DevelopmentPub Date : 2024-10-15Epub Date: 2024-09-03DOI: 10.1242/dev.202968
Christopher J Johnson, Zheng Zhang, Haifeng Zhang, Renjie Shang, Katarzyna M Piekarz, Pengpeng Bi, Alberto Stolfi
{"title":"A change in cis-regulatory logic underlying obligate versus facultative muscle multinucleation in chordates.","authors":"Christopher J Johnson, Zheng Zhang, Haifeng Zhang, Renjie Shang, Katarzyna M Piekarz, Pengpeng Bi, Alberto Stolfi","doi":"10.1242/dev.202968","DOIUrl":"10.1242/dev.202968","url":null,"abstract":"<p><p>Vertebrates and tunicates are sister groups that share a common fusogenic factor, Myomaker (Mymk), that drives myoblast fusion and muscle multinucleation. Yet they are divergent in when and where they express Mymk. In vertebrates, all developing skeletal muscles express Mymk and are obligately multinucleated. In tunicates, Mymk is expressed only in post-metamorphic multinucleated muscles, but is absent from mononucleated larval muscles. In this study, we demonstrate that cis-regulatory sequence differences in the promoter region of Mymk underlie the different spatiotemporal patterns of its transcriptional activation in tunicates and vertebrates. Although in vertebrates myogenic regulatory factors (MRFs) such as MyoD1 alone are required and sufficient for Mymk transcription in all skeletal muscles, we show that transcription of Mymk in post-metamorphic muscles of the tunicate Ciona requires the combinatorial activity of MRF, MyoD and Early B-cell Factor (Ebf). This macroevolutionary difference appears to be encoded in cis, likely due to the presence of a putative Ebf-binding site adjacent to predicted MRF binding sites in the Ciona Mymk promoter. We further discuss how Mymk and myoblast fusion might have been regulated in the last common ancestor of tunicates and vertebrates, for which we propose two models.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11441980/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141901235","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-10-28DOI: 10.1242/dev.203015
Brennan D McDonald, Abdull J Massri, Alejandro Berrio, Maria Byrne, David R McClay, Gregory A Wray
{"title":"Contrasting the development of larval and adult body plans during the evolution of biphasic lifecycles in sea urchins.","authors":"Brennan D McDonald, Abdull J Massri, Alejandro Berrio, Maria Byrne, David R McClay, Gregory A Wray","doi":"10.1242/dev.203015","DOIUrl":"10.1242/dev.203015","url":null,"abstract":"<p><p>Biphasic lifecycles are widespread among animals, but little is known about how the developmental transition between larvae and adults is regulated. Sea urchins are a unique system for studying this phenomenon because of the stark differences between their bilateral larval and pentaradial adult body plans. Here, we use single-cell RNA sequencing to analyze the development of Heliocidaris erythrogramma (He), a sea urchin species with an accelerated, non-feeding mode of larval development. The sequencing time course extends from embryogenesis to roughly a day before the onset of metamorphosis in He larvae, which is a period that has not been covered by previous datasets. We find that the non-feeding developmental strategy of He is associated with several changes in the specification of larval cell types compared to sea urchins with feeding larvae, such as the loss of a larva-specific skeletal cell population. Furthermore, the development of the larval and adult body plans in sea urchins may utilize largely different sets of regulatory genes. These findings lay the groundwork for extending existing developmental gene regulatory networks to cover additional stages of biphasic lifecycles.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11529275/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142497092","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-08-19DOI: 10.1242/dev.203084
Federico D Brown, Edson Ishengoma, Georg Mayer, Natalia Pabón-Mora, M Emília Santos, Karen E Sears, Ivo de Sena Oliveira
{"title":"Uncovering developmental diversity in the field.","authors":"Federico D Brown, Edson Ishengoma, Georg Mayer, Natalia Pabón-Mora, M Emília Santos, Karen E Sears, Ivo de Sena Oliveira","doi":"10.1242/dev.203084","DOIUrl":"https://doi.org/10.1242/dev.203084","url":null,"abstract":"<p><p>Many developmental biologists seldom leave the lab for research, relying instead on establishing colonies of traditional and emerging model systems. However, to fully understand the mechanisms and principles of development and evolution, including the role of ecology and the environment, it is important to study a diverse range of organisms in context. In this Perspective, we hear from five research teams from around the world about the importance and challenges of going into the field to study their organisms of interest. We also invite you to share your own fieldwork stories on the Node.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141999584","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-09-13DOI: 10.1242/dev.202732
Samuel Boscq, Bernard Billoud, Ioannis Theodorou, Tanweer Joemmanbaks, Tanguy Dufourt, Bénédicte Charrier
{"title":"MUM, a maternal unknown message, inhibits early establishment of the medio-lateral axis in the embryo of the kelp Saccharina latissima.","authors":"Samuel Boscq, Bernard Billoud, Ioannis Theodorou, Tanweer Joemmanbaks, Tanguy Dufourt, Bénédicte Charrier","doi":"10.1242/dev.202732","DOIUrl":"10.1242/dev.202732","url":null,"abstract":"<p><p>Brown algae are multicellular photosynthetic organisms that have evolved independently of plants and other algae. Here, we have studied the determinism of body axis formation in the kelp Saccharina latissima. After microdissection of the embryo, we show that the stalk, an empty cell that retains the embryo on the maternal tissue, represses longitudinal cell divisions in the early embryo, thereby reinforcing the establishment of the initial apico-basal axis. In addition, it promotes cell growth and controls cell shape and arrangement in the flat oblong embryo composed of cells aligned in rows and columns. Although the stalk persists for several weeks until the embryo reaches at least 500 cells, proper embryogenesis requires connection to maternal tissue only during the first 4 days after fertilisation, i.e. before the embryo reaches the 8-cell stage. Transplantation experiments indicate that the maternal signal is not diffused in seawater, but requires contact between the embryo and the maternal tissue. This first global quantitative study of brown algal embryogenesis highlights the role of MUM, an unknown maternal message, in the control of growth axes and tissue patterning in kelp embryos.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11423915/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142072343","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-08-07DOI: 10.1242/dev.202821
Jenaid M Rees, Katie Kirk, Giacomo Gattoni, Dorit Hockman, Victoria A Sleight, Dylan J Ritter, Èlia Benito-Gutierrez, Ela W Knapik, J Gage Crump, Peter Fabian, J Andrew Gillis
{"title":"A pre-vertebrate endodermal origin of calcitonin-producing neuroendocrine cells.","authors":"Jenaid M Rees, Katie Kirk, Giacomo Gattoni, Dorit Hockman, Victoria A Sleight, Dylan J Ritter, Èlia Benito-Gutierrez, Ela W Knapik, J Gage Crump, Peter Fabian, J Andrew Gillis","doi":"10.1242/dev.202821","DOIUrl":"10.1242/dev.202821","url":null,"abstract":"<p><p>Vertebrate calcitonin-producing cells (C-cells) are neuroendocrine cells that secrete the small peptide hormone calcitonin in response to elevated blood calcium levels. Whereas mouse C-cells reside within the thyroid gland and derive from pharyngeal endoderm, avian C-cells are located within ultimobranchial glands and have been reported to derive from the neural crest. We use a comparative cell lineage tracing approach in a range of vertebrate model systems to resolve the ancestral embryonic origin of vertebrate C-cells. We find, contrary to previous studies, that chick C-cells derive from pharyngeal endoderm, with neural crest-derived cells instead contributing to connective tissue intimately associated with C-cells in the ultimobranchial gland. This endodermal origin of C-cells is conserved in a ray-finned bony fish (zebrafish) and a cartilaginous fish (the little skate, Leucoraja erinacea). Furthermore, we discover putative C-cell homologs within the endodermally-derived pharyngeal epithelium of the ascidian Ciona intestinalis and the amphioxus Branchiostoma lanceolatum, two invertebrate chordates that lack neural crest cells. Our findings point to a conserved endodermal origin of C-cells across vertebrates and to a pre-vertebrate origin of this cell type along the chordate stem.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141897072","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-10-21DOI: 10.1242/dev.202681
Li Cong Chua, On Sun Lau
{"title":"Stomatal development in the changing climate.","authors":"Li Cong Chua, On Sun Lau","doi":"10.1242/dev.202681","DOIUrl":"10.1242/dev.202681","url":null,"abstract":"<p><p>Stomata, microscopic pores flanked by symmetrical guard cells, are vital regulators of gas exchange that link plant processes with environmental dynamics. The formation of stomata involves the multi-step progression of a specialized cell lineage. Remarkably, this process is heavily influenced by environmental factors, allowing plants to adjust stomatal production to local conditions. With global warming set to alter our climate at an unprecedented pace, understanding how environmental factors impact stomatal development and plant fitness is becoming increasingly important. In this Review, we focus on the effects of carbon dioxide, high temperature and drought - three environmental factors tightly linked to global warming - on stomatal development. We summarize the stomatal response of a variety of plant species and highlight the existence of species-specific adaptations. Using the model plant Arabidopsis, we also provide an update on the molecular mechanisms involved in mediating the plasticity of stomatal development. Finally, we explore how knowledge on stomatal development is being applied to generate crop varieties with optimized stomatal traits that enhance their resilience against climate change and maintain agricultural productivity.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11528219/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142460565","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-09-26DOI: 10.1242/dev.203026
Sjoerd Woudenberg, Melissa Dipp Alvarez, Juriaan Rienstra, Victor Levitsky, Victoria Mironova, Enrico Scarpella, Andre Kuhn, Dolf Weijers
{"title":"Analysis of auxin responses in the fern Ceratopteris richardii identifies the developmental phase as a major determinant for response properties.","authors":"Sjoerd Woudenberg, Melissa Dipp Alvarez, Juriaan Rienstra, Victor Levitsky, Victoria Mironova, Enrico Scarpella, Andre Kuhn, Dolf Weijers","doi":"10.1242/dev.203026","DOIUrl":"10.1242/dev.203026","url":null,"abstract":"<p><p>The auxin signaling molecule regulates a range of plant growth and developmental processes. The core transcriptional machinery responsible for auxin-mediated responses is conserved across all land plants. Genetic, physiological and molecular exploration in bryophyte and angiosperm model species have shown both qualitative and quantitative differences in auxin responses. Given the highly divergent ontogeny of the dominant gametophyte (bryophytes) and sporophyte (angiosperms) generations, however, it is unclear whether such differences derive from distinct phylogeny or ontogeny. Here, we address this question by comparing a range of physiological, developmental and molecular responses to auxin in both generations of the model fern Ceratopteris richardii. We find that auxin response in Ceratopteris gametophytes closely resembles that of a thalloid bryophyte, whereas the sporophyte mimics auxin response in flowering plants. This resemblance manifests both at the phenotypic and transcriptional levels. Furthermore, we show that disrupting auxin transport can lead to ectopic sporophyte induction on the gametophyte, suggesting a role for auxin in the alternation of generations. Our study thus identifies developmental phase, rather than phylogeny, as a major determinant of auxin response properties in land plants.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11449451/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142343727","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Stable germline transgenesis using the Minos Tc1/mariner element in the sea urchin Lytechinus pictus.","authors":"Elliot W Jackson, Emilio Romero, Svenja Kling, Yoon Lee, Evan Tjeerdema, Amro Hamdoun","doi":"10.1242/dev.202991","DOIUrl":"10.1242/dev.202991","url":null,"abstract":"<p><p>Stable transgenesis is a transformative tool in model organism biology. Although the sea urchin is one of the oldest animal models in cell and developmental biology, studies in this animal have largely relied on transient manipulation of wild animals, without a strategy for stable transgenesis. Here, we build on recent progress to develop a more genetically tractable sea urchin species, Lytechinus pictus, and establish a robust transgene integration method. Three commonly used transposons (Minos, Tol2 and piggyBac) were tested for non-autonomous transposition, using plasmids containing a polyubiquitin promoter upstream of a H2B-mCerulean nuclear marker. Minos was the only transposable element that resulted in significant expression beyond metamorphosis. F0 animals were raised to sexual maturity, and spawned to determine germline integration and transgene inheritance frequency, and to characterize expression patterns of the transgene in F1 progeny. The results demonstrate transgene transmission through the germline, the first example of a germline transgenic sea urchin and, indeed, of any echinoderm. This milestone paves the way for the generation of diverse transgenic resources that will dramatically enhance the utility, reproducibility and efficiency of sea urchin research.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11361634/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141632962","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Regulation of ROP GTPase cycling between active and inactive states is essential for vegetative organogenesis in Marchantia polymorpha.","authors":"Yuuki Sakai, Aki Ueno, Hiroki Yonetsuka, Tatsuaki Goh, Hirotaka Kato, Yuki Kondo, Hidehiro Fukaki, Kimitsune Ishizaki","doi":"10.1242/dev.202928","DOIUrl":"10.1242/dev.202928","url":null,"abstract":"<p><p>Rho/Rac of plant (ROP) GTPases are plant-specific proteins that function as molecular switches, activated by guanine nucleotide exchange factors (GEFs) and inactivated by GTPase-activating proteins (GAPs). The bryophyte Marchantia polymorpha contains single copies of ROP (MpROP), GEFs [ROPGEF and SPIKE (SPK)] and GAPs [ROPGAP and ROP ENHANCER (REN)]. MpROP regulates the development of various tissues and organs, such as rhizoids, gemmae and air chambers. The ROPGEF KARAPPO (MpKAR) is essential for gemma initiation, but the functions of other ROP regulatory factors are less understood. This study focused on two GAPs: MpROPGAP and MpREN. Mpren single mutants showed defects in thallus growth, rhizoid tip growth, gemma development, and air-chamber formation, whereas Mpropgap mutants showed no visible abnormalities. However, Mpropgap Mpren double mutants had more severe phenotypes than the Mpren single mutants, suggesting backup roles of MpROPGAP in processes involving MpREN. Overexpression of MpROPGAP and MpREN resulted in similar gametophyte defects, highlighting the importance of MpROP activation/inactivation cycling (or balancing). Thus, MpREN predominantly, and MpROPGAP as a backup, regulate gametophyte development, likely by controlling MpROP activation in M. polymorpha.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141916323","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
DevelopmentPub Date : 2024-10-15Epub Date: 2024-10-14DOI: 10.1242/dev.203046
Frédéric Berger
{"title":"Meiosis as a mechanism for epigenetic reprogramming and cellular rejuvenation.","authors":"Frédéric Berger","doi":"10.1242/dev.203046","DOIUrl":"https://doi.org/10.1242/dev.203046","url":null,"abstract":"<p><p>Meiosis is a hallmark of sexual reproduction because it represents the transition from one life cycle to the next and, in animals, meiosis produces gametes. Why meiosis evolved has been debated and most studies have focused on recombination of the parental alleles as the main function of meiosis. However, 40 years ago, Robin Holliday proposed that an essential function of meiosis is to oppose the consequence of successive mitoses that cause cellular aging. Cellular aging results from accumulated defective organelles and proteins and modifications of chromatin in the form of DNA methylation and histone modifications referred to collectively as epigenetic marks. Here, recent findings supporting the hypothesis that meiosis opposes cellular aging are reviewed and placed in the context of the diversity of the life cycles of eukaryotes, including animals, yeast, flowering plants and the bryophyte Marchantia.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142460564","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}