Structural divergence and loss of phosphoinositide-specific phospholipase C signaling components during the evolution of the green plant lineage: implications from structural characteristics of algal components.

Abstract

Phosphatidylinositol (PtdIns) is involved not only in the structural composition of eukaryotic cellular membranes but also in the regulation of a wide variety of physiological processes influencing growth and development (Xue et al., 2009; Janda et al., 2013). Because molecules that participate in PtdIns signaling are generated via PtdIns metabolism, extensive attention has been paid to genes encoding enzymes involved in this metabolism in order to elucidate developmental and stress-response mechanisms. PtdIns is synthesized from CDP-diacylglycerol and cytoplasmic inositol by PtdIns synthase (PIS) and is phosphorylated sequentially on its inositol ring to produce PtdIns4P and PtdIns(4,5)P2 by PtdIns 4-kinase (PI4K) and PtdIns phosphate-kinase (PIPK), respectively (Xue et al., 2009; Janda et al., 2013). Subsequently, PtdIns(4,5)P2 is cleaved by phosphoinositide-specific phospholipase C (PI-PLC) into the second messengers diacylglycerol and inositol-1,4,5-trisphosphate [Ins(1,4,5)P3, IP3] (Xue et al., 2009; Janda et al., 2013), which then activate protein kinase C (PKC) and the IP3 receptor involved in release of Ca2+ from the ER into the cytoplasm, respectively, in animal cells (Rebecchi and Pentyala, 2000; Suh et al., 2008). In fact, genes encoding orthologs of PKC and the IP3 receptor are not found in terrestrial plant genomes, suggesting differences in second messenger systems between animals and plants. Significant genomic information has been accumulated for unicellular algae including the green alga Chlamydomonas reinhardtii (Merchant et al., 2007), the red alga Cyanidioschyzon merolae (Matsuzaki et al., 2004), for the diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Armbrust et al., 2004; Bowler et al., 2008), and also for multicellular seaweeds such as the red seaweeds Pyropia yezoensis (Nakamura et al., 2013) and Chondrus crispus (Collen et al., 2013), and brown seaweed Ectocarpus siliculosus (Cock et al., 2010). In addition, large-scale EST information has been accumulated for the red seaweeds Porphyra umbilicalis and Porphyra purpurea (Chan et al., 2012; Stiller et al., 2012). Because understanding the evolutionary aspects of PtdIns signaling can help us to understand the process of establishment of the plant PtdIns signaling system, algal PI-PLC and PIPK protein structures have been compared with those of terrestrial plants.