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Review
. 2008 Apr;66(6):565-85.
doi: 10.1007/s11103-007-9287-z. Epub 2008 Feb 22.

Comparative molecular biological analysis of membrane transport genes in organisms

Toshifumi Nagata  1 , Shigemi Iizumi, Kouji Satoh, Shoshi Kikuchi
Affiliations
Review

Comparative molecular biological analysis of membrane transport genes in organisms

Toshifumi Nagata et al. Plant Mol Biol. 2008 Apr.

Abstract

Comparative analyses of membrane transport genes revealed many differences in the features of transport homeostasis in eight diverse organisms, ranging from bacteria to animals and plants. In bacteria, membrane-transport systems depend mainly on single genes encoding proteins involved in an ATP-dependent pump and secondary transport proteins that use H(+) as a co-transport molecule. Animals are especially divergent in their channel genes, and plants have larger numbers of P-type ATPase and secondary active transporters than do other organisms. The secondary transporter genes have diverged evolutionarily in both animals and plants for different co-transporter molecules. Animals use Na(+) ions for the formation of concentration gradients across plasma membranes, dependent on secondary active transporters and on membrane voltages that in turn are dependent on ion transport regulation systems. Plants use H(+) ions pooled in vacuoles and the apoplast to transport various substances; these proton gradients are also dependent on secondary active transporters. We also compared the numbers of membrane transporter genes in Arabidopsis and rice. Although many transporter genes are similar in these plants, Arabidopsis has a more diverse array of genes for multi-efflux transport and for response to stress signals, and rice has more secondary transporter genes for carbohydrate and nutrient transport.

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Figures

Fig. 1
Fig. 1
Numbers of membrane transporter proteins of each class. Membrane transporter proteins were categorized into three classes (ATP-dependent [pump], channel, and secondary transporter) and compared among Escherichia coli K12-MG1655, Arabidopsis thaliana, Oryza sativa, Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens NCBI, Neurospora crassa 74-OR23-IVA, and Saccharomyces cerevisiae S228C
Fig. 2
Fig. 2
Comparison of numbers of pump genes among various organisms. Pump gene numbers were compared among Escherichia coli K12-MG1655, Arabidopsis thaliana, Oryza sativa, Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens NCBI, Neurospora crassa 74-OR23-IVA, and Saccharomyces cerevisiae S228C. ABC: ATP-binding Cassette; ArsAB: Arsenite-antimonite Efflux; F-ATPase: H+ or Na+-translocating F-type, V-type and A-type ATPase; H+-Ppase: H+-translocating Pyrophosphatase; IISP: General Secretory Pathway (Sec); MPT: Mitochondrial Protein Translocase; P-ATPase: P-type ATPase
Fig. 3
Fig. 3
Comparison of numbers of channel genes among various organisms. Channel gene numbers were compared among many organisms (E. coli K12-MG1655, A. thaliana, O. sativa, C. elegans, D. melanogaster, H. sapiens NCBI, N. crassa 74-OR23-IVA, and S. cerevisiae S228C). ACC: ATP-gated Cation Channel; Bcl-2: Bcl-2; Bestrophin: Anion Channel-forming Bestrophin; CD20: CD20 Ca2+ Channel; ClC: Chloride Channel; Connexin: Gap Junction-forming Connexin; CytB: gp91phox Phagocyte NADPH Oxidase-associated Cytochrome b558 (CytB) H+-channel; E-ClC: Epithelial Chloride Channel; EnaC: Epithelial Na+ Channel; GIC: Glutamate-gated Ion Channel; Hsp70: Cation Channel-forming Heat Shock Protein-70; ICC: Intracellular Chloride Channel; Icln: Nucleotide-sensitive Anion-selective Channel; Innexin: Gap Junction-forming Innexin; IRK-C: Inward Rectifier K+ Channel; LIC: Ligand-gated Ion Channel of Neurotransmitter Receptors; Mid1: Yeast Stretch-Activated, Cation-Selective Ca2+ Channel Mid1; MIP: Major Intrinsic Protein; MIT: CorA Metal Ion Transporter; MscL: Large Conductance Mechanosensitive Ion Channel; MscS: Small Conductance Mechanosensitive Ion Channel; NSCC2: Non-selective Cation Channel-2; O-ClC: Organellar Chloride Channel; PCC: Polycystin Cation Channel; PLM: Phospholemman; RIR-CaC; Ryanodine-Inositol 1,4,5-triphosphate Receptor Ca2+ Channel; Tic110: Chloroplast Envelope Anion Channel-forming Tic110; TRP-CC: Transient Receptor Potential Ca2+ Channel; UT: Urea Transporter; VIC: Voltage-gated Ion Channel
Fig. 4
Fig. 4
Comparison of numbers of secondary transport genes among organisms. Secondary transporter gene numbers were compared among Escherichia coli K12-MG1655, Arabidopsis thaliana, Oryza sativa, Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens NCBI, Neurospora crassa 74-OR23-IVA, and Saccharomyces cerevisiae S228C. AAAP: Amino Acid/Auxin Permease; AE: Anion Exchanger; AEC: Auxin Efflux Carrier; Amt: Ammonium or Ammonia Transporter; APC: Amino Acid-Polyamine-Organocation; BASS: Bile Acid:Na+ Symporter; BCCT: Betaine/Carnitine/Choline Transporter; BenE: Benzoate:H+ Symporter; CaCA: Ca2+:Cation Antiporter; CCC: Cation-Chloride Cotransporter; CDF: Cation Diffusion Facilitator; CNT: Concentrative Nucleoside Transporter; CPA1: Monovalent Cation:Proton Antiporter-1; CPA2: Monovalent Cation:Proton Antiporter-2; DAACS: Dicarboxylate/Amino Acid:Cation (Na+ or H+) Symporter; DASS: Divalent Anion:Na+ Symporter; DcuC: C4-dicarboxylate Uptake C; DMT: Drug/Metabolite Transporter; ENT: Equilibrative Nucleoside Transporter; FBT: Folate-Biopterin Transporter; GntP: Gluconate:H+ Symporter; GPH: Glycoside-Pentoside-Hexuronide (GPH):Cation Symporter; HAAAP: Hydroxy/Aromatic Amino Acid Permease; KUP: K+ Uptake Permease; LCT: Lysosomal Cystine Transporter; MC: Mitochondrial Carrier; MET: 4 TMS Multidrug Endosomal Transporter; MFS: Major Facilitator Superfamily; MOP: Multidrug/Oligosaccharidyl-lipid/Polysaccharide Flippase Superfamily; NCS2: Nucleobase:Cation Symporter-2; Nramp: Metal Ion (Mn2+–iron) Transporter; NSS: Neurotransmitter:Sodium Symporter; OAT: Organo Anion Transporter; OPT: Oligopeptide Transporter; PnaS: Phosphate:Na+ Symporter; POT: Proton-dependent Oligopeptide Transporter; RFC: Reduced Folate Carrier; RhtB: Resistance to Homoserine/Threonine; RND: Resistance-Nodulation-Cell Division; SSS: Solute:Sodium Symporter; SulP: Sulfate Permease; TDT: Tellurite-resistance/Dicarboxylate Transporter; Trk: K+ Transporter; ZIP: Zinc (Zn2+)–Iron (Fe2+) Permease
Fig. 5
Fig. 5
Comparison of co-transport molecules of secondary active transporters among various organisms. Numbers of co-transport molecules of secondary active transporters were compared among Escherichia coli K12-MG1655, Arabidopsis thaliana, Oryza sativa, Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens NCBI, Neurospora crassa 74-OR23-IVA, and Saccharomyces cerevisiae S228C
Fig. 6
Fig. 6
Comparison of membrane transport genes in Arabidopsis and rice. Numbers of the membrane transporter gene families are compared in Arabidopsis and rice. ABC: ATP-binding Cassette; P-ATPase: P-type ATPase; CytB: gp91phox Phagocyte NADPH Oxidase-associated Cytochrome b558 (CytB) H+-channel; GIC: Glutamate-gated Ion Channel; MIP: Major Intrinsic Protein; VIC: Voltage-gated Ion Channel; AAAP: Amino Acid/Auxin Permease; Amt: Ammonium or Ammonia Transporter; CaCA: Ca2+:Cation Antiporter; CPA2: Monovalent Cation:Proton Antiporter-2; DMT: Drug/Metabolite Transporter; KUP: K+ Uptake Permease; MFS: Major Facilitator Superfamily; MOP: Multidrug/Oligosaccharidyl-lipid/Polysaccharide Flippase Superfamily; NCS2: Nucleobase:Cation Symporter-2; OPT: Oligopeptide Transporter; POT: Proton-dependent Oligopeptide Transporter; SulP: Sulfate Permease; ZIP: Zinc (Zn2+)–Iron (Fe2+) Permease; PUP: Peptide Uptake or Activated Fatty Acid Export Permease
Fig. 7
Fig. 7
Summaries of comparison of membrane transport genes in bacteria, animals, and plants. Bacteria-specific genes = blue; animal-specific genes = red; plant-specific genes = green; bacteria- and animal-specific genes = purple; bacteria- and plant-specific genes = brown; genes with divergent numbers in organisms = yellow. ABC: ATP-binding Cassette; ArsAB: Arsenite-Antimonite Efflux; F-ATPase: H+or Na+-translocating F-type, V-type and A-type ATPase; H+-Ppase: H+-translocating Pyrophosphatase; IISP: General Secretory Pathway (Sec); MPT: Mitochondrial Protein Translocase; P-ATPase: P-type ATPase; ACC: ATP-gated Cation Channel; Annexin: Annexin; Bcl-2: Bcl-2; Bestrophin: Anion Channel-forming Bestrophin; CD20: CD20 Ca2+ Channel; ClC: Chloride Channel; Connexin: Gap Junction-forming Connexin; CSC: Chloroplast Outer Envelope Solute Channel; CytB: gp91phox Phagocyte NADPH Oxidase-associated Cytochrome b558 (CytB) H+-channel; E-ClC: Epithelial Chloride Channel; EnaC: Epithelial Na+ Channel; GIC: Glutamate-gated Ion Channel; Hsp70: Cation Channel-forming Heat Shock Protein-70; ICC: Intracellular Chloride Channel; Ic ln: Nucleotide-sensitive Anion-selective Channel; Innexin: Gap Junction-forming Innexin; IRK-C: Inward Rectifier K+ Channel; LIC: Ligand-gated Ion Channel of Neurotransmitter Receptors; Mid1: Yeast Stretch-Activated, Cation-Selective Ca2+ Channel Mid1; MIP: Major Intrinsic Protein; MIT: CorA Metal Ion Transporter; MscL: Large Conductance Mechanosensitive Ion Channel; MscS: Small Conductance Mechanosensitive Ion Channel; NSCC2: Non-selective Cation Channel-2; O-ClC: Organellar Chloride Channel; PCC: Polycystin Cation Channel; PLM: Phospholemman; RIR-CaC; Ryanodine-Inositol 1,4,5-triphosphate Receptor Ca2+ Channel; Tic110: Chloroplast Envelope Anion Channel-forming Tic110; TRP-CC: Transient Receptor Potential Ca2+ Channel; UT: Urea Transporter; VIC: Voltage-gated Ion Channel; AAA: ATP:ADP Antiporter; AAAP: Amino Acid/Auxin Permease; AAE: Aspartate:Alanine Exchanger; AbgT: p-Aminobenzoyl-glutamate Transporter; ACR3: Arsenical Resistance-3; AE: Anion Exchanger; AEC: Auxin Efflux Carrier; AGCS: Alanine or Glycine:Cation Symporter; Amt: Ammonium or Ammonia Transporter; APC: Amino Acid-Polyamine-Organocation; ArsB: Arsenite-Antimonite (ArsB) Efflux; BASS: Bile Acid:Na+ Symporter; BCCT: Betaine/Carnitine/Choline Transporter; BenE: Benzoate:H+ Symporter; CaCA: Ca2+:Cation Antiporter; CCC: Cation-Chloride Cotransporter; CDF: Cation Diffusion Facilitator; CHR: Chromate Ion Transporter; CNT: Concentrative Nucleoside Transporter; CPA1: Monovalent Cation:Proton Antiporter-1; CPA2: Monovalent Cation:Proton Antiporter-2; DAACS: Dicarboxylate/Amino Acid:Cation (Na+ or H+) Symporter; DASS: Divalent Anion:Na+ Symporter; Dcu: C4-Dicarboxylate Uptake; DcuC: C4-dicarboxylate Uptake C; DMT: Drug/Metabolite Transporter; ENT: Equilibrative Nucleoside Transporter; ESS: Glutamate:Na+ Symporter; FBT: Folate-Biopterin Transporter; FNT: Formate-Nitrite Transporter; GntP: Gluconate:H+ Symporter; GPH: Glycoside-Pentoside-Hexuronide (GPH):Cation Symporter; GUP: Glycerol Uptake; HAAAP: Hydroxy/Aromatic Amino Acid Permease; KDGT: 2-Keto-3-Deoxygluconate Transporter; KUP: K+ Uptake Permease; LCT: Lysosomal Cystine Transporter; LctP: Lactate Permease; LIV-E: Branched Chain Amino Acid Exporter; LIVCS: Branched Chain Amino Acid:Cation Symporter; LysE: L-Lysine Exporter; MC: Mitochondrial Carrier; MET: 4 TMS Multidrug Endosomal Transporter; MFS: Major Facilitator Superfamily; MOP: Multidrug/Oligosaccharidyl-lipid/Polysaccharide Flippase Superfamily; MTC: Mitochondrial Tricarboxylate Carrier; NCS1: Nucleobase:Cation Symporter-1; NCS2: Nucleobase:Cation Symporter-2; NhaA: Na+:H+ Antiporter A; NhaB: Na+:H+ Antiporter B; NhaD: Na+:H+ Antiporter D; NiCoT: Ni2+–Co2+ Transporter; Nramp: Metal Ion (Mn2+–iron) Transporter; NSS: Neurotransmitter:Sodium Symporter; OAT: Organo Anion Transporter; OPT: Oligopeptide Transporter; OST: Organic Solute Transporter; Oxa1: Cytochrome Oxidase Biogenesis; PiT: Inorganic Phosphate Transporter; PnaS: Phosphate:Na+ Symporter; POT: Proton-dependent Oligopeptide Transporter; RFC: Reduced Folate Carrier; RhtB: Resistance to Homoserine/Threonine; RND: Resistance-Nodulation-Cell Division; SSS: Solute:Sodium Symporter; SulP: Sulfate Permease; Tat: Twin Arginine Targeting; TDT: Tellurite-resistance/Dicarboxylate Transporter; ThrE: Threonine/Serine Exporter; TRAP-T: Tripartite ATP-independent Periplasmic Transporter; Trk: K+ Transporter; ZIP: Zinc (Zn2+)–Iron (Fe2+) Permease; GPTS: general carbohydrate phosphotransferase; SSPTS: sugar specific phosphotransferase; Ctr1: Dipicolinic Acid Transporter; Ctr2: Copper Transporter; FeoB: Ferrous Iron Uptake; FeT: Low Affinity Fe2+ Transporter; FP: Ferroportin; LPI: Lysosomal Protein Import; OfeT: Iron/Lead Transporter; PnuC: nicotinamide mononucleotide(NMN) uptake permease; PPI: Peroxisomal Protein Importer; PUP: Peptide Uptake or Activated Fatty Acid Export Permease
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