Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium‐based signalling

Abstract

SummaryMuch of our current knowledge on the mechanisms by which Ca 2+ signals are generated in photosynthetic eukaryotes comes from studies of a relatively small number of model species, particularly green plants and algae, revealing some common features and notable differences between 'plant' and 'animal' systems. Physiological studies from a broad range of algal cell types have revealed the occurrence of animal-like signalling properties, including fast action potentials and fast propagating cytosolic Ca 2+ waves. Genomic studies are beginning to reveal the widespread occurrence of conserved channel types likely to be involved in Ca 2+ signalling. However, certain widespread 'ancient' channel types appear to have been lost by certain groups, such as the embryophytes. More recent channel gene loss is also evident from comparisons of more closely related algal species. The underlying processes that have given rise to the current distributions of Ca 2+

Evolution of voltage-gated ion channels at the emergence of Metazoa

“…Na V s are thought to have evolved as a result of gene duplication and diversification of an ancestral Ca V , as the four domains of Na V s show higher sequence similarity to the corresponding domains of Ca V s than to each other and have in turn the lowest levels of similarity with K V s (Hille, 1989). Moreover, the fact that Ca V s have a wider phylogenetic distribution than Na V s supports this scenario as well (Verret et al, 2010) (see below). The discovery of bacterial sodium-selective channels (NaChBac) (Ren et al, 2001;Yue et al, 2002;Koishi et al, 2004) has somewhat blurred the evolutionary history of Ca V s and Na V s as NaChBac genes encode a single 6-TM domain that assembles into a tetramer (Durell and Guy, 2001;Ren et al, 2001;Payandeh et al, 2011), and as their selectivity pattern resembles that of animal Na V channels but their filter sequence resembles that of Ca V s, it was suggested that NaChBac channels rather than K V s might be the true ancestors of animal Na V s and Ca V s (Charalambous and Wallace, 2011).…”

“…Hence, it would seem that four-domain Ca V s would be widespread in protozoa. Surprisingly, they are absent in many protist lineages (Verret et al, 2010), although well represented in a few lineages such as ciliates. Most of the increases in cytosolic Ca 2+ influx in protists appear to be through ligand-gated channels, transient receptor potential (TRP) channels or internal stores.…”

“…Because of the phylogenetic distance to the metazoans, the loss of Ca V s genes in many lineages (especially in fungi) and the high likelihood of horizontal gene transfers, a well-resolved phylogeny of protist Ca V s, especially their relationship to metazoan Ca V s, has been elusive. Moreover, it is clear that multiple losses of Ca V s have occurred in other lineages such as land plants (Verret et al, 2010). However, the presence of Ca V s in green algae by itself is sufficient to strongly suggest that these channels were already present in the common ancestor of plants and animals (Fujiu et al, 2009;Verret et al, 2010).…”

Evidence for gravitactic behaviour in benthic diatoms

“…Benthic Euglena species, which are common in microphytobenthic biofilms and also show vertical migratory rhythms (Palmer & Round, 1965;Kingston, 1999Kingston, , 2002, probably share the same form of graviperception with planktonic species of the same genus. Furthermore, diatoms possess voltage-and mechanosensitive calcium channels, whose operation is linked to rapid changes in membrane potential (Taylor, 2009), and increases in cytosolic calcium concentration as a response to mechanical stimulus have been reported for Phaeodactylum tricornutum (Falciatore et al, 2000;Verret et al, 2010). Also, the operation of calcium ion channels and changes in cytosolic concentration are known to be involved in benthic diatom motility (Cohn & Disparti, 1994;McLachlan et al, 2009).…”

Interactions of Auxinic Compounds on Ca2+ Signaling and Root Growth in <i>Arabidopsis thaliana</i>

“…Generally, rapid and local Ca 2+ signals generated in the cytosol depend on a Ca 2+ current driven by a steep concentration gradient between the cytosol (nanomolar range) and its adjacent organelles or extracellular space (millimolar range). This allows the induction of a rapid and strong Ca 2+ rise in the cytosol required for immediate activation of an appropriate response by the simple opening of a few Ca 2+ channels [25] [26]. A calcium signature (characterized by amplitude, duration, frequency and location) can encode a message that contributes to a specific physiological response, after downstream decoding.…”