Protein Phylogenetic Analysis of Ca2+/cation Antiporters and Insights into their Evolution in Plants

Abstract

Cation transport is a critical process in all organisms and is essential for mineral nutrition, ion stress tolerance, and signal transduction. Transporters that are members of the Ca2+/cation antiporter (CaCA) superfamily are involved in the transport of Ca2+ and/or other cations using the counter exchange of another ion such as H+ or Na+. The CaCA superfamily has been previously divided into five transporter families: the YRBG, Na+/Ca2+ exchanger (NCX), Na+/Ca2+, K+ exchanger (NCKX), H+/cation exchanger (CAX), and cation/Ca2+ exchanger (CCX) families, which include the well-characterized NCX and CAX transporters. To examine the evolution of CaCA transporters within higher plants and the green plant lineage, CaCA genes were identified from the genomes of sequenced flowering plants, a bryophyte, lycophyte, and freshwater and marine algae, and compared with those from non-plant species. We found evidence of the expansion and increased diversity of flowering plant genes within the CAX and CCX families. Genes related to the NCX family are present in land plant though they encode distinct MHX homologs which probably have an altered transport function. In contrast, the NCX and NCKX genes which are absent in land plants have been retained in many species of algae, especially the marine algae, indicating that these organisms may share “animal-like” characteristics of Ca2+ homeostasis and signaling. A group of genes encoding novel CAX-like proteins containing an EF-hand domain were identified from plants and selected algae but appeared to be lacking in any other species. Lack of functional data for most of the CaCA proteins make it impossible to reliably predict substrate specificity and function for many of the groups or individual proteins. The abundance and diversity of CaCA genes throughout all branches of life indicates the importance of this class of cation transporter, and that many transporters with novel functions are waiting to be discovered.

CAX‐ing a wide net: Cation/H+ transporters in metal remediation and abiotic stress signalling

“…2006; Emery et al . 2012). CAXs have also been found in some invertebrates and vertebrates, but absent in virtually all mammals.…”

“…CAXs are found in many algae, particularly within green algae, and within early land plants such as the lycophyte spikemoss Selaginella moellendorffii and the bryophyte moss Physcomitrella patens (Emery et al . 2012). Two or more CAX genes are seen within some of these photosynthetic organisms, but it is within the higher land plants that CAX genes are present as larger multi‐gene families.…”

“…On average 5–6 CAX genes per species are found in monocots and dicots, and some species like soybean ( Glycine max ) have 14 CAXs (Emery et al . 2012; Pittman & Hirschi 2016). It is still not fully clear whether this expansion in gene family number has led to CAX functional diversity.…”

“…The schematic phylogenetic tree was derived from an analysis of 120 CAX genes and 34 NCL genes from plant, algal, fungal, protist, animal and prokaryotic sequences of Emery et al . (2012). The Type 1A‐H and Type 2 CAX sub‐groups are indicated using the definitions as described in Shigaki et al .…”

“…It is unclear whether CAXs are essential for the function and Ca 2+ loading of acidic organelles in other species but they are not involved in this process in higher mammals, including humans, as CAX genes were apparently lost in the higher mammalian lineage (Emery et al . 2012; Melchionda et al . 2016).…”