Involvement of auxin signaling mediated by IAA14 and ARF7/19 in membrane lipid remodeling during phosphate starvation

Abstract

In higher plants, phosphate (Pi) deficiency induces the replacement of phospholipids with the nonphosphorous glycolipids digalactosyldiacylglycerol (DGDG) and sulfoquinovosyldiacylglycerol (SQDG). Genes involved in membrane lipid remodeling are coactivated in response to Pi starvation, but the mechanisms that guide this response are largely unknown. Previously, we reported the importance of auxin transport for DGDG accumulation during Pi starvation. To understand the role of auxin signaling in Arabidopsis membrane lipid remodeling, we analyzed slr-1, a gain-of-function mutant of IAA14 (a repressor of auxin signaling), and arf7arf19, a loss-of-function mutant of auxin response factors ARF7 and ARF19. In slr-1 and arf7arf19, Pi stress-induced accumulation of DGDG and SQDG was suppressed. Reduced upregulation of glycolipid synthase and phospholipase genes in these mutants under Pi-deficient conditions indicates that IAA14 and ARF7/19 affect membrane lipid remodeling at the level of transcription. Pi stress-dependent induction of a non-protein-coding gene, IPS1, was also lower in slr-1 and arf7arf19, whereas expression of At4 (another Pi stress-inducible non-protein-coding gene), anthocyanin accumulation, and phosphodiesterase induction were not reduced in the shoot. High free Pi content was observed in slr-1 and arf7arf19 even under Pi-deficient conditions, suggesting that Pi homeostasis during Pi starvation is altered in these mutants. These results demonstrate a requirement of auxin signaling mediated by IAA14 and ARF7/19 for low-Pi adaptation in Arabidopsis.

Transcriptional regulation of thylakoid galactolipid biosynthesis coordinated with chlorophyll biosynthesis during the development of chloroplasts in Arabidopsis

“…In a previous report, we have shown that galactolipids accumulate in the root of slr-1 mutants without upregulation of MGD2 , MGD3 , DGD1 , and DGD2 under nutrient-sufficient conditions (Narise et al, 2010). Furthermore, MGD1 expression in the slr-1 root remained at the same level as in the wild-type plants ( Figure 5A ), indicating that the increase in galactolipids in the slr-1 roots was not due to the transcriptional activation of the galactolipid synthesis genes.…”

Salicylic acid modulates levels of phosphoinositide dependent-phospholipase C substrates and products to remodel the Arabidopsis suspension cell transcriptome

“…flu1 plants accumulate protochlorophyllide, an intermediate in the chlorophyll biosynthesis pathway and release singlet oxygen in plastids upon a dark/light shift (Laloi et al, 2006). arf7arf19 is a loss-of-function mutant of the auxin response factors ARF7 and ARF19 (Narise et al, 2010). Therefore, the genes of cluster B, while responding to SA, appear to be less characteristic of a typical SA response, and might correspond to a more general stress response like the oxidative stress response.…”

Monogalactosyldiacylglycerol synthesis in the outer envelope membrane of chloroplasts is required for enhanced growth under sucrose supplementation

“…In shoots of WT plants, the molar ratio of DGDG in the total membrane lipids was increased when sucrose was supplemented, whereas that of MGDG was decreased (Figure 5A). Although the level of MGD3 mRNA in OE7 under sucrose supplementation was markedly higher than that observed in WT plants grown under Pi depletion (Figure 3A; Narise et al, 2010), only a small increase in DGDG mol% was observed in OE7 shoots compared with WT shoots (Figure 5A). Thus, we also analyzed lipid composition of the microsomal fraction extracted from shoots of WT and OE7 supplemented with sucrose (Figure 5B).…”

“…Although NPC5 , DGD1 , and DGD2 are responsive to Pi starvation and are involved in membrane lipid remodeling under Pi depletion (Härtel et al, 2000; Kelly and Dörmann, 2002; Kelly et al, 2003; Gaude et al, 2008), their expression in shoots was not significantly affected by sucrose supplementation (Figure 1A). IPS1 and At4 are non-protein-coding genes that are strongly and specifically induced by Pi starvation but are not related to lipid synthesis (Martín et al, 2000; Rubio et al, 2001; Bari et al, 2006; Narise et al, 2010). Expression of both IPS1 and At4 in shoots was increased by sucrose supplementation.…”

“…Unexpectedly, although MGD3 expression was significantly higher in OE7 than in WT (Figure 3A), the DGDG molar ratio in membrane lipids was only slightly different between OE7 and WT (Figure 5). Indeed, the level of MGD3 mRNA is markedly higher in OE7 than in WT plants grown under Pi depletion (Narise et al, 2010). In shoots of WT grown under Pi depletion, the molar ratio of DGDG in the total membrane lipids is ~15% higher than in plants grown under Pi-sufficient conditions (Kobayashi et al, 2009a).…”