{"title":"Parallel Evolution at the Regulatory Base-Pair Level Contributes to Mammalian Interspecific Differences in Polygenic Traits.","authors":"Alexander S Okamoto, Terence D Capellini","doi":"10.1093/molbev/msae157","DOIUrl":"10.1093/molbev/msae157","url":null,"abstract":"<p><p>Parallel evolution occurs when distinct lineages with similar ancestral states converge on a new phenotype. Parallel evolution has been well documented at the organ, gene pathway, and amino acid sequence level but in theory, it can also occur at individual nucleotides within noncoding regions. To examine the role of parallel evolution in shaping the biology of mammalian complex traits, we used data on single-nucleotide polymorphisms (SNPs) influencing human intraspecific variation to predict trait values in other species for 11 complex traits. We found that the alleles at SNP positions associated with human intraspecific height and red blood cell (RBC) count variation are associated with interspecific variation in the corresponding traits across mammals. These associations hold for deeper branches of mammalian evolution as well as between strains of collaborative cross mice. While variation in RBC count between primates uses both ancient and more recently evolved genomic regions, we found that only primate-specific elements were correlated with primate body size. We show that the SNP positions driving these signals are flanked by conserved sequences, maintain synteny with target genes, and overlap transcription factor binding sites. This work highlights the potential of conserved but tunable regulatory elements to be reused in parallel to facilitate evolutionary adaptation in mammals.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11321361/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141788559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"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 Possible Earliest Allopolyploidization in Tracheophytes Revealed by Phylotranscriptomics and Morphology of Selaginellaceae.","authors":"Jong-Soo Kang, Ji-Gao Yu, Qiao-Ping Xiang, Xian-Chun Zhang","doi":"10.1093/molbev/msae153","DOIUrl":"10.1093/molbev/msae153","url":null,"abstract":"<p><p>Selaginellaceae, originated in the Carboniferous and survived the Permian-Triassic mass extinction, is the largest family of lycophyte, which is sister to other tracheophytes. It stands out from tracheophytes by exhibiting extraordinary habitat diversity and lacking polyploidization. The organelle genome-based phylogenies confirmed the monophyly of Selaginella, with six or seven subgenera grouped into two superclades, but the phylogenetic positions of the enigmatic Selaginella sanguinolenta clade remained problematic. Here, we conducted a phylogenomic study on Selaginellaceae utilizing large-scale nuclear gene data from RNA-seq to elucidate the phylogeny and explore the causes of the phylogenetic incongruence of the S. sanguinolenta clade. Our phylogenetic analyses resolved three different positions of the S. sanguinolenta clade, which were supported by the sorted three nuclear gene sets, respectively. The results from the gene flow test, species network inference, and plastome-based phylogeny congruently suggested a probable hybrid origin of the S. sanguinolenta clade involving each common ancestor of the two superclades in Selaginellaceae. The hybrid hypothesis is corroborated by the evidence from rhizophore morphology and spore micromorphology. The chromosome observation and Ks distributions further suggested hybridization accompanied by polyploidization. Divergence time estimation based on independent datasets from nuclear gene sets and plastid genome data congruently inferred that allopolyploidization occurred in the Early Triassic. To our best knowledge, the allopolyploidization in the Mesozoic reported here represents the earliest record of tracheophytes. Our study revealed a unique triad of phylogenetic positions for a hybrid-originated group with comprehensive evidence and proposed a hypothesis for retaining both parental alleles through gene conversion.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11299036/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141889762","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ryan Seamus McGee, Grant Kinsler, Dmitri Petrov, Mikhail Tikhonov
{"title":"Improving the Accuracy of Bulk Fitness Assays by Correcting Barcode Processing Biases.","authors":"Ryan Seamus McGee, Grant Kinsler, Dmitri Petrov, Mikhail Tikhonov","doi":"10.1093/molbev/msae152","DOIUrl":"10.1093/molbev/msae152","url":null,"abstract":"<p><p>Measuring the fitnesses of genetic variants is a fundamental objective in evolutionary biology. A standard approach for measuring microbial fitnesses in bulk involves labeling a library of genetic variants with unique sequence barcodes, competing the labeled strains in batch culture, and using deep sequencing to track changes in the barcode abundances over time. However, idiosyncratic properties of barcodes can induce nonuniform amplification or uneven sequencing coverage that causes some barcodes to be over- or under-represented in samples. This systematic bias can result in erroneous read count trajectories and misestimates of fitness. Here, we develop a computational method, named REBAR (Removing the Effects of Bias through Analysis of Residuals), for inferring the effects of barcode processing bias by leveraging the structure of systematic deviations in the data. We illustrate this approach by applying it to two independent data sets, and demonstrate that this method estimates and corrects for bias more accurately than standard proxies, such as GC-based corrections. REBAR mitigates bias and improves fitness estimates in high-throughput assays without introducing additional complexity to the experimental protocols, with potential applications in a range of experimental evolution and mutation screening contexts.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11316221/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141748582","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ana Cristina Barragan, Sergio M Latorre, Angus Malmgren, Adeline Harant, Joe Win, Yu Sugihara, Hernán A Burbano, Sophien Kamoun, Thorsten Langner
{"title":"Multiple Horizontal Mini-chromosome Transfers Drive Genome Evolution of Clonal Blast Fungus Lineages.","authors":"Ana Cristina Barragan, Sergio M Latorre, Angus Malmgren, Adeline Harant, Joe Win, Yu Sugihara, Hernán A Burbano, Sophien Kamoun, Thorsten Langner","doi":"10.1093/molbev/msae164","DOIUrl":"10.1093/molbev/msae164","url":null,"abstract":"<p><p>Crop disease pandemics are often driven by asexually reproducing clonal lineages of plant pathogens that reproduce asexually. How these clonal pathogens continuously adapt to their hosts despite harboring limited genetic variation, and in absence of sexual recombination remains elusive. Here, we reveal multiple instances of horizontal chromosome transfer within pandemic clonal lineages of the blast fungus Magnaporthe (Syn. Pyricularia) oryzae. We identified a horizontally transferred 1.2Mb accessory mini-chromosome which is remarkably conserved between M. oryzae isolates from both the rice blast fungus lineage and the lineage infecting Indian goosegrass (Eleusine indica), a wild grass that often grows in the proximity of cultivated cereal crops. Furthermore, we show that this mini-chromosome was horizontally acquired by clonal rice blast isolates through at least nine distinct transfer events over the past three centuries. These findings establish horizontal mini-chromosome transfer as a mechanism facilitating genetic exchange among different host-associated blast fungus lineages. We propose that blast fungus populations infecting wild grasses act as genetic reservoirs that drive genome evolution of pandemic clonal lineages that afflict cereal crops.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11346369/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141897819","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Marc Beringer, Rimjhim Roy Choudhury, Terezie Mandáková, Sandra Grünig, Manuel Poretti, Ilia J Leitch, Martin A Lysak, Christian Parisod
{"title":"Biased Retention of Environment-Responsive Genes Following Genome Fractionation.","authors":"Marc Beringer, Rimjhim Roy Choudhury, Terezie Mandáková, Sandra Grünig, Manuel Poretti, Ilia J Leitch, Martin A Lysak, Christian Parisod","doi":"10.1093/molbev/msae155","DOIUrl":"10.1093/molbev/msae155","url":null,"abstract":"<p><p>The molecular underpinnings and consequences of cycles of whole-genome duplication (WGD) and subsequent gene loss through subgenome fractionation remain largely elusive. Endogenous drivers, such as transposable elements (TEs), have been postulated to shape genome-wide dominance and biased fractionation, leading to a conserved least-fractionated (LF) subgenome and a degenerated most-fractionated (MF) subgenome. In contrast, the role of exogenous factors, such as those induced by environmental stresses, has been overlooked. In this study, a chromosome-scale assembly of the alpine buckler mustard (Biscutella laevigata; Brassicaceae) that underwent a WGD event about 11 million years ago is coupled with transcriptional responses to heat, cold, drought, and herbivory to assess how gene expression is associated with differential gene retention across the MF and LF subgenomes. Counteracting the impact of TEs in reducing the expression and retention of nearby genes across the MF subgenome, dosage balance is highlighted as a main endogenous promoter of the retention of duplicated gene products under purifying selection. Consistent with the \"turn a hobby into a job\" model, about one-third of environment-responsive duplicates exhibit novel expression patterns, with one copy typically remaining conditionally expressed, whereas the other copy has evolved constitutive expression, highlighting exogenous factors as a major driver of gene retention. Showing uneven patterns of fractionation, with regions remaining unbiased, but with others showing high bias and significant enrichment in environment-responsive genes, this mesopolyploid genome presents evolutionary signatures consistent with an interplay of endogenous and exogenous factors having driven gene content following WGD-fractionation cycles.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11306978/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141788631","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lester J Pérez, Guy Baele, Samuel L Hong, Gavin A Cloherty, Michael G Berg
{"title":"Ecological Changes Exacerbating the Spread of Invasive Ticks has Driven the Dispersal of Severe Fever with Thrombocytopenia Syndrome Virus Throughout Southeast Asia.","authors":"Lester J Pérez, Guy Baele, Samuel L Hong, Gavin A Cloherty, Michael G Berg","doi":"10.1093/molbev/msae173","DOIUrl":"10.1093/molbev/msae173","url":null,"abstract":"<p><p>Severe fever with thrombocytopenia syndrome virus (SFTSV) is a tick-borne virus recognized by the World Health Organization as an emerging infectious disease of growing concern. Utilizing phylodynamic and phylogeographic methods, we have reconstructed the origin and transmission patterns of SFTSV lineages and the roles demographic, ecological, and climatic factors have played in shaping its emergence and spread throughout Asia. Environmental changes and fluctuations in tick populations, exacerbated by the widespread use of pesticides, have contributed significantly to its geographic expansion. The increased adaptability of Lineage L2 strains to the Haemaphysalis longicornis vector has facilitated the dispersal of SFTSV through Southeast Asia. Increased surveillance and proactive measures are needed to prevent further spread to Australia, Indonesia, and North America.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11349436/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142080920","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Thomas Lund Koch, Samuel D Robinson, Paula Flórez Salcedo, Kevin Chase, Jason Biggs, Alexander E Fedosov, Mark Yandell, Baldomero M Olivera, Helena Safavi-Hemami
{"title":"Prey Shifts Drive Venom Evolution in Cone Snails.","authors":"Thomas Lund Koch, Samuel D Robinson, Paula Flórez Salcedo, Kevin Chase, Jason Biggs, Alexander E Fedosov, Mark Yandell, Baldomero M Olivera, Helena Safavi-Hemami","doi":"10.1093/molbev/msae120","DOIUrl":"10.1093/molbev/msae120","url":null,"abstract":"<p><p>Venom systems are complex traits that have independently emerged multiple times in diverse plant and animal phyla. Within each venomous lineage there typically exists interspecific variation in venom composition where several factors have been proposed as drivers of variation, including phylogeny and diet. Understanding these factors is of broad biological interest and has implications for the development of antivenom therapies and venom-based drug discovery. Because of their high species richness and the presence of several major evolutionary prey shifts, venomous marine cone snails (genus Conus) provide an ideal system to investigate drivers of interspecific venom variation. Here, by analyzing the venom gland expression profiles of ∼3,000 toxin genes from 42 species of cone snail, we elucidate the role of prey-specific selection pressures in shaping venom variation. By analyzing overall venom composition and individual toxin structures, we demonstrate that the shifts from vermivory to piscivory in Conus are complemented by distinct changes in venom composition independent of phylogeny. In vivo injections of venom from piscivorous cone snails in fish further showed a higher potency compared with venom of nonpiscivores demonstrating a selective advantage. Together, our findings provide compelling evidence for the role of prey shifts in directing the venom composition of cone snails and expand our understanding of the mechanisms of venom variation and diversification.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11296725/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141469542","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mitchell Cummins, Cadel Watson, Richard J Edwards, John S Mattick
{"title":"The evolution of ultraconserved elements in vertebrates.","authors":"Mitchell Cummins, Cadel Watson, Richard J Edwards, John S Mattick","doi":"10.1093/molbev/msae146","DOIUrl":"10.1093/molbev/msae146","url":null,"abstract":"<p><p>Ultraconserved elements (UCEs) were discovered two decades ago, arbitrarily defined as sequences that are identical over a length ≥200 bp in the human, mouse and rat genomes. The definition was subsequently extended to sequences ≥100 bp identical in at least three of five mammalian genomes (including dog and cow), and shown to have undergone rapid expansion from ancestors in fish and strong negative selection in birds and mammals. Since then, many more genomes have become available, allowing better definition and more thorough examination of UCE distribution and evolutionary history. We developed a fast and flexible analytical pipeline for identifying UCEs in multiple genomes, dedUCE, which allows manipulation of minimum length, sequence identity, and number of species with a detectable UCE according to specified parameters. We suggest an updated definition of UCEs as sequences ≥100 bp and ≥97% sequence identity in ≥50% of placental mammal orders (12813 UCEs). By mapping UCEs to ∼200 species we find that placental UCEs appeared early in vertebrate evolution, well before land colonisation, suggesting the evolutionary pressures driving UCE selection were present in aquatic environments in the Cambrian-Devonian periods. Most (>90%) UCEs likely appeared after the divergence of gnathostomes from jawless predecessors, were largely established in sequence identity by early Sarcopterygii evolution - before the divergence of lobe-finned fishes from tetrapods - and became near fixed in the amniotes. UCEs are mainly located in the introns of protein-coding and non-coding genes involved in neurological and skeletomuscular development, enriched in regulatory elements, and dynamically expressed throughout embryonic development.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-07-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141627180","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Clara Iglhaut, Jūlija Pečerska, Manuel Gil, Maria Anisimova
{"title":"Please Mind the Gap: Indel-Aware Parsimony for Fast and Accurate Ancestral Sequence Reconstruction and Multiple Sequence Alignment Including Long Indels.","authors":"Clara Iglhaut, Jūlija Pečerska, Manuel Gil, Maria Anisimova","doi":"10.1093/molbev/msae109","DOIUrl":"10.1093/molbev/msae109","url":null,"abstract":"<p><p>Despite having important biological implications, insertion, and deletion (indel) events are often disregarded or mishandled during phylogenetic inference. In multiple sequence alignment, indels are represented as gaps and are estimated without considering the distinct evolutionary history of insertions and deletions. Consequently, indels are usually excluded from subsequent inference steps, such as ancestral sequence reconstruction and phylogenetic tree search. Here, we introduce indel-aware parsimony (indelMaP), a novel way to treat gaps under the parsimony criterion by considering insertions and deletions as separate evolutionary events and accounting for long indels. By identifying the precise location of an evolutionary event on the tree, we can separate overlapping indel events and use affine gap penalties for long indel modeling. Our indel-aware approach harnesses the phylogenetic signal from indels, including them into all inference stages. Validation and comparison to state-of-the-art inference tools on simulated data show that indelMaP is most suitable for densely sampled datasets with closely to moderately related sequences, where it can reach alignment quality comparable to probabilistic methods and accurately infer ancestral sequences, including indel patterns. Due to its remarkable speed, our method is well suited for epidemiological datasets, eliminating the need for downsampling and enabling the exploitation of the additional information provided by dense taxonomic sampling. Moreover, indelMaP offers new insights into the indel patterns of biologically significant sequences and advances our understanding of genetic variability by considering gaps as crucial evolutionary signals rather than mere artefacts.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-07-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11221656/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141262020","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Natalia A S Przelomska, Rudy A Diaz, Fabio Andrés Ávila, Gustavo A Ballen, Rocío Cortés-B, Logan Kistler, Daniel H Chitwood, Martha Charitonidou, Susanne S Renner, Oscar A Pérez-Escobar, Alexandre Antonelli
{"title":"Morphometrics and Phylogenomics of Coca (Erythroxylum spp.) Illuminate Its Reticulate Evolution, With Implications for Taxonomy.","authors":"Natalia A S Przelomska, Rudy A Diaz, Fabio Andrés Ávila, Gustavo A Ballen, Rocío Cortés-B, Logan Kistler, Daniel H Chitwood, Martha Charitonidou, Susanne S Renner, Oscar A Pérez-Escobar, Alexandre Antonelli","doi":"10.1093/molbev/msae114","DOIUrl":"10.1093/molbev/msae114","url":null,"abstract":"<p><p>South American coca (Erythroxylum coca and E. novogranatense) has been a keystone crop for many Andean and Amazonian communities for at least 8,000 years. However, over the last half-century, global demand for its alkaloid cocaine has driven intensive agriculture of this plant and placed it in the center of armed conflict and deforestation. To monitor the changing landscape of coca plantations, the United Nations Office on Drugs and Crime collects annual data on their areas of cultivation. However, attempts to delineate areas in which different varieties are grown have failed due to limitations around identification. In the absence of flowers, identification relies on leaf morphology, yet the extent to which this is reflected in taxonomy is uncertain. Here, we analyze the consistency of the current naming system of coca and its four closest wild relatives (the \"coca clade\"), using morphometrics, phylogenomics, molecular clocks, and population genomics. We include name-bearing type specimens of coca's closest wild relatives E. gracilipes and E. cataractarum. Morphometrics of 342 digitized herbarium specimens show that leaf shape and size fail to reliably discriminate between species and varieties. However, the statistical analyses illuminate that rounder and more obovate leaves of certain varieties could be associated with the subtle domestication syndrome of coca. Our phylogenomic data indicate extensive gene flow involving E. gracilipes which, combined with morphometrics, supports E. gracilipes being retained as a single species. Establishing a robust evolutionary-taxonomic framework for the coca clade will facilitate the development of cost-effective genotyping methods to support reliable identification.</p>","PeriodicalId":18730,"journal":{"name":"Molecular biology and evolution","volume":null,"pages":null},"PeriodicalIF":11.0,"publicationDate":"2024-07-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11233275/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141563759","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}