PHR1 positively regulates phosphate starvation-induced anthocyanin accumulation through direct upregulation of genes F3’H and LDOX in Arabidopsis

Liu, Zhongjuan; Wu, Xue‐Qian; Wang, Enhui; Liu, Yanan; Wang, Yi; Zheng, Qianqian; Han, Yizhen; Chen, Zhongze; Zhang, Yongqiang

doi:10.1007/s00425-022-03952-w

Cited by 17 publications

(10 citation statements)

References 46 publications

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“…Several studies have preliminarily revealed the positive role of PHR1 in the regulation of Pi deficiency‐induced anthocyanin accumulation (Rubio et al, 2001; Bustos et al, 2010; Ren et al, 2012; Puga et al, 2014). A recent study has showed that PHR1 directly activates the expression of anthocyanin biosynthetic genes in Arabidopsis (Liu et al, 2022), providing direct evidence that PHR1 mediates anthocyanin accumulation. However, little is known about the mechanism of PHR1‐mediated anthocyanin biosynthesis under Pi starvation conditions, especially in woody plants such as apple.…”

Section: Discussionmentioning

confidence: 99%

“…However, under Pi deficiency conditions, the interaction between SPX4 and PAP1 is weakened, resulting in the release of PAP1 to promote anthocyanin accumulation by directly activating the expression of DFR , a key anthocyanin biosynthetic gene (He et al, 2021). A recent study showed that PHR1 positively regulates low Pi‐induced anthocyanin accumulation by directly activating the expression of the anthocyanin biosynthetic genes F3H and LDOX in Arabidopsis (Liu et al, 2022). Although PHR1 is a central regulator of Pi deficiency‐induced anthocyanin biosynthesis, the molecular mechanisms by which PHR1 regulates anthocyanin biosynthesis remain elusive.…”

Section: Introductionmentioning

confidence: 99%

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The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis

Liu

et al. 2023

JIPB

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PHR1 (PHOSPHATE STARVATION RESPONSE1) plays key roles in the inorganic phosphate (Pi) starvation response and in Pi deficiency‐induced anthocyanin biosynthesis in plants. However, the post‐translational regulation of PHR1 is unclear, and the molecular basis of PHR1‐mediated anthocyanin biosynthesis remains elusive. In this study, we determined that MdPHR1 was essential for Pi deficiency‐induced anthocyanin accumulation in apple (Malus × domestica). MdPHR1 interacted with MdWRKY75, a positive regulator of anthocyanin biosynthesis, to enhance the MdWRKY75‐activated transcription of MdMYB1, leading to anthocyanin accumulation. In addition, the E3 ubiquitin ligase SEVEN IN ABSENTIA1 (MdSINA1) negatively regulated MdPHR1‐promoted anthocyanin biosynthesis via the ubiquitination‐mediated degradation of MdPHR1. Moreover, the protein kinase apple BRASSINOSTEROID INSENSITIVE2 (MdBIN2) phosphorylated MdPHR1 and positively regulated MdPHR1‐mediated anthocyanin accumulation by attenuating the MdSINA1‐mediated ubiquitination degradation of MdPHR1. Taken together, these findings not only demonstrate the regulatory role of MdPHR1 in Pi starvation induced anthocyanin accumulation, but also provide an insight into the post‐translational regulation of PHR1.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis

Liu

et al. 2023

JIPB

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“…Both AtPHR1 and AtPHL2 can directly regulate the transcriptional expression of AtPAP10 to enhance APase activity in response to LP stress (Sun et al, 2016). Also, AtPHR1 was thought to be a key regulator involved in the regulation of LP-induced anthocyanin synthesis (Bustos et al, 2010;He et al, 2021;Liu et al, 2022), but it was recently discovered to be involved in the Despite the mutations in the P1BS motifs of proSlPAP7(I), proSl-PAP12(I), and proSlPAP17b(I), SlPHL1 was still able to interact with these fragments, albeit to a lesser extent (Figure 5). This observation aligns with our prior finding that SlPHL1 binds to the SlPT7 promoter region, but the P1BS motif does not appear to be required (Zhang et al, 2021), perhaps suggesting that SlPHL1 interacts with the promoters of its target genes not only through P1BS motifs but also through other elements such as P1BS-like motifs.…”

Section: Discussionmentioning

confidence: 99%

“…The primers utilized for construction are shown in Table S4. For Y1H, the constructs of each pro::LacZ and GAD-cSlPHL1 were transformed into Saccharomyces cerevisiae (S. cerevisiae) strain EGY48 through the Matchmaker GAL4-based Two-Hybrid System (Clontech) in pairs, and the interaction between cSlPHL1 and promoter fragments was subsequently analyzed using Y1H according to the previous method (Lin et al, 2007;Liu et al, 2022;Wu et al, 2023). Briefly, after transformed yeast cells were grown on drop-out synthetic dropout and Leu but containing X-gal (SC/ÀTrp/-Ura/ÀLeu/+X-gal) after about 3 days of culture at 30 C. At least four randomly selected clones were employed for analysis with similar results.…”

Section: Yeast One-hybrid (Y1h) and Modified Yeast One-hybrid (My1h)mentioning

confidence: 99%

SlPHL1 positively modulates acid phosphatase in response to phosphate starvation by directly activating the genes SlPAP10b and SlPAP15 in tomato

Liu,

Li,

Zhang

et al. 2024

Physiologia Plantarum

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Increased acid phosphatase (APase) activity is a prominent feature of tomato (Solanum lycopersicum) responses to inorganic phosphate (Pi) restriction. SlPHL1, a phosphate starvation response (PHR) transcription factor, has been identified as a positive regulator of low Pi (LP)‐induced APase activity in tomato. However, the molecular mechanism underlying this regulation remains to be elucidated. Here, SlPHL1 was found to positively regulate the LP‐induced expression of five potential purple acid phosphatase (PAP) genes, namely SlPAP7, SlPAP10b, SlPAP12, SlPAP15, and SlPAP17b. Furthermore, we provide evidence that SlPHL1 can stimulate transcription of these five genes by binding directly to the PHR1 binding sequence (P1BS) located on their promoters. The P1BS mutation notably weakened SlPHL1 binding to the promoters of SlPAP7, SlPAP12, and SlPAP17b but almost completely abolished SlPHL1 binding to the promoters of SlPAP10b and SlPAP15. As a result, the transcriptional activation of SlPHL1 on SlPAP10b and SlPAP15 was substantially diminished. In addition, not only did transient overexpression of either SlPAP10b or SlPAP15 in tobacco leaves increase APase activity, but overexpression of SlPAP15 in Arabidopsis and tomato also increased APase activity and promoted plant growth. Subsequently, two SPX proteins, SlSPX1 and SlSPX4, were shown to physically interact with SlPHL1. Moreover, SlSPX1 inhibited the transcriptional activation of SlPHL1 on SlPAP10b and SlPAP15 and negatively regulated the activity of APase. Taken together, these results demonstrate that SlPHL1‐mediated LP signaling promotes APase activity by activating the transcription of SlPAP10b and SlPAP15, which may provide valuable insights into the mechanisms of tomato response to Pi‐limited stress.

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“…A decrease in cellular P i concentration impairs production of the inositol pyrophosphate species InsP8, relieving PHR1/PHLs of suppression by SPX (for SYG1/Pho81/XPR1) domain-containing proteins, thus linking transcription factor activity to P i availability (Puga et al, 2014; Dong et al, 2019; Zhu et al, 2019; Ried et al, 2021). The transcriptional response to P i scarcity leads to scavenging of external and internal P i sources through phosphatase induction (Morcuende et al, 2007) and altered lipid metabolism (Misson et al, 2005; Pant et al, 2015b), anthocyanin biosynthesis (Nilsson et al, 2012; Liu et al, 2022; Li et al, 2023), and protection from photodamage (Nilsson et al, 2012), to name a selection. PHR1/PHLs are characterized as transcriptional activators (Nilsson et al, 2007; Bustos et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

PHR1 and PHL1 mediate rapid high-light responses and acclimation to triose phosphate oversupply

Ackermann

Müller

Hieber

et al. 2023

Preprint

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Fluctuations in light intensity require immediate metabolic adjustment which includes reprogramming of both plastidial and nuclear gene expression, but the signaling pathways behind such responses are not fully understood. Here we report the identification of an early high-light responsive pathway in Arabidopsis thaliana that depends on PHOSPHATE STARVATION RESPONSE 1 (PHR1) and PHR1-LIKE 1 (PHL1) transcription factors involved in low phosphate (Pi) signaling. High-light treatment rapidly induced the accumulation of PHR1-responsive transcripts in wildtype plants grown under nutrient-sufficient conditions, but not in phr1 phl1 double knockout plants. Differences in starch accumulation and ATP levels were detected between wildtype and phr1 phl1 mutants subjected to high light, suggesting a link between Pi signaling, carbohydrate partitioning, and energy status during stress. In line with a function of PHR1/PHL1 upon triose phosphate accumulation, we observed that blocking starch biosynthesis in the phr1 phl1 double mutant, by introducing the agd1-1 allele, causes a severe growth defect. Phenotypes of the adg1 phr1 phl1 triple mutant such as high-light sensitivity and growth restriction in the absence of exogenously supplied sucrose resemble the previously described double mutant adg1 tpt-2, lacking a functional copy of the TRIOSE PHOSPHATE/PHOSPHATE TRANSLOCATOR (TPT), and we show that Pi responses are disturbed in adg1 tpt-2. We propose that Pi sequestration by photosynthesis and import of Pi into the chloroplast transiently depletes cytosolic Pi reserves upon sudden increases in light intensity. The low-Pi sensing machinery in the nucleus consequently implements early high-light transcriptional responses, qualifying Pi as a new operational retrograde signal.

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PHR1 positively regulates phosphate starvation-induced anthocyanin accumulation through direct upregulation of genes F3’H and LDOX in Arabidopsis

Cited by 17 publications

References 46 publications

The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis

The E3 ubiquitin ligase SINA1 and the protein kinase BIN2 cooperatively regulate PHR1 in apple anthocyanin biosynthesis

SlPHL1 positively modulates acid phosphatase in response to phosphate starvation by directly activating the genes SlPAP10b and SlPAP15 in tomato

PHR1 and PHL1 mediate rapid high-light responses and acclimation to triose phosphate oversupply

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