Abstract
Changes in gene expression have been hypothesized to play an important role in the evolution of divergent morphologies. To test this hypothesis in a model system, we examined differences in fruiting body morphology of five filamentous fungi in the Sordariomycetes, culturing them in a common garden environment and profiling genome-wide gene expression at five developmental stages. We reconstructed ancestral gene expression phenotypes, identifying genes with the largest evolved increases in gene expression across development. Conducting knockouts and performing phenotypic analysis in two divergent species typically demonstrated altered fruiting body development in the species that had evolved increased expression. Our evolutionary approach to finding relevant genes proved far more efficient than other gene deletion studies targeting whole genomes or gene families. Combining gene expression measurements with knockout phenotypes facilitated the refinement of Bayesian networks of the genes underlying fruiting body development, regulation of which is one of the least understood processes of multicellular development.
Highlights
In the evolution of complex phenotypes, changes in gene regulation have long been argued to play a greater role than changes in protein function [1,2,3,4,5,6,7,8]
Stage 1 was initiated as the ascogenous hyphae began to develop from the perithecium initials; Stage 2 was initiated as the perithecial wall differentiated; Stage 3 began as the paraphyses started to form; Stage 4 began as the asci emerged; Stage 5 began as the ascospores differentiated, and ended with mature spores
In the case of fungal fruiting body development within the Sordariomycetes, we have shown that few developmental genes whose expression evolves retain common phenotypes or even phenotypes corresponding to a common stage of development, yet numerous genes do retain some function within the the larger fruiting body developmental process
Summary
In the evolution of complex phenotypes, changes in gene regulation have long been argued to play a greater role than changes in protein function [1,2,3,4,5,6,7,8]. Estimation of gene expression phenotypes in ancestral lineages provides a means of identifying putative changes in gene expression that may be key to morphological and adaptive innovation. Identification of the changes in the genetic network architecture underlying altered ancestral expression and regulation could open up the “black box” linking genotype to phenotype through development, revealing relevant gene network modularity and identifying the origins of diversity [30]
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