Evolution of Electrogenic Ammonium Transporters (AMTs)
Abstract
The ammonium transporter gene family consists of three main clades, AMT, MEP, and Rh. The evolutionary history of the AMT/MEP/Rh gene family is characterized by multiple horizontal gene transfer events, gene family expansion and contraction, and gene loss; thus the gene tree for this family of transporters is unlike the organismal tree. The genomes of angiosperms contain genes for both electrogenic and electroneutral ammonium transporters, but it is not clear how far back in the land plant lineage electrogenic ammonium transporters occur. Here, we place Marchantia polymorpha ammonium transporters in the AMT/MEP/Rh phylogeny and we show that AMTs from the liverwort M. polymorpha are electrogenic. This information suggests that electrogenic ammonium transport evolved at least as early as the divergence of bryophytes in the land plant lineage.
- Authors:
-
- St. Catherine Univ., St.Paul, MN (United States). Biology Dept.
- Univ. of Minnesota, St. Paul, MN (United States). Dept. of Plant Biology
- Publication Date:
- Research Org.:
- St. Catherine Univ., St.Paul, MN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1393413
- Grant/Contract Number:
- FG02-10ER15886; FG02-07ER15886
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 7; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; ammonium transporters; electrophysiology; Marchantia polymorpha; phylogeny; electrogenicity
Citation Formats
McDonald, Tami R., and Ward, John M. Evolution of Electrogenic Ammonium Transporters (AMTs). United States: N. p., 2016.
Web. doi:10.3389/fpls.2016.00352.
McDonald, Tami R., & Ward, John M. Evolution of Electrogenic Ammonium Transporters (AMTs). United States. https://doi.org/10.3389/fpls.2016.00352
McDonald, Tami R., and Ward, John M. Thu .
"Evolution of Electrogenic Ammonium Transporters (AMTs)". United States. https://doi.org/10.3389/fpls.2016.00352. https://www.osti.gov/servlets/purl/1393413.
@article{osti_1393413,
title = {Evolution of Electrogenic Ammonium Transporters (AMTs)},
author = {McDonald, Tami R. and Ward, John M.},
abstractNote = {The ammonium transporter gene family consists of three main clades, AMT, MEP, and Rh. The evolutionary history of the AMT/MEP/Rh gene family is characterized by multiple horizontal gene transfer events, gene family expansion and contraction, and gene loss; thus the gene tree for this family of transporters is unlike the organismal tree. The genomes of angiosperms contain genes for both electrogenic and electroneutral ammonium transporters, but it is not clear how far back in the land plant lineage electrogenic ammonium transporters occur. Here, we place Marchantia polymorpha ammonium transporters in the AMT/MEP/Rh phylogeny and we show that AMTs from the liverwort M. polymorpha are electrogenic. This information suggests that electrogenic ammonium transport evolved at least as early as the divergence of bryophytes in the land plant lineage.},
doi = {10.3389/fpls.2016.00352},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Thu Mar 31 00:00:00 EDT 2016},
month = {Thu Mar 31 00:00:00 EDT 2016}
}
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Works referenced in this record:
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014
- Stamatakis, Alexandros
- Bioinformatics, Vol. 30, Issue 9
Different Transport Mechanisms in Plant and Human AMT/Rh-type Ammonium Transporters
journal, January 2006
- Mayer, Maria; Schaaf, Gabriel; Mouro, Isabelle
- Journal of General Physiology, Vol. 127, Issue 2
Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels
journal, March 2006
- Kustu, S.; Inwood, W.
- Transfusion Clinique et Biologique, Vol. 13, Issue 1-2
Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus
journal, October 2005
- Andrade, S. L. A.; Dickmanns, A.; Ficner, R.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 42
An Improved General Amino Acid Replacement Matrix
journal, April 2008
- Le, S. Q.; Gascuel, O.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Multiple Horizontal Gene Transfers of Ammonium Transporters/Ammonia Permeases from Prokaryotes to Eukaryotes: Toward a New Functional and Evolutionary Classification
journal, June 2011
- McDonald, T. R.; Dietrich, F. S.; Lutzoni, F.
- Molecular Biology and Evolution, Vol. 29, Issue 1
Arabidopsis Sucrose Transporter AtSUC9. High-Affinity Transport Activity, Intragenic Control of Expression, and Early Flowering Mutant Phenotype
journal, November 2006
- Sivitz, Alicia B.; Reinders, Anke; Johnson, Meghan E.
- Plant Physiology, Vol. 143, Issue 1
Amt/MEP/Rh proteins conduct ammonia
journal, November 2005
- Winkler, Fritz K.
- Pflügers Archiv - European Journal of Physiology, Vol. 451, Issue 6
Structural and mechanistic aspects of Amt/Rh proteins
journal, June 2007
- Javelle, Arnaud; Lupo, Domenico; Li, Xiao-Dan
- Journal of Structural Biology, Vol. 158, Issue 3
Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks
journal, September 2012
- Huson, Daniel H.; Scornavacca, Celine
- Systematic Biology, Vol. 61, Issue 6
Creating the CIPRES Science Gateway for inference of large phylogenetic trees
conference, November 2010
- Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri
- 2010 Gateway Computing Environments Workshop (GCE)
Electroneutral ammonium transport by basolateral rhesus B glycoprotein: Ammonium transport by rhesus B glycoprotein
journal, September 2004
- Ludewig, Uwe
- The Journal of Physiology, Vol. 559, Issue 3
Ammonia acquisition in enteric bacteria: Physiological role of the ammonium/methylammonium transport B (AmtB) protein
journal, June 1998
- Soupene, E.; He, L.; Yan, D.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
The rice OsAMT1;1 is a proton-independent feedback regulated ammonium transporter
journal, November 2014
- Yang, Shunying; Hao, Dongli; Cong, Yu
- Plant Cell Reports, Vol. 34, Issue 2
The 1.3-A resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins
journal, November 2007
- Lupo, D.; Li, X. -D.; Durand, A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
jModelTest: Phylogenetic Model Averaging
journal, April 2008
- Posada, D.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Construction of male and female PAC genomic libraries suitable for identification of Y-chromosome-specific clones from the liverwort, Marchantia polymorpha: Male and female PAC libraries of Marchantia
journal, November 2000
- Okada, Sachiko; Fujisawa, Masaki; Sone, Takefumi
- The Plant Journal, Vol. 24, Issue 3
The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli
journal, November 2004
- Zheng, L.; Kostrewa, D.; Berneche, S.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 49
Structure of the Nitrosomonas europaea Rh protein
journal, November 2007
- Li, X.; Jayachandran, S.; Nguyen, H. -H. T.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
Uniport of NH by the Root Hair Plasma Membrane Ammonium Transporter LeAMT1;1
journal, January 2002
- Ludewig, Uwe; von Wirén, Nico; Frommer, Wolf B.
- Journal of Biological Chemistry, Vol. 277, Issue 16
Characterization of Arabidopsis AtAMT2, a novel ammonium transporter in plants
journal, February 2000
- Sohlenkamp, Christian; Shelden, Megan; Howitt, Susan
- FEBS Letters, Vol. 467, Issue 2-3
Antennal-Expressed Ammonium Transporters in the Malaria Vector Mosquito Anopheles gambiae
journal, October 2014
- Pitts, R. Jason; Derryberry, Stephen L.; Pulous, Fadi E.
- PLoS ONE, Vol. 9, Issue 10
Function of human Rh based on structure of RhCG at 2.1 A
journal, May 2010
- Gruswitz, F.; Chaudhary, S.; Ho, J. D.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
ProtTest: selection of best-fit models of protein evolution
journal, January 2005
- Abascal, F.; Zardoya, R.; Posada, D.
- Bioinformatics, Vol. 21, Issue 9
Mechanism of Ammonia Transport by Amt/MEP/Rh: Structure of AmtB at 1.35 A
journal, September 2004
- Khademi, S.
- Science, Vol. 305, Issue 5690
Evolutionary conservation and diversification of Rh family genes and proteins
journal, October 2005
- Huang, C. -H.; Peng, J.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 43
Channel-like NH 3 flux by ammonium transporter AtAMT2
journal, July 2009
- Neuhäuser, Benjamin; Dynowski, Marek; Ludewig, Uwe
- FEBS Letters, Vol. 583, Issue 17
Switching substrate specificity of AMT/MEP/ Rh proteins
journal, October 2014
- Neuhäuser, Benjamin; Dynowski, Marek; Ludewig, Uwe
- Channels, Vol. 8, Issue 6
The Dionaea muscipula Ammonium Channel DmAMT1 Provides NH4+ Uptake Associated with Venus Flytrap’s Prey Digestion
journal, September 2013
- Scherzer, Sönke; Krol, Elzbieta; Kreuzer, Ines
- Current Biology, Vol. 23, Issue 17
Transport Activity of Rice Sucrose Transporters OsSUT1 and OsSUT5
journal, December 2009
- Sun, Y.; Reinders, A.; LaFleur, K. R.
- Plant and Cell Physiology, Vol. 51, Issue 1
Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae.
journal, August 1994
- Marini, A. M.; Vissers, S.; Urrestarazu, A.
- The EMBO Journal, Vol. 13, Issue 15
Identification of a high affinity NH4+ transporter from plants.
journal, August 1994
- Ninnemann, O.; Jauniaux, J. C.; Frommer, W. B.
- The EMBO Journal, Vol. 13, Issue 15
Identification of a high affinity NH4+ transporter from plants.
journal, August 1994
- Ninnemann, O.; Jauniaux, J. C.; Frommer, W. B.
- The EMBO Journal, Vol. 13, Issue 15
The rice OsAMT1;1 is a proton-independent feedback regulated ammonium transporter
journal, November 2014
- Yang, Shunying; Hao, Dongli; Cong, Yu
- Plant Cell Reports, Vol. 34, Issue 2
Amt/MEP/Rh proteins conduct ammonia
journal, November 2005
- Winkler, Fritz K.
- Pflügers Archiv - European Journal of Physiology, Vol. 451, Issue 6
The Dionaea muscipula Ammonium Channel DmAMT1 Provides NH4+ Uptake Associated with Venus Flytrap’s Prey Digestion
journal, September 2013
- Scherzer, Sönke; Krol, Elzbieta; Kreuzer, Ines
- Current Biology, Vol. 23, Issue 17
Channel-like NH 3 flux by ammonium transporter AtAMT2
journal, July 2009
- Neuhäuser, Benjamin; Dynowski, Marek; Ludewig, Uwe
- FEBS Letters, Vol. 583, Issue 17
Structural and mechanistic aspects of Amt/Rh proteins
journal, June 2007
- Javelle, Arnaud; Lupo, Domenico; Li, Xiao-Dan
- Journal of Structural Biology, Vol. 158, Issue 3
Biological gas channels for NH3 and CO2: evidence that Rh (Rhesus) proteins are CO2 channels
journal, March 2006
- Kustu, S.; Inwood, W.
- Transfusion Clinique et Biologique, Vol. 13, Issue 1-2
The Rh (Rhesus) blood group polypeptides are related to NH4+ transporters
journal, December 1997
- Marini, Anne-Marie; Urrestarazu, Antonio; Beauwens, Renaud
- Trends in Biochemical Sciences, Vol. 22, Issue 12
Mating pair stabilization mediates bacterial conjugation species specificity
journal, June 2022
- Low, Wen Wen; Wong, Joshua L. C.; Beltran, Leticia C.
- Nature Microbiology, Vol. 7, Issue 7
Ammonium ion transport by the AMT/Rh homologue LeAMT1;1
journal, May 2006
- Mayer, Maria; Dynowski, Marek; Ludewig, Uwe
- Biochemical Journal, Vol. 396, Issue 3
Construction of male and female PAC genomic libraries suitable for identification of Y-chromosome-specific clones from the liverwort, Marchantia polymorpha: Male and female PAC libraries of Marchantia
journal, November 2000
- Okada, Sachiko; Fujisawa, Masaki; Sone, Takefumi
- The Plant Journal, Vol. 24, Issue 3
The 1.3-A resolution structure of Nitrosomonas europaea Rh50 and mechanistic implications for NH3 transport by Rhesus family proteins
journal, November 2007
- Lupo, D.; Li, X. -D.; Durand, A.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
Structure of the Nitrosomonas europaea Rh protein
journal, November 2007
- Li, X.; Jayachandran, S.; Nguyen, H. -H. T.
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 49
Function of human Rh based on structure of RhCG at 2.1 A
journal, May 2010
- Gruswitz, F.; Chaudhary, S.; Ho, J. D.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 21
Ammonia acquisition in enteric bacteria: Physiological role of the ammonium/methylammonium transport B (AmtB) protein
journal, June 1998
- Soupene, E.; He, L.; Yan, D.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 12
Uncoupling of Ionic Currents from Substrate Transport in the Plant Ammonium Transporter At AMT1;2
journal, March 2014
- Neuhäuser, Benjamin; Ludewig, Uwe
- Journal of Biological Chemistry, Vol. 289, Issue 17
Pv AMT1;1, a Highly Selective Ammonium Transporter That Functions as H + /NH 4 + Symporter
journal, July 2011
- Ortiz-Ramirez, Carlos; Mora, Silvia I.; Trejo, Jorge
- Journal of Biological Chemistry, Vol. 286, Issue 36
Different Transport Mechanisms in Plant and Human AMT/Rh-type Ammonium Transporters
journal, January 2006
- Mayer, Maria; Schaaf, Gabriel; Mouro, Isabelle
- Journal of General Physiology, Vol. 127, Issue 2
ProtTest: selection of best-fit models of protein evolution
journal, January 2005
- Abascal, F.; Zardoya, R.; Posada, D.
- Bioinformatics, Vol. 21, Issue 9
jModelTest: Phylogenetic Model Averaging
journal, April 2008
- Posada, D.
- Molecular Biology and Evolution, Vol. 25, Issue 7
Multiple Horizontal Gene Transfers of Ammonium Transporters/Ammonia Permeases from Prokaryotes to Eukaryotes: Toward a New Functional and Evolutionary Classification
journal, June 2011
- McDonald, T. R.; Dietrich, F. S.; Lutzoni, F.
- Molecular Biology and Evolution, Vol. 29, Issue 1
Transport Activity of Rice Sucrose Transporters OsSUT1 and OsSUT5
journal, December 2009
- Sun, Y.; Reinders, A.; LaFleur, K. R.
- Plant and Cell Physiology, Vol. 51, Issue 1
Mechanism of Ammonia Transport by Amt/MEP/Rh: Structure of AmtB at 1.35 A
journal, September 2004
- Khademi, S.
- Science, Vol. 305, Issue 5690
Switching substrate specificity of AMT/MEP/ Rh proteins
journal, October 2014
- Neuhäuser, Benjamin; Dynowski, Marek; Ludewig, Uwe
- Channels, Vol. 8, Issue 6
Works referencing / citing this record:
Isolation and characterization of a high-affinity ammonium transporter ApAMT1;1 in alligatorweed
journal, September 2019
- Guo, Xiaotong; Sheng, Yuting; Yang, Shunying
- Plant Growth Regulation, Vol. 89, Issue 3
A two-lane mechanism for selective biological ammonium transport
journal, November 2019
- Williamson, Gordon; Tamburrino, Giulia; Mirandela, Gaëtan Dias
- Access Microbiology
Nitrogen isotope signature evidences ammonium deprotonation as a common transport mechanism for the AMT-Mep-Rh protein superfamily
journal, September 2018
- Ariz, Idoia; Boeckstaens, Mélanie; Gouveia, Catarina
- Science Advances, Vol. 4, Issue 9
Ammonia excretion in aquatic invertebrates: new insights and questions
journal, January 2018
- Weihrauch, Dirk; Joseph, Garett; Allen, Patrick
- The Journal of Experimental Biology, Vol. 221, Issue 2
Understanding transport processes in lichen, Azolla–cyanobacteria, ectomycorrhiza, endomycorrhiza, and rhizobia–legume symbiotic interactions
journal, January 2020
- Roy, Rahul; Reinders, Anke; Ward, John M.
- F1000Research, Vol. 9
Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer
journal, March 2017
- Brouwer, Paul; Bräutigam, Andrea; Buijs, Valerie A.
- Frontiers in Plant Science, Vol. 8
A two-lane mechanism for selective biological ammonium transport
journal, July 2020
- Williamson, Gordon; Tamburrino, Giulia; Bizior, Adriana
- eLife, Vol. 9
Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer
text, January 2017
- Brouwer, Paul; Bräutigam, Andrea; Buijs, Valerie A.
- RWTH Aachen University
A two-lane mechanism for selective biological ammonium transport
journal, July 2020
- Williamson, Gordon; Dias Mirandela, Gaetan; Tamburrino, Giulia
- Access Microbiology, Vol. 2, Issue 7A
Nitrogen isotope signature evidences ammonium deprotonation as a common transport mechanism for the AMT-Mep-Rh protein superfamily
journal, September 2018
- Ariz, Idoia; Boeckstaens, Mélanie; Gouveia, Catarina
- Science Advances, Vol. 4, Issue 9
Metabolic Adaptation, a Specialized Leaf Organ Structure and Vascular Responses to Diurnal N2 Fixation by Nostoc azollae Sustain the Astonishing Productivity of Azolla Ferns without Nitrogen Fertilizer
text, January 2017
- Brouwer, Paul; Bräutigam, Andrea; Buijs, Valerie A.
- RWTH Aachen University