Molecular specificity, convergence and constraint shape adaptive evolution in nutrient-poor environments.
Molecular specificity, convergence and constraint shape adaptive evolution in nutrient-poor environments.
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DOI:
10.1371/journal.pgen.1004041
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发表时间:
2014-01
期刊:
影响因子:
4.5
通讯作者:
Gresham D
中科院分区:
文献类型:
--
作者:
Hong J;Gresham D
One of the central goals of evolutionary biology is to explain and predict the molecular basis of adaptive evolution. We studied the evolution of genetic networks in Saccharomyces cerevisiae (budding yeast) populations propagated for more than 200 generations in different nitrogen-limiting conditions. We find that rapid adaptive evolution in nitrogen-poor environments is dominated by the de novo generation and selection of copy number variants (CNVs), a large fraction of which contain genes encoding specific nitrogen transporters including PUT4, DUR3 and DAL4. The large fitness increases associated with these alleles limits the genetic heterogeneity of adapting populations even in environments with multiple nitrogen sources. Complete identification of acquired point mutations, in individual lineages and entire populations, identified heterogeneity at the level of genetic loci but common themes at the level of functional modules, including genes controlling phosphatidylinositol-3-phosphate metabolism and vacuole biogenesis. Adaptive strategies shared with other nutrient-limited environments point to selection of genetic variation in the TORC1 and Ras/PKA signaling pathways as a general mechanism underlying improved growth in nutrient-limited environments. Within a single population we observed the repeated independent selection of a multi-locus genotype, comprised of the functionally related genes GAT1, MEP2 and LST4. By studying the fitness of individual alleles, and their combination, as well as the evolutionary history of the evolving population, we find that the order in which these mutations are acquired is constrained by epistasis. The identification of repeatedly selected variation at functionally related loci that interact epistatically suggests that gene network polymorphisms (GNPs) may be a frequent outcome of adaptive evolution. Our results provide insight into the mechanistic basis by which cells adapt to nutrient-limited environments and suggest that knowledge of the selective environment and the regulatory mechanisms important for growth and survival in that environment greatly increase the predictability of adaptive evolution. We studied adaptive evolution in different nitrogen-limited environments using long-term selection of asexually reproducing Saccharomyces cerevisiae populations in chemostats. Using next generation sequencing and DNA microarrays, we identified all acquired genetic variation associated with increased fitness, in both individual lineages and entire populations. We find that amplification alleles that include nutrient transporter genes specific to the molecular form of the nitrogen present in the environment are a common mechanism underlying increased fitness. In addition, we identified a general strategy for adaptation to nitrogen-limited environments that entails remodeling of phospholipid biogenesis required for producing important cellular components including vacuoles and autophagosomes. More general strategies for adaptation to nutrient-limited environments point to a role for re-wiring of signaling pathways that coordinate cell growth with nutrient availability. We reconstructed the evolutionary dynamics of a population evolving in ammonium-limited conditions and find that a multi-locus genotype is repeatedly selected within the population and constrained by epistasis. We propose that this genotype constitutes a “gene network polymorphism (GNP),” which may be a common outcome of adaptive evolution. Our study suggests that when the selective pressure is understood the molecular basis of adaptive evolution in large microbial populations may be predicted with reasonable precision.
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影响因子:
14.8
作者:
Gietz, R. Daniel;Schiestl, Robert H.
通讯作者:
Schiestl, Robert H.
影响因子:
7
作者:
Ge, B;Gurd, S;Pastinen, T
通讯作者:
Pastinen, T
影响因子:
3.7
作者:
Gerstein AC;Otto SP
通讯作者:
Otto SP
DOI:
10.1126/science.1166426
发表时间:
2009-01-23
期刊:
Science (New York, N.Y.)
影响因子:
--
作者:
Gerke J;Lorenz K;Cohen B
通讯作者:
Cohen B
影响因子:
2.6
作者:
Andréasson, C;Neve, EPA;Ljungdahl, PO
通讯作者:
Ljungdahl, PO