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ORIGINAL RESEARCH article

Front. Cell Dev. Biol.
Sec. Morphogenesis and Patterning
Volume 12 - 2024 | doi: 10.3389/fcell.2024.1526795
This article is part of the Research Topic Editors’ Showcase 2024: Insights in Morphogenesis and Patterning View all 4 articles

Cell-Cell Heterogeneity in Phosphoenolpyruvate Carboxylase Biases Early Cell Fate Priming in Dictyostelium discoideum

Provisionally accepted
Kenichi Abe Kenichi Abe 1Hidenori Hashimura Hidenori Hashimura 2Haruka Hiraoka Haruka Hiraoka 3Shoko Fujishiro Shoko Fujishiro 2Narufumi Kameya Narufumi Kameya 4Kazuteru Taoka Kazuteru Taoka 4Satoshi Kuwana Satoshi Kuwana 2Masashi Fukuzawa Masashi Fukuzawa 4Satoshi Sawai Satoshi Sawai 1,5,6*
  • 1 Department of Biologial Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo, Japan
  • 2 Graduate School of Arts and Sciences, The University of Tokyo, Bunkyo, Tōkyō, Japan
  • 3 Graduate School of Frontier Biosciences, Osaka University, Suita, Ōsaka, Japan
  • 4 Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Aomori, Japan
  • 5 Research Center for Complex Systems Biology, Universal Biology Institute, The University of Tokyo, Meguro-ku, Tokyo, Japan
  • 6 Department of Basic Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Meguro-ku, Japan

The final, formatted version of the article will be published soon.

    Glucose metabolism is a key factor characterizing the cellular state during multicellular development. In metazoans, the metabolic state of undifferentiated cells correlates with growth/differentiation transition and cell fate determination. Notably, the cell fate of the Amoebozoa species Dictyostelium discoideum is biased by the presence of glucose and is also correlated with early differences in intracellular ATP. However, the relationship between early cell-cell heterogeneity, cell differentiation, and the metabolic state is unclear. To address the link between glucose metabolism and cell differentiation in D. discoideum, we studied the role of phosphoenolpyruvate carboxylase (PEPC), a key enzyme in the PEP-oxaloacetate-pyruvate node, a core junction that dictates the metabolic flux of glycolysis, the TCA cycle, and gluconeogenesis. We demonstrate that there is cellcell heterogeneity in PEPC promoter activity in vegetative cells, which depends on nutrient conditions, and that cells with high PEPC promoter activity differentiate into spores. The PEPC null mutant exhibited an aberrantly high prestalk/prespore ratio, and the spore mass of the fruiting body was glassy and consisted of immature spores. Furthermore, the PEPC null mutant had high ATP levels and low mitochondrial membrane potential. Our results suggest the importance of cell-cell heterogeneity in the levels of metabolic enzymes during early cell fate priming.

    Keywords: PEPC1, cell fate2, cell metabolism3, Cell heterogeneity4, Cell differentiation5, Dictyostelium discoideum6

    Received: 12 Nov 2024; Accepted: 31 Dec 2024.

    Copyright: © 2024 Abe, Hashimura, Hiraoka, Fujishiro, Kameya, Taoka, Kuwana, Fukuzawa and Sawai. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

    * Correspondence: Satoshi Sawai, Research Center for Complex Systems Biology, Universal Biology Institute, The University of Tokyo, Meguro-ku, Tokyo, Japan

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