Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid‐localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation

Abstract

SUMMARYGlycerophosphodiester phosphodiesterase (GDPD), which hydrolyzes glycerophosphodiesters into snglycerol-3-phosphate (G-3-P) and the corresponding alcohols, plays an important role in various physiological processes in both prokaryotes and eukaryotes. However, little is known about the physiological significance of GDPD in plants. Here, we characterized the Arabidopsis GDPD family that can be classified into canonical GDPD (AtGDPD1-6) and GDPD-like (AtGDPDL1-7) subfamilies. In vitro analysis of enzymatic activities showed that AtGDPD1 and AtGDPDL1 hydrolyzed glycerolphosphoglycerol, glycerophosphocholine and glycerophosphoethanolamine, but the maximum activity of AtGDPD1 was much higher than that of AtGDPDL1 under our assay conditions. Analyses of gene expression patterns revealed that all AtGDPD genes except for AtGDPD4 were transcriptionally active in flowers and siliques. In addition, the gene family displayed overlapping and yet distinguishable patterns of expression in roots, leaves and stems, indicating functional redundancy as well as specificity of GDPD genes. AtGDPDs but not AtGDPDLs are up-regulated by inorganic phosphate (P i ) starvation. Loss-of-function of the plastid-localized AtGDPD1 leads to a significant decrease in GDPD activity, G-3-P content, P i content and seedling growth rate only under P i starvation compared with the wild type (WT). However, membrane lipid compositions in the P i -deprived seedlings remain unaltered between the AtGDPD1 knockout mutant and WT. Thus, we suggest that the GDPD-mediated lipid metabolic pathway may be involved in release of P i from phospholipids during P i starvation.

The Phosphate Fast-Responsive Genes PECP1 and PPsPase1 Affect Phosphocholine and Phosphoethanolamine Content

“…In response to a lack of Pi, we observed that NPC4, PLDz2, and GDPD1, 2, 3, 5, and 6 were induced in wild-type plants as previously reported (Supplemental Fig. 5; Nakamura et al, 2005;Li et al, 2006;Cheng et al, 2011), even if GDPD2 and 5 were only moderately induced. PLDz1 and PAH2 did not respond to Pi deficiency, and PAH1 was moderately (yet consistently) induced in the absence of Pi.…”

“…To verify if altered levels of PCho and PEth could lead to the transcriptomic activation or inhibition of specific lipid metabolism pathways, we selected several genes representative of membrane lipid recycling pathways triggered during Pi starvation (Nakamura, 2013). These genes included NPC4 (representative of the nonspecific PLC pathway; Nakamura et al, 2005), PLDz1 and 2, PAH1 and 2 (for the PLD/PAP pathway; Qin and Wang, 2002;Li et al, 2006;Nakamura et al, 2009;Eastmond et al, 2010), and GDPD1, 2, 3, 5, and 6 (for the LAH/GDPD pathway; Cheng et al, 2011). In response to a lack of Pi, we observed that NPC4, PLDz2, and GDPD1, 2, 3, 5, and 6 were induced in wild-type plants as previously reported (Supplemental Fig.…”

Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain‐containing proteins

“…Of note, despite lacking the SPX domain, two glycerophosphodiester phosphodiesterases have recently been involved in maintaining cellular phosphate homeostasis in plants [63,64].…”

Lipid Biosynthesis and Protein Concentration Respond Uniquely to Phosphate Supply during Leaf Development in Highly Phosphorus-Efficient Hakea prostrata

“…Lipid remodeling similar to that observed in P-limited Arabidopsis shoots (Kobayashi et al, 2009a) also occurred in H. prostrata leaves; galactolipids showed a negative correlation with Pi supply in all except senescing leaves, and phospholipids showed a positive correlation with Pi supply in all except young H. prostrata leaves. The decrease in galactolipid concentrations in young and mature leaves with Pi supply could be attributed to the P-dependent 4-to 5-fold decreases in transcripts encoding putative H. prostrata orthologs of the phosphodiesterase GDPD1 and the type B MGDG synthase MGD3 (Dubots et al, 2010;Cheng et al, 2011). The concomitant increase in phospholipids was accompanied by a modest 2-fold decrease in HpNPC4 and a 4-fold increase in HpNMT2 expression.…”

“…Alternatively, phospholipids can be deacylated by either phospholipase A in combination with lysophospholipase, phospholipase B, or lipid acyl hydrolase activities (Matos and Pham-Thi, 2009). GLYCEROPHOSPHODIESTER PHOSPHODI-ESTERASE (GDPD) subsequently hydrolyzes glycerophosphodiesters such as glycerophosphocholine into glycerol-3-phosphate and choline (Cheng et al, 2011).…”