Biology subjects

McKinney, E. C.

Publications and source records attributed to McKinney, E. C..

5 recordsLinked to original sources

bioRxiv2017

Chromatin accessibility changes between Arabidopsis stem cells and mesophyll cells illuminate cell type-specific transcription factor networks

BackgroundCell differentiation is driven by changes in transcription factor (TF) activity and subsequent alterations in transcription. To study this process, differences in TF binding between cell types can be deduced by methods that probe chromatin accessibility. We used cell type-specific nuclei purification followed by the Assay for Transposase Accessible Chromatin (ATAC-seq) to delineate differences in chromatin accessibility and TF regulatory networks between stem cells of the shoot apical meristem (SAM) and differentiated leaf mesophyll cells of Arabidopsis thaliana.\n\nResultsChromatin accessibility profiles of SAM stem cells and leaf mesophyll cells were highly similar at a qualitative level, yet thousands of regions of quantitatively different chromatin accessibility were also identified. We found that chromatin regions preferentially accessible in mesophyll cells tended to also be substantially accessible in the stem cells as compared to the genome-wide average, whereas the converse was not true. Analysis of genomic regions preferentially accessible in each cell type identified hundreds of overrepresented TF binding motifs, highlighting a set of TFs that are likely important for each cell type. Among these, we found evidence for extensive co-regulation of target genes by multiple TFs that are preferentially expressed in one cell type or the other. For example, a set of zinc-finger TFs appear to control a suite of growth-and development-related genes specifically in stem cells, while another TF set co-regulates genes involved in light responses and photosynthesis specifically in mesophyll cells. Interestingly, the TFs within both of these sets also show evidence of extensively co-regulating each other.\n\nConclusionsQuantitative analysis of chromatin accessibility differences between stem cells and differentiated mesophyll cells allowed us to identify TF regulatory networks and downstream target genes that are likely to be functionally important in each cell type. Our findings that mesophyll cell-enriched accessible sites tend to already be substantially accessible in stem cells, but not vice versa, suggests that widespread regulatory element accessibility may be important for the developmental plasticity of stem cells. This work also demonstrates the utility of cell type-specific chromatin accessibility profiling in quickly developing testable models of regulatory control differences between cell types.

plant biology↗

bioRxiv2017

Early developmental morphology reflects independence from parents in social beetles

The variation in degree of offspring dependence in parents where parental care has evolved is striking, from feeding independence at birth to complete dependence on parents for all nutritional resources. This presents an evolutionary puzzle. Why lose the ability to feed as a contingency when parents may die or abandon broods? Comparisons of altricial and precocial vertebrates suggest that there may be life-history and developmental costs to early independence1-3. The generality of this beyond vertebrates is unclear, but we can extend the comparison as invertebrate species also vary in the level of independence in early life-history stages. For example, larvae of several burying beetle species (Nicrophorus), a genus in which parents regurgitate pre-digested food to begging larvae, have lost the ability to self-feed thus creating complete parental dependency for first instars4. Here, we ask whether variation in dependency amongst burying beetles is related to heterochrony in development of a more complex morphological structures. We show that the rate of development and allometry of mandibles of precocial larvae that can self-feed from birth are the same as those in altricial larvae that cannot survive without parenting. Instead, self-feeding is associated with shape variation in mandibles. In altricial species first instar larvae have smooth mandibles, whereas in precocial species mandibles are serrated. Later instars, which can self-feed in all species, have serrated mandibles. Serrations on teeth generally function to \"grip and rip\"5, whereas smooth blades function more to puncture6, and broods of altricial but not precocial Nicrophorus larvae show evidence for siblicide. We therefore suggest that altricial first-instar mandibles function more as weapons than feeding tools when released from self-feeding. This study presents a novel coevolution between developmental timing and parenting potentially mediated by sibling competition.

evolutionary biology↗

bioRxiv2017

Changes Of Gene Expression But Not Cytosine Methylation Are Associated With Behavioural Plasticity Of Parental Care

Behaviour is often on the front line of plasticity in response to different environments. At the genetic level, behavioural changes are likely to be associated with changes of gene expression. Most studies to date have focused on gene expression differences associated with discrete behavioural states reflecting development or age-related changes, such as honey bee castes. However, more rapidly flexible behaviour is often observed in response to social context or simple individual variation. The differences in genetic influences for the different forms of plasticity are poorly understood. In this study we contrasted gene expression during male parental care of the burying beetle, Nicrophorus vespilloides, in a factorial design. Male N. vespilloides males typically do not provide care when females are present. However, male care is inducible by the removing female and has parental effects equivalent to female care. We used this experimental manipulation to isolate gene expression and cytosine methylation associated with differences of behavioural state, differences of social context, or differences of individual flexibility for expressing care. The greatest number of differentially expressed genes was associated with behavioural state, followed by differences of social contexts, and lastly differences of individual variation. DNA methylation has been hypothesized to regulate the transcriptional architecture that regulates behavioural transitions. We tested this hypothesis by quantifying differences of cytosine methylation that were associated with differences of behavioural state and individual flexibility. Changes of cytosine methylation were not associated with changes of gene expression. Our results suggest a hierarchical association between gene expression and the different sources of variation that influence behaviour, but that this process is not controlled by DNA methylation despite reflecting levels of plasticity in behaviour. Our results further suggest that the extent that a behaviour is transient plays an underappreciated role in determining the molecular mechanisms that underpin the behaviour.

genetics↗

bioRxiv2017

Duplication And Sub/Neofunctionalization Of malvolio, An Insect Homolog Of Nramp, In The Subsocial Beetle Nicrophorus vespilloides

Gene duplication has long been thought to play a facilitating role in evolution. With growing numbers of sequenced genomes, increasing numbers of duplicate genes are uncovered with unknown functions. Here we examine malvolio, a gene involved in heavy metal transport but that also affects behavior in honey bees and Drosophila. There is only one copy of malvolio in honey bees and Drosophila despite its different roles. A phylogenetic analysis in insects suggests that malvolio has duplicated multiple times in different orders. To test if the two copies might have different functions, we examined expression levels of malvolio in brain, fat bodies, Malpighian tubules, midgut, ovaries, testes and thoracic musculature in the beetle Nicrophorus vespilloides. We found that mvl1 was expressed in all tissues, with highest expression in fat bodies and relatively lower expression in testes, Malpighian tubules, and brain, and ovaries. Expression of mvl2 differed, with significant expression only seen in brain and midgut. Because malvolio has been implicated in behavior, and these beetles have highly developed parenting behavior, we next examined expression during different behavioral states including virgin, mating, preparing resources for offspring, feeding offspring and post care. We found differing expression patterns for the two copies, with mvl1 increasing in expression during resource preparation and feeding offspring, and mvl2 decreasing in these same states. Given these patterns of expression, we suggest that malvolio in N. vespilloides has experienced sub/neofunctionalization following its duplication, and is evolving differing and tissue-specific roles in behavior and physiology.

evolutionary biology↗

bioRxiv2017

The transcriptional basis of quantitative behavioral variation

What causes individuals to produce quantitatively different phenotypes? While substantial research has focused on the allelic changes that affect phenotype, we know less about how gene expression accompanies variable phenotypes. Here, we investigate the transcriptional basis of variation in parental provisioning using two species of burying beetle, Nicrophorus orbicollis and Nicrophorus vespilloides. Specifically, we used RNA-seq to compare the transcriptomes of parents that provided high amounts of provisioning behavior versus low amounts in males and females of each species. We found that there were no overarching transcriptional patterns that distinguish high from low caring parents, and no informative transcripts that displayed particularly large expression differences in females or males. However, we did find more subtle gene expression changes between high and low provisioning parents that are consistent across sexes as well as between the two species. Furthermore, we show that transcripts previously implicated in transitioning into parental care in N. vespilloides had high variance in the levels of transcription and were unusually likely to display differential expression between high and low provisioning parents. Thus, quantitative behavioral variation appears to reflect many transcriptional differences of small effect. We show that nuanced regulation of the same gene products that are required for the transition of one behavioral state to another are also those influencing variation within a behavioral state.\n\nAuthor SummaryBurying beetles in the genus Nicrophorus breed on vertebrate carcasses and provide advanced parental care to their offspring by regurgitating partially digested flesh. However, all adult beetles do not uniformly express this trait. Some provide a large amount of parenting to their offspring, and some only a little. Here, we investigate the genetic causes of why some Nicrophorus beetles feed their offspring more than others. We demonstrate that this difference is likely caused by many small changes in gene expression, rather than a few genes that have major effects. We also find that some of the same genes that help to turn on parental care behavior in burying beetles also seem to play a role in determining how much care a beetle gives. These results provide new angles on longstanding questions about the complexity of the mechanisms that underlie quantitative variation in populations.

genetics↗