Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosensory cell types - a lineage-specific sensory-effector known as the cnidocyte, and a classical mechanosensory neuron referred to as the hair cell. While developmental genetics of cnidocytes is increasingly understood, genes essential for cnidarian hair cell development are unknown. Here we show that the class IV POU homeodomain transcription factor (POU-IV) - an indispensable regulator of mechanosensory cell differentiation in Bilateria and cnidocyte differentiation in Cnidaria - controls hair cell development in the sea anemone cnidarian Nematostella vectensis. N. vectensis POU-IV is postmitotically expressed in tentacular hair cells, and is necessary for development of the apical mechanosensory apparatus, but not of neurites, in hair cells. Moreover, it binds to deeply conserved DNA recognition elements, and turns on a unique set of effector genes - including the transmembrane-receptor-encoding gene polycystin 1 - specifically in hair cells. Our results suggest that POU-IV directs differentiation of cnidarian hair cells and cnidocytes via distinct gene regulatory mechanisms, and support an evolutionarily ancient role for POU-IV in defining the mature state of mechanosensory neurons.

CRISPR/Cas9 knockout of EPFL10 reduces stomatal density while maintaining photosynthesis and enhancing water conservation in rice

Rice production is of paramount importance for global nutrition and potential yields will be detrimentally affected by climate change. Rice stomatal developmental genetics were explored as a mechanism to improve water use efficiency while maintaining yield under climate stress. Gene-editing of STOMAGEN and its paralog, EPFL10, using CRISPR/Cas9 in rice cv. Nipponbare yielded lines with altered stomatal densities that were functionally characterized. CRISPR/Cas9 mediated knockouts of EPFL10 and STOMAGEN yielded lines with c. 80% and 25% of wild-type stomata, respectively. epfl10 lines with small reductions in stomatal densities are able to conserve water to similar extents as stomagen lines with large stomatal density reductions but do not suffer from any concomitant reductions in stomatal conductance, carbon assimilation, or thermoregulation. The duplicate of STOMAGEN, EPFL10, is a weak positive regulator of stomatal development in rice. epfl10 lines maintained wild-type physiological characteristics while conserving more water. Modest reductions in stomatal densities may be a climate-adaptive approach in rice that can safeguard yield.

On the Nature of Organs and Organ Systems – A Chapter in the History and Philosophy of Biology

Contrasting definitions of organs based either on function or on strictly morphological criteria are the legacy of a tradition starting with Aristotle. This floating characterization of organs in terms of both form and function extends also to organ systems. The first section of this review outlines the notions of organ and body part as defined, explicitly or implicitly, in representative works of nineteenth century’s comparative morphology. The lack of a clear distinction between the two notions led to problems in Owen’s approach to the comparative method (definition of homolog vs. nature of the vertebrate archetype) and to a paradoxical formulation, by Anton Dohrn, of the principle of functional change. Starting from the second half of the twentieth century, with the extensive use of morphological data in phylogenetic analyses, both terms – organ and body part – have been often set aside, to leave room for a comparison between variously characterized attributes (character states) of the taxa to be compared. Throughout the last two centuries, there have been also efforts to characterize organs or body parts in terms of the underlying developmental dynamics, both in the context of classical descriptive embryology and according to models suggested by developmental genetics. Functionally defined organ are occasionally co-extensive with morphologically defined body parts, nevertheless a clear distinction between the former and the latter is a necessary prerequisite to a study of their evolution: this issue is discussed here on the example of the evolution of hermaphroditism and gonad structure and function.

The evolution of ovary-specific gene expression in Hawaiian Drosophilidae

As detailed data on gene expression become accessible from more species, we have an opportunity to test the extent to which our understanding of developmental genetics from model organisms helps predict expression patterns across species. Central to this is the question: how much variation in gene expression do we expect to observe between species? Here we provide an answer by comparing RNAseq data between twelve species of Hawaiian Drosophilidae flies, focusing on gene expression differences between the ovary and other tissues. We show that there exists a cohort of ovary-specific genes that is stable across species, and that largely corresponds to described expression patterns from laboratory model Drosophila species. However, our results also show that, as phylogenetic distance increases, variation between species overwhelms variation between tissues. Using ancestral state reconstruction of expression, we describe the distribution of evolutionary changes in tissue-biased expression profiles, and use this to identify gains and losses of ovarian expression across these twelve species. We then use this distribution to calculate the correlation in expression evolution between genes, and demonstrate that genes with known interactions in D. melanogaster are significantly more correlated in their evolution than genes with no or unknown interactions. Finally, we use this correlation matrix to infer new networks of genes that have similar evolutionary trajectories, and we provide these as a dataset of novel testable hypotheses about genetic roles and interactions.

Hex Hox: De Novo Transcriptome Assembly and Embryonic Hox Gene Expression in the Burrowing Mayfly Hexagenia Limbata (Ephemeridae)

Background: Hox genes are key regulators of appendage development in the insect body plan. The body plan of Mayfly (Ephemeroptera) nymphs differs due to the presence of evolutionarily significant abdominal appendages called gills. Despite mayflies’ basal phylogenetic position and novel morphology amongst insects, little is known of their developmental genetics. Here we present an annotated transcriptome for the mayfly Hexagenia limbata, with annotated sequences for putative Hox peptides and embryonic expression profiles for the Hox genes Antp and Ubx/abd-A. Results: Transcriptomic sequencing of early instar H. limbata nymphs yielded a high-quality assembly of 83,795 contigs, of which 22,975 were annotated against Folsomia candida, Nilaparvata lugens, Zootermopsis nevadensis and UniRef90 protein databases. Peptide annotations included eight of the ten canonical Hox genes (lab, pb, Dfd, Scr, Antp, Ubx, abd-A and Abd-B), most of which contained all functional domains and motifs conserved in insects. Expression patterns of Antp and Ubx/abd-A in H. limbata were visualized from early to late embryogenesis, and are also highly conserved with patterns reported for other non-holometabolous insects.Conclusions: We present evidence that both H. limbata Hox peptide sequences and embryonic expression patterns for Antp and Ubx/abd-A are extensively conserved with other insects. These findings suggest mayfly Antp and Ubx/abd-A play similar appendage promoting and repressing roles in the thorax and abdomen, respectively. The identified expression of Ubx and abd-A in early instar nymphs further suggests that mayfly gill development is not subject to Ubx or abd-A repression. Previous studies have shown that insect Ubx and abd-A repress appendages by inhibiting their distal structures, which can permit the development of proximal appendage types. In line with past morphology-based work, we propose that mayfly gills are proximal appendage structures, possibly homologous to the proximal appendage structures of crustaceans.

Comprehensive multi-omics integration identifies differentially active enhancers during human brain development with clinical relevance

Background Non-coding regulatory elements (NCREs), such as enhancers, play a crucial role in gene regulation, and genetic aberrations in NCREs can lead to human disease, including brain disorders. The human brain is a complex organ that is susceptible to numerous disorders; many of these are caused by genetic changes, but a multitude remain currently unexplained. Understanding NCREs acting during brain development has the potential to shed light on previously unrecognized genetic causes of human brain disease. Despite immense community-wide efforts to understand the role of the non-coding genome and NCREs, annotating functional NCREs remains challenging. Methods Here we performed an integrative computational analysis of virtually all currently available epigenome data sets related to human fetal brain. Results Our in-depth analysis unravels 39,709 differentially active enhancers (DAEs) that show dynamic epigenomic rearrangement during early stages of human brain development, indicating likely biological function. Many of these DAEs are linked to clinically relevant genes, and functional validation of selected DAEs in cell models and zebrafish confirms their role in gene regulation. Compared to enhancers without dynamic epigenomic rearrangement, DAEs are subjected to higher sequence constraints in humans, have distinct sequence characteristics and are bound by a distinct transcription factor landscape. DAEs are enriched for GWAS loci for brain-related traits and for genetic variation found in individuals with neurodevelopmental disorders, including autism. Conclusion This compendium of high-confidence enhancers will assist in deciphering the mechanism behind developmental genetics of human brain and will be relevant to uncover missing heritability in human genetic brain disorders.

Three-dimensional reconstruction of the face and feeding apparatus of the predatory nematode Pristionchus pacificus

Pristionchus pacificus is a nematode model for the developmental genetics of morphological polyphenism, especially at the level of individual cells. The polyphenism of P. pacificus includes an evolutionary novelty, moveable teeth, which have enabled predatory feeding in this species and others in its family (Diplogastridae). From transmission electron micrographs of serial thin sections through an adult hermaphrodite of P. pacificus, we three-dimensionally reconstructed the 73 epithelial cells of its face, mouth, and pharynx. We found that the epithelia that produce the predatory morphology of P. pacificus are identical to Caenorhabditis elegans in the number of cell classes and nuclei. However, differences in cell form, connectivity, and nucleus position correlate with gross morphological differences from C. elegans and outgroups. Moreover, we identified fine-structural features, especially in the anteriormost pharyngeal muscles, that underlie the conspicuous, left-right asymmetry that characterizes the P. pacificus feeding apparatus. Our reconstruction provides an anatomical map for studying the genetics of polyphenism, feeding behaviour, and the development of novel form in a satellite model to C. elegans.

Cnidarian hair cell development illuminates an ancient role for the class IV POU transcription factor in defining mechanoreceptor identity

Although specialized mechanosensory cells are found across animal phylogeny, early evolutionary histories of mechanoreceptor development remain enigmatic. Cnidaria (e.g. sea anemones and jellyfishes) is the sister group to well-studied Bilateria (e.g. flies and vertebrates), and has two mechanosensory cell types – a lineage-specific sensory-effector known as the cnidocyte, and a classical mechanosensory neuron referred to as the hair cell. While developmental genetics of cnidocytes is increasingly understood, genes essential for hair cell development are unknown. Here we show that the class IV POU homeodomain transcription factor (POU-IV) – an indispensable regulator of mechanosensory cell differentiation in Bilateria and cnidocyte differentiation in Cnidaria – controls hair cell development in the sea anemone cnidarian Nematostella vectensis. N. vectensis POU-IV is postmitotically expressed in tentacular hair cells, and is necessary for development of the apical mechanosensory apparatus, but not of neurites, in hair cells. Moreover, it binds to deeply conserved DNA recognition elements, and turns on a unique set of effector genes – including the transmembrane-receptor-encoding gene polycystin 1 – specifically in hair cells. Our results suggest that POU-IV directs differentiation of cnidarian hair cells and cnidocytes via distinct gene regulatory mechanisms, and support an evolutionarily ancient role for POU-IV in defining the mature state of mechanosensory neurons.