Factors governing the transcriptome changes and chronological lifespan of fission yeast during phosphate starvation

Garg, Angad; Sanchez, Ana M.; Schwer, Beate; Shuman, Stewart

doi:10.1016/j.jbc.2024.105718

Cited by 3 publications

(1 citation statement)

References 36 publications

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“…(Ohtsuka et al, 2024;Ohtsuka, Shimasaki, & Aiba, 2021c, 2021d. Autophagy is crucial for the long CLS, including longevity under sulfur starvation (Garg et al, 2024;Shimasaki et al, 2020;Vega et al, 2022). Since Sdr1 regulates autophagy induction under sulfur depletion, Sdr1 may be required for the CLS extension under this condition.…”

Section: Sdr1 + Is Required To Maintain Clsmentioning

confidence: 99%

A novel transcription factor Sdr1 involving sulfur depletion response in fission yeast

Ohtsuka,

Ohara,

Shimasaki

et al. 2024

Genes to Cells

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In the fission yeast Schizosaccharomyces pombe, the response to sulfur depletion has been less studied compared to the response to nitrogen depletion. Our study reveals that the fission yeast gene, SPCC417.09c, plays a significant role in the sulfur depletion response. This gene encodes a protein with a Zn2Cys6 fungal‐type DNA‐binding domain and a transcription factor domain, and we have named it sdr1+ (sulfur depletion response 1). Interestingly, while sulfur depletion typically induces autophagy akin to nitrogen depletion, we found that autophagy was not induced under sulfur depletion in the absence of sdr1+. This suggests that sdr1+ is necessary for the induction of autophagy under conditions of sulfur depletion. Although sdr1+ is not essential for the growth of fission yeast, its overexpression, driven by the nmt1 promoter, inhibits growth. This implies that Sdr1 may possess cell growth‐inhibitory capabilities. In addition, our analysis of Δsdr1 cells revealed that sdr1+ also plays a role in regulating the expression of genes associated with the phosphate depletion response. In conclusion, our study introduces Sdr1 as a novel transcription factor that contributes to an appropriate cellular nutrient starvation response. It does so by inhibiting inappropriate cell growth and inducing autophagy in response to sulfur depletion.

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Section: Sdr1 + Is Required To Maintain Clsmentioning

confidence: 99%

A novel transcription factor Sdr1 involving sulfur depletion response in fission yeast

Ohtsuka,

Ohara,

Shimasaki

et al. 2024

Genes to Cells

View full text Add to dashboard Cite

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The putative polyamine transporter Shp2 facilitates phosphate export in an Xpr1-independent manner and contributes to high phosphate tolerance

Komamura,

Nishimura,

Ohta

et al. 2025

Journal of Biological Chemistry

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Efn1 and Efn2 are extracellular 5'-nucleotidases induced during the fission yeast response to phosphate starvation

Innokentev,

Sanchez,

Monetti

et al. 2024

mBio

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The fission yeast PHO regulon genes pho1 , pho84 , and tgp1 —encoding a cell surface-associated acid phosphatase (Pho1), a plasma membrane inorganic phosphate transporter (Pho84), and a plasma membrane glycerophosphocholine transporter (Tgp1)—are strongly upregulated in response to acute phosphate starvation, as are the SPBPB2B2.06c and SPAC1039.02 genes that encode putative 5'-nucleotidase paralogs of the binuclear metallophosphoesterase enzyme superfamily. Via proteomic analysis of the medium harvested from phosphate-replete and phosphate-starved fission yeast, we define a starvation secretome that includes SPBPB2B2.06c (renamed Efn1, for e xtracellular f ive-prime n ucleotidase), SPAC1039.02 (henceforth Efn2), and Pho1 among the most abundant exported proteins elaborated by phosphate-starved cells. We demonstrate and characterize a 5'-nucleotidase activity secreted into the medium of phosphate-starved efn1 + efn2 + cells, which is eliminated by simultaneous deletion of efn1 and efn2 . By singly deleting efn1 and efn2 , we find that Efn1 contributes the greater share of secreted 5'-nucleotidase activity. Efn1 and Efn2 catalyze the release of inorganic phosphate from all four standard ribonucleoside monophosphates, in order of preference: CMP > UMP > AMP > GMP. Whereas efn1 + efn2 + cells can use extracellular CMP as a source of phosphate during phosphate starvation, efn1 ∆ efn2 ∆ cells cannot. The secretion of 5'-nucleotidase enzymes during phosphate limitation is a newly appreciated facet of fission yeast phosphate homeostasis. IMPORTANCE Schizosaccharomyces pombe adapts to phosphate starvation by upregulating the expression of a cell surface acid phosphatase that mobilizes inorganic phosphate from the extracellular milieu, as well as transmembrane transporters that take up inorganic phosphate and glycerophosphocholine. This study identifies two paralogous extracellular 5'-nucleotidase enzymes, Efn1 and Efn2, encoded by genes that are highly transcriptionally induced during acute phosphate starvation, as major proteins secreted into the medium by phosphate-starved fission yeast cells. Secreted Efn1 and Efn2 catalyze the release of inorganic phosphate from all ribonucleoside monophosphates, with a preference for CMP. Secretion of Efn1 and Efn2 enables phosphate-starved fission yeast to thrive by using extracellular CMP as a source of inorganic phosphate. The starvation-induced production of extracellular 5'-nucleotidases adds a new layer of pro-adaptive function during phosphate limitation.

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Factors governing the transcriptome changes and chronological lifespan of fission yeast during phosphate starvation

Cited by 3 publications

References 36 publications

A novel transcription factor Sdr1 involving sulfur depletion response in fission yeast

A novel transcription factor Sdr1 involving sulfur depletion response in fission yeast

The putative polyamine transporter Shp2 facilitates phosphate export in an Xpr1-independent manner and contributes to high phosphate tolerance

Efn1 and Efn2 are extracellular 5'-nucleotidases induced during the fission yeast response to phosphate starvation

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