{"title":"Interspecific comparisons of anuran embryonic epidermal landscapes and energetic trade-offs in response to changes in salinity.","authors":"Kourtnie Whitfield, Erica J Crespi","doi":"10.1002/dvdy.70016","DOIUrl":"https://doi.org/10.1002/dvdy.70016","url":null,"abstract":"<p><strong>Background: </strong>Freshwater salinization is an emerging stressor in amphibian populations, and embryonic stages are most vulnerable. To better understand the variation in embryonic osmoregulation, we challenged embryos of two phylogenetically diverse anuran species, Xenopus laevis and Lithobates (Rana) sylvaticus, along a gradient of non-lethal salinities. We hypothesized embryos at higher salinities will display epidermal plasticity as a coping response and increase energy expenditure related to osmoregulation demands, thereby reducing energy for growth and development.</p><p><strong>Results: </strong>Scanning electron microscopy revealed an extra mucus-secreting cell type and higher ionocyte proportions in the X. laevis epidermis, suggesting more osmoregulatory machinery than L. sylvaticus. Under elevated salinity, X. laevis displayed greater increases in goblet cell proportions, mucus secretion, and reductions in ionocyte apical area compared with L. sylvaticus. Although both species increased oxygen consumption rates and reduced body length with elevated salinity, these effects were proportionally greater in L. sylvaticus at the highest salinity, and only this species slowed developmental rates.</p><p><strong>Conclusion: </strong>These findings support the hypothesis that frog embryos respond to salinity by altering the cellular landscape of their epidermis. We show that epidermal cell types, as well as the magnitude of epidermal plasticity and energetic trade-offs in response to salinity, vary among amphibian species.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143647400","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Philip L Reno, Sherrie Wallace, Sarah N Doelp, Maria Biancaniello, Kelsey M Kjosness
{"title":"The role of the PTHrP/Ihh feedback loop in the unusual growth plate location in mammalian metatarsals and pisiforms.","authors":"Philip L Reno, Sherrie Wallace, Sarah N Doelp, Maria Biancaniello, Kelsey M Kjosness","doi":"10.1002/dvdy.70013","DOIUrl":"https://doi.org/10.1002/dvdy.70013","url":null,"abstract":"<p><strong>Background: </strong>Longitudinal skeletal growth takes place in the cartilaginous growth plates. While growth plates are found at either end of conventional long bones, they occur at a variety of locations in the mammalian skeleton. For example, the metacarpals and metatarsals (MT) in the hands and feet form only a single growth plate at one end, and the pisiform in the wrist is the only carpal bone to contain a growth plate. We take advantage of this natural anatomical variation to test which components of the PTHrP/Ihh feedback loop, a fundamental regulator of chondrocyte differentiation, are specific to growth plate function.</p><p><strong>Results: </strong>Parathyroid hormone-like hormone (Pthlh), the gene that transcribes parathyroid hormone-related peptide (PTHrP), is expressed in the reserve zone of the growth plate-forming end of the MT. At the opposite end, the absence of a PTHrP+ reserve zone results in premature chondrocyte differentiation and Indian hedgehog (Ihh) expression. Pthlh is expressed in the reserve zone of the developing pisiform, confirming the existence of a true growth plate.</p><p><strong>Conclusion: </strong>A pool of PTHrP+ reserve zone chondrocytes is a defining characteristic of growth plates, and its patterning may be key to evolved differences in growth plate location in the mammalian skeleton.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143633774","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kathy Jacyniak, Karemna Barrera Jaimes, Minh Hanh Doan, Jordyn M Chartrand, Matthew K Vickaryous
{"title":"Squamate ventricular cardiomyocytes: Ploidy, proliferation, and heart muscle cell size in the leopard gecko (Eublepharis macularius).","authors":"Kathy Jacyniak, Karemna Barrera Jaimes, Minh Hanh Doan, Jordyn M Chartrand, Matthew K Vickaryous","doi":"10.1002/dvdy.70015","DOIUrl":"https://doi.org/10.1002/dvdy.70015","url":null,"abstract":"<p><strong>Background: </strong>While heart function is broadly conserved across vertebrates, the cellular phenotype of muscle cells (cardiomyocytes) varies across taxa and throughout ontogeny. Emerging evidence suggests that some attributes may correlate with the capacity for spontaneous cardiomyocyte replacement following injury. For example, among non-regenerating taxa like adult mammals and birds, cardiomyocytes are polyploid, rarely proliferate, and are large in size. In contrast, in regeneration-competent zebrafish and amphibians, cardiomyocytes are diploid, spontaneously proliferate, and are comparatively small. For other species, less is known.</p><p><strong>Results: </strong>Here, we investigate these attributes in the squamate Eublepharis macularius, the leopard gecko. Using the nuclear counterstain DAPI to measure fluorescence intensity as a proxy for DNA content, we found that >90% of adult cardiomyocytes are diploid. Using serial histology and immunostaining for markers of DNA synthesis and mitosis, we determined that adult gecko cardiomyocytes spontaneously proliferate, albeit at significantly lower levels than previously reported in subadults. Furthermore, using wheat germ agglutinin, we found that the cross-sectional area is maintained across ontogeny and that gecko cardiomyocytes are 10× smaller than those of mice.</p><p><strong>Conclusions: </strong>Taken together, our data show that gecko cardiomyocytes share several key cellular attributes with regeneration-competent species and that postnatal ventricular growth occurs via cardiomyocyte hyperplasia.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143633773","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Stephen Spurgin, Ange Michelle Nguimtsop, Fatima N Chaudhry, Sylvia N Michki, Jocelynda Salvador, M Luisa Iruela-Arispe, Jarod A Zepp, Saikat Mukhopadhyay, Ondine Cleaver
{"title":"Dynamics of primary cilia in endothelial and mesenchymal cells throughout mouse lung development.","authors":"Stephen Spurgin, Ange Michelle Nguimtsop, Fatima N Chaudhry, Sylvia N Michki, Jocelynda Salvador, M Luisa Iruela-Arispe, Jarod A Zepp, Saikat Mukhopadhyay, Ondine Cleaver","doi":"10.1002/dvdy.70008","DOIUrl":"10.1002/dvdy.70008","url":null,"abstract":"<p><p>Cilia are specialized structures found on a variety of mammalian cells, with variable roles in the transduction of mechanical and biological signals (by primary cilia, PC), as well as in the generation of fluid flow (by motile cilia). Their critical role in the establishment of a left-right axis in early development is well described, as well as in the defense immune function of multiciliated upper airway epithelium. By contrast, detailed analysis of the ciliary status of specific cell types during organogenesis and postnatal development has received less attention. In this study, we investigate the progression of ciliary status within the endothelium and mesenchyme of the lung. Remarkably, we find that pulmonary endothelial cells (ECs) lack PC at all stages of development, except in low numbers in the proximal portions of older pulmonary arteries. Mesenchymal cells, by contrast, widely exhibit PC in early development, and a large subset of PDGFRα+ fibroblasts maintain PC into adulthood. The dynamic and differential ciliation of multiple cellular populations in the developing lung both challenges prior assertions that PC are found on all cells and highlights a need to understand their spatiotemporal functions.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143583722","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Human stem cell model of neural crest cell differentiation reveals a requirement of SF3B4 in survival, maintenance, and differentiation.","authors":"Casey Griffin, Jean-Pierre Saint-Jeannet","doi":"10.1002/dvdy.70009","DOIUrl":"10.1002/dvdy.70009","url":null,"abstract":"<p><strong>Background: </strong>In vitro modeling is a powerful approach to investigate the pathomechanisms driving human congenital conditions. Here, we use human embryonic stem cells (hESCs) to model Nager and Rodriguez syndromes, two craniofacial conditions characterized by hypoplastic neural crest-derived craniofacial bones, caused by pathogenic variants of SF3B4, a core component of the spliceosome.</p><p><strong>Results: </strong>We observed that siRNA-mediated knockdown of SF3B4 interferes with the production of hESC-derived neural crest cells, as seen by a marked reduction in neural crest gene expression. This phenotype is associated with an increase in neural crest cell apoptosis and premature neuronal differentiation.</p><p><strong>Conclusions: </strong>Altogether, these results point to a role of SF3B4 in neural crest cell survival, maintenance, and differentiation. We propose that the dysregulation of these processes may contribute to Nager/Rodriguez syndrome-associated craniofacial defects.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143566316","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Editorial highlights","authors":"Paul A. Trainor","doi":"10.1002/dvdy.70007","DOIUrl":"https://doi.org/10.1002/dvdy.70007","url":null,"abstract":"<p>Every organism is a model organism for understanding development, evolution, disease, and regeneration, and we have only begun to scratch the surface of the interdisciplinary genetic, molecular, cellular, and developmental mechanisms that regulate these biological processes. These “highlights” denote exciting advances recently reported in <i>Developmental Dynamics</i> that illustrate the complex dynamics of developmental biology.</p><p><b>Regeneration</b> “Functional significance of earthworm clitellum in regulating the various biological aspects of cell survival and regeneration” by Jackson Durairaj Selvan Christyraj, Ashwin Barath Vaidhyalingham, Chandini Sengupta, Kamarajan Rajagopalan, Kayalvizhi Vadivelu, Nandha Kumar Suresh, and Bharathi Venkatachalam <i>Dev Dyn</i> 254.3, pp. 212–221, https://doi.org/10.1002/dvdy.751. Earthworms exhibit a remarkable ability to rapidly heal and completely regenerate within a short period of time. Earthworms are therefore an ideal model for studying the mechanisms that regulate stem cell biology and regeneration. Over 7000 different species of earthworms have been identified and described, and this review describes new insights into the functions of the clitellum, which is a glandular structure that sits near the head. During epimorphosis, undifferentiated stem cells that reside in the clitellar region divide and form a blastema, which then develops into new tissue. In contrast, during morphallaxis, in which regeneration occurs without the formation of a blastema, it is thought that cells in the clitellum undergo trans-differentiation. Either way, the clitellum is regarded as a stem cell reservoir that regulates regeneration. However, in addition to regeneration, the clitellum plays essential roles in reproduction, organogenesis, and aging.</p><p><b>Cardiovascular Biology</b> “Modulation of mechanosensitive genes during embryonic aortic arch development” by Hummaira Banu Siddiqui, Tansu Golcez, Merve Çelik, Börteçine Sevgin, Mervenur Çoban, İlke Süder, Özen Kaya, Nesrin Özören, and Kerem Pekkan <i>Dev Dyn</i> 254.3, pp. 222–239, https://doi.org/10.1002/dvdy.728. The embryonic aortic arches are dynamic vascular structures that develop into the great arteries of the cardiovascular system. The extracellular matrix is known to play important roles in aortic arch and vascular morphogenesis, and computational and other types of modeling have linked mechanical properties such as blood pressure, wall shear stress, outflow tract orientation, and blood flow, to the developmental morphology of the aortic arches. Developmental malformations of the aortic arches manifest as congenital heart defects. In this study, the authors modulated the activity of genes associated with wall shear stress such as TGFβ3 and MMP2. TGFβ3 knockdown results in decreases in collagen and elastin density, with corresponding alterations in hemodynamics and blood pressure, that lead to detrimental effects on lumen diameter and the accumulatio","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":"254 3","pages":"210-211"},"PeriodicalIF":2.0,"publicationDate":"2025-03-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/dvdy.70007","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143535791","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The synergistic link between sonic hedgehog signaling pathway and gut-lung axis: Its influential role toward chronic obstructive pulmonary disease progression.","authors":"Nidhi Mahajan, Vishal Chopra, Kranti Garg, Siddharth Sharma","doi":"10.1002/dvdy.70006","DOIUrl":"https://doi.org/10.1002/dvdy.70006","url":null,"abstract":"<p><p>Sonic Hedgehog (SHH) is an evolutionarily conserved signaling pathway essential for embryonic development, tissue homeostasis, and tumorigenesis. Aberrant activation of the SHH pathway induces various types of cancer and different types of immune dysregulation. SHH is an extremely important morphogen during lung development, as it regulates the interaction between epithelial and mesenchymal transitions (EMT) in the airways. Cigarette smoking triggers the EMT and activates the SHH signaling pathway, which leads to lung damage and the development of various lung diseases, such as COPD, a smoker's disease. SHH also directs the gut-lung axis (GLA) formation via epithelial-mesenchymal signaling. The abruption or alteration of GLA formation is also responsible for COPD pathogenesis. In this review, we elucidate an overview of the SHH pathway and its inhibitor HHIP, SHH's prominence during lung development, and the dysregulation of the SHH signaling pathway in COPD pathogenesis and its link with COPD clinical features. We also provide insights into the SHH pathway linked with the nicotine pathway and gut-lung axis and their influence on COPD pathogenesis.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143540525","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jason C Mills, Nattapon Thanintorn, Yongjun Yin, Helen McNeill, David M Ornitz, Spencer G Willet
{"title":"Gastric hypoplasia in mice lacking fibroblast growth factor 9.","authors":"Jason C Mills, Nattapon Thanintorn, Yongjun Yin, Helen McNeill, David M Ornitz, Spencer G Willet","doi":"10.1002/dvdy.70000","DOIUrl":"10.1002/dvdy.70000","url":null,"abstract":"<p><strong>Background: </strong>Fibroblast Growth Factor 9 (Fgf9) and its paralog Fgf20 are expressed in the developing stomach. We investigate the role of these growth factors during gastric development, using combinations of null alleles.</p><p><strong>Results: </strong>Analysis of expression databases showed that Fgf9 is expressed in gastric endoderm and surrounding mesoderm such as the mesothelium as early as E8.5, and Fgf20 is expressed in the gastric progenitors of the glandular stomach. To explore whether Fgf9 and Fgf20 are important for gastric development, we examined embryonic stomachs from Fgf9 and Fgf20 null (Fgf9<sup>LacZ/LacZ</sup> and Fgf20<sup>Cre.GFP/Cre.GFP</sup>) mice during development. At E18.5, Fgf9<sup>LacZ/LacZ</sup> stomachs were hypoplastic, lacking the squamous forestomach. No changes to glandular stomach differentiation were observed using representative markers of glandular lineages. Fgf9<sup>LacZ/LacZ</sup> stomachs were smaller during early development (E12.5 and E15.5). RNA-seq analysis of Fgf9<sup>LacZ/LacZ</sup> mice at E15.5 showed that squamous-epithelium-associated transcripts were underrepresented, and glandular epithelial transcripts were overrepresented. Analysis of gastric patterning at E12.5 revealed loss of early squamous progenitors in the epithelium, characterized by loss of SOX2<sup>+</sup>; GATA4<sup>-</sup> cells. We further show that loss of Fgf20 does not alone impact gastric development nor modify the Fgf9<sup>LacZ/LacZ</sup> phenotype.</p><p><strong>Conclusions: </strong>Fgf9 drives gastric growth and squamous epithelial identity during gastric development.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-03-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143531265","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Claudio Araya, Raegan Boekemeyer, Francesca Farlie, Lauren Moon, Freshta Darwish, Chris Rookyard, Leanne Allison, Gema Vizcay-Barrena, Roland Fleck, Millaray Aranda, Masa Tada, Jonathan D W Clarke
{"title":"An analysis of contractile and protrusive cell behaviors at the superficial surface of the zebrafish neural plate.","authors":"Claudio Araya, Raegan Boekemeyer, Francesca Farlie, Lauren Moon, Freshta Darwish, Chris Rookyard, Leanne Allison, Gema Vizcay-Barrena, Roland Fleck, Millaray Aranda, Masa Tada, Jonathan D W Clarke","doi":"10.1002/dvdy.70001","DOIUrl":"https://doi.org/10.1002/dvdy.70001","url":null,"abstract":"<p><strong>Background: </strong>The forces underlying convergence and internalization of the teleost neural plate remain unknown. To help understand this morphogenesis, we analyzed collective and individual cell behaviors at the superficial surface of the neural plate as internalization begins to form the neural keel in the hindbrain region of the zebrafish embryo.</p><p><strong>Results: </strong>Convergence to the midline is not accompanied by anteroposterior elongation at this stage, and it is characterized by oscillatory contractile behaviors at the superficial surface of the neural plate, a punctate distribution of Cdh2 and medially polarized actin-rich protrusions at the surface of the neural plate. We also characterize the intimate relationship and dynamic protrusive cell behaviors between the surfaces of the motile neural plate and the stationary overlying non-neural enveloping layer.</p><p><strong>Conclusions: </strong>Superficial neural plate cells are coupled by a punctate distribution of Cdh2-rich adhesions. At this surface, cells tug on neighbors using oscillatory contractions. Oscillatory contractions accompany convergence and shrinkage of the cells' superficial surface for internalization during keeling. Some shrinkage for internalization occurs without oscillations. The deep surface of the overlying non-neural enveloping layer is in contact with the superficial surface of the neural plate, suggesting that it may constrain the neural plate movements of convergence and internalization.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-02-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143476344","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nishanthi Mathiyalagan, Travis K Johnson, Zachary Di Pastena, Jarrad N Fuller, Lee B Miles, Sebastian Dworkin
{"title":"Loss of the epithelial transcription factor grhl3 leads to variably penetrant developmental phenotypes in zebrafish.","authors":"Nishanthi Mathiyalagan, Travis K Johnson, Zachary Di Pastena, Jarrad N Fuller, Lee B Miles, Sebastian Dworkin","doi":"10.1002/dvdy.70003","DOIUrl":"https://doi.org/10.1002/dvdy.70003","url":null,"abstract":"<p><strong>Background: </strong>Environmental influence is critical for embryogenesis but is significantly under-appreciated under lab conditions, which are not typically designed to robustly test environmental variability. Here, we report environmental effects on the developmental phenotype of zebrafish lacking the transcription factor Grainyhead-like 3 (grhl3), a highly conserved gene that is pivotal in epithelial barrier formation, neurulation, craniofacial development, and convergence-extension.</p><p><strong>Results: </strong>We had previously reported that deletion of grhl3 led to embryonic lethality by 11 h post-fertilization (hpf); however, housing these grhl3-lines in a different aquatic facility led to substantial differences in phenotypic presentation in grhl3-nullizygous (grhl3<sup>-/-</sup>) embryos. We found that grhl3<sup>-/-</sup> embryos presented with three distinct phenotypes, characterized by significant reductions in body length, aberrant orofacial cavity formation and craniofacial morphogenesis and impaired intestinal barrier maintenance.</p><p><strong>Conclusions: </strong>Our study describes a new model of partial phenotypic penetrance in genetically identical embryos. This may serve as a valuable model system in which to understand gene-environment interactions in developmental and epithelial homeostasis.</p>","PeriodicalId":11247,"journal":{"name":"Developmental Dynamics","volume":" ","pages":""},"PeriodicalIF":2.0,"publicationDate":"2025-02-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143457182","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}