Carbon- and nitrogen-quality signaling to translation are mediated by distinct GATA-type transcription factors.
The target of rapamycin (Tor) proteins sense nutrients and control transcription and translation relevant to cell growth. Treating cells with the immunosuppressant rapamycin leads to the intracellular formation of an Fpr1p-rapamycin-Tor ternary complex that in turn leads to translational down-regulation. A more rapid effect is a rich transcriptional response resembling that when cells are shifted from high- to low-quality carbon or nitrogen sources. This transcriptional response is partly mediated by the nutrient-sensitive transcription factors GLN3 and NIL1 (also named GAT1). Here, we show that these GATA-type transcription factors control transcriptional responses that mediate translation by several means. Four observations highlight upstream roles of GATA-type transcription factors in translation. In their absence, processes caused by rapamycin or poor nutrients are diminished: translation repression, eIF4G protein loss, transcriptional down-regulation of proteins involved in translation, and RNA polymerase I/III activity repression. The Tor proteins preferentially use Gln3p or Nil1p to down-regulate translation in response to low-quality nitrogen or carbon, respectively. Functional consideration of the genes regulated by Gln3p or Nil1p reveals the logic of this differential regulation. Besides integrating control of transcription and translation, these transcription factors constitute branches downstream of the multichannel Tor proteins that can be selectively modulated in response to distinct (carbon- and nitrogen-based) nutrient signals from the environment.
Kuruvilla
F G
FG
Department of Chemistry and Chemical Biology, Howard Hughes Medical Institute, Harvard University, 12 Oxford Street, Cambridge, MA 02138, USA.
Shamji
A F
AF
Schreiber
S L
SL
D000596:Amino Acids / Q000378:metabolism; D001692:Biological Transport; D002244:Carbon / Q000378:metabolism; D002952:Citric Acid Cycle; D003470:Culture Media; D004268:DNA-Binding Proteins / Q000378:metabolism*; D004734:Energy Metabolism; D005656:Fungal Proteins / Q000378:metabolism*; D050980:GATA Transcription Factors; D015966:Gene Expression Regulation, Fungal / Q000502:physiology*; D008954:Models, Biological; D009584:Nitrogen / Q000378:metabolism; D014176:Protein Biosynthesis; D012097:Repressor Proteins; D012441:Saccharomyces cerevisiae / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism*; D029701:Saccharomyces cerevisiae Proteins; D015398:Signal Transduction; D014157:Transcription Factors / Q000378:metabolism*; D014158:Transcription, Genetic; D016335:Zinc Fingers
D000596:Amino Acids; D003470:Culture Media; D004268:DNA-Binding Proteins; D005656:Fungal Proteins; C096100:GAT1 protein, S cerevisiae; D050980:GATA Transcription Factors; C071664:GLN3 protein, S cerevisiae; D012097:Repressor Proteins; D029701:Saccharomyces cerevisiae Proteins; D014157:Transcription Factors; D002244:Carbon; D009584:Nitrogen