The Arabidopsis transcription factor PHR1 is essential for adaptation to high light and retaining functional photosynthesis during phosphate starvation

Abstract

The transcription factor PHR1 (PHOSPHATE STARVATION RESPONSE 1; encoded by gene At4g28610) is central for adaptation to phosphate deficiency in Arabidopsis (Arabidopsis thaliana). A rapid turnover of phosphate pools in the leaves is essential for energy transfer and metabolism within photosynthesis, and consequently, we hypothesized that PHR1 is needed for adaptation to high-light stress during P deficiency. We analyzed three Arabidopsis plant lines: wild-type, a transgenic PHR1 overexpressor line and a knockout mutant, phr1. The plants were grown under phosphate-limiting and sufficient conditions and exposed to different light conditions. Photosynthetic activity and light stress of the leaves were characterized by analyzing accumulation of carbohydrates, chlorophyll fluorescence, immunoblot detection of photosystem subunits and anthocyanin accumulation. Compared to the wild-type and the overexpressor line, the phr1 mutant has decreased levels of phosphate, anthocyanins and carbohydrates during combined P deficiency and light stress. The stressed mutant also has strongly decreased photosystem II (PSII) quantum efficiency, and shows degradation of the core units of PSII demonstrating extensive irreversible photodamage. We conclude that PHR1 is needed for the metabolic balance, for retaining P(i) levels and for inducing anthocyanin production, and during P deficiency PHR1 is vital for adaptations to avoid permanent damage to photosystems during high-light conditions.

A Shoot-Specific Hypoxic Response of Arabidopsis Sheds Light on the Role of the Phosphate-Responsive Transcription Factor PHOSPHATE STARVATION RESPONSE1

“…Analysis of mutants of the hypoxia signaling pathway (prt6 and ate1/ate2; Gibbs et al, 2011; Licausi et al, 2011) and of the low-phosphate signaling pathway (phr1 and phl1; Rubio et al, 2001;Gaude et al, 2008;Bustos et al, 2010;Nilsson et al, 2012) revealed that only the phosphate-dependent signal transduction pathway, namely the one depending on PHR1, induces MGD2, MGD3, and At5g20790 under illuminated hypoxia, as inferred from mutant transcript analyses and protoplast transactivation assays (Fig. 4).…”

“…We further cannot rule out the involvement of mitochondrial retrograde signaling, which would indicate mitochondrial disturbances that are likely under the two stress conditions, but those would be also restricted to illumination conditions. Under phosphate deficiency, photosynthesis was also inhibited (Fredeen et al, 1990;Lawlor, 1992, 1993;Nilsson et al, 2012), although this response generally occurred at later time points than under hypoxia. Therefore, the induction of responsive genes was also slower (,2 h after the beginning of hypoxia versus .24 h after the treatment start of phosphate deficiency).…”

“…Recent studies with Arabidopsis indicate that PHR1 is mainly responsible for the adaptation of photosynthesis to low-phosphate conditions, including the accumulation of anthocyanins (Nilsson et al, 2012). Therefore, it is hypothesized that short-term hypoxia and long-term phosphate deficiency result in a comparable disturbance of photosynthesis that leads to the modification of expression of genes, including galactolipid-related genes, via the activation of PHR1.…”

“…One important regulator of the phosphate deficiency response is the MYB transcription factor PHOSPHATE STARVATION RESPONSE1 (PHR1; At4g28610; Rubio et al, 2001;Bustos et al, 2010). Arabidopsis phr1 knockout mutant plants show a reduced induction of phosphate-responsive genes (Rubio et al, 2001;Gaude et al, 2008;Bustos et al, 2010;Nilsson et al, 2012). However, the expression of PHR1 per se is not influenced by phosphate deficiency (Rubio et al, 2001;Gaude et al, 2008).…”

Integrative Comparison of the Role of the PHOSPHATE RESPONSE1 Subfamily in Phosphate Signaling and Homeostasis in Rice

“…For example, PHR1 regulates shoot-to-root sulfate transport by directly binding to the promoters of sulfate transporter-encoding genes SULFATE TRANSPORT1;3 (SULTR1;3) and SULTR3;4 (Rouached et al, 2011). Because the phr1 mutant is much more sensitive to photochemical stress than the wild type, Nilsson et al (2012) proposed that PHR1 is essential for plant adaptation to high-light levels and maintaining functional photosynthesis during Pi starvation. Arabidopsis FERRITIN1 is regulated by AtPHR1, showing a direct molecular link between iron and Pi homeostasis (Bournier et al, 2013).…”