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Peer-reviewedCC BY-NC 4.0Molecular Biology and Evolution

Evolutionary diversification of invertase paralogs couples carbon metabolism and sexual reproduction in fission yeasts

Abstract

Dynamic patterns of gene gain and loss play a major role in the diversification of eukaryotes, reflecting adaptation to a broad range of ecological contexts. Reconstructing the evolutionary history of genes provides a powerful framework for understanding how functional innovation shapes life-history traits. Here, we report a comprehensive analysis of gene gain and loss across the fission yeast clade, whose evolutionary trajectory remains elusive. Reductive evolution of metabolic genes is a major contributor to species diversification, as observed in other fungal taxa. Notably, we uncovered an evolutionary scenario in which an ancestral gene duplication was followed by lineage-specific loss of one or the other paralog, except in Schizosaccharomyces pombe, which retained both. We demonstrate that these paralogs encode catalytically active invertases, named Inv1 and Inv2, with distinct enzymatic properties, localization, regulation, and physiological roles. Inv1 is a secreted enzyme subject to glucose-catabolite repression and is the sole invertase required for sucrose assimilation, resembling canonical yeast invertases. In contrast, Inv2 is intracellular, constitutively expressed, and required for inducing sexual differentiation in response to nutrient availability. Overall, these findings reveal an unexpected role for carbon metabolism in modulating the haploid-diploid cycle of fission yeasts, suggesting that diversification of core metabolic functions may contribute to adaptation to environments with distinct sugar compositions.

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BibTeX
@article{noly2026evolutionary,
  title = {{Evolutionary diversification of invertase paralogs couples carbon metabolism and sexual reproduction in fission yeasts}},
  author = {Ambre Noly and Céline Faux and Maria Shaldaeva and Louison Bois-Naegelin and Philippe Fort and Dominique Helmlinger},
  journal = {Molecular Biology and Evolution},
  year = {2026},
  month = sep,
  doi = {10.1093/molbev/msag233},
  url = {https://hal.science/hal-05769859v1},
  note = {CC BY-NC 4.0},
}
RIS
TY  - JOUR
TI  - Evolutionary diversification of invertase paralogs couples carbon metabolism and sexual reproduction in fission yeasts
AU  - Ambre Noly
AU  - Céline Faux
AU  - Maria Shaldaeva
AU  - Louison Bois-Naegelin
AU  - Philippe Fort
AU  - Dominique Helmlinger
PY  - 2026
DA  - 2026/09/01
JO  - Molecular Biology and Evolution
DO  - 10.1093/molbev/msag233
UR  - https://hal.science/hal-05769859v1
AB  - Dynamic patterns of gene gain and loss play a major role in the diversification of eukaryotes, reflecting adaptation to a broad range of ecological contexts. Reconstructing the evolutionary history of genes provides a powerful framework for understanding how functional innovation shapes life-history traits. Here, we report a comprehensive analysis of gene gain and loss across the fission yeast clade, whose evolutionary trajectory remains elusive. Reductive evolution of metabolic genes is a major contributor to species diversification, as observed in other fungal taxa. Notably, we uncovered an evolutionary scenario in which an ancestral gene duplication was followed by lineage-specific loss of one or the other paralog, except in Schizosaccharomyces pombe, which retained both. We demonstrate that these paralogs encode catalytically active invertases, named Inv1 and Inv2, with distinct enzymatic properties, localization, regulation, and physiological roles. Inv1 is a secreted enzyme subject to glucose-catabolite repression and is the sole invertase required for sucrose assimilation, resembling canonical yeast invertases. In contrast, Inv2 is intracellular, constitutively expressed, and required for inducing sexual differentiation in response to nutrient availability. Overall, these findings reveal an unexpected role for carbon metabolism in modulating the haploid-diploid cycle of fission yeasts, suggesting that diversification of core metabolic functions may contribute to adaptation to environments with distinct sugar compositions.
SN  - 0737-4038
SN  - 1537-1719
ER  -