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

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

Inositol-1,4,5-trisphosphate [Ins(1,4,5)P3, IP3] is a second messenger involved in transient release of Ca2+ from the ER that activates cytosolic Ca2+ 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 IP3 [3,4]. These second messengers then activate protein kinase C (PKC) and the ER-localised IP3 receptor, respectively, in animal cells [1,2]. However, although the PI-PLC signaling cascade is present in plants [5-7], genes encoding PKC and the IP3 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 [8-23] as shown in (Table 1). In addition, large-scale EST information for the red seaweeds Porphyra umbilicalis and Porphyra purpurea has been accumulated [24-26]. Such rich gene information enables us to identify the genes encoding IP3 receptor gene homologues in algae to hypothesize the evolutionary route of the loss of the IP3 gene in plant lineages.
The origin of the IP3 receptor-dependent transient Ca2+ release system predates the divergence of animals and fungi [27,28]. Indeed, homologues of genes encoding the IP3 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 IP3 receptor gene was the target of endosymbiosis with an ancient cyanobacterium to produce plant cells, after which the IP3 gene was lost from plant lineages. At present, IP3 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 IP3 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 IP3 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 IP3 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 IP3 receptor gene homologue during their evolution, although some of Heterokontophyta that evolved by secondary symbiosis retain an ancient progenitor of the IP3 receptor gene to this date. Moreover, in the green plant lineage, streptophytes have an impaired IP3 receptor that is structurally similar to that in animals, Volvocales of chlorophytes, and brown seaweed (Figure 1). Thus, the loss of the IP3 receptor may also occurred after the divergence of chlorophytes and streptophytes. Accordingly, there have been multiple occasions upon which the IP3 receptor was lost from plant lineages. In contrast to the above conclusions drawn from genomic sequence information, there is evidence of IP3-dependent Ca2+ release in terrestrial plants [36-42], which suggests the presence of a Ca2+ channel functionally resembling the IP3 receptor in streptophytes. However, IP3-dependent Ca2+ release has been reported only in green algae among plants [43,44]. Because the major intracellular store of Ca2+ in plant cells is the vacuole [45,46], IP3 receptor activity is thought to be localised to vacuolar membranes in green algae and streptophytes. Such is the case in the fungus Neurospora crassa, in which IP3-mediated Ca2+ release occurs from vacuoles [47], as it also does in protozoan ciliates and trypanosomes, in which the IP3 receptor has been visualized on vacuolar membranes [27,28]. Thus, the green plant lineage has maintained an ancient system for transient release of Ca2+ from vacuoles, which is distinct from ER-mediated Ca2+ release in animal cells that do not possess vacuoles.

Citation: Mikami K (2014) Comparative Genomic View of The Inositol-1,4,5-Trisphosphate Receptor in Plants. J Plant Biochem Physiol 2:132. doi: 10.4172/2329-9029.1000132

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