Abstract
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 cell-specific 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.
Highlights
Cells have evolved mechanisms to regulate ion and pH homeostasis in order to respond to developmental cues and to adapt to a constantly changing environment
We first examined the evolutionary origin of plant cation–proton antiporters (CPA1 and CPA2) using Arabidopsis and rice as representatives of flowering plants
Our analysis shows that ancestral NhaP evolved and diverged to give two distinct types: Na+– H+ exchanger (NHX) and Na+/H+ antiporter (NHAP) (Figure 2)
Summary
Cells have evolved mechanisms to regulate ion and pH homeostasis in order to respond to developmental cues and to adapt to a constantly changing environment. In prokaryotes, this feat is accomplished with a diverse array of transporters at the plasma membrane. The purpose of this study is to understand the evolutionary relationship of NHX, KEA, and CHX homologs from algae to flowering plants, to use comparative biology to infer functions of uncharacterized plant genes (Chang et al, 2004), and hopefully reveal new model systems to determine functions of KEA and CHX genes which remain largely uncharacterized
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