C2 binuclear site. We find that single amino acid mutations within both the transmembrane domain A site and the B site in both CDFs result in a cellular metal sensitivity similar to that of the corresponding null mutants. However, multiple mutations in the predicted cytoplasmic C1/C2 cluster of MntE have no impact on cellular Mn resistance, in contrast to the analogous substitutions in CzcD, which do have on impact on cellular Zn resistance. Deletion of the MntE-specific C-terminal tail, present only in Mn-specific bacterial CDFs, resulted in only a modest growth phenotype. Further analysis of MntE-CzcD functional chimeric transporters showed that Asn and Asp in the ND-DD A-site motif of MntE and the most N-terminal His in the HD-HD site A of CzcD (the specified amino acids are underlined) play key roles in transporter metal selectivity.Cation diffusion facilitator (CDF) proteins are divalent metal ion transporters that are conserved in organisms ranging from bacteria to humans and that play important roles in cellular physiology, from metal homeostasis and resistance to type I diabetes in vertebrates. The respiratory pathogen Streptococcus pneumoniae expresses two metal CDF transporters, CzcD and MntE. How CDFs achieve metal selectivity is unclear. We show here that CzcD and MntE are true paralogs, as CzcD transports zinc, while MntE selectively transports manganese. Through the use of an extensive collection of pneumococcal variants, we show that a primary determinant for metal selectivity is the A site within the transmembrane domain. This extends our understanding of how CDFs discriminate among transition metals.

Dataset Information

Implications for Cation Selectivity and Evolution by a Novel Cation Diffusion Facilitator Family Member From the Moderate Halophile Planococcus dechangensis.

Publications

Implications for Cation Selectivity and Evolution by a Novel Cation Diffusion Facilitator Family Member From the Moderate Halophile <i>Planococcus dechangensis</i>.

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