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Gene expression divergence through evolutionary processes is thought to be important for achieving programmed development in multicellular organisms. To test this premise in filamentous fungi, we investigated transcriptional profiles of 3,942 single-copy orthologous genes (SCOGs) in five related sordariomycete species that have morphologically diverged in the formation of their flask-shaped perithecia. We compared expression of the SCOGs to inferred gene expression levels of the most recent common ancestor of the five species, ranking genes from their largest increases to smallest increases in expression during perithecial development in each of the five species. We found that a large proportion of the genes that exhibited evolved increases in gene expression were important for normal perithecial development in Fusarium graminearum. Many of these genes were previously uncharacterized, encoding hypothetical proteins without any known functional protein domains. Interestingly, the developmental stages during which aberrant knockout phenotypes appeared largely coincided with the elevated expression of the deleted genes. In addition, we identified novel genes that affected normal perithecial development in Magnaporthe oryzae and Neurospora crassa, which were functionally and transcriptionally diverged from the orthologous counterparts in F. graminearum. Furthermore, comparative analysis of developmental transcriptomes and phylostratigraphic analysis suggested that genes encoding hypothetical proteins are generally young and transcriptionally divergent between related species. This study provides tangible evidence of shifts in gene expression that led to acquisition of novel function of orthologous genes in each lineage and demonstrates that several genes with hypothetical function are crucial for shaping multicellular fruiting bodies. IMPORTANCE The fungal class Sordariomycetes includes numerous important plant and animal pathogens. It also provides model systems for studying fungal fruiting body development, as its members develop fruiting bodies with a few well-characterized tissue types on common growth media and have rich genomic resources that enable comparative and functional analyses. To understand transcriptional divergence of key developmental genes between five related sordariomycete fungi, we performed targeted knockouts of genes inferred to have evolved significant upward shifts in expression. We found that many previously uncharacterized genes play indispensable roles at different stages of fruiting body development, which have undergone transcriptional activation in specific lineages. These novel genes are predicted to be phylogenetically young and tend to be involved in lineage- or species-specific function. Transcriptional activation of genes with unknown function seems to be more frequent than ever thought, which may be crucial for rapid adaption to changing environments for successful sexual reproduction.

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Genome-wide assays of expression between species and their hybrids have identified genes that become either over- or underexpressed relative to the parental species (i.e., transgressive). Transgressive expression in hybrids is of interest because it highlights possible changes in gene regulation linked to hybrid dysfunction. Previous studies in Drosophila that used long-diverged species pairs with complete or nearly complete isolation (i.e., full sterility and partial inviability of hybrids) and high-levels of genome misregulation have found correlations between expression and coding sequence divergence. The work highlighted the possible effects of directional selection driving sequence divergence and transgressive expression. Whether the same is true for taxa at early stages of divergence that have only achieved partial isolation remains untested. Here, we reanalyze previously published genome expression data and available genome sequence reads from a pair of partially isolated subspecies of Drosophila to compare expression and sequence divergence. We find a significant correlation in rates of expression and sequence evolution, but no support for directional selection driving transgressive expression in hybrids. We find that most transgressive genes in hybrids show no differential expression between parental subspecies and used SNP data to explore the role of stabilizing selection through compensatory mutations. We also examine possible misregulation through cascade effects that could be driven by interacting gene networks or co-option of off-target cis-regulatory elements.

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KEY MESSAGE: Here we uncover the major evolutionary events shaping the evolution of the GID1 family of gibberellin receptors in land plants at the sequence, structure and gene expression levels. Gibberellic acid (gibberellin, GA) controls key developmental processes in the life cycle of land plants. By interacting with the GIBBERELLIN INSENSITIVE DWARF1 (GID1) receptor, GA regulates the expression of a wide range of genes through different pathways. Here we report the systematic identification and classification of GID1s in 54 plants genomes, encompassing from bryophytes and lycophytes, to several monocots and eudicots. We investigated the evolutionary relationship of GID1s using a comparative genomics framework and found strong support for a previously proposed phylogenetic classification of this family in land plants. We identified lineage-specific expansions of particular subfamilies (i.e. GID1ac and GID1b) in different eudicot lineages (e.g. GID1b in legumes). Further, we found both, shared and divergent structural features between GID1ac and GID1b subgroups in eudicots that provide mechanistic insights on their functions. Gene expression data from several species show that at least one GID1 gene is expressed in every sampled tissue, with a strong bias of GID1b expression towards underground tissues and dry legume seeds (which typically have low GA levels). Taken together, our results indicate that GID1ac retained canonical GA signaling roles, whereas GID1b specialized in conditions of low GA concentrations. We propose that this functional specialization occurred initially at the gene expression level and was later fine-tuned by mutations that conferred greater GA affinity to GID1b, including a Phe residue in the GA-binding pocket. Finally, we discuss the importance of our findings to understand the diversification of GA perception mechanisms in land plants.

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The elevated rate of evolution for genes on sex chromosomes compared with autosomes (Fast-X or Fast-Z evolution) can result either from positive selection in the heterogametic sex or from nonadaptive consequences of reduced relative effective population size. Recent work in birds suggests that Fast-Z of coding sequence is primarily due to relaxed purifying selection resulting from reduced relative effective population size. However, gene sequence and gene expression are often subject to distinct evolutionary pressures; therefore, we tested for Fast-Z in gene expression using next-generation RNA-sequencing data from multiple avian species. Similar to studies of Fast-Z in coding sequence, we recover clear signatures of Fast-Z in gene expression; however, in contrast to coding sequence, our data indicate that Fast-Z in expression is due to positive selection acting primarily in females. In the soma, where gene expression is highly correlated between the sexes, we detected Fast-Z in both sexes, although at a higher rate in females, suggesting that many positively selected expression changes in females are also expressed in males. In the gonad, where intersexual correlations in expression are much lower, we detected Fast-Z for female gene expression, but crucially, not males. This suggests that a large amount of expression variation is sex-specific in its effects within the gonad. Taken together, our results indicate that Fast-Z evolution of gene expression is the product of positive selection acting on recessive beneficial alleles in the heterogametic sex. More broadly, our analysis suggests that the adaptive potential of Z chromosome gene expression may be much greater than that of gene sequence, results which have important implications for the role of sex chromosomes in speciation and sexual selection.

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