A crucial step in vertebrate muscle development is the activation of myogenic regulatory factors (MRFs) that direct myogenesis. A new paper in Development investigates the roles of Fgf signalling and Tbx transcription factors in zebrafish MRF induction. We caught up with the paper’s two first authors, Daniel Osborn and Kuoyu Li, and their supervisor Simon Hughes, MRC Scientist and Professor of Developmental Cell Biology at King’s College London, to hear more about the story.
Daniel, Kuoyu and Simon (L to R)
Simon, can you give us your scientific biography and the questions your lab is trying to answer?
SH After studying biochemistry as an undergrad and doing a PhD on rhodopsins with Martin Brand in Cambridge, I did a postdoc with Martin Raff in UCL on cell lineage in the optic nerve. In 1987 it was difficult to study cell lineage in vivo in the central nervous system, and the molecules that controlled cell fate were completely mysterious. But MyoD was discovered that year, so I switched to skeletal muscle, doing a second postdoc with Helen Blau at Stanford on how myoblasts generate slow and fast muscle fibres in specific patterns in each muscle. All three advisors taught me so much about both science and life. Before I moved back to London, I worked for a few months in David Botstein’s large group. We were sequencing the yeast genome, a precursor to the Human Genome Project and one of the first high-throughput ‘big science’ projects in biology; really exciting, but not my kind of science. In 1992, I joined the Medical Research Council Biophysics Unit at King’s College London, where Franklin and Wilkins had done their DNA structure work. It was an ideal place for me – Nigel Holder and Roger Patient had just set up a Developmental Biology Research Centre, and my lab linked that to the MRC Unit. We initially worked mainly on mouse and chick muscle, but Nigel soon inveigled me into zebrafish and I fell in love with the simplicity and ability to watch tissue development in real time. I was really lucky to meet, learn from, and collaborate with Monte Westerfield and Phil Ingham and their colleagues, whose differing approaches helped me combine genetics with our developmental cell biology. We have remained true to our original question of understanding the molecular genetics of muscle tissue patterning, though much of our work now focuses on later developmental stages, when zebrafish muscle is growing from committed muscle stem cells. I am really pleased with Dan and Kuoyu’s paper because, although it had a 20 year gestation, I think it fills in a missing link between patterning of early mesoderm and muscle.
Daniel, how did you come to work in Simon’s lab?
DO I started in Simon’s lab as a research technician back in 2001 where my primary role was running the then MRC/KCL zebrafish facility as well as contributing to the group’s research. It was a fantastically encouraging environment for a young biology graduate and I was immediately immersed in exciting developmental biology, the bright lights of London and my first salaried position. I loved the lab work and to fuel my interest Simon offered me a part-time PhD and KCL agreed to waive my bench fees. This sent me down the academic research career path and I haven’t looked back since. My thesis looked at the regulation of myogenic bHLH proteins during zebrafish slow muscle development. A substantial amount of work came out of it, contributing to four papers, and it is now with great pleasure that this collaborative effort has produced a fifth, and perhaps final, paper stemming from my thesis, which was completed 12 years ago.
How are each of you coping in the current COVID-19 pandemic?
DO I am now based at St George’s University of London where I run my own zebrafish group (my group is still very much interested in muscle development, but I am more of a gene hunter these days). Everything is now in stasis until the pandemic passes. It has been difficult to be away from the lab – we have a number of manuscripts in their final stages that need experiments completing before submission and it is frustrating not being able to get these done. Although experiments have stopped, I am still supporting undergraduate students and courses that are now running online, and it’s the time of year for marking dissertations. I also have three young children thrown into my daily mix. They are kindly humouring me by allowing me to explain to them genetic variation using Lego (different coloured bricks for different traits), perform crude DNA extractions from strawberries, and help them mount samples from around the house/garden on slides for viewing down our microscope. Luckily the weather has been surprisingly good, so we have been out in the garden exercising, home-schooling and indulging in plenty of fresh air.
KL I now work in a laboratory in the China Zebrafish Resource Center in Wuhan, having moved back at the end of 2010. By chance, I left Wuhan 2 h before the city was shut, to unite with my family for Spring Festival. At that moment, we didn’t realise how serious this pandemic would be. In our small town in Hubei we self-quarantined at home for 49 days. We ordered supplies online and volunteers brought them to our door every 2-3 days. The institute was shut, with no staff in the labs. Part-time staff came briefly every 4 days to feed the fish. Now, I am back in Wuhan and preparing to return to work next week (30 March). We hope the city will be back to normal after 2 months cold shock.
SH Experiments have been completely shut down and one of my team is recovering from COVID-19, but our many lines of fish are still happy, as far as I am aware. Just like Kuoyu’s, our Biological Services staff are doing a heroic job in very difficult circumstances. My family has escaped to rural Wales, so for me it’s email, FaceTime and Microsoft Teams between spring birdsong and isolated walks – quite idyllic. I’ve volunteered to run PCRs in local hospitals, but no call yet. I feel for my colleagues stuck in small flats in London as we await the approaching medical storm.
Let’s get back to the paper then – what led you to study the roles of Fgf and Tbx in myogenesis?
SH I had known about the importance of Fgf in mesoderm patterning since the work of Kimelman and Kirschner in 1987, and then the finding by my KCL colleagues Kevin Griffin and Nigel Holder that Fgf signalling was important in zebrafish trunk myogenesis. Kevin and Nigel proposed there was a gene they called ‘no trunk’ (by analogy with ‘no tail’, which is what the zebrafish T gene was called at the time). Kevin went as a postdoc to Dave Kimelman’s lab and showed that no trunk really existed; it was tbx16. Tbx16 is mainly known for controlling gastrulation movements at trunk levels; it was originally discovered as a mutant called spadetail that lacks most dorsal trunk tissue, and Sharon Amacher and Chuck Kimmel had shown this nicely. During the course of our study, both Dave Kimelman’s and Sharon Amacher’s labs showed that various Tbx genes collaborate in the formation of dorsal mesoderm. And Stephen Devoto’s lab had also shown that Tbx6, a close relative of Tbx16, is a negative regulator of presomitic mesoderm myogenesis. So it was really a no-brainer to examine this in our myogenic context, particularly with Fiona Wardle as a neighbour.
DO When the work began nearly 20 years ago almost all the MRF loss-of-function analyses had been done in mouse. So it was unclear how general the role of MRFs was in vertebrate myogenesis, particularly bearing in mind that Myod is not required for most myogenesis in flies. Our early experiments used morpholinos because that was the cutting-edge technology at the time; nowadays, we would do it by CRISPR genome editing. I was excited to see that zebrafish MRFs were initiated in the absence of Hh signalling in anterior somites, just as our lab had seen working with Betsy Pownall in Xenopus and as Andy McMahon had shown in smoothened mutants in mouse. Strikingly, just as Anne-Gaëlle Borycki showed in mouse, I saw that Hh signalling was more important in more caudal somites, so I asked what other signalling might be important to turn on the MRFs in anterior somites. SU5402 had been found to block Fgf signalling and it worked. Monte Westerfield’s lab found and published the same thing before us, which was both disappointing and encouraging, and meant we had to do more to publish something meaningful. So, I had shown with loss- and gain-of-function experiments that Fgfs in the tailbud and in the base of the notochord were important for myogenesis. It was one chapter in my thesis – I left at this point and Kuoyu took over the project.
KL When I joined Simon’s lab, we wanted to pursue two aspects of Dan’s thesis. I looked downstream of MRFs at how they drove slow myogenesis; the first paper Dan and I published together was on how Cdkn1c (p57) cooperates with Myod to drive slow myogenesis. But I also began looking at how Fgf might activate MRF transcription. I found that MRFs were no longer induced by Fgf signalling in tbx16 mutants and in morpholino conditions, and that Fgf signalling cooperates with Tbx16 to drive MRF expression, which again argued that both Fgf and Tbx16 are needed within the presomitic tissue to initiate MRF expression and myogenesis.
SH At that point, the project came to a halt. But luckily, Fiona Wardle and colleagues had data on Tbx16 and Tbxta binding to myf5 and myod that moved the project forward.
MRF expression in tbx16 mutant embryos, with or without injected fgf4 mRNA.
Can you give us the key results of the paper in a paragraph?
The key result is that, in addition, to their role in paraxial mesoderm migration, Fgf signalling from the tailbud midline triggers Tbx16 to bind and directly activate the myf5 and myod genes. The same goes for Tbxta on the myod gene, and that initiates slow muscle fibre formation adjacent to the base of the forming notochord. Combined with Andrew and Fiona’s data on Tbx binding to the MRF loci, this encouraged Steve Cutty to use the glucocorticoid receptor-Tbx16 fusion protein plus dexamethasone to show that binding triggers myf5 and myod transcription directly, without new protein synthesis from other genes.
What do you think explains the differences in transcriptional targets between Tbx16 and Tbxta?
DO, KL & SH That’s an interesting question. The consensus binding sequences don’t seem to differ, so presumably their differential binding at certain sites in myf5 and myod has to do with collaborating accessory proteins and/or local chromatin structure. But another issue is whether they are competing for binding at sites where we detected both bound; in the embryo tbx16 and tbxta are expressed in only partially overlapping cell populations, so they could do different things in separate cell types. There is also the possibility that cell signalling and post-translational modifications could make them differentially active, even when bound to the same site. There’s a lot to work out if one wants to fully understand it.
What do your findings suggest about the evolution of vertebrate musculature?
DO, KL & SH It’s now clear that Tbxt/6/16 family genes are required in all major chordate lineages for myogenesis in the body and tail (but not the head). We think this is likely the ancestral way muscle was made in vertebrates. But several kinds of muscle are made in the somites of all vertebrates, and we think diversification of this Tbxt/6/16 gene family allowed the evolutionary diversification that gave vertebrates their advantage. For example, Tbxt genes are famous now for specifying notochord and thus controlling midline Hh expression. We think it is no coincidence that Hh induces both muscle and motoneuron diversification and that in the most primitive extant chordate, Amphioxus, notochord has muscle character. Perhaps the evolutionary origin of notochord was a special kind of dorsalmost muscle.
When doing the research, did you have any particular result or eureka moment that has stuck with you?
DO For me, the eureka moment that catalysed this project was finding that blocking Fgf signalling inhibited early myf5 and myod induction. I had spent a great deal of time analysing myf5 and myod expression in young but not older adaxial cells of Hh mutants. I was determined to find what midline-derived signals might be involved in regulating the initial Hh-independent MRF expression, and the localisation of Fgf signals made them particularly attractive candidates. Then finding that overexpression of either Fgf4 or Fgf6a could ectopically induce myf5 and myod was the icing on the cake – we knew we were onto something.
KL I think the best was finding that Tbx16 was essential for initial myf5 expression. I found it first with a morpholino; the mutant confirmed it. And then when Fgf4 overexpression could not rescue in the tbx16 mutant background.
And what about the flipside: any moments of frustration or despair?
DO Nothing that really stands out: although there are often such moments in science, it’s just the way it is. For this project it probably revolved around cloning – coming in early to find no colonies on my plates. That’s why it feels so good when experiments go to plan or give an unexpected exciting result. The bitter makes the sweet taste so much better!
KL I was very frustrated not to finish this Fgf story before leaving for China in 2010 due to my (or rather the UK Government’s) problem with visas. At that time, there was a temporary MRC funding hiatus caused by the 2008 financial crisis and the new Government was clamping down on immigrants like me. The result was that I had to leave the country before the end of the year. I finished what experiments I could over Christmas and flew back to China on 31 December 2010. Simon offered me a PhD place to continue the project, but my wife (also a scientist) was back in Wuhan starting her own lab, so in the end I stayed here. I now work in the China Zebrafish Resource Center as a member of the technical staff. My prime duty is to keep the aquarium running properly; no more experiments in my life, which is a great sadness to me.
The bitter makes the sweet taste so much better!
Finally, let’s move outside the lab – what do you like to do in your spare time in London and Wuhan?
DO Family is very important to me, especially with my children being so young (6-10 years). Most of my spare time revolves around taxiing between clubs. However, I have recently got into rock climbing (which the kids do too) and I love tinkering around on my motorbike when given half a chance.
KL I spend most of my spare time with my daughter. She is 4 years old. I teach her English and tell her stories about my life in London. She likes Pocoyo and learns a lot from this cute blue guy.
SH Though I enjoy London’s cultural offerings, my favourite spare time is spent in the hills, either the small ones surrounding our Welsh cottage, or larger ones in places like Argentina; they clear your head with a different kind of excitement and provide space to think. It has never been more important for people to (re-)connect with nature.
The Department of Biological Sciences at Louisiana State University invites applications for a tenure-track Assistant Professor position in all areas of stem cell and regenerative biology, including neurobiology, developmental biology, and molecular-cell biology. Biological Sciences is a large and dynamic department, with research ranging across all levels of biological organization, and the successful candidate will complement these strengths. Researchers utilizing non-traditional model organisms and those who would appreciate joining diverse and interactive faculty are especially encouraged to apply. In addition to the Department of Biological Sciences, opportunities for collaboration research are available at the LSU School of Veterinary Medicine, the LSU College of the Coast & Environment, the LSU College of Agriculture, and the LSU Pennington Biomedical Research Center. Successful candidates will be expected to establish and maintain a vigorous, extramurally funded research program and to contribute to undergraduate and graduate teaching. Applicants should have a Ph.D. in Biological Sciences or related field, a successful track record of productive research and publication, and postdoctoral experience.
Our department is dedicated to the goal of building a culturally diverse and pluralistic faculty, and we strongly encourage applications from women, minorities, individuals with disabilities, veterans, and other members of groups underrepresented in science. We seek candidates whose research, teaching, or service has prepared them to contribute to diversity and inclusion in higher education. Candidates should include a statement describing how they will promote an inclusive learning environment, and how their scholarship and mentoring practices support a diverse academic community.
The Sumigray lab in the Department of Genetics at Yale School of Medicine invites applications for a postdoctoral scientist to work on an exciting project at the interface of cell biology, morphogenesis and stem cell biology. The successful applicant will have a strong background in cell and developmental biology, genetics and/or stem cell biology and a track-record of original and impactful research in biomedical science.
The Sumigray lab studies the molecular and cellular processes that drive intestinal crypt morphogenesis and the importance of crypt architecture on intestinal stem cell activity/function. We use a combination of in vivo and in vitro models combined with live imaging, confocal microscopy and next-generation sequencing. For more information about the lab’s research, please see sumigraylab.org.
Applicants should possess a Ph.D. in molecular biology, cell biology, biochemistry, genetics, or a related field. Experience in mammalian cell culture is preferred but not required.
Please submit i) a cover letter with a brief description of your research experience and motivations for joining the lab, ii) CV and iii) contact details for 2-3 references to Dr. Kaelyn Sumigray (kaelyn.sumigray@yale.edu).
The Giraldez laboratory at Yale University is seeking to recruit a highly qualified Associate Research Scientist as a long-term scientist in the laboratory (www.giraldezlab.org). Prerequisites for appointment on the research scientist track include a doctoral degree and relevant postdoctoral experience.
The successful candidate will be a highly-motived scientist with excellent organizational, mentoring and leadership skills. They will be responsible for coordinating the overall scientific operations of the Giraldez lab and will provide critical training and mentoring to individual lab members. In addition, the successful candidate will have the opportunity to participate in multiple research projects and drive a scientific project aligned with the major interests of the laboratory. The successful candidate will have the following attributes:
A doctoral degree and relevant postdoctoral experience
Excellent interpersonal and communication skills
Excellent organizational skills and attention to detail
Solid publication record and the ability to drive long-term, successful research projects
Expertise in one or more of the following: molecular biology, chromatin biology, developmental
biology, genomics, and/or imaging
This appointment can be renewed indefinitely provided the need for the position continues, the funding for the position is available.
Tenure-track position in the Division of Biological Sciences
The Center for Craniofacial Molecular Biology (CCMB) of the Herman Ostrow School of Dentistry of the University of Southern California is recruiting outstanding candidates for a tenure-track position at the rank of Assistant Professor in the Division of Biomedical Sciences to conduct cutting-edge research in the areas of cell and developmental biology, tissue regeneration, cell signaling, gene regulation, computational modeling and human diseases using genetic and genomic approaches. At the CCMB, these disciplines focus on craniofacial biology and there are significant resources to support all aspects of our research. The University of Southern California offers an exciting, and highly supportive environment to conduct collaborative basic, clinical, and translational research. At the health science campus, faculty members at CCMB have access to all research centers and graduate students in all programs.
Candidates must have a Ph.D. in developmental biology, stem cell biology, or molecular biology. Candidates with both a Ph.D. and either a D.D.S. or D.M.D. degree are encouraged to apply. Candidates must have a strong record of high-quality research with significant publications in their field. Candidates with K99/R00 or other independent support are strongly encouraged to apply. For more information: https://usccareers.usc.edu/job/los-angeles/assistant-professor-of-dentistry/1209/17867982
Consideration of applicants will begin immediately and will continue until the position is filled. USC is an equal-opportunity educator and employer, proudly pluralistic and firmly committed to providing equal opportunity for outstanding persons of every race, gender, creed, and background. The University particularly encourages women, members of underrepresented groups, veterans, and individuals with disabilities to apply. USC will make reasonable accommodations for qualified individuals with known disabilities unless doing so would result in an undue hardship. Further information is available by contacting uschr@usc.edu.
A postdoctoral position is available immediately in Yang Chai‘s laboratory at the Center for Craniofacial Molecular Biology, University of Southern California in Los Angeles, California. We are interested in the regulation of developmental patterning, organogenesis, and mesenchymal stem cells. Our studies will seek to define molecular mechanisms governing both normal and abnormal craniofacial development, providing scientific rationales for future therapeutic strategies to prevent and treat craniofacial birth defects, as well as stem cell based craniofacial tissue regeneration. The candidate must have a PhD and be experienced with molecular and developmental biology. Supported by the NIDCR, NIH. For details, please visit http://chailab.usc.edu/
Send application, resume, and three letters of recommendation to
Wen, Q., Jing, J., Han, X., Feng, J., Yuan, Y., Ma, Y., Chen, S., Ho, T.H., and Chai, Y. (2020) Runx2 regulates mouse tooth root development via activation of Wnt inhibitor Notum. JBMR,PMID 32569388.
Jing, J., Feng, J., Li, J., Han, X., He, J., Ho, T., Du, J., Zhou, X., Urata, M., and Chai, Y. (2019) Antagnistic interaction between Ezh2 and Arid1a coordinate dental root patterning via Cdkn2a. eLife, Jul 1;8. e46426.
Guo, Y., Yuan, Y., Wu, L., Ho, T., Jing, J., Sugii, H., Li, J., Han, X., Guo, C., and Chai, Y. (2018) BMP-IHH-mediated interplay between mesenchymal stem cells and osteoclasts supports calvarial bone homeostasis and repair. Bone Research. 6, 355-367. PMCID: PMC6193039
Li, J., Parada, C., and Chai, Y. (2017) Cellular and Molecular Regulatory Mechanism of Tooth Root Development. Development, 144, 374-384. PMCID: PMC5341797
Brinkley, J.F., Fisher, S., Harris, M., Holmes, G., Hooper, J.E., Wang Jabs, E., Jones, K.L., Kesselman, C., Klein, O.D., Maas, R.L., Marazita, M.L., Selleri, L., Spritz, R.A., van Bakel, H., Visel, A., Williams, T.J., Wysocka, J., the FaceBase Consortium, and Chai, Y. (2016) The FaceBase Consortium: A comprehensive resource for craniofacial researchers. Development, 143, 2677-2688.PMCID: PMC4958338.
Zhao, H., Feng, J., Ho, T. V., Grimes, W. C., Urata, M., and Chai, Y. (2015) The suture provides a niche for mesenchymal stem cells of craniofacial bones. Nature Cell Biology, 17, 386-396. PMCID: PMC4380556
Zhao, H., Feng, J., Seidel, K., Shi, S., Klein, O., Sharpe, P., and Chai, Y. (2014) Secretion of Shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell 14, 160-173. PMCID:PMC3951379
In this episode we’re taking a look at the story and the characters behind one of the most transformative – and ubiquitous – techniques in modern molecular biology: the polymerase chain reaction.
Anyone who has worked with DNA in the laboratory is undoubtedly familiar with the polymerase chain reaction – PCR, as it’s usually known. Invented in 1985, PCR is an indispensable molecular biology tool that can replicate any stretch of DNA, copying it billions of times in a matter of hours, providing enough DNA to use in sequencing or further research, or for applications like forensics, genetic testing, ancient DNA analysis or medical diagnostics.
It’s hard to overstate the transformation that PCR brought to the world of molecular biology and biomedical research. Suddenly, researchers could amplify and study DNA in a way that had been simply impossible before, kickstarting the genetic revolution that’s still going strong today. But where did this revolutionary technology come from? Officially, PCR was invented in 1985 by a colourful character called Kary Mullis, who won a Nobel Prize for the discovery, but, as we’ll see, all the components of PCR were in place by the early 1980s – it just took a creative leap to assemble them into one blockbusting technique.
Image: Illustration depicting semi-conservative DNA replication. Three generations of DNA are shown. After separation of the DNA double helix, two new complementary DNA strands are synthesised (indicated by a new colour). Complementary base pairing and hydrogen bonding results in formation of a new double helix. Credit: Susan Lockhart. Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
If you enjoy the show, please do rate and review on Apple podcasts and help to spread the word on social media. And you can always send feedback and suggestions for future episodes and guests to podcast@geneticsunzipped.com Follow us on Twitter – @geneticsunzip
A postdoctoral research position is available to study the cellular, genetic, and epigenetic mechanisms of maternal age effects on offspring health and lifespan. The project will focus on the role of mitochondrial dynamics and function in maternal age effects, using molecular, bioinformatic, biochemical, and imaging techniques.
This is an NIH-funded project in the laboratory of Dr. Kristin Gribble at the Marine Biological Laboratory, Woods Hole, MA. The lab researches the mechanisms and evolution of aging and maternal and transgenerational effects on offspring health. We use rotifers as a model system for our work. For more information about the lab’s research and publications, see mbl.edu/jbpc/gribble.
Applicants should possess a Ph.D. molecular biology, cell biology, biochemistry, genetics, bioinformatics, or a related field. The ideal candidate will have a record of scientific rigor, productivity, and creativity. Excellent oral and written communication skills are required. Knowledge of rotifer biology is not required; highly motivated individuals with experience in other model systems and with a background in bioinformatics, cell biology, biochemistry, epigenetics, and/or imaging are encouraged to apply. Salary commensurate with experience and qualifications.
Applicants must apply for this position via the Marine Biological Laboratory careers website. Please submit (1) a cover letter with a brief description of your research experience and how you will contribute to research on the mechanisms of maternal effects on offspring, (2) a CV, and (3) contact information for at least three references.
Development invites you to submit your latest research to our upcoming special issue: Imaging development, stem cells and regeneration.
Imaging-based approaches have long played a role in the field of developmental biology. However, recent technical advances now provide us with the ability to visualise cell and developmental processes at extraordinary resolution and in real-time. From progress in light sheet and super-resolution microscopy, to the development of tissue-clearing techniques and sophisticated image analysis platforms, we are now able to capture and quantitatively analyse the beauty and dynamics of development across different scales – from individual molecules and cells, to complete tissues and embryos. This Special Issue aims to showcase articles that, at their core, have applied such advanced techniques in innovative ways to further our understanding of developmental and regenerative processes. We also encourage the submission of articles that report the development or application of a novel imaging-based technique.
Prospective authors are welcome to send pre-submission enquiries to dev.specialissue@biologists.com. We also invite proposals for Review articles: if you are interested in contributing a Review, please send a summary of your proposed article to us by 15 December 2020.
The Special Issue will be published in mid-2021 (although note that, in our new continuous publication model, we will aim to publish your article as soon as it is accepted*). The issue will be widely promoted online and at key global conferences, guaranteeing maximum exposure for your work.
For information about article types and manuscript preparation, please refer to our author guidelines. To submit your article, visit our online submission system; please highlight in your cover letter that the submission is to be considered for this Special Issue.
The deadline for submitting articles is 30 March 2021.
Why choose Development?
Submissions handled by expert Academic Editors
Competitive decision speeds and rapid publication
Format-free submission
Strong commitment at first decision – over 95% of invited revisions accepted
Free to publish – no page or colour charges, no hidden fees
Easy one-click transfer option to Biology Open
Not-for-profit publisher
* Please note that not all articles accepted for publication will be included in the Special Issue; they may instead be published in earlier or later issues of the journal based on timing and editorial discretion.
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In this episode we’re taking a look at the story and the characters behind one of the most transformative – and ubiquitous – techniques in modern molecular biology: the polymerase chain reaction.
