Conserved and Diversified Gene Families of Monovalent Cation/H+ Antiporters from Algae to Flowering Plants

Chanroj, Salil; Wang, Guoying; Venema, Kees; Zhang, Muren Warren; Delwiche, Charles F.; Sze, Heven

doi:10.3389/fpls.2012.00025

Conserved and Diversified Gene Families of Monovalent Cation/H+ Antiporters from Algae to Flowering Plants

Journal Article · Sun Jan 01 00:00:00 EST 2012 · Frontiers in Plant Science

DOI:https://doi.org/10.3389/fpls.2012.00025· OSTI ID:1628221

Chanroj, Salil ^[1]; Wang, Guoying ^[2]; Venema, Kees ^[3]; Zhang, Muren Warren ^[2]; Delwiche, Charles F. ^[2]; Sze, Heven ^[2]

Univ. of Maryland, College Park, MD (United States). Maryland Agricultural Experiment Station. Dept. of Cell Biology and Molecular Genetics; DOE/OSTI
Univ. of Maryland, College Park, MD (United States). Maryland Agricultural Experiment Station. Dept. of Cell Biology and Molecular Genetics
Consejo Superior de Investigaciones Científicas, Granada (Spain). Estación Experimental del Zaidín. Biología Celular y Molecular de Plantas. Departmento de Bioquímica

All organisms have evolved strategies to regulate ion and pH homeostasis in response to developmental and environmental cues. One strategy is mediated by monovalent cation– proton antiporters (CPA) that are classified in two superfamilies. Many CPA1 genes from bacteria, fungi, metazoa, and plants have been functionally characterized; though roles of plant CPA2 genes encoding K+-efflux antiporter (KEA) and cation/H+ exchanger (CHX) families are largely unknown. Phylogenetic analysis showed that three clades of the CPA1 Na+–H+ exchanger (NHX) family have been conserved from single-celled algae to Arabidopsis. These are (i) plasma membrane-bound SOS1/AtNHX7 that share ancestry with prokaryote NhaP, (ii) endosomal AtNHX5/6 that is part of the eukaryote Intracellular-NHE clade, and (iii) a vacuolar NHX clade (AtNHX1–4) specific to plants. Early diversification of KEA genes possibly from an ancestral cyanobacterium gene is suggested by three types seen in all plants. Intriguingly, CHX genes diversified from three to four members in one subclade of early land plants to 28 genes in eight subclades of Arabidopsis. Homologs from Spirogyra or Physcomitrella share high similarity with AtCHX20, suggesting that guard cellspecific AtCHX20 and its closest relatives are founders of the family, and pollen-expressed CHX genes appeared later in monocots and early eudicots. AtCHX proteins mediate K+ transport and pH homeostasis, and have been localized to intracellular and plasma membrane.Thus KEA genes are conserved from green algae to angiosperms, and their presence in red algae and secondary endosymbionts suggest a role in plastids. In contrast, AtNHX1– 4 subtype evolved in plant cells to handle ion homeostasis of vacuoles. The great diversity of CHX genes in land plants compared to metazoa, fungi, or algae would imply a significant role of ion and pH homeostasis at dynamic endomembranes in the vegetative and reproductive success of flowering plants.

View Accepted Manuscript (DOE)

Research Organization:: Univ. of Maryland, College Park, MD (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Earth and Environmental Systems Science Division

Grant/Contract Number:: FG02-07ER15883

OSTI ID:: 1628221

Journal Information:: Frontiers in Plant Science, Journal Name: Frontiers in Plant Science Vol. 3; ISSN 1664-462X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Plastidial transporters KEA1, -2, and -3 are essential for chloroplast osmoregulation, integrity, and pH regulation in Arabidopsis Kunz, H. -H.; Gierth, M.; Herdean, A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 20 https://doi.org/10.1073/pnas.1323899111	journal	May 2014
Plant endosomal NHX antiporters: Activity and function Qiu, Quan-Sheng Plant Signaling & Behavior, Vol. 11, Issue 5 https://doi.org/10.1080/15592324.2016.1147643	journal	May 2016
Distinct Roles for SOS1 in the Convergent Evolution of Salt Tolerance in Eutrema salsugineum and Schrenkiella parvula Jarvis, David E.; Ryu, Choong-Hwan; Beilstein, Mark A. Molecular Biology and Evolution, Vol. 31, Issue 8 https://doi.org/10.1093/molbev/msu152	journal	May 2014
The Potassium Transporters HAK2 and HAK3 Localize to Endomembranes in Physcomitrella patens. HAK2 is Required in Some Stress Conditions Haro, Rosario; Fraile-Escanciano, Ana; González-Melendi, Pablo Plant and Cell Physiology, Vol. 54, Issue 9 https://doi.org/10.1093/pcp/pct097	journal	July 2013
Two Endosomal NHX-Type Na+/H+ Antiporters are Involved in Auxin-Mediated Development in Arabidopsis thaliana Dragwidge, Jonathan Michael; Ford, Brett Andrew; Ashnest, Joanne Rachel Plant and Cell Physiology, Vol. 59, Issue 8 https://doi.org/10.1093/pcp/pcy090	journal	May 2018
ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity Osakabe, Yuriko; Yamaguchi-Shinozaki, Kazuko; Shinozaki, Kazuo New Phytologist, Vol. 202, Issue 1 https://doi.org/10.1111/nph.12613	journal	November 2013
Biochemical pH clamp: the forgotten resource in membrane bioenergetics Wegner, Lars H.; Shabala, Sergey New Phytologist, Vol. 225, Issue 1 https://doi.org/10.1111/nph.16094	journal	August 2019
Increased salt tolerance with overexpression of cation/proton antiporter 1 genes: a meta-analysis Ma, Yuan-Chun; Augé, Robert M.; Dong, Chao Plant Biotechnology Journal, Vol. 15, Issue 2 https://doi.org/10.1111/pbi.12599	journal	September 2016
Two NHX-type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress Zeng, Yang; Li, Qing; Wang, Haiya Plant Biotechnology Journal, Vol. 16, Issue 1 https://doi.org/10.1111/pbi.12773	journal	September 2017
Na ⁺ ,K ⁺ /H ⁺ antiporters regulate the pH of endoplasmic reticulum and auxin-mediated development: NHX antiporters and auxin homeostasis Fan, Ligang; Zhao, Lei; Hu, Wei Plant, Cell & Environment, Vol. 41, Issue 4 https://doi.org/10.1111/pce.13153	journal	February 2018
Golgi-localized cation/proton exchangers regulate ionic homeostasis and skotomorphogenesis in Arabidopsis: Golgi-Localized KEAs Regulate Ionic Homeostasis Wang, Yuan; Tang, Ren-Jie; Yang, Xiyan Plant, Cell & Environment, Vol. 42, Issue 2 https://doi.org/10.1111/pce.13452	journal	November 2018
Potato transformation with the HvNHX3 gene and the improvement of transformant salt tolerance Krivosheeva, A. B.; Varlamova, T. V.; Yurieva, N. O. Russian Journal of Plant Physiology, Vol. 61, Issue 6 https://doi.org/10.1134/s1021443714060119	journal	October 2014
Seed size evolution and biogeography of Plukenetia (Euphorbiaceae), a pantropical genus with traditionally cultivated oilseed species Cardinal-McTeague, Warren M.; Wurdack, Kenneth J.; Sigel, Erin M. BMC Evolutionary Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12862-018-1308-9	journal	January 2019
OsNHX5-mediated pH homeostasis is required for post-Golgi trafficking of seed storage proteins in rice endosperm cells Zhu, Jianping; Ren, Yulong; Wang, Yunlong BMC Plant Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12870-019-1911-y	journal	July 2019
NHX-type Na ⁺ (K ⁺ )/H ⁺ antiporters are required for TGN/EE trafficking and endosomal ion homeostasis in Arabidopsis thaliana Dragwidge, Jonathan Michael; Scholl, Stefan; Schumacher, Karin Journal of Cell Science, Vol. 132, Issue 7 https://doi.org/10.1242/jcs.226472	journal	March 2019
A Novel AtKEA Gene Family, Homolog of Bacterial K+/H+ Antiporters, Plays Potential Roles in K+ Homeostasis and Osmotic Adjustment in Arabidopsis Zheng, Sheng; Pan, Ting; Fan, Ligang PLoS ONE, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pone.0081463	journal	November 2013
AtNHX5 and AtNHX6 Control Cellular K+ and pH Homeostasis in Arabidopsis: Three Conserved Acidic Residues Are Essential for K+ Transport Wang, Liguang; Wu, Xuexia; Liu, Yafen PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0144716	journal	December 2015
Genome-Wide Identification and Analysis of Arabidopsis Sodium Proton Antiporter (NHX) and Human Sodium Proton Exchanger (NHE) Homologs in Sorghum bicolor Hima Kumari, P.; Anil Kumar, S.; Ramesh, Katam Genes, Vol. 9, Issue 5 https://doi.org/10.3390/genes9050236	journal	May 2018
New Insights into the Structure-Function Relationship of the Endosomal-Type Na+, K+/H+ Antiporter NHX6 from Mulberry (Morus notabilis) Cao, Boning; Xia, Zhongqiang; Liu, Changying International Journal of Molecular Sciences, Vol. 21, Issue 2 https://doi.org/10.3390/ijms21020428	journal	January 2020

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