Comparative Genomic View of The Inositol-1,4,5-Trisphosphate Receptor in Plants

Abstract

Inositol-1,4,5-trisphosphate [Ins(1,4,5)P 3 , IP 3 ] is a second messenger involved in transient release of Ca 2+ from the ER that activates cytosolic Ca 2+ signalling cascades in response to extracellular and intracellular stimuli [1,2]. Phosphatidylinositol-4,5-bisphosphate is cleaved by phosphoinositide-specific phospholipase C (PI-PLC) into the second messengers diacylglycerol (DAG) and IP 3 [3,4]. These second messengers then activate protein kinase C (PKC) and the ER-localised IP 3 receptor, respectively, in animal cells [1,2]. However, although the PI-PLC signaling cascade is present in plants [5][6][7], genes encoding PKC and the IP 3 receptor have not been found in terrestrial plant genomes, suggesting differences in second messenger systems between animals and plants. To date, the genomes of a variety of unicellular and multicellular algae have been sequenced [8][9][10][11][12][13][14][15][16][17][18][19][20][21][22][23] as shown in (Table 1). In addition, large-scale EST information for the red seaweeds Porphyra umbilicalis and Porphyra purpurea has been accumulated [24][25][26]. Such rich gene information enables us to identify the genes encoding IP 3 receptor gene homologues in algae to hypothesize the evolutionary route of the loss of the IP 3 gene in plant lineages.The origin of the IP 3 receptor-dependent transient Ca 2+ release system predates the divergence of animals and fungi [27,28]. Indeed, homologues of genes encoding the IP 3 receptor have been identified in protozoa such as the choanoflagellate Monosiga brevicollis [29], the myxomycete Dictyostelium discoideum [30], the ciliate Paramecium tetraurelia [31], and the parasite Trypanosoma brucei [32]. Thus, it is plausible that an ancient eukaryotic cell containing an IP 3 receptor gene was the target of endosymbiosis with an ancient cyanobacterium to produce plant cells, after which the IP 3 gene was lost from plant lineages. At present, IP 3 receptor homologues have been found in green algae, such as Chlamydomonas reinhardtii [10] and Volvox carteri [33,34], and in heterokont algae including Aureococcus anophagefferrens [21] and Ectocarpus siliculosus [22], but have not been identified in red algae or streptophytes (land plants and charophytic algae) (Figure 1). These findings have led to proposals that the IP 3 receptor gene homologue was lost on multiple occasions during plant evolution. Because an ancestor of both green and red photosynthetic algal cells appeared after the primary endosymbiosis of a cyanobacterium into an ancient non-photosynthetic eukaryotic cell [35], the IP 3 receptor homologue was probably lost from lineages of red algae and green algae except for Volvocales (Figure 1). In fact, the genomes of unicellular Aureococcus anophagefferrens and multicellular Ectocarpus siliculosus carry an IP 3 receptor gene homologue (Figure 1). Because both photosynthetic algae arose from secondary endosymbiosis of a red algal cell into an ancient non-photosynthetic eukaryotic cell [35], it appears that red algae subsequently lost the IP...

Modeling the Action Potential in Characeae Nitellopsis obtusa: Effect of Saline Stress

“…The IP 3 signaling in plants is controversial (Munnik and Vermeer, 2010), but there is increasing experimental evidence connecting transient concentration increases of IP 3 and cytoplasmic Ca 2+ in circadian rhythms and upon exposure to range of abiotic stresses in higher plants (Krinke et al, 2007; Tang et al, 2007). Further, IP 3 and DAG (diacylglycerol, formed at the same time as IP 3 ) can be phosphorylated in plants to form IP 6 and phosphatidic acid, which may also act as second messengers (Mikami, 2014).…”