Vienna, Austria

July 2018

The use of salamanders in regeneration and developmental research has a long history filled with luminaries of the life sciences. Thomas Hunt Morgan, Hans Spemann and Hilde Mangold, Ross Granville Harrison, Inez Whipple Wilder, and August Weismann all employed salamanders in their work ^1,2. Current experimental research on salamanders largely focuses on studies of regeneration. Their abilities to regenerate limbs, brain, kidney, heart, and tail³ is enviable from the perspective of our limited human regenerative abilities. There is a large and growing toolkit of experimental manipulations, mutant and transgenic lines, and genomic resources that have advanced the use of salamanders to probe critical questions on the evolution of regeneration and its loss. These offer opportunities to discover mechanisms that could lead to new therapies for tissue repair.

The first “Salamander Models in Cross-Disciplinary Biological Research” meeting, organized by Elly Tanaka, Jessica Whited, Karen Echeverri, and Randal Voss, was held this past July (2018) at the Research Institute of Molecular Pathology (IMP) in Vienna, Austria. The meeting was hosted by the intrepid Dr. Tanaka, who is a Senior Scientist at the IMP and a leader in the regenerative biology field. This was a gathering of principal investigators working on various aspects of salamander regeneration, development, genetics, and genomics. The major goals included reviewing recent advances in research tools, along with nuanced tips for employing them, while also establishing a master “to-do” list for the field. Another objective was to lay the groundwork for organizing future salamander meetings intended for the broader community, including postdoctoral and pre-doctoral trainees and potentially representatives from funding agencies.

The Salamanders

Unlike “the” worm or “the” fly, there are multiple salamander models used in molecular studies of development and regeneration. These prominently include the Mexican axolotl (Ambystoma mexicanum), the Iberian ribbed newt (Pleurodeles waltl), the Japanese newt (Cynops pyrrhogaster) and to a lesser extent the North American eastern newt (Notophthalmus viridescens) and several species of lungless salamanders (Plethodontidae). Currently the most commonly used model is the axolotl, which has the longest captive history of any laboratory animal¹. This history includes the importation of a founder population to Paris in 1864, some of which contained the mutant “white” phenotype (an edn3 mutant), and deliberate introgression of an A. tigrinum locus found in 1962, which confers albinism through a tyrosinase mutation^4,5. These salamander species are representatives of three families (Ambystomatidae, Plethodontidae, and Salamandridae – the newts) out of the ten extant salamander families, which likely had extensive limb regenerative abilities at the base of the their clade⁶.

Genomics

Our sessions started with a review of the impressive new work in salamander genomics. Recent published genomes for both the Iberian ribbed newt (Pleurodeles waltl⁷) and Mexican axolotl (Ambystoma mexicanum⁸) provide tremendous new resources for the field. The axolotl genome is roughly ten times the size of the human genome, making it the largest genome to be sequenced and assembled to date (sorry loblolly pine). The publication of both of these genomes promises to help resolve the loci of multiple established mutant lines⁵, and offers the opportunity to establish future forward and reverse genetic screens that will improve our mechanistic understanding of regenerative processes. The community identified additional work needed to make consistent annotations, resolving 5’ ends of genes, and approaching a chromosome scale resolution of contiguous sequence. The latter was recently made available through a bioRxiv preprint from the Smith and Voss labs at University of Kentucky. The lack of whole-genome sequences in salamanders has been a major impediment to the field, and though the assemblies will still require extensive refinements, having these resources should prove to be enormously beneficial to labs currently working with these species as well as those interested in starting salamander research.

Tansgenics and Genome Editing

Genome editing approaches are now available for the axolotl^9,10, the Iberian newt^11,7 and the Japanese fire-bellied newt Cynops pyrrhogaster¹² using TALEN and CRISPR-based approaches. The most recent protocols developed by Ji-Feng Fei¹³ (now at the South China Normal University) for knock-out and knock-in approaches were reviewed. Current best practice techniques focused on improving knock-in strategies without relying on homology-directed repair. These include targeting introns for knock-in’s, screening injected embryo knockouts for efficient guide RNA’s prior to knock-ins, and non-homologous end joining approaches with “ORF Baits.”

The advent of CRISPR and TALEN approaches to genome editing in Pleurodeles was reviewed by Ken-Ichi Suzuki from Hiroshima University. The Suzuki lab is currently working to identify a ROSA-like locus for constitutive expression of knock-in constructs that would also provide a “safe harbor” for exogenous DNA. The intent of this approach is to develop a site that would both be minimally disruptive to normal cellular physiology while experiencing minimal interference from histone modifications in different cell lineages.

A wide range of transgenic and CRISPR edited lines are becoming available, especially in the axolotl. These include constitutive RFP and GFP reporter lines (available from the University of Kentucky’s Ambystoma Stock Center – AGSC), a pax7-mcherry muscle satellite cell marker, a neuronal marker, and a brainbow axolotl¹⁴. Discussions focused on prioritizing existing stocks and facilitating their dissemination through the AGSC (primarily in North America), Medipol University, Max Planck Dresden, and MPI (in Europe). The need to pursue financial resources to enable more extensive repository functions for salamanders, including cryopreservation to biobank lines, was also addressed. A long-term goal of the community is to secure resource funding for these types of valuable operations, which will be necessary to advance discoveries in regenerative biology through this growing research community.

Temporal control of transgene expression

Many genes implicated in regenerative processes have pleiotrophic roles in early development. These make knock out experiments in studying adult regeneration difficult as they can be embryonic lethal. Therefore both temporal and spatial control of gene expression is critical for furthering regeneration research.

There are several creative approaches available to address this potential stumbling block. These include inducible cre-lox systems¹⁵, constitutive cas-9 expression in genomic “safe harbors” with drug inducible guide RNA’s, and viral delivery of foreign transgenes into regenerative blastemas¹⁶¹⁷¹⁸. The latter approach has been championed by both Jessica Whited’s group at Harvard University and the Tanaka lab at MPI. These pseudotyped retroviruses have tremendous potential for further labeling and functional studies of the limb blastema, without raising transgenic embryos or modifying the expression of pleiotrophic genes outside the limb.

Open discussions evaluating approaches and avenues for future research allowed individual labs to share their own research objectives with a collective eye toward developing critical methodologies to advance the community.

Resources needed for the field

The real value of this PI-focused meeting was to allow researchers to define limiting resources they found most pressing for the field. Several additional needs were identified in addition to continued improvements to genome annotations and the temporal control of gene expression. These included detailed histological atlases of regeneration, master lists of validated antibodies, and more stable cell lines for in vitro experiments. One of the most obvious resources needed was the continued communication between labs with subsequent salamander research conferences that should continue to strengthen this growing research community.

Coordination and prioritization of a model system

Several research communities have benefitted from the intentional development and promotion of particular model organisms¹⁹. One-stop repositories of information such as Flybase, Wormbase, ZFinBase, Xenbase, and Sal-Site have all expanded the research capabilities of participating labs. While many of these labs focus on Developmental Biology, the reach of these model systems includes studies of neuroscience, evolutionary biology, physiology, and ecology. Emulating this deliberate approach will provide vital cohesion and an undoubted boon to investigators studying salamander regeneration and development. While salamanders are a remarkable “model” for regenerative research they are also remarkable organisms for their unique evolutionary histories, ecological roles, life history variation, and conservation biology. Development of tools and resources for the molecular biologists and biochemists working on salamanders will undoubtedly have unintentional spillover benefits into a wider range of research fields.

Outlook

Salamander models continue to be fertile ground for amazing discoveries on regenerative biology, cell differentiation, and development. This conference generated a tremendous amount of motivation for its participants. We have planned a broader 2019 meeting in Massachusetts, which will be a showcase for these recent developments and an iterative checkup on this rapidly growing experimental field.

References

1. Reiß, C., Olsson, L. & Hoßfeld, U. The history of the oldest self-sustaining laboratory animal: 150 years of axolotl research. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 324, 393–404 (2015).
2. Wilder, I. W. The Morphology of Amphibian Metamorphosis. (Smith College, 1925).
3. In Salamanders in Regeneration Research Methods and Protocols (eds. Kumar, A & Andras, S) (Humana Press, 2015).
4. Humphrey, R. R. Albino axolotls from an albino tiger salamander through hybridization. J. Hered. 58, 95–101 (1967).
5. Woodcock, M. R. et al. Identification of mutant genes and introgressed tiger salamander DNA in the laboratory axolotl, Ambystoma mexicanum. Scientific Reports 7, (2017).
6. Fröbisch, N. B., Bickelmann, C. & Witzmann, F. Early evolution of limb regeneration in tetrapods: evidence from a 300-million-year-old amphibian. Proc. Biol. Sci. 281, 20141550 (2014).
7. Elewa, A. et al. Reading and editing the Pleurodeles waltl genome reveals novel features of tetrapod regeneration. Nat Commun 8, 2286 (2017).
8. Nowoshilow, S. et al. The axolotl genome and the evolution of key tissue formation regulators. Nature 554, 50–55 (2018).
9. Fei, J.-F. et al. CRISPR-mediated genomic deletion of Sox2 in the axolotl shows a requirement in spinal cord neural stem cell amplification during tail regeneration. Stem cell reports 3, 444–459 (2014).
10. Flowers, G. P., Timberlake, A. T., McLean, K. C., Monaghan, J. R. & Crews, C. M. Highly efficient targeted mutagenesis in axolotl using Cas9 RNA-guided nuclease. Development (Cambridge, England) 141, 2165–2171 (2014).
11. Hayashi, T. & Takeuchi, T. Gene manipulation for regenerative studies using the Iberian ribbed newt, Pleurodeles waltl. Methods Mol. Biol. 1290, 297–305 (2015).
12. Nakajima, K., Nakajima, T. & Yaoita, Y. Generation of albino Cynops pyrrhogaster by genomic editing of the tyrosinase Gene. Zool. Sci. 33, 290–294 (2016).
13. Fei, J.-F. et al. Efficient gene knockin in axolotl and its use to test the role of satellite cells in limb regeneration. Proc. Natl. Acad. Sci. U.S.A. 114, 12501–12506 (2017).
14. Currie, J. D. et al. Live imaging of axolotl digit regeneration reveals spatiotemporal choreography of diverse connective tissue progenitor pools. Dev. Cell 39, 411–423 (2016).
15. Khattak, S. et al. Optimized axolotl (Ambystoma mexicanum) husbandry, breeding, metamorphosis, transgenesis and tamoxifen-mediated recombination. Nat Protoc 9, 529–540 (2014).
16. Kuo, T.-H. & Whited, J. L. Pseudotyped retroviruses for infecting axolotl. Methods Mol. Biol. 1290, 127–140 (2015).
17. Khattak, S. et al. Foamy virus for efficient gene transfer in regeneration studies. BMC Dev. Biol. 13, 17 (2013).
18. Oliveira, C. R. et al. Pseudotyped baculovirus is an effective gene expression tool for studying molecular function during axolotl limb regeneration. Dev. Biol. 433, 262–275 (2018).
19. Abzhanov, A. et al. Are we there yet? Tracking the development of new model systems. Trends Genet. 24, 353–360 (2008).

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Position Description
The Boston College Biology Department seeks outstanding candidates for a tenure-track faculty position in the area of Cell and Developmental Biology. Applicants are sought at the Assistant Professor level; however, exceptionally strong candidates will be considered at the Associate Professor level. The university provides competitive startup funds and research space with the expectation that the successful candidate will establish, or bring to the university, a vigorous, funded research program. Special consideration will be given to candidates whose research program synergizes with current faculty interests. We especially encourage applicants whose research utilizes embryonic model systems, those who study developmental neurobiology, and/or those who work at the interface of biophysics and cell biology. The successful candidate will join an active and expanding department with current strengths in cytoskeletal regulation, developmental biology, cancer biology, as well as microbiology, infectious disease, and computational biology.

Visit www.bc.edu/bc-web/schools/mcas/departments/biology/research/faculty-research.html for profiles of the Biology Department’s current research programs.

The university is situated on a beautiful campus dating back to the beginning of the twentieth century and is closely located to downtown Boston and Cambridge. The Biology Department has strong ongoing collaborative efforts with other departments including Chemistry and Physics, surrounding institutes including BU, Harvard, MIT, Northeastern University and Tufts University, and has state of the art (core-) facilities including next-gen sequencing, cleanrooms for nanofabrication, FACS, microscopy (including super-resolution microscopy), microfluidics, robotics, NMR and mass-spec. Moreover, the university has recently announced its decision to establish an interdisciplinary Institute for Integrated Science and Society, and the building is scheduled for construction beginning Spring 2019.

How to Apply
Applicants should submit a cover letter, curriculum vitae, a statement of research plans, a statement of teaching interests, and arrange for three letters of reference. All application materials should be submitted via Interfolio at http://apply.interfolio.com/53713. Review of applications will begin on October 1st and will continue until the position is filled.

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The University of Virginia invites applications for a tenure-track Assistant Professor position in the Department of Biology. We seek applicants who have a research vision that addresses new or longstanding fundamental questions in cell biology. Located within the College of Arts and Sciences, the Department of Biology provides an interdisciplinary and collaborative environment for basic research and teaching that spans multiple levels of biological organization, enhanced by close collaborations with colleagues at our Schools of Medicine and Engineering & Applied Sciences. A successful candidate is expected to establish a vigorous, independent, and externally funded research program as well as provide instruction and scientific training at the undergraduate and graduate levels. Applicants with a respect for diversity and a passion for making a positive impact on the world in a collaborative environment are strongly encouraged to apply. The position will begin on August 25, 2019.

Applicants must have a Ph.D. or other doctoral degree and post-doctoral research experience. A successful applicant will also have research accomplishments and plans of outstanding quality and significance as well as a commitment to excellence in teaching and mentoring. Commitment to participate in and further develop a diverse, collegial, interdisciplinary, and collaborative environment is strongly preferred.

To apply, jobs.virginia.edu/applicants/Central?quickFind=85482. Complete a candidate profile online, attach a cover letter that succinctly highlights your most significant research accomplishments, experiences, and qualifications; a curriculum vitae; a research statement that describes your vision for your research program at the university (≤ 3 pages); a statement of teaching goals; and the contact information of three references. The deadline for receipt of applications is October 31, 2018.

For questions regarding the position, please contact search chair Keith Kozminski, Associate Professor of Biology, at biocellsearch@virginia.edu; for questions about the application process, please contact Savanna Galambos, Faculty Search Advisor, at: skh7b@virginia.edu

UVA assists faculty spouses and partners seeking employment in the Charlottesville area. To learn more please visit  http://provost.virginia.edu/dual-career

For more information about UVA and the surrounding area, please visit http://uvacharge.virginia.edu/guide.html

The University of Virginia is an equal opportunity and affirmative action employer. Women, minorities, veterans and persons with disabilities are encouraged to apply.

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The Department of Biological Sciences at the University of South Carolina invites applications for a tenure-track position as an Assistant Professor with a research program in neurobiology. The successful candidate will be expected to establish an independent, extramurally funded research program focusing on cell-cell communication in neural development and/or disease. We are especially interested in applicants studying how interactions among neurons or between neurons and other cell types such as astrocytes, oligodendrocytes, Schwann cells, microglia, macrophages or endothelial cells contribute to nervous system development, disease, or response to injury in any experimental or model system. The successful candidate will have a Ph.D. or an M.D., and will have completed post-doctoral training in a relevant area of neuroscience or biomedical sciences. He or she will interact with research groups in Biological Sciences, including the Center for Childhood Neurotherapeutics that includes neuroscientists focusing on mechanisms of neural development and neural repair. Additionally, the University has a highly interactive neuroscience research community that encourages and precipitates collaborations. The candidate will be responsible for teaching at undergraduate and graduate levels in courses appropriate to his/her expertise.

To ensure full consideration, applications should be received by November 16, 2018. All applicants must fill out an online application at the USC employment website at: http://uscjobs.sc.edu/postings/39584. Qualified candidates should include with their application a curriculum vita, research statement (3 pages) and teaching philosophy (1 page). The names, email addresses and phone numbers of at least three references should also be provided. Additional information on the position and the Department of Biological Sciences can be found at http://www.biol.sc.edu/. For questions or further information, please contact Dr. Fabienne Poulain (fpoulain@mailbox.sc.edu).

The University of South Carolina is an affirmative action, equal opportunity employer. Minorities and women are encouraged to apply. The University of South Carolina does not discriminate in educational or employment opportunities on the basis of race, color, religion, national origin, sex, sexual orientation, gender, age, disability, veteran status or genetics.

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Welcome to our monthly summary of developmental biology (and related) preLights.

preLighters are early-career researchers who select and highlight preprints which they feel are interesting for the life-science community. While writing highlight posts is mostly an individual effort, plenty of interactions between the preLights team members take place on our Slack channel. This is where last month several preLighters decided to respond to a controversial World View article in Nature about the danger of preprints, and they shared their well-argued (and highly read) commentary here on the Node. Apart from that, the month of August was not short of exciting developmental biology (and related) preLights, we hope you enjoy this selection!

Gene expression and cell fate

There was a good mix of preLights dealing with gene expression in various models, such as fish, flies and living neuronal tissue. Idoia Quintana-Urzainqui discussed a preprint showing that in zebrafish embryos, this first wave of transcription is restricted to a special nuclear compartment. Later on in development, transcription factors, which are often tissue-specific, regulate cell fate. Amanda Haage highlighted how the progression from pluripotent blastula cells to neural crest cells is regulated by a transition from SoxB1 to SoxE transcription factors in zebrafish. Moving to flies, Clarice Hong’s and Natalie Dye’s preLight both dealt with transcription factor function. Clarice discussed how binding site orientation and spacing determines the activity and specificity of Hox transcription factors, while Natalie reported on how the transcription factor Doublesex is involved in the decision making of male vs. female gonad stem cell niches. Finally, Theresa Rayon illustrated how cells make transitions during neurogenesis. The study she preLighted imaged the Hes5 transcription factor in real-time and showed that its fluctuating expression in neuronal progenitors turns oscillatory as cells enter differentiation.

Neurodevelopment and morphogenesis

Neurogenesis during development of the cortex was the focus of Boyan Bonev’s preLight. By using a new labelling approach, the study uncovered the temporal order in the production of diverse neuronal subtypes and found that many of them emerge simultaneously. Ashrifia Adomako-Ankomah highlighted the spectacular morphogenetic events occurring during development of the eye. The research identified an important role for the protein nidogen, secreted by the surrounding neurocrest cells, in shaping the optic cup in zebrafish. Nidogen also featured in the preLight of Nargess Khalilgharibi, and it turned out that this protein is not essential for Drosophila morphogenesis, but still has tissue-specific functions. Lastly, Andreas van Impel reviewed how the local translation of a transcript at the leading edge of migrating endothelial cells regulates blood vessel formation.

Tools & Technologies

Undoubtedly, new methodologies are key in paving the way for discoveries in developmental biology. Hannah Brunsdon covered  a technique with enormous potential, in which the authors combined CRISPR lineage tracing with single-cell RNA sequencing to decode early mammalian development. Tools to regulate gene expression are highly desired not only for basic research, but also for potential future gene therapies. Tim Fessenden highlighted a clever technique to control the level of transgene expression by integrating synthetic miRNA target sites into the transgene. Tuning gene expression by changing the regulatory 3D interactions was the focus of Ivan Candido-Ferreira’s highlight, which showcased the use of CRISPR technology in combination with optogenetics. While optogenetics is broadly used in many experimental systems, it seems tricky to get it to work in some organisms, such as the C. elegans embryo. Angika Basant discussed an approach in her preLight that showed how such a limitation (in this case germline silencing) could be overcome. Lastly, Samantha Seah preLighted the development of a microfluidic device that allows imaging of sea anemone larvae, which are models for coral symbiosis. Make sure to read the authors’ comments who tell us about how the project was created.

Do also visit the preLights website to discover further interesting preprint highlights, such as Gautam Dey’s post on a statistical tool that provides an alternative to the p-value , or Nicola Stevenson’s highlight on the horizontal transfer of RNAs in honeybees!

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Last week, Development and our sister journal Journal of Cell Science signed an open letter coordinated by ASAPbio, signalling our intention to publish peer review reports alongside published papers. I’m really delighted to be making this commitment and wanted to take the opportunity to say a few words about our thinking behind this decision.

So why publish peer review reports and why start doing it now? The commentary in Nature that came out to accompany the open letter does, in my opinion, a great job of explaining the both the benefits and the potential pitfalls involved in publishing peer review reports and associated correspondence.  Above all, what we gain is transparency: both in terms of providing the reader additional information about the published paper and in opening up the journal’s decision-making process. Referee reports and author point-by-point responses give valuable insight into why a paper is seen by referees as important for the field, what the caveats with the work might be, and how a paper has evolved through the peer review process. I am proud of the job that Development’s Academic Editors do in helping to select papers to be published in the journal, and I’m happy to showcase the work they do in a more transparent manner.

We still have many details to work out in terms of exactly what information we will be making public, and how we will be doing it, but one thing we are clear on is that referees should still have the right to remain anonymous – both to the authors and the reader. We know from talking to the community that many referees would feel uncomfortable signing their name on a report. While open identities are a nice idea in theory, there is a strong risk that forcing referees to sign their names might compromise the quality and rigour of peer review – would you to be happy to openly criticise a paper written by someone you think might review your next manuscript, or sit on your next grant panel?  If referees want to sign their name, they are more than welcome to do so, but we do not want to make this essential.

With the protection of anonymity, though, we hope that referees will continue to do the excellent job they do in assessing papers for Development. I was part of the team at The EMBO Journal when they initiated their policy of transparent peer review, and we were concerned that referees would refuse to review papers, or would provide only ‘bland’ reports. Neither of these concerns came to pass, and the positive experience I had with transparent peer review there convinced me that it would be a good thing to implement across journals more broadly.

Development has been considering publishing peer review reports for some years. A few of our editors have been strong proponents of the policy for a long time; others have been more cautious – primarily for the reasons detailed above and in the Nature commentary. A few years ago, we conducted a community survey asking about priorities in peer review innovations, and this told us that there were other things our readers cared about more – such as introducing cross-referee commenting (which we implemented a couple of years ago). Now, however, we feel that the time is right to start planning for publishing referee reports – and this is something that our incoming Editor-in-Chief James Briscoe is  keen to implement, with the full support of all our editors. Early reactions to our announcement on social media suggest that this move will be welcomed by the community. We will be working with Journal of Cell Science to implement transparent peer review; the other Company of Biologists journals will be reviewing how things go at Development and Journal of Cell Science and consulting with their communities before deciding on their own plans.

We hope to introduce this policy in early 2019. For now, though, we welcome any feedback you may have, and look forward to sharing further details as our plans progress.

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The Developmental Biology Unit seeks to understand the general principles and mechanisms underlying the development of multicellular organisms. Researchers in the unit combine the power of genetic model organisms with quantitative imaging and -omics technologies, synthetic biology, reduced (in vitro) systems and theoretical modelling, to create a cross-cutting approach to modern developmental biology.

Research in the Developmental Biology Unit is firmly embedded within the overall EMBL environment, with extensive in-house collaborations, access to outstanding graduate students and postdoctoral fellows, and support from cutting-edge facilities, including genomics, transgenesis, metabolomics, mass-spectrometry, and microscopy. EMBL brings together the most talented scientists, empowering them to explore bold new areas of biological inquiry and carry out interdisciplinary research.

We are seeking to recruit outstanding group leaders who aim to establish novel approaches to investigate multicellular development at all scales, from the cellular and tissue, to the whole organism level.

For more information and for the application please go to the following links:

https://www.embl.de/jobs/searchjobs/index.php?ref=HD01364&newlang=1&pos[]=FAC

EMBL_GL_Developmental_Biology Unit

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Axon guidance relies on the reception and integration of molecular cues from the environment by growth cones, and defective pathfinding results in misplaced projection patterns in the mature nervous system. A new paper in Development investigates this process in the Drosophila neuromucular system, as well as the consequences of axonal miswiring to locomotion. We caught up with lead author Jaqueline Kinold and her supervisor Hermann Aberle, Professor in the Department of Functional Cell Morphology at Heinrich Heine University, Düsseldorf.

Hermann, can you give us your scientific biography and the questions your lab is trying to answer?

HA In retrospect, I find it quite interesting that my work was all the time somehow associated with cell adhesion and cellular junctions. I started off as a PhD student in Rolf Kemler‘s lab in Freiburg, working on vertebrate Cadherin-Catenin complexes, which connect neighbouring epithelial cells at adherens junctions. As a postdoctoral fellow, I switched topics and changed to Drosophila neuromuscular junctions (NMJs) in Corey Goodman‘s lab at UC Berkeley, where I was involved in a large-scale mutagenesis screen searching for genes that affected the morphology of these terminals. After cloning and functional characterization of the wishful thinking gene, I moved to Christiane Nüsslein-Volhard‘s lab at the MPI for Developmental Biology in Tübingen. There, we cloned several other genes that came out of the screen, including tolloid-related, mical, ankyrin-2 and neuroligin-1. During this time, and inspired by work of Darren Gilmour, we also developed tools and techniques to image migrating motor axons in living Drosophila embryos. Receiving a grant from the German Research Foundation and a generous invitation to join Christian Klämbt‘s department, we moved to the University of Münster, where we not only had fantastic imaging opportunities but also focussed more and more on the function of the axon guidance molecule sidestep (side), which also came out of the screen. In 2010, I received a call from the Heinrich Heine University in Düsseldorf, where we developed the idea to search for behavioural consequences of wiring defects.

Jaqueline, how did you come to join the lab, and what drives your research?

JK I studied biology at the University of Kassel and did my diploma thesis on the topic of spermatogenesis in Drosophila under the supervision of Mireille Schäfer. Afterwards, I wanted to continue my research with Drosophila, but I could imagine a change of topic and laboratory for my PhD very well. Hermann’s job advertisement and also his project description during my interview fascinated me very much. On the one hand, the correct wiring of the muscles is a multifaceted process in which many different components interlock and, on the other hand, the different methods and starting points spoke in favour of joining Hermann’s laboratory.

When did your lab first get interested in the link between neuronal wiring and locomotion in flies?

HA Since the phenotype of side mutants is really strong, I was once asked after a talk if this has any consequences for viability or eclosion. This question stuck in my mind and I started to realize that most papers in the field dealt with the guidance process itself, in embryos, and hardly anybody was exploring postembryonic stages, when the neuromuscular system is actually functional and constantly contracting. Together with the Drosophila community moving more and more into circuit analysis and behavioural studies, I asked myself which behaviour could be affected by our mutations. It took a while until I realized that locomotion and movements are the underlying basis for most, if not all, behaviours. However, it took a while until we had all the necessary technical equipment. In fact, everything truly started as the high-speed video camera arrived.

Can you give us the key results of the paper in a paragraph?

HA We examined the final innervation pattern on all muscles in side mutant third instar larvae. From this survey, we derived three major conclusions. First, innervation defects were permanent, i.e. even if potential rescue mechanisms exist, they failed to restore NMJs at non-innervated muscles. Second, loss of side affected all peripheral motor pathways and thus all body wall regions. Third, innervation errors were non-stereotypical and appeared in each hemisegment differentially. Since Side functions as a substrate-bound attractant, ventral bypass phenotypes or lack of NMJs at distal-most muscles, could be explained by insufficient attraction, which either inhibits defasciculation or slows axonal growth, respectively.

JK Also, overexpression of Side attracted motor axons at the wrong time to the wrong place, resulted in innervation defects. This was particularly evident when we expressed Side in muscle precursors. Attraction was that strong that individual axons travelling in the ISN were stretched into opposite directions leading to split pathways and complete lack of NMJs on dorsal-most muscles. This caused also amazing locomotion phenotypes. During crawling, larvae detached from the substrate and excessively lifted their head and tail segments into the air, despite lack of dorsal innervation. Nobody was expecting such a phenotype. Crawling seems to be much more complex than anticipated.

side mutants show considerably variable phenotypes, even in adjacent hemisegments. What do you think this tells us about how axon guidance works in flies?

HA At the beginning of the screen, in Corey Goodman’s lab, we discussed a lot what kind of phenotypes we might possibly find. One such idea was that we might find genes that affect only a single NMJ on a specific muscle fibre, because we imagined a key-and-lock mechanism for wiring 30 muscle fibres, where unique ligands on motor axons connect to cognate receptors on muscles. Inactivating such a receptor by point mutations should in theory prevent the formation of the associated NMJ. Unfortunately, we did not find this phenotypic class, nor did anybody else. We therefore think that motor axon guidance in Drosophila is not hard-wired by high-affinity ligand-receptor complexes but rather functions via co-operative actions of several guidance molecules. Newer finding in Pablo Labrador‘s laboratory also push this older idea originally developed in the Keshishian and Goodman labs. Guidance decisions therefore seem to be made at several points and sum up along the entire path. If several decisions go wrong in a row, phenotypes become noticeable.

Do the locomotion defects you found in larvae have anything to tell us about movement disorders in mammals?

HA Oh yes, I think this is one of the interesting parts of our story. Similar to Drosophila, there are only a few mammalian studies that correlate axon guidance errors with muscle innervation patterns. But these studies made several interesting observations. First, in mice, if a motor nerve branch fails to develop or is severely stalled, entire muscle fields are not innervated after birth causing muscle atrophy. In limbs, this can lead to paralysis and aberrant locomotion patterns. Second, the phenotypes are not necessarily symmetrical and occasionally affect only one side of the body, i.e. very similar to the unilateral defects observed in side mutants. Third, feet and ankles of affected limbs are occasionally twisted inward in newborn mice, a deformity highly reminiscent to congenital clubfoot in humans. The aetiology of clubfoot is still not fully understood, but since it frequently develops unilaterally, one speculative possibility is that it could develop due to innervation defects.

When doing the research, did you have any particular result or eureka moment that has stuck with you?

JK There was not one key moment that has stuck with me, but several small highlights, especially at the laser-scanning microscope. I am over and over again enthusiastic about how “beautiful” the axonal pattern in the embryo or larva is.  Further, I had such special moments when larvae showed particularly strong or unusual phenotypes during crawling, which looks sometimes quite funny.

Drosophila larva overexpressing Side in muscles and showing an extreme crawling phenotype.

And what about the flipside: any moments of frustration or despair?

JK Yes, there were some of these frustrating moments, especially handling living larvae for videography. During my research, I have realized that Drosophila larvae have sometimes their own mind, as they decided not to crawl at all or not to crawl in a straight line for the high-speed videography, but rather to crawl away from the nicely prepared agar block.

What next for you after this paper?

JK Since this paper is only a partial project of my PhD thesis, I plan for the next months to press ahead with another project for publication – hopefully we can submit the manuscript successfully at the end of this year.

And where will this work take the Aberle lab?

HA One direction we are heading is how locomotion in animals with hydrostatic skeletons works after all. Crawling behaviour is much more sophisticated and fine-tuned than it appears at first glance. We would like to understand how specific muscle groups contribute to particular movements and how this is antagonized by the liquid-filled body cavity.  Which muscle groups, for example, induce rolling escape behaviours during attacks of predatory wasps or coordinate jumping in some dipteran larvae. Ultimately we would like to find mutations or conditions which activate or inactivate particular movements, in order to better understand the underlying circuitry and machinery. Another line of research will certainly be the functional analysis of the entire Sidestep family. There are 7 Side paralogs in the Drosophila genome and virtually nothing is currently known about their functions.

Finally, let’s move outside the lab – what do you like to do in your spare time in Düsseldorf?

JK As I am a very water-loving person, I like to spend my spare time along the Rhine river – whether for a walk or to make myself comfortable on a blanket on its shores and let my soul dangle watching the ships passing by. I also like to take advantage of the city’s concert events, as two of my favourite bands, “Die Toten Hosen” and “Broilers”, come from Düsseldorf and regularly give concerts in the city. Furthermore, the whole laboratory and I like to celebrate the Düsseldorf Carnival, which takes place every spring.

HA Düsseldorf has a quite lively art scene, and since I enjoyed landscape photography very much during my undergraduate years, I am particularly drawn to the “Düsseldorf School of Photography”, founded by Bernd and Hilla Becher. Whenever there are exhibitions by Andreas Gursky, Axel Hütte, Thomas Ruff, to name a few, I try to not miss the vernissage. I also love to shop for coffee-table books in local stores.

Sidestep-induced neuromuscular miswiring causes severe locomotion defects in Drosophila larvae
Jaqueline C. Kinold, Carsten Pfarr, Hermann Aberle
Development 2018 145: dev163279 doi: 10.1242/dev.163279

This is #49 in our interview series. Browse the archive here.

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Welcome to our monthly trawl for developmental biology (and other related/just plain cool) preprints. 

This month we found a tonne of  papers dealing with various aspects of inheritance in worms, a flush of fly mechanics, and more single cell sequencing than you could shake a stick at. And as summer draws to a close, it’s raining cats and dogs (and wolves) in our ‘Why not…’ section.

The preprints were hosted on bioRxiv, PeerJ, and arXiv. Let us know if we missed anything, and use these links to get to the section you want:

Developmental biology

| Patterning & signalling

| Morphogenesis & mechanics

| Genes & genomes

| Stem cells, regeneration & disease modelling

Evo-devo & evo

Cell biology

Modelling

Tools & resources

Research practice & education

Why not…

Developmental biology

| Patterning & signalling

Formation of periodic pigment spots by the reaction-diffusion mechanism
Baoqing Ding, Erin L. Patterson, Srinidhi Holalu, Jingjian Li, Grace A. Johnson, Lauren E. Stanley, Anna B. Greenlee, Foen Peng, H. D. Bradshaw Jr., Benjamin K. Blackman, Yao-Wu Yuan

SOL1 and SOL2 Regulate Fate Transition and Cell Divisions in the Arabidopsis Stomatal Lineage
Abigail R Simmons, Kelli A Davies, Wanpeng Wang, Zhongchi Liu, Dominique C Bergmann

Paralogues of the PXY and ER receptor kinases enforce radial patterning in plant vascular tissue.
Ning Wang, Kristine S Bagdassarian, Rebecca E Doherty, Xiao Y Wang, Johannes T Kroon, Wei Wang, Ian H Jermyn, Simon R Turner, Peter Etchells

Maize EHD1 is Required for Kernel Development and Vegetative Growth through Regulating Auxin Homeostasis
Yafei Wang, Wenwen Liu, Hongqiu Wang, Qingguo Du, Zhiyuan Fu, Wen-Xue Li, Jihua Tang

A galling insect activates plant reproductive programs during gall development
Jack C Schultz, Patrick P Edger, Melanie JA Body, Heidi M Appel

The RopGEF KARAPPO is Essential for the Initiation of Vegetative Reproduction in Marchantia
Takuma Hiwatashi, Koh Li Quan, Yukiko Yasui, Hideyuki Takami, Masataka Kajikawa, Hiroyuki Kirita, Mayuko Sato, Mayumi Wakazaki, Katsushi Yamaguchi, Shuji Shigenobu, Hidehiro Fukaki, Tetsuro Mimura, Katsuyuki T. Yamato, Kiminori Toyooka, Shinichiro Sawa, Daisuke Urano, Takayuki Kohchi, Kimitsune Ishizaki

Xenopus hybrids provide insight into cell and organism size control
Romain Gibeaux, Kelly Miller, Rachael Acker, Taejoon Kwon, Rebecca Heald

EGFR signaling coordinates patterning with cell survival during Drosophila epidermal development
Samuel Henry Crossman, Sebastian J Streichan, Jean-Paul Vincent

Drosophila R8 photoreceptor cell subtype specification requires Notch and hibris.
Hong Tan, Ruth E Fulton, Wen-Hai Chou, Denise A Birkholz, Meridee P Mannino, David M Yamaguchi, Steven G Britt

PHASE TRANSITIONED NUCLEAR OSKAR PROMOTES CELL DIVISION OF DROSOPHILA PRIMORDIAL GERM CELLS
Kathryn E. Kistler, Tatjana Trcek, Thomas R. Hurd, Ruoyu Chen, Feng-Xia Liang, Joseph Sall, Masato Kato, Ruth Lehmann

tudor-domain containing protein 5-prime promotes male sexual identity in the Drosophila germline and is repressed in females by Sex lethal
Shekerah Primus, Caitlin Pozmanter, Kelly Baxter, Mark Van Doren

ELYS coordinates NF-κB pathway dynamics during development in Drosophila
Saurabh Jayesh Kumar Mehta, Vimlesh Kumar, Ram Kumar Mishra

Dual role of Bnl/Fgf signaling in proliferation and endoreplication of Drosophila tracheal adult progenitor cells
Xavier Franch-Marro, Cristina de miguel, Josefa Cruz, David Martín

A screen for targets of the Drosophila pseudokinase Tribbles identifies Neuralized and Mindbomb, ubiquitin ligases that mediate Notch signaling
Anna Shipman, Christopher Nauman, Britney Haymans, Rachel Silverstein, Leonard Dobens Jr.

Neuronal constituents and putative interactions within the Drosophila ellipsoid body neuropil
Jaison Jiro Omoto, Bao-Chau Minh Nguyen, Pratyush Kandimalla, Jennifer Kelly Lovick, Jeffrey Michael Donlea, Volker Hartenstein

Staufen2 mediated RNA recognition and localization requires combinatorial action of multiple domains
Simone Heber, Imre Gaspar, Jan-Niklas Tants, Johannes Günther, Sandra M Fernández Moya, Robert Janowski, Anne Ephrussi, Michael Sattler, Dierk Niessing

CTP synthase regulation by miR-975 controls cell proliferation and differentiation in Drosophila melanogaster
Wai-Kan Woo, Najat Dzaki, Ghows Azzam

Neuropeptides required for Drosophila development under nutritional stress are regulated by the ER-Ca2+ sensor STIM
Megha M, Christian Wegener, Gaiti Hasan

Deterministic Nature of Cellular Position Noise During C. elegans Embryogenesis
Xiaoyu Li, Zhiguang Zhao, Weina Xu, Rong Fan, Long Xiao, Xuehua Ma, Zhuo Du

MicroRNA regulation of BMP signaling; cross-talk between endothelium and vascular smooth muscle cells
Charlene Watterston, Lei Zeng, Abidemi Onabadejo, Sarah J Childs

Wnt/Fgf crosstalk is required for the specification of tracheal basal progenitor cells
Zhili Hou, Qi Wu, Xin Sun, Huaiyong Chen, Yu Li, Yongchun Zhang, Munemasa Mori, Ying Yang, Ming Jiang, Jianwen Que

WNT ligands stimulate transient signaling in human pluripotent cells and synergize with TGF-β ligands to stimulate sustained signaling during differentiation
Joseph Massey, Yida Liu, Omar Alvarenga, Teresa Saez, Matthew Schmerer, Aryeh Warmflash

EGFR confers exquisite specificity of Wnt9a-Fzd9b signaling in hematopoietic stem cell development
Stephanie Grainger, Nicole Nguyen, Jenna Richter, Jordan Setayesh, Brianna Lonquich, Chet Huan Oon, Jacob M Wozniak, Rocio Barahona, Caramai N. Kamei, Jack Houston, Marvic Carrillo-Terrazas, Iain A. Drummond, David Gonzalez, Karl Willert, David Traver

Foxp1 controls neural stem cell competence and bias towards deep layer cortical fate.
Caroline Alayne Pearson, Destaye Moore, Haley Tucker, Joseph Dekker, Hui Hu, Amaya Miquelajáuregui, Bennett Novitch

Sequential Specification of Oligodendrocyte and NG2 Cell Fates by Distinct Levels of Hedgehog Signaling
Bruce Appel, Andrew Ravanelli, Christina Kearns, Rani Powers, Yuying Wang, Jacob Hines, Maranda Donaldson

The endosomal sorting adaptor HD-PTP is required for ephrin-B:EphB signalling in cell collapse and motor axon guidance
Sylvie Lahaie, Daniel Morales, Halil Bagci, Noumeira Hamoud, Charles-Etienne Castonguay, Jalal M Kazan, Guillaume Desrochers, Avihu Klar, Anne-Claude Gingras, Arnim Pause, Jean-François Côté, Artur Kania

Conserved cell types with divergent features between human and mouse cortex
Rebecca D Hodge, Trygve E Bakken, Jeremy A Miller, Kimberly A Smith, Eliza R Barkan, Lucas T Graybuck, Jennie L Close, Brian Long, Osnat Penn, Zizhen Yao, Jeroen Eggermont, Thomas Hollt, Boaz P Levi, Soraya I Shehata, Brian Aevermann, Allison Beller, Darren Bertagnolli, Krissy Brouner, Tamara Casper, Charles Cobbs, Rachel Dalley, Nick Dee, Song-Lin Ding, Richard G Ellenbogen, Olivia Fong, Emma Garren, Jeff Goldy, Ryder P Gwinn, Daniel Hirschstein, C Dirk Keene, Mohamed Keshk, Andrew L Ko, Kanan Lathia, Ahmed Mahfouz, Zoe Maltzer, Medea McGraw, Thuc Nghi Nguyen, Julie Nyhus, Jeffrey G Ojemann, Aaron Oldre, Sheana Parry, Shannon Reynolds, Christine Rimorin, Nadiya V Shapovalova, Saroja Somasundaram, Aaron Szafer, Elliot R Thomsen, Michael Tieu, Richard H Scheuermann, Rafael Yuste, Susan M Sunkin, Boudewijn Lelieveldt, David Feng, Lydia Ng, Amy Bernard, Michael Hawrylycz, John Phillips, Bosiljka Tasic, Hongkui Zeng, Allan R Jones, Christof Koch, Ed S Lein

Molecular recording of mammalian embryogenesis
Michelle Chan, Zachary D Smith, Stefanie Grosswendt, Helene Kretzmer, Thomas Norman, Britt Adamson, Marco Jost, Jeffrey J Quinn, Dian Yang, Alexander Meissner, Jonathan S Weissman

The Warburg effect and lactate signaling augment Fgf signaling to promote sensory-neural development in the otic vesicle
Bruce Riley, Husniye Kantarci, Yunzi Gou

Nell2 regulates the contralateral-versus-ipsilateral visual projection as a layer-specific positional cue
Chizu Nakamoto, Elaine Durward, Masato Horie, Masaru Nakamoto

mRNA localisation in endothelial cells regulates blood vessel sprouting
Guilherme Costa, Nawseen Tarannum, Shane Herbert

Planar cell polarity pathway and development of the human visual cortex
Jean Shin, Shaojie Ma, Edith Hofer, Yash Patel, Gennady Roshchupkin, Andre M Sousa, Xueqiu Jian, Rebecca Gottesmann, Thomas H Mosley, Myriam Fornage, Yasaman Saba, Lukas Pirpamer, Reinhold Schmidt, Helena Schmidt, Bernard Mazoyer, Amaia Carrion-Castillo, Joshua Bis, Shuo Li, Qiong Yang, Michelle Luciano, Sherif Karama, Lindsay Lewis, Mark Bastin, Matthew A Harris, Ian Deary, Joanna M Wardlaw, Markus Scholz, Markus Loeffler, Veronica Witte, Frauke Beyer, Arno Villringer, Hieab HHH Adams, M Arfan Ikrum, William S Kremen, Nathan A Gillespie, Nenad Sestan, Zdenka Pausova, Sudha Seshadri, Tomas Paus

Yes-associated protein (YAP) is required in maintaining normal ovarian follicle development and function
Michele Plewes, Xiaoying Hou, Pan Zhang, Jennifer Wood, Andrea Cupp, John Davis

Developmental Effects of the Pesticide Imidacloprid on Zebrafish Body Length and Mortality
Akshay Krishnan, Christin Clyburn, Patrick Newcombe

Myocardial Notch-Rbpj deletion does not affect heart development or function
Alejandro Salguero-Jiménez, Joaquim Grego-Bessa, Gaetano D’Amato, Luis Jesús Jiménez-Borreguero, Jose Luis de la Pompa

Synchronization of Hes1 oscillations coordinate and refine condensation formation and patterning of the avian limb skeleton
Ramray Bhat, Tilmann Glimm, Marta Linde-Medina, Cheng Cui, Stuart Newman

Reduced insulin/IGF-1 signalling in adult parents increases offspring fitness
Martin I Lind, Sanjana Ravindran, Zuzana Sekajova, Hanne Carlsson, Andrea Hinas, Alexei A Maklakov

Bacterial community dynamics during embryonic and larval development of three confamilial echinoids
Tyler Carrier, Adam Reitzel

| Morphogenesis & mechanics

Hydraulic control of embryo size, tissue shape and cell fate
Chii Jou Chan, Maria Costanzo, Teresa Ruiz-Herrero, Gregor Monke, Ryan Petrie, L Mahadevan, Takashi Hiiragi

Brain folding is initiated by mechanical constraints without a cellular pre-pattern
Andrew K Lawton, Tyler Engstrom, Daniel Rohrbach, Masaaki Omura, Daniel H Turnbull, Jonathan Mamou, Teng Zhang, Jennifer M Schwarz, Alexandra L Joyner

Ectopic expression of Hoxb1 induces cardiac and craniofacial malformations
Stéphane Zaffran, Gaelle Odelin, Sonia Stefanovic, Fabienne Lescroart, Heather Etchevers

Unique morphogenetic signatures define mammalian neck muscles and associated connective tissues
Eglantine Heude, Marketa Tesarova, Elizabeth M. Sefton, Estelle Jullian, Noritaka Adachi, Alexandre Grimaldi, Tomas Zikmund, Jozef Kaiser, Gabrielle Kardon, Robert Kelly, Shahragim Tajbakhsh

Basolateral localization of MMP14 drives apicobasal polarity change during EMT independently of its catalytic activity
Cyril Andrieu, Audrey Montigny, Dominique Alfandari, Eric Theveneau

Epigenetic inactivation of miR-203 as a key step in neural crest epithelial-to-mesenchymal transition
Estefania Sanchez-Vasquez, Marianne Bronner, Pablo Hernan Strobl-Mazzulla

Cdc42 negatively regulates endocytosis during apical plasma membrane maintenance and development in mouse tubular organs in vivo
Akiko Shitara, Lenka Malec, Seham Ebrahim, Desu Chen, Christopher Bleck, Matthew P Hoffman, Roberto Weigert

Genetic control of cellular morphogenesis in Müller glia
Mark Charlton-Perkins, Alexandra D Almeida, Ryan B MacDonald, William A Harris

Fndc3a (Fibronectin Domain Containing Protein 3A) influences median fin fold development and caudal fin regeneration in zebrafish by ECM alteration.
Daniel Liedtke, Melanie Orth, Michelle Meissler, Sinje Geuer, Sabine Knaup, Isabell Koblitz, Eva Klopocki

The transmembrane protein Crb2a regulates cardiomyocyte apicobasal polarity and adhesion in zebrafish
Jimenez-Amilburu Vanesa, Didier Y.R. Stainier

Zebrafish Otolith Biomineralization Requires Polyketide Synthase
Kevin D Thiessen, Lisa Higuchi, Kenneth L Kramer

Arterio-Venous Remodeling in the Zebrafish Trunk Is Controlled by Genetic Programming and Flow-Mediated Fine-Tuning
Ilse Geudens, Baptiste Coxam, Silvanus Alt, Veronique Gebala, Anne-Clemence Vion, Andre Rosa, Holger Gerhardt

Tbx1 regulates extracellular matrix-cell interactions in the second heart field.
Daniela Alfano, Alessandra Altomonte, Claudio Cortes, Marchesa Bilio, Robert G Kelly, Antonio Baldini

Abnormalities of placental development and function are associated with the different fetal growth patterns of hypoplastic left heart syndrome and transposition of the great arteries.
Weston Troja, Kathryn J Owens, Jennifer Courtney, Andrea C Hinton, Robert B Hinton, James F Cnota, Helen N Jones

Polarity signaling ensures epidermal homeostasis by coupling cellular mechanics and genomic integrity
Martim Dias Gomes, Soriba Letzian, Michael Saynisch, Sandra Iden

Morphogenesis of neurons and glia within an epithelium
Isabel I. C. Low, Claire R. Williams, Megan K. Chong, Ian G. McLachlan, Bradley M. Wierbowski, Irina Kolotuev, Maxwell G. Heiman

Aurora B is required for programmed variations of cytokinesis during morphogenesis in the C. elegans embryo
Xiaofei Bai, Po-Yi Lee, Chin-Yi Chen, James R. Simmons, Benjamin Nebenfuehr, Diana Mitchell, Lindsey R Klebanow, Nicholas Mattson, Christopher G Sorensen Turpin, Bi-Chang Chen, Eric Betzig, Joshua N Bembenek

Regulation of tensile stress in response to external forces coordinates epithelial cell shape transitions with organ growth and elongation
Ramya Balaji, Vanessa Weichselberger, Anne-Kathrin Classen

Actomyosin-driven tension at compartmental boundaries orients cell division independently of cell geometry in vivo
Elena Scarpa, Cedric Finet, eGuy Blanchard, Benedicte Sanson

Distinct contributions of tensile and shear stress on E-cadherin levels during morphogenesis
Girish R Kale, Xingbo Yang, Jean-Marc Philippe, Madhav Mani, Pierre-Francois Lenne, Thomas Lecuit

3D Tissue elongation via ECM stiffness-cued junctional remodeling
Dong-Yuan Chen, Justin Crest, Sebastian J Streichan, David Bilder

A Fasciclin 2 functional switch controls organ size in Drosophila
Emma Velasquez, Jose A Gomez-Sanchez, Emmanuelle Donier, Carmen Grijota-Martinez, Hugo Cabedo, Luis A Garcia-Alonso

Morphogenetic processes as data: Quantitative structure in the Drosophila eye imaginal disc
Bradly Alicea, Thomas E Portegys, Diana Gordon, Richard Gordon

KATANIN-dependent mechanical properties of the stigmatic cell wall regulate pollen tube pathfinding
Lucie Riglet, Frederique Rozier, Chie Kodera, Isabelle Fobis-Loisy, Thierry Gaude

| Genes & genomes

Sensory neurons control heritable adaptation to stress through germline reprogramming
Zuco Giusy, Vikas Kache, Pedro Robles, Jyotiska Chaudhuri, Beth Hill, Christine Bateson, Andre Pires da Silva

Alterations in sperm long RNA contribute to the epigenetic inheritance of the effects of postnatal trauma
Katharina Gapp, Gretchen van Steenwyk, Pierre-Luc Germain, Wayo Matsushima, Konrad Rudolph, Francesca Manuella, Martin Roszkowski, Gregoire Vernaz, Tanay Gosh, Pawel Pelczar, Isabelle M Mansuy, Eric Miska

H3K9me3 is Required for Transgenerational Inheritance of Small RNAs that Target a Unique Subset of Newly Evolved Genes
Itamar Lev, Hila Gingold, Oded Rechavi

HERI-1 is a Chromodomain Protein that Negatively Regulates Transgenerational Epigenetic Inheritance
Roberto Perales, Daniel Pagano, Gang Wan, Brandon Fields, Arneet L. Saltzman, Scott Kennedy

Transgenerational sterility of Piwi pathway mutants in response to germ granule dysfunction
Katherine Kretovich Billmyre, Bree Heestand, Maya Spichal, Stephen Frenk, Shawn Ahmed

Nematode germ granule assembly is linked to mRNA repression
Scott T Aoki, Sarah L Crittenden, Tina R Lynch, Craig A Bingman, Marvin Wickens, Judith Kimble

Gene silencing by double-stranded RNA from C. elegans neurons reveals functional mosaicism of RNA interference
Snusha Ravikumar, Sindhuja Devanapally, Antony M Jose

Trans-splicing of the C. elegans let-7 primary transcript developmentally regulates let-7 microRNA biogenesis and let-7 family microRNA activity
Charles Nelson, Victor Ambros

Multi-modal regulation of C. elegans hermaphrodite spermatogenesis by the GLD-1-FOG-2 complex
Shuang Hu, Lauren E. Ryan, Ebru Kaymak, Lindsay Freeberg, Te-Wen Lo, Scott Kuersten, Sean P. Ryder, Eric S. Haag

C. elegans exhibits coordinated oscillation in gene activation in single-cell developmental data
Luke A. D. Hutchison, Bonnie Berger, Isaac Kohane

Tissue- and sex-specific small RNAomes reveal sex differences in response to the environment
Alexandra Bezler, Fabian Braukmann, Sean West, Arthur Duplan, Raffaell Conconi, Frederic Schuetz, Pierre Goenczy, Fabio Piano, Kristin Gunsalus, Eric Miska, Laurent Keller

Identification of functional long non-coding RNAs in C. elegans
Alper Akay, David Jordan, Isabela C. Navarro, Tomasz Wrzesinski, Chris P. Ponting, Eric A. Miska, Wilfried Haerty

Necessity and contingency in developmental genetic screens: LIN-3, Wnt and semaphorin pathways in vulval induction of the nematode Oscheius tipulae
Marie-Anne Félix, Amhed Missael Vargas Velazquez, Fabrice Besnard

A bipartite boundary element restricts UBE3A imprinting to mature neurons.
Jack S Hsiao, Noelle D Germain, Andrea Wilderman, Christopher Stoddard, Luke A Wojenski, Geno J Villafano, Leighton Core, Justin Cotney, Stormy J Chamberlain

Single-cell transcriptome analysis of human, marmoset and mouse embryos reveals common and divergent features of preimplantation development
Thorsten Boroviak, Giuliano G Stirparo, Sabine Dietmann, Irene H Herraez, Hisham Mohammed, Wolf Reik, Austin Smith, Erika Sasaki, Jennifer Nichols, Paul Bertone

Complex cell-state changes revealed by single cell RNA sequencing of 76,149 microglia throughout the mouse lifespan and in the injured brain
Timothy R Hammond, Connor Dufort, Lasse Dissing-Olesen, Stefanie Giera, Adam Young, Alec Wysoker, Alec J Walker, Michael Segel, James Nemesh, Arpiar Saunders, Evan Macosko, Robin JM Franklin, Xianhua Piao, Steve McCarroll, Beth Stevens

A single cell transcriptomic analysis of human neocortical development
Damon Polioudakis, Luis de la Torre-Ubieta, Justin Langerman, Andrew G Elkins, Jason L Stein, Celine K Vuong, Carli K Opland, Daning Lu, William Connell, Elizabeth K Ruzzo, Jennifer K Lowe, Tarik Hadzic, Flora I Hinz, Shan Sabri, William E Lowry, Kathrin Plath, Daniel H Geschwind

Single-cell RNA-seq reveals dynamic transcriptome profiling in human early neural differentiation
Zhouchun Shang, Dongsheng Chen, Quanlei Wang, Shengpeng Wang, Qiuting Deng, Liang Wu, Chuanyu Liu, Xiangning Ding, Shiyou Wang, Jixing Zhong, Doudou Zhang, Xiaodong Cai, Shida Zhu, Huanming Yang, Longqi Liu, J. Lynn Fink, Fang Chen, Xiaoqing Liu, Zhengliang Gao, Xun Xu

Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex
Nereo Kalebic, Carlotta Gilardi, Mareike Albert, Takashi Namba, Katherine R. Long, Milos Kostic, Barbara Langen, Wieland B. Huttner

Single cell dynamics of embryonic muscle progenitor cells in zebrafish
Priyanka Sharma, Tyler D Ruel, Katrinka M Kocha, Shan Liao, Peng Huang

Epigenetic factors coordinate intestinal development
Julia Ganz, Ellie Melancon, Catherine Wilson, Angel Amores, Peter Batzel, Marie Strader, Ingo Braasch, Parham Diba, Julie A Kuhlman, John H Postlethwait, Judith S Eisen

Single-cell RNA-seq reveals distinct dynamic behavior of sex chromosomes during early human embryogenesis
Qing Zhou, Taifu Wang, Lizhi Leng, Wei Zheng, Jinrong Huang, Fang Fang, Ling Yang, Jian Wang, Huanming Yang, Fang Chen, Ge Lin, Wen-Jing Wang, Karsten Kristiansen

Single cell RNA-seq study of wild type and Hox9,10,11 mutant developing uterus
S. Steven Potter, Michael L. Mucenski, Robert Mahoney, Mike Adam, Andrew S. Potter

MiR-505-3p is a Repressor of the Puberty Onset in Female Mice
Yuxun Zhou, li tong, maochun wang, xueying chang, sijia wang, kai li, Junhua Xiao

An Evolutionarily Conserved piRNA-producing Locus Required for Male Mouse Fertility
Pei-Hsuan Wu, Yu Fu, Katharine Cecchini, Deniz M Ozata, Zhiping Weng, Phillip D Zamore

Genetic deletion of genes in the cerebellar rhombic lip lineage can stimulate compensation through adaptive reprogramming of ventricular zone-derived progenitors
Alexandre Wojcinski, Morgane Morabito, Andrew K Lawton, Daniel N Stephen, Alexandra L Joyner

Mapping Transgene Insertion Sites Reveals Complex Interactions Between Mouse Transgenes And Neighboring Endogenous Genes
Mallory A Laboulaye, Xin Duan, Mu Qiao, Irene E Whitney, Joshua Sanes

An homeotic post-transcriptional network controlled by the RNA-binding protein RBMX
Paola Zuccotti, Daniele Peroni, Valentina Potrich, Alessandro Quattrone, Erik Dassi

KLF4 binding during reprogramming is involved in 3D architectural rewiring and transcriptional regulation of enhancer hubs
Dafne Campigli Di Giammartino, Yiyuan Liu, Andreas Kloetgen, Alexander Prokopios Polyzos, Daleum Kim, Matthias Stadtfeld, Aristotelis Tsirigos, Effie Apostolou

Analysis of novel domain-specific mutations in the zebrafish ndr2/cyclops gene generated using CRISPR-Cas9 RNPs
Ashley N Turner, Reagan S Andersen, Ivy E Bookout, Lauren N Brashear, James C Davis, David M Gahan, John P Gotham, Baraa A Hijaz, Ashish S Kaushik, Jordan B McGill, Victoria L Miller, Zachariah P Moseley, Cerissa L Nowell, Riddhi K Patel, Mia C Rodgers, Yazen A Shihab, Austin P Walker, Sarah R Glover, Samantha D Foster, Anil Kumar Challa

Compensatory mechanisms render Tcf7l1a dispensable for eye formation despite its requirement in eye field specification
Rodrigo M Young, Florencia Cavodeassi, Thomas A Hawkins, Heather L Stickney, Quenten Schwarz, Lisa M Lawrence, Claudia Wierzbicki, Gaia Gestri, Elizabeth Mayela Ambrosio, Allison Klosner, Jasmine Rowell, Isaac H. Bianco, Miguel L Allende, Stephen W Wilson

Myc is dispensable for cardiac development in the mouse but rescues Mycn-deficient hearts through functional replacement and cell competition
Noelia Muñoz-Martín, Rocío Sierra, Thomas Schimmang, Cristina Villa del Campo, Miguel Torres

The splicing regulator Prp31 prevents retinal degeneration in Drosophila by regulating Rhodopsin levels
Malte Lehmann, Sarita Hebbar, Sarah Behrens, Weihua Leng, Michaela Yuan, Sylke Winkler, Elisabeth Knust

Asymmetric histone incorporation during DNA replication in Drosophila male germline stem cells
Matthew Wooten, Jonathan Snedeker, Zehra Nizami, Xinxing Yang, Elizabeth Urban, Xinyu Ashlee Feng, Jee Min Kim, Joseph Gall, Jie Xiao, Xin Chen

Deterministic splicing of Dscam2 is regulated by Muscleblind
Joshua Shing Shun Li, S Sean Millard

Effects of the maternal factor Zelda on zygotic enhancer activity in the Drosophila embryo
Xiao-Yong Li, Michael B Eisen

Computations performed by shadow enhancers and enhancer duplications vary across the Drosophila embryo
Clarissa Scholes, Kelly M Biette, Timothy T Harden, Angela H DePace

Chromatin architecture reorganisation during neuronal cell differentiation in Drosophila genome
Keerthi T Chathoth, Nicolae Radu Zabet

SWI/SNF chromatin remodeling controls Notch-responsive enhancer accessibility
Zoe Pillidge, Sarah J. Bray

A variably imprinted epiallele impacts seed development
Daniela Pignatta, Katherine Novitzky, P.R. V. Satyaki, Mary Gehring

Over-expression of the photoperiod response regulator ZmCCT10 modifies plant architecture, flowering time and inflorescence morphology in maize
Elizabeth Stephenson, Stacey Estrada, Xin Meng, Jesse Ourada, Michael G Muszynski, Jeffrey E Habben, Olga Danilevskaya

Maize YABBY drooping leaf genes regulate floret development and floral meristem determinacy
Josh Strable, Erik Vollbrecht

Methyl-CpG-binding domain 9 (MBD9) is required for H2A.Z incorporation into chromatin at a subset of H2A.Z-enriched regions in the Arabidopsis genome
Paja Sijacic, Dylan H Holder, Marko Bajic, Roger B. Deal

Functional dissection of the ARGONAUTE7 promoter
J Steen Hoyer, Jose L Pruneda-Paz, Ghislain Breton, Mariah A Hassert, Emily E Holcomb, Halley Fowler, Kaylyn M Bauer, Jacob Mreen, Steve A Kay, James C Carrington

A Genome-Wide Association Study Reveals a Novel Regulator of Ovule Number and Fertility in Arabidopsis thaliana
Jing Yuan, Sharon A Kessler

A transmissible RNA pathway in honey bees
Eyal Maori, Yael Garbian, Vered Kunik, Rita Mozes-Koch, Osnat Malka, Haim Kalev, Niv Sabath, Ilan Sela, Sharoni Shafir

| Stem cells, regeneration & disease modelling

The RNA-Binding Protein DND1 Acts Sequentially as a Negative Regulator of Pluripotency and a Positive Regulator of Epigenetic Modifiers Required for Germ Cell Reprogramming
Victor A Ruthig, Matthew B Friedersdorf, Jason A Garness, Steve C Munger, Corey Bunce, Jack D Keene, Blanche Capel

Delayed aneuploidy stress response of neural stem cells impairs adult lifespan in flies
Mihailo Mirkovic, Leonardo G Guilgur, Diogo Passagem-Santos, Raquel A Oliveira

Drosophila small ovary gene ensures germline stem cell maintenance and differentiation by silencing transposons and organising heterochromatin
Ferenc Jankovics, Melinda Bence, Rita Sinka, Aniko Farago, Laszlo Bodai, Aladar Pettko-Szandtner, Karam Ibrahim, Zsanett Takacs, Alexandra B. Szarka-Kovacs, Miklos Erdelyi

Epigenetic analyses of planarian stem cells demonstrate conservation of bivalent histone modifications in animal stem cells.
Anish Dattani, Damian Kao, Yuliana Mihaylova, Prasad Abnave, Samantha Hughes, Alvina Lai, Sounak Sahu, Aziz Aboobaker

Nucleosome dynamics of human iPSC during the early stages of neurodevelopment
Janet C Harwood, Nicholas A Kent, Nicholas D Allen, Adrian J Harwood

Gene Correction for SCID-X1 in Long-Term Hematopoietic Stem Cells
Mara Pavel-Dinu, Volker Wiebking, Beruh T Dejene, Waracharee Srifa, Sruthi Mantri, Carmencita Nicolas, Ciaran Lee, Gang Bao, Eric J Kildebeck, Niraj Punjya, Camille Sindhu, Matthew A Inlay, Nivi Saxena, Suk See DeRavin, Harry Malech, Maria Grazia Roncarolo, Kenneth I Weinberg, Matthew Porteus

Human pluripotent stem cell-derived brain pericyte-like cells induce blood-brain barrier properties
Matthew J Stebbins, Benjamin D Gastfriend, Scott G Canfield, Ming-Song Lee, Drew Richards, Madeline G Faubion, Wan-Ju Li, Richard Daneman, Sean P Palecek, Eric V Shusta

Signalling pathways drive heterogeneity of ground state pluripotency
Kirsten R McEwen, Sarah Linnett, Harry G Leitch, Prashant Srivastava, Lara Al-Zouabi, Tien-Chi Huang, Maxime Rotival, Alex Sardini, Thalia E Chan, Sarah Filippi, Michael Stumpf, Enrico Petretto, Petra Hajkova

Need for high-resolution Genetic Analysis in iPSC: Results and Lessons from the ForIPS Consortium
Bernt Popp, Mandy Krumbiegel, Janina Grosch, Annika Sommer, Steffen Uebe, Zacharias Kohl, Sonja Ploetz, Michaela Farrell, Udo Trautmann, Cornelia Kraus, Arif B Ekici, Reza Asadollahi, Martin Regensburger, Katharina Guenther, Anita Rauch, Frank Edenhofer, Juergen Winkler, Beate Winner, Andre Reis

Inter-species differences in response to hypoxia in iPSC-derived cardiomyocytes from humans and chimpanzees
Michelle C Ward, Yoav Gilad

Synthetic and genomic regulatory elements reveal aspects of cis-regulatory grammar in Mouse Embryonic Stem Cells
Dana M King, Brett B. Maricque, Barak A. Cohen

Cerebrovascular Injuries Induce Lymphatic Invasion into Brain Parenchyma to Guide Vascular Regeneration in Zebrafish
Jingying Chen, Jianbo He, Qifen Yang, Yaoguang Zhang, Lingfei Luo

A human cell model of cardiac pathophysiological valvulogenesis
Tui Neri, Emylie Hiriart, Piet Van Vliet, Emilie Faure, Russel Norris, Batoul Farhat, Julie Lefrancois, Thomas Moore-Morris, Stephane Zaffran, Randolph Faustino, Alexander Zambon, Jean-Pierre Devisgnes, David Salgado, Yukiko Sugi, Robert Levine, Jose Luis de la Pompa, Andre Terzic, Sylvia Evans, Roger Markwald, michel Puceat

Metformin Intervention Prevents Cardiac Dysfunction in a Murine Model of Adult Congenital Heart Disease
Mauro W. Costa, Julia C. Wilmanns, Raghav Pandey, Olivia Hon, Anjana Chandran, Jan M. Schilling, Qizhu Wu, Gael Cagnone, Preeti Bais, Vivek Phillip, Heidi Kocalis, Stuart K. Archer, James T. Pearson, Mirana Ramialison, Joerg Heineke, Hemal H. Patel, Nadia A. Rosenthal, Milena B. Furtado

Regeneration-Associated Cells Improve Recovery from Myocardial Infarction through Enhanced Vasculogenesis, Anti-inflammation, and Cardiomyogenesis
Amankeldi A Salybekov, Akira T Kawaguchi, Haruchika Masuda, Kosit Vorateera, Chisa Okada, Takayuki Asahara

Evidence for minimal cardiogenic potential of Sca-1 positive cells in the adult mouse heart
Lauren E. Neidig, Florian Weinberger, Nathan J. Palpant, John Mignone, Amy M. Martinson, Daniel Sorensen, Ingrid Bender, Natsumi Nemoto, Hans Reinecke, Lil Pabon, Jeffery D Molkentin, Charles E. Murry, Jop van Berlo

Recapitulating bone development for tissue regeneration through engineered mesenchymal condensations and mechanical cues
Anna M. McDermott, Samuel Herberg, Devon E. Mason, Hope B. Pearson, James H. Dawahare, Joseph M. Collins, Rui Tang, Amit Patwa, Mark W. Grinstaff, Daniel J. Kelly, Eben Alsberg, Joel D. Boerckel

De novo genesis of retinal ganglion cells by targeted expression of KLF4 in vivo
Mauricio Rocha-Martins, Beatriz C de Toledo, Pedro L Santos-Franca, Viviane M Oliveira-Valenca, Carlos Henrique H Vieira e Vieira, Gabriel E Matos-Rodrigues, Rafael Linden, Caren Norden, Rodrigo A P Martins, Mariana S Silveira

Mesenchymal stem cells protect retinal ganglion cells from degeneration via mitochondrial donation
Dan JIANG, Hong Feng, Zhao Zhang, Bin Yan, Ling Chen, Chuiyan Ma, Cheng Li, Shuo Han, Yuelin Zhang, Peikai Chen, Hung-Fat Tse, Qingling Fu, Kin Chiu, Qizhou Lian

CDK inhibitors reduce cell proliferation and reverse hypoxia-induced metastasis of neuroblastoma tumours in a chick embryo model
Rasha R Swadi, Keerthika Sampat, Anne Herrmann, Paul D Losty, Violaine See, Diana Moss

Comprehensive modeling of Spinal Muscular Atrophy in Drosophila melanogaster
Ashlyn M. Spring, Amanda C. Raimer, Christine D. Hamilton, Michela J. Schillinger, A. Gregory Matera

Modeling motor neuron resilience in ALS using stem cells
Ilary Allodi, Jik Nijssen, Julio Cesar Aguila Benitez, Gillian Bonvicini, Ming Cao, Eva Hedlund

Genome-wide chromatin accessibility and transcriptome profiling show minimal epigenome changes and coordinated transcriptional dysregulation of hedgehog signaling in Danforth’s short tail mice
Peter Orchard, James S. White, Peedikayil E. Thomas, Anna Mychalowych, Anya Kiseleva, John Hensley, Benjamin Allen, Stephen C.J. Parker, Catherine E. Keegan

Enhanced axonal Neuregulin-1 type-III signaling ameliorates disease severity in a CMT1B mouse model
Cristina Scapin, Cinzia Ferri, Emanuela Pettinato, Désiree Zambroni, Francesca Bianchi, Sophie Belin, Ubaldo Del Carro, Nico Mitro, Donatella Caruso, Marta Pellegatta, Carla Taveggia, Markus H. Schwab, Klaus-Armin Nave, Maria Laura Feltri, Lawrence Wrabetz, Maurizio D’Antonio

Evo-devo & evo

Ankyrin domain encoding genes resulting from an ancient horizontal transfer are functionally integrated into developmental gene regulatory networks in the wasp Nasonia
Jeremy Lynch, Daniel Pers

A large-scale systemic RNAi screen in the red flour beetle Tribolium castaneum identifies novel genes involved in arthropod muscle development
Dorothea Schultheis, Matthias Weißkopf, Christoph Schaub, Salim Ansari, Van-Anh Dao, Daniela Grossmann, Upalparna Majumdar, Muhammad Salim Din Muhammad, Nicole Troelenberg, Tobias Richter, Christian Schmitt-Engel, Jonas Schwirz, Nadia Ströhlein, Matthias Teuscher, Gregor Bucher, Manfred Frasch

RNAi screen in Tribolium reveals involvement of F-BAR proteins in myoblast fusion and visceral muscle morphogenesis in arthropods
Dorothea Schultheis, Jonas Schwirz, Manfred Frasch

Decoupling from yolk sac is required for extraembryonic tissue spreading in the scuttle fly Megaselia abdita.
Francesca Caroti, Everardo González Avalos, Viola Noeske, Paula González Avalos, Dimitri Kromm, Maike Wosch, Lucas Schütz, Lars Hufnagel, Steffen Lemke

Influence of temperature on the development, reproduction and regeneration in the flatworm model organism Macrostomum lignano
Jakub Wudarski, Kirill Ustyantsev, Lisa Glazenburg, Eugene Berezikov

DEVELOPMENTAL DYNAMICS OF GREEN FLUORESCENT CHROMATOPHORES IN THE DAGGERBLADE GRASS SHRIMP, PALAEMONETES PUGIO HOLTHUIS, 1949 (DECAPODA, CARIDEA, PALAEMONIDAE)
Michael P Phelps

Proliferation of Superficial Neuromasts During Lateral Line Development in the Round Goby, Neogobius melanostomus
Juleen Dickson, John A Janssen

Clownfishes are a genetic model of exceptional longevity and reveal molecular convergence in the evolution of lifespan
Arne Sahm, Pedro Almaida-Pagan, Martin Bens, Mirko Mutalipassi, Alejandro Lucas-Sanchez, Jorge de Costa Ruiz, Matthias Goerlach, Alessandro Cellerino

Choanoflagellate transfection illuminates their cell biology and the ancestry of animal septins
David Booth, Heather Middleton, Nicole King

Glycosyltransferases promote development and prevent promiscuous cell aggregation in the choanoflagellate S. rosetta
Laura Wetzel, Tera Levin, Ryan E Hulett, Daniel Chan, Grant King, Reef Aldayafleh, David Booth, Monika Abedin Sigg, Nicole King

Adaptive evolution of animal proteins over development: support for the Darwin selection opportunity hypothesis of Evo-Devo
Jialin Liu, Marc Robinson-Rechavi

Phenotypic Effects of Somatic Mutations Accumulating during Vegetative Growth
Mitch Cruzan, Matthew Streisfeld, Jaime Schwoch

An integrative genomic analysis of the Longshanks selection experiment for longer limbs in mice
João L. P. Castro, Michelle N. Yancoskie, Marta Marchini, Stefanie Belohlavy, Marek Kučka, William H. Beluch, Ronald Naumann, Isabella Skuplik, John Cobb, Nick H Barton, Campbell Rolian, Yingguang Frank Chan

Adaptive evolution of sperm proteins depends on sperm competition in a pair of Lepidoptera
Andrew J. Mongue, Megan E. Hansen, Liuqi Gu, Clyde E. Sorenson, James R. Walters

Evolutionary proteomics reveals distinct patterns of complexity and divergence between lepidopteran sperm morphs
Emma Whittington, Tim Karr, Andrew J Mongue, Steve Dorus, James Walters

Non-linear phenotypic variation uncovers the emergence of heterosis in Arabidopsis thaliana
Francois VASSEUR, Louise Fouqueau, Dominique de Vienne, thibault nidelet, Cyrille Violle, Detlef Weigel

Repeated evolution of asexuality involves convergent gene expression changes
Darren J Parker, Jens Bast, Kirsten Jalvingh, Zoé Dumas, Marc Robinson-Rechavi, Tanja Schwander

Comparative genomics of ten new Caenorhabditis species
Lewis Stevens, Marie-Anne Félix, Toni Beltran, Christian Braendle, Carlos Caurcel, Sarah Fausett, David HA Fitch, Lise Frézal, Taniya Kaur, Karin C Kiontke, Matt D Newton, Luke M Noble, Aurélien Richaud, Matthew V Rockman, Walter Sudhaus, Mark Blaxter

The Genomic Basis of Arthropod Diversity
Gregg W. C. Thomas, Elias Dohmen, Daniel S. T. Hughes, Shwetha C. Murali, Monica Poelchau, Karl Glastad, Clare A. Anstead, Nadia A. Ayoub, Phillip Batterham, Michelle Bellair, Gretta J Binford, Hsu Chao, Yolanda H Chen, Christopher Childers, Huyen Dinh, HarshaVardhan Doddapaneni, Jian J Duan, Shannon Dugan, Lauren A Esposito, Markus Friedrich, Jessica Garb, Robin B. B Gasser, Michael A. D. Goodisman, Dawn E Gundersen-Rindal, Yi Han, Alfred M Handler, Masatsugu Hatakeyama, Lars Hering, Wayne B Hunter, Panagiotis Ioannidis, Joy C Jayaseelan, Divya Kalra, Abderrahman Khila, Pasi K Korhonen, Carol Eunmi Lee, Sandra L Lee, Yiyuan Li, Amelia R.I. Lindsey, Georg Mayer, Alistair P McGregor, Duane D. McKenna, Bernhard Misof, Mala Munidasa, Monica Munoz-Torres, Donna M Muzny, Oliver Niehuis, Nkechinyere Osuji-Lacy, Subba R. Palli, Kristen A. Panfilio, Matthias Pechmann, Trent Perry, Ralph S. Peters, Helen C Poynton, Nikola-Michael Prpic, Jiaxin Qu, Dorith Rotenberg, Coby Schal, Sean D Schoville, Erin D Scully, Evette Skinner, Daniel B Sloan, Richard Stouthamer, Michael R Strand, Nikolaus U Szucsich, Asela Wijeratne, Neil D Young, Eduardo E Zattara, Joshua B Benoit, Evgeny M Zdobnov, Michael E Pfrender, Kevin J Hackett, John H Werren, Kim C Worley, Richard A Gibbs, Ariel D Chipman, Robert M Waterhouse, Erich Bornberg-Bauer, Matthew W Hahn, Stephen Richards

New phylogenomic analysis of the enigmatic phylum Telonemia further resolves the eukaryote tree of life
Jürgen F. H. Strassert, Mahwash Jamy, Alexander P. Mylnikov, Denis V. Tikhonenkov, Fabien Burki

Cell biology

Activation of polarized cell growth by inhibition of cell polarity
Marco Geymonat, Anatole Chessel, James Dodgson, Hannah Punter, Felix Horns, Attila Csikasz-Nagy, Rafael E Carazo-Salas

Efa6 regulates axon growth, branching and maintenance by eliminating off-track microtubules at the cortex
Yue Qu, Ines Hahn, Meredith Lees, Jill Parkin, Andre Voelzmann, Karel Dorey, Alex Rathbone, Claire Friel, Victoria Allan, Pilar Okenve-Ramos, Natalia Sanchez-Soriano, Andreas Prokop

Aurora A depletion reveals centrosome-independent polarization mechanism in C. elegans
Kerstin Klinkert, Nicolas Levernier, Peter Gross, Christian Gentili, Lukas von Tobel, Marie Pierron, Coralie Busso, Sarah Herrman, Stephan W Grill, Karsten Kruse, Pierre Gonczy

Cell type-specific structural plasticity of the ciliary transition zone in C. elegans
Jyothi S Akella, Malan S Silva, Natalia S. Morsci, Ken C.Q. Nguyen, William Rice, David H. Hall, Maureen M Barr

Centrosome Aurora A gradient ensures a single PAR-2 polarity axis by regulating RhoGEF ECT-2 localization in C. elegans embryos
Sachin Kotak, Sukriti Kapoor

Cyclin B3 promotes APC/C activation and anaphase I onset in oocyte meiosis
Mehmet E. Karasu, Nora Bouftas, Scott Keeney, Katja Wassmann

Protein Kinase A activity is regulated by actomyosin contractility during cell migration and is required for durotaxis
Andrew J McKenzie, Tamara F Williams, Kathryn V Svec, Alan K Howe

Balancing dynamic tradeoffs to drive cellular reprogramming
Kimberley N Babos, Kate E Galloway, Kassandra K Kisler, Madison Zitting, Yichen Li, Brooke Quintino, Robert H Chow, Berislav V Zlokovic, Justin K Ichida

Transcription factor activity and nucleosome organisation in mitosis
Nicola Festuccia, Nick Owens, Thaleia Papadopoulou, Inma Gonzalez, Alexandra Tachtsidi, Sandrine Vandoermel-Pournin, Elena Gallego, Nancy Gutierrez, Agnes Dubois, Michel Cohen-Tannoudji, Pablo Navarro

Superresolution architecture of pluripotency guarding adhesions
Aki Stubb, Camilo Guzmán, Elisa Närvä, Jesse Aaron, Teng-Leong Chew, Markku Saari, Mitro Miihkinen, Guillaume Jacquemet, Johanna Ivaska

Troponin-I localizes selected apico-basal cell polarity signals
Sergio Casas-Tinto, Alberto Ferrus

Spatial Organization of Rho GTPase signaling by RhoGEF/RhoGAP proteins
Paul Markus Mueller, Juliane Rademacher, Richard D Bagshaw, Keziban Merve Alp, Girolamo Giudice, Louise E Heinrich, Carolin Barth, Rebecca L Eccles, Marta Sanchez-Castro, Lennart Brandenburg, Geraldine Mbamalu, Monika Tucholska, Lisa Spatt, Celina Wortmann, Maciej T Czajkowski, Robert William Welke, Sunqu Zhang, Vivian Nguyen, Trendelina Rrustemi, Philipp Trnka, Kiara Freitag, Brett Larsen, Oliver Popp, Philipp Mertins, Chris Bakal, Anne-Claude Gingras, Olivier Pertz, Frederick P Roth, Karen Colwill, Tony Pawson, Evangelia Petsalaki, Oliver Rocks

Mitotic chromosome binding predicts transcription factor properties in interphase
Mahe Raccaud, Andrea B Alber, Elias T Friman, Harsha Agarwal, Cedric Deluz, Timo Kuhn, J. Christof M Gebhardt, David M Suter

Single-molecule imaging reveals the interplay between transcription factors, nucleosomes, and transcriptional bursting
Benjamin T Donovan, Anh Huynh, David A Ball, Michael G Poirier, Daniel R Larson, Matthew L Ferguson, Tineke L Lenstra

β-actin mRNA interactome mapping by proximity biotinylation
Joyita Mukherjee, Orit Hermesh, Nicolas Nalpas, Mirita Franz-Wachtel, Boris Macek, Ralf-Peter Jansen

F-actin dynamics transform filopodial bridges into intercellular nanotubes capable of distant cell communication
Minhyeok Chang, Jaeho Oh, Junsang Doh, Jong-Bong Lee

Lysosome exocytosis is required for mitosis
Charlotte Nugues, Nordine Helassa, Robert Burgoyne, Lee Haynes

Excitable dynamics of Ras triggers self-organized PIP3 signaling for spontaneous cell migration
Seiya Fukushima, Satomi Matsuoka, Masahiro Ueda

Fine Tuning of Histone Demethylase KDM6A/B Improves the Development of Nuclear Transfer Embryo
Lei Yang, Lishuang Song, Xuefei Liu, Lige Bai, Guangpeng Li

Modelling

Toward a 3D model of phyllotaxis based on a biochemically plausible auxin-transport mechanism
Félix P Hartmann, Pierre Barbier de Reuille, Cris Kuhlemeier

Mathematical modeling supports fate restriction in neurogenic progenitors of the embryonic ventral spinal cord
Manon Azaïs, Eric Agius, Stéphane Blanco, Jacques Gautrais, Angie Molina, Fabienne Pituello, Jean-Marc Trégan

Toward deciphering developmental patterning with deep neural network
Jingxiang Shen, Mariela D Petkova, Feng Liu, Chao Tang

A Gene Regulatory Model of Cortical Neurogenesis
Sabina Pfister, Andreas Hauri, Frederic Zubler, Gabriela Michel, Henry Kennedy, Colette DeHay, Rodney Douglas

Crawling migration under chemical signalling: a stochastic particle model
Christèle Etchegaray , Nicolas Meunier

A stochastic model for protrusion activity
Christèle Etchegaray, Nicolas Meunier

Mechanistic and experimental models of cell migration reveal the importance of intercellular interactions in cell invasion
Oleksii Matisaka, Ruth Baker, Esha Shah, Matthew Simpson

A hybrid cellular automaton model of cartilage regeneration capturing the interactions between cellular dynamics and scaffold porosity
Simone Cassani, Sarah D. Olson

Cooperation of dual modes of cell motility promotes epithelial stress relaxation to accelerate wound healing
Michael F. Staddon, Dapeng Bi, A. Pasha Tabatabai, Visar Ajeti, Michael P. Murrell, Shiladitya Banerjee

A least microenvironmental uncertainty principle (LEUP) as a generative model of collective cell migration mechanisms.
Arnab Barua, Josue Manik Navas Sedeno, Haralampos Hatzikirou

Tools & resources

Maintaining trunk neural crest cells as crestospheres
Sofie Mohlin, Ezgi Kunttas, Camilla U Persson, Reem Abdel-Haq, Aldo Castillo, Christina Murko, Marianne E Bronner, Laura Kerosuo

iProteinDB: an integrative database of Drosophila post-translational modifications
Yanhui Hu, Richelle Sopko, Verena Chung, Romain A Studer, Sean D Landry, Daniel Liu, Leonard Rabinow, Florian Gnad, Pedro Beltrao, Norbert Perrimon

Micro computed tomography as an accessible imaging platform for exploring organism development and human disease modeling
Todd Schoborg, Samantha Smith, Lauren Smith, H. Douglas Morris, Nasser M Rusan

Selective volume illumination microscopy offers synchronous volumetric imaging with high contrast
Thai V. Truong, Daniel B. Holland, Sara Madaan, Andrey Andreev, Joshua V. Troll, Daniel E. S. Koo, Kevin Keomanee-Dizon, Margaret McFall-Ngai, Scott E. Fraser

Three-Dimensional Histology of Whole Zebrafish by Sub-Micron Synchrotron X-ray Micro-Tomography
Yifu Ding, Daniel J Vanselow, Maksim A Yakovlev, Spencer R Katz, Alex Y Lin, Darin P Clark, Phillip Vargas, Xuying Xin, Jean E Copper, Victor A Canfield, Khai C Ang, Yuxin Wang, Xianghui Xiao, Francesco De Carlo, Damian B. van Rossum, Patrick La Rivière, Keith C Cheng

Fast, versatile, and quantitative annotation of complex images
Kathleen Bates, Shen Jiang, Ruth Bates, Shivesh Chaudhary, Emily Jackson-Holmes, Melinda Jue, Erin McCaskey, Daniel Goldman, Hang Lu

A Multimodal Adaptive Super-Resolution and Confocal Microscope
Liyana Valiya Peedikakkal, Andrew Furley, Ashley J Cadby

Three-photon light-sheet fluorescence microscopy
Adrià Escobet-Montalbán, Federico M Gasparoli, Jonathan Nylk, Pengfei Liu, Zhengyi Yang, Kishan Dholakia

KymoButler: A deep learning software for automated kymograph tracing and analysis
Maximilian Jakobs, Andrea Dimitracopoulos, Kristian Franze

Raincloud plots: a multi-platform tool for robust data visualization

Micah Allen​, Davide Poggiali, Kirstie Whitaker, Tom R Marshall, Rogier Kievit

Comparative analysis of the effect of genomic isolators flanking transgenes to avoid positional effects in Arabidopsis
Ana Pérez-González, Elena Caro

High Aspect Ratio Nanomaterials Enable Delivery of Functional Genetic Material Without DNA Integration in Mature Plants
Gozde S. Demirer, Huan Zhang, Juliana Matos, Natalie Goh, Francis J Cunningham, Younghun Sung, Roger Chang, Abhishek J Aditham, Linda Chio, Myeong-Je Cho, Brian Staskawicz, Markita P. Landry

Rapid and efficient C-terminal labeling of nanobodies for DNA-PAINT
Valentin Fabricius, Jonathan Lefebre, Hylkje Geertsema, Stephen F Marino, Helge Ewers

A Multiplexed DNA FISH strategy for Assessing Genome Architecture in C. elegans
Brandon D Fields, Son C Nguyen, Guy Nir, Scott Kennedy

Translocation and duplication from CRISPR-Cas9 editing in Arabidopsis thaliana
Peter G Lynagh, Soichi Inagaki, Kirk R Amundson, Mohan P.A. Marimithu, Brett R. Pike, Isabelle M. Henry, Ek Han Tan, Luca Comai

Optimized Cas9 expression systems for highly efficient Arabidopsis genome editing facilitate isolation of complex alleles in a single generation
Jana Ordon, Mauro Bressan, Carola Kretschmer, Luca Dall’Osto, Sylvestre Marillonnet, Roberto Bassi, Johannes Stuttmann

Haplotype-phased Callithrix jacchus embryonic stem cell line for genome editing using CRISPR/Cas9
Bo Zhou, Steve S. Ho, Louis C. Leung, Thomas R. Ward, Marcus Ho, Melanie J. Plastini, Scott C. Vermilyea, Marina E. Emborg, Thaddeus G. Golos, Philippe Mourrain, Dimitri Perrin, Karen J. Parker, Alexander E. Urban

Target-specific precision of CRISPR-mediated genome editing
Anob M Chakrabarti, Tristan Henser-Brownhill, Josep Monserrat, Anna R Poetsch, Nicholas M Luscombe, Paola Scaffidi

New human chromosomal safe harbor sites for genome engineering with CRISPR/Cas9, TAL effector and homing endonucleases
Stefan Pellenz, Michael P Phelps, Weiliang Tang, Blake T Hovde, Ryan Sinit, Wenqing Fu, Hui Li, Eleanor Chen, Raymond Monnat Jr.

Efficient Zygotic Genome Editing via RAD51-Enhanced Interhomolog Repair
Jonathan J Wilde, Tomomi Aida, Martin Wienisch, Qiangge Zhang, Peimin Qi, Guoping Feng

Deep learning image recognition enables efficient genome editing in zebrafish by automated injections
Maria Lorena Cordero-Maldonado, Simon Perathoner, Kees-Jan van der Kolk, Ralf Boland, Ursula Heins-Marroquin, Herman P. Spaink, Annemarie H. Meijer, Alexander D. Crawford, Jan de Sonneville

Clonal analysis by tunable CRISPR-mediated excision
Anna F Gilles, Johannes B Schinko, Magdalena I Schacht, Camille Enjolras, Michalis Averof

Analysis and comparison of genome editing using CRISPResso2
Kendell Clement, Holly Rees, Matthew Canver, Jason Gehrke, Rick Farouni, Jonathan Hsu, Mitchel Cole, David R Liu, J. Keith Joung, Daniel E. Bauer, Luca Pinello

Mutations generated by repair of Cas9-induced double strand breaks are predictable from surrounding sequence
Felicity R Allen, Luca R Crepaldi, Clara Alsinet-Armengol, Alexander Strong, Vitalii Kleshchevnikov, Pietro De Angeli, Petra Palenikova, Michal Kosicki, Andrew R Bassett, Heather Harding, Yaron Galanty, Francisco Munoz Martinez, Emmanouil Metzakopian, Stephen P Jackson, Leopold Parts

Homology Directed Repair by Cas9:Donor Co-localization in Mammalian Cells
Philip JR Roche, Heidi Gytz, Faiz Hussain, Christopher JF Cameron, Denis Paquette, Mathieu Blanchette, Josée Dostie, Bhushan Nagar, Uri David Akavia

Decomposing cell identity for transfer learning across cellular measurements, platforms, tissues, and species.
Genevieve L Stein-O’Brien, Brian S. Clark, Thomas Sherman, Christina Zibetti, Qiwen Hu, Rachel Sealfon, Sheng Liu, Jiang Qian, Carlo Colantuoni, Seth Blackshaw, Loyal A. Goff, Elana J. Fertig

High-throughput single-cell transcriptome profiling of plant cell types
Christine N Shulse, Benjamin J Cole, Gina M Turco, Yiwen Zhu, Siobhan M Brady, Diane E Dickel

One read per cell per gene is optimal for single-cell RNA-Seq
Martin J. Zhang, Vasilis Ntranos, David Tse

Cell lineage inference from SNP and scRNA-Seq data
Jun Ding, Chieh Lin, Ziv Bar-Joseph

droplet-Tn-Seq combines microfluidics with Tn-Seq identifying complex single-cell phenotypes
Derek Thibault, Stephen Wood, Paul Jensen, Tim van Opijnen

SIS-seq, a molecular ‘time machine’, connects single cell fate with gene programs
Tian Luyi, Jaring Schreuder, Daniela Amann-Zalcenstein, Jessica Tran, Nikolce Kocovski, Shian Su, Peter Diakumis, Melanie Bahlo, Toby Sargeant, Matthew Ritchie, Philip Hodgkin, Shalin Naik

MULTI-seq: Scalable sample multiplexing for single-cell RNA sequencing using lipid-tagged indices
Christopher S McGinnis, David M Patterson, Juliane Winkler, Marco Y Hein, Vasudha Srivastava, Daniel N Conrad, Lyndsay M Murrow, Jonathan S Weissman, Zena Werb, Eric D Chow, Zev J Gartner

Simultaneous multiplexed amplicon sequencing and transcriptome profiling in single cells
Mridusmita Saikia, Philip Burnham, Sara H Keshavjee, Michael F Z Wang, Michael Heyang, Pablo Moral-Lopez, Meleana M Hinchman, Charles G Danko, John S L Parker, Iwijn De Vlaminck

High-throughput mapping of long-range neuronal projection using in situ sequencing
Xiaoyin Chen, Justus M Kebschull, Huiqing Zhan, Yu-Chi Sun, Anthony M Zador

SABER enables highly multiplexed and amplified detection of DNA and RNA in cells and tissues
Jocelyn Y. Kishi, Brian J. Beliveau, Sylvain W. Lapan, Emma R. West, Allen Zhu, Hiroshi M. Sasaki, Sinem K. Saka, Yu Wang, Constance L. Cepko, Peng Yin

Palantir characterizes cell fate continuities in human hematopoiesis
Manu Setty, Vaidotas Kiseliovas, Jacob Levine, Adam Gayoso, Linas Mazutis, Dana Pe’er

Mass-spectrometry of single mammalian cells quantifies proteome heterogeneity during cell differentiation
Bogdan Budnik, Ezra Levy, Guillaume Harmange, Nikolai Slavov

The Signaling Pathways Project: an integrated ‘omics knowledgebase for mammalian cellular signaling pathways
Scott Ochsner, David Abraham, Kirt Martin, Wei Ding, Apollo McOwiti, Zichen Wang, Kaitlyn Andreano, Ross Hamilton, Yue Chen, Angelica Hamilton, Marin Gantner, Michael Dehart, Shijing Qu, Susan Hilsenbeck, Lauren Becnel, Dave Bridges, Avi Maayan, Janice Huss, Fabio Stossi, Charles Foulds, Anastasia Kralli, Donald McDonnell, Neil McKenna

Research practice & education

Gender and international diversity improves equity in peer review
Dakota Murray, Kyle Siler, Vincent Lariviére, Wei Mun Chan, Andrew M. Collings, Jennifer Raymond, Cassidy R Sugimoto

Maintaining confidence in the reporting of scientific outputs

Sarabipour S, Wissink EM, Burgess SJ, Hensel Z, Debat H, Emmott E, Akay A, Akdemir K, Schwessinger B

Research Infrastructures offer capacity to address scientific questions never attempted before: Are all taxa equal? 

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