Evolution and genetics of accessory gland transcriptome divergence between Drosophila melanogaster and D. simulans.

Studies of allele-specific expression in interspecific hybrids have provided important insights into gene-regulatory divergence and hybrid incompatibilities. Many such investigations in Drosophila have used transcriptome data from complex mixtures of many tissues or from gonads, however, regulatory divergence may vary widely among species, sexes, and tissues. Thus, we lack sufficiently broad sampling to be confident about the general biological principles of regulatory divergence. Here, we seek to fill some of these gaps in the literature by characterizing regulatory evolution and hybrid misexpression in a somatic male sex organ, the accessory gland, in F1 hybrids between Drosophila melanogaster and D. simulans. The accessory gland produces seminal fluid proteins, which play an important role in male and female fertility and may be subject to adaptive divergence due to male-male or male-female interactions. We find that trans differences are relatively more abundant than cis, in contrast to most of the interspecific hybrid literature, though large effect-size trans differences are rare. Seminal fluid protein genes have significantly elevated levels of expression divergence and tend to be regulated through both cis and trans divergence. We find limited misexpression (over- or underexpression relative to both parents) in this organ compared to most other Drosophila studies. As in previous studies, male-biased genes are overrepresented among misexpressed genes and are much more likely to be underexpressed. ATAC-Seq data show that chromatin accessibility is correlated with expression differences among species and hybrid allele-specific expression. This work identifies unique regulatory evolution and hybrid misexpression properties of the accessory gland and suggests the importance of tissue-specific allele-specific expression studies.

PHYD prevents secondary dormancy establishment of seeds exposed to high temperature and is associated with lower PIL5 accumulation.

Dormancy cycling controls the seasonal conditions under which seeds germinate, and these conditions strongly influence growth and survival of plants. Several endogenous and environmental signals affect the dormancy status of seeds. Factors such as time, light, and temperature influence the balance between abscisic acid (ABA) and gibberellic acid (GA), two phytohormones that play a key role in seed dormancy and germination. High temperatures have been shown to increase ABA level and prevent seed germination, a process known as thermoinhibition. High temperature can also cause the acquisition of secondary dormancy, preventing germination of seeds upon their return to favorable germination conditions. The mechanisms and conditions linking thermoinhibition and secondary dormancy remain unclear. Phytochromes are photoreceptors known to promote seed germination of many plant species including Arabidopsis thaliana. Here, we demonstrate a role for PHYD in modulating secondary dormancy acquisition in seeds exposed to high temperature. We found that a functional PHYD gene is required for the germination of seeds that experienced high temperature, and that ABA- and GA-related gene expression during and after pre-incubation at high temperatures was altered in a phyD mutant. We further show that the level of PHYD mRNA increased in seeds pre-incubated at high temperature and that this increase correlates with efficient removal of the germination repressor PIL5.

The autonomous flowering-time pathway pleiotropically regulates seed germination in Arabidopsis thaliana.

Background and Aims: Two critical developmental transitions in plants are seed germination and flowering, and the timing of these transitions has strong fitness consequences. How genetically independent the regulation of these transitions is can influence the expression of life cycles. Method: This study tested whether genes in the autonomous flowering-time pathway pleiotropically regulate flowering time and seed germination in the genetic model Arabidopsis thaliana, and tested whether the interactions among those genes are concordant between flowering and germination stages. Key Results: Several autonomous-pathway genes promote flowering and impede germination. Moreover, the interactions among those genes were highly concordant between the regulation of flowering and germination. Conclusions: Despite some degree of functional divergence between the regulation of flowering and germination by autonomous-pathway genes, the autonomous pathway is highly functionally conserved across life stages. Therefore, genes in the autonomous flowering-time pathway are likely to contribute to genetic correlations between flowering and seed germination, possibly contributing to the winter-annual life history.

Maternal vernalization and vernalization-pathway genes influence progeny seed germination.

Different life stages frequently respond to the same environmental cue to regulate development so that each life stage is matched to its appropriate season. We investigated how independently each life stage can respond to shared environmental cues, focusing on vernalization, in Arabidopsis thaliana plants. We first tested whether effects of rosette vernalization persisted to influence seed germination. To test whether genes in the vernalization flowering pathway also influence germination, we assessed germination of functional and nonfunctional alleles of these genes and measured their level of expression at different life stages in response to rosette vernalization. Rosette vernalization increased seed germination in diverse ecotypes. Genes in the vernalization flowering pathway also influenced seed germination. In the Columbia accession, functional alleles of most of these genes opposed the germination response observed in the ecotypes. Some genes influenced germination in a manner consistent with their known effects on FLOWERING LOCUS C gene regulation during the transition to flowering. Others did not, suggesting functional divergence across life stages. Despite persistent effects of environmental conditions across life stages, and despite pleiotropy of genes that affect both flowering and germination, the function of these genes can differ across life stages, potentially mitigating pleiotropic constraints and enabling independent environmental regulation of different life stages.