Biological processes in living cells are often carried out by gene networks in which signals and reactions are integrated through network hubs. Despite their functional importance, it remains unclear to what extent network hubs are evolvable and how alterations impact long-term evolution. We investigated these issues using heat shock protein 90 (Hsp90), a central hub of proteostasis networks. When native Hsp90 in Saccharomyces cerevisiae cells was replaced by the ortholog from hypersaline-tolerant Yarrowia lipolytica that diverged from S. cerevisiae about 270 million years ago, the cells exhibited improved growth in hypersaline environments but compromised growth in others, indicating functional divergence in Hsp90 between the two yeasts. Laboratory evolution shows that evolved Y. lipolytica-HSP90–carrying S. cerevisiae cells exhibit a wider range of phenotypic variation than cells carrying native Hsp90. Identified beneficial mutations are involved in multiple pathways and are often pleiotropic. Our results show that cells adapt to a heterologous Hsp90 by modifying different subnetworks, facilitating the evolution of phenotypic diversity inaccessible to wild-type cells.
In many animals, germ cell segregation occurs during early embryogenesis to protect the genome, but its origin in basal metazoans is controversial. Here, we show in the freshwater polyp Hydra by clonal analysis and transgenic animals that interstitial stem cells comprise two separate stem cell populations, i.e., germline and multipotent somatic stem cells. We isolated genetically labelled stem cells for a global transcriptome study and discovered a broad set of germline-specific/enriched genes including Prdm9, Pax5, Dmrt1. In an alternative splicing analysis, we identified many genes with germline-specific isoforms; among them, male-specific isoforms of Dmrt1 and Snf5. The somatic interstitial stem cell lineage was characterized by numerous neuronal control genes like Neurog. But all stem cells in Hydra also share a core of stemness genes that has its roots in unicellular eukaryotes. This suggests an evolutionary scenario in which, at the emergence of animal multicellularity, there was an early split into a stable germline and different somatic stem cell lineages.
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