Background: Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings.
Results: We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism's ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments.
Conclusions: Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.
{"title":"Degenerated vision, altered lipid metabolism, and expanded chemoreceptor repertoires enable Lindaspio polybranchiata to thrive in deep-sea cold seeps.","authors":"Yujie Yan, Inge Seim, Yang Guo, Xupeng Chi, Zhaoshan Zhong, Dantong Wang, Mengna Li, Haining Wang, Huan Zhang, Minxiao Wang, Chaolun Li","doi":"10.1186/s12915-025-02112-2","DOIUrl":"10.1186/s12915-025-02112-2","url":null,"abstract":"<p><strong>Background: </strong>Lindaspio polybranchiata, a member of the Spionidae family, has been reported at the Lingshui Cold Seep, where it formed a dense population around this nascent methane vent. We sequenced and assembled the genome of L. polybranchiata and performed comparative genomic analyses to investigate the genetic basis of adaptation to the deep sea. Supporting this, transcriptomic and fatty acid data further corroborate our findings.</p><p><strong>Results: </strong>We report the first genome of a deep-sea spionid, L. polybranchiata. Over long-term adaptive evolution, genes associated with vision and biological rhythmicity were lost, which may indirectly benefit oligotrophy by eliminating energetically costly processes. Compared to its shallow-sea relatives, L. polybranchiata has a significantly higher proportion of polyunsaturated fatty acids (PUFAs) and expanded gene families involved in the biosynthesis of unsaturated fatty acids and chromatin stabilization, possibly in response to high hydrostatic pressure. Additionally, L. polybranchiata has broad digestive scope, allowing it to fully utilize the limited food resources in the deep sea to sustain a large population. As a pioneer species, L. polybranchiata has an expanded repertoire of genes encoding potential chemoreceptor proteins, including ionotropic receptors (IRs) and gustatory receptor-like receptors (GRLs). These proteins, characterized by their conserved 3D structures, may enhance the organism's ability to detect chemical cues in chemosynthetic ecosystems, facilitating rapid settlement in suitable environments.</p><p><strong>Conclusions: </strong>Our results shed light on the adaptation of Lindaspio to the darkness, high hydrostatic pressure, and food deprivation in the deep sea, providing insights into the molecular basis for L. polybranchiata becoming a pioneer species.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"13"},"PeriodicalIF":4.4,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11730519/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142977758","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}
Pub Date : 2025-01-13DOI: 10.1186/s12915-025-02117-x
Andrea Becchimanzi, Giovanna De Leva, Rosanna Mattossovich, Serena Camerini, Marialuisa Casella, Giovanni Jesu, Ilaria Di Lelio, Sabrina Di Giorgi, Joachim R de Miranda, Anna Valenti, Silvia Gigliotti, Francesco Pennacchio
Background: Deformed wing virus (DWV) is a major honey bee pathogen that is actively transmitted by the parasitic mite Varroa destructor and plays a primary role in Apis mellifera winter colony losses. Despite intense investigation on this pollinator, which has a unique environmental and economic importance, the mechanisms underlying the molecular interactions between DWV and honey bees are still poorly understood. Here, we report on a group of honey bee proteins, identified by mass spectrometry, that specifically co-immunoprecipitate with DWV virus particles.
Results: Most of the proteins identified are involved in fundamental metabolic pathways. Among the co-immunoprecipitated proteins, one of the most interesting was arginine kinase (ArgK), a conserved protein playing multiple roles both in physiological and pathological processes and stress response in general. Here, we investigated in more detail the relationship between DWV and this protein. We found that argK RNA level positively correlates with DWV load in field-collected honey bee larvae and adults and significantly increases in adults upon DWV injection in controlled laboratory conditions, indicating that the argK gene was upregulated by DWV infection. Silencing argK gene expression in vitro, using RNAi, resulted in reduced DWV viral load, thus confirming that argK upregulation facilitates DWV infection, likely through interfering with the delicate balance between metabolism and immunity.
Conclusions: In summary, these data indicate that DWV modulates the host ArgK through transcriptional regulation and cooptation to enhance its fitness in honey bees. Our findings open novel perspectives on possible new therapies for DWV control by targeting specific host proteins.
{"title":"Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera).","authors":"Andrea Becchimanzi, Giovanna De Leva, Rosanna Mattossovich, Serena Camerini, Marialuisa Casella, Giovanni Jesu, Ilaria Di Lelio, Sabrina Di Giorgi, Joachim R de Miranda, Anna Valenti, Silvia Gigliotti, Francesco Pennacchio","doi":"10.1186/s12915-025-02117-x","DOIUrl":"10.1186/s12915-025-02117-x","url":null,"abstract":"<p><strong>Background: </strong>Deformed wing virus (DWV) is a major honey bee pathogen that is actively transmitted by the parasitic mite Varroa destructor and plays a primary role in Apis mellifera winter colony losses. Despite intense investigation on this pollinator, which has a unique environmental and economic importance, the mechanisms underlying the molecular interactions between DWV and honey bees are still poorly understood. Here, we report on a group of honey bee proteins, identified by mass spectrometry, that specifically co-immunoprecipitate with DWV virus particles.</p><p><strong>Results: </strong>Most of the proteins identified are involved in fundamental metabolic pathways. Among the co-immunoprecipitated proteins, one of the most interesting was arginine kinase (ArgK), a conserved protein playing multiple roles both in physiological and pathological processes and stress response in general. Here, we investigated in more detail the relationship between DWV and this protein. We found that argK RNA level positively correlates with DWV load in field-collected honey bee larvae and adults and significantly increases in adults upon DWV injection in controlled laboratory conditions, indicating that the argK gene was upregulated by DWV infection. Silencing argK gene expression in vitro, using RNAi, resulted in reduced DWV viral load, thus confirming that argK upregulation facilitates DWV infection, likely through interfering with the delicate balance between metabolism and immunity.</p><p><strong>Conclusions: </strong>In summary, these data indicate that DWV modulates the host ArgK through transcriptional regulation and cooptation to enhance its fitness in honey bees. Our findings open novel perspectives on possible new therapies for DWV control by targeting specific host proteins.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"12"},"PeriodicalIF":4.4,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11727705/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142969720","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}
Pub Date : 2025-01-13DOI: 10.1186/s12915-024-02091-w
Armando J Cruz-Laufer, Maarten P M Vanhove, Lutz Bachmann, Maxwell Barson, Hassan Bassirou, Arnold R Bitja Nyom, Mare Geraerts, Christoph Hahn, Tine Huyse, Gyrhaiss Kapepula Kasembele, Samuel Njom, Philipp Resl, Karen Smeets, Nikol Kmentová
Background: Stress responses are key the survival of parasites and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the evolution of molecular pathways dealing with environmental stressors in parasitic animals remains limited. Here, we tested the link between adaptive evolution of parasite stress response genes and their ecological diversity and species richness. We comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two model parasitic flatworm lineages with contrasting ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monopisthocotyla), through whole-genome sequencing of 11 species followed by in silico exon bait capture as well as phylogenetic and codon analyses.
Results: We assembled the sequences of 48 stress-related genes and report the first foraging (For) gene orthologs in flatworms. We found duplications of heat shock (Hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (Hsp) and behaviour (For) in species of Cichlidogyrus infecting East African cichlids-a host lineage under adaptive radiation. These patterns are consistent with a potential adaptation linked to a co-radiation of these parasites and their hosts. Additionally, the absence of cytochrome P450 and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes considered essential for metazoan life.
Conclusions: This study potentially identifies the first molecular function linked to a flatworm radiation. Furthermore, the observed gene duplications and positive selection indicate the potentially important role of stress responses for the ecological adaptation of parasite species.
{"title":"Adaptive evolution of stress response genes in parasites aligns with host niche diversity.","authors":"Armando J Cruz-Laufer, Maarten P M Vanhove, Lutz Bachmann, Maxwell Barson, Hassan Bassirou, Arnold R Bitja Nyom, Mare Geraerts, Christoph Hahn, Tine Huyse, Gyrhaiss Kapepula Kasembele, Samuel Njom, Philipp Resl, Karen Smeets, Nikol Kmentová","doi":"10.1186/s12915-024-02091-w","DOIUrl":"10.1186/s12915-024-02091-w","url":null,"abstract":"<p><strong>Background: </strong>Stress responses are key the survival of parasites and, consequently, also the evolutionary success of these organisms. Despite this importance, our understanding of the evolution of molecular pathways dealing with environmental stressors in parasitic animals remains limited. Here, we tested the link between adaptive evolution of parasite stress response genes and their ecological diversity and species richness. We comparatively investigated antioxidant, heat shock, osmoregulatory, and behaviour-related genes (foraging) in two model parasitic flatworm lineages with contrasting ecological diversity, Cichlidogyrus and Kapentagyrus (Platyhelminthes: Monopisthocotyla), through whole-genome sequencing of 11 species followed by in silico exon bait capture as well as phylogenetic and codon analyses.</p><p><strong>Results: </strong>We assembled the sequences of 48 stress-related genes and report the first foraging (For) gene orthologs in flatworms. We found duplications of heat shock (Hsp) and oxidative stress genes in Cichlidogyrus compared to Kapentagyrus. We also observed positive selection patterns in genes related to mitochondrial protein import (Hsp) and behaviour (For) in species of Cichlidogyrus infecting East African cichlids-a host lineage under adaptive radiation. These patterns are consistent with a potential adaptation linked to a co-radiation of these parasites and their hosts. Additionally, the absence of cytochrome P450 and kappa and sigma-class glutathione S-transferases in monogenean flatworms is reported, genes considered essential for metazoan life.</p><p><strong>Conclusions: </strong>This study potentially identifies the first molecular function linked to a flatworm radiation. Furthermore, the observed gene duplications and positive selection indicate the potentially important role of stress responses for the ecological adaptation of parasite species.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"10"},"PeriodicalIF":4.4,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11727194/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142969719","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}
Pub Date : 2025-01-13DOI: 10.1186/s12915-025-02116-y
Jiaying Wu, Min Li, Wanni Wang, Yiren Su, Jie Li, Jiaxin Gong, Xianfeng Meng, Chenyuan Lin, Qiantong Zhang, Yanyan Yang, Chunyan Xu, Limei Zeng, Jihong Jiang, Xuqin Yang
Background: The variations in alliin content are a crucial criterion for evaluating garlic quality and is the sole precursor for allicin biosynthesis, which is significant for the growth, development, and stress response of garlic. WRKY transcription factors are essential for enhancing stress resistance by regulating the synthesis of plant secondary metabolites. However, the molecular mechanisms regulating alliin biosynthesis remain unexplored. Here, we report for the first time that a WRKY family transcription factor regulates the expression of a key enzyme gene in the alliin biosynthesis pathway, enhancing the accumulation of alliin.
Results: AsWRKY9 was most highly expressed in garlic leaves, and its expression was significantly upregulated at various time points following leaf injury. Moreover, we established an improved garlic callus induction medium based on MS medium with 1.5 mg/L 2,4-D and 0.5 mg/L NAA, suitable for "PiZi" garlic bulbils. In transgenic callus overexpressing AsWRKY9, the transcription level of the key enzyme flavin-containing monooxygenase gene (AsFMO1) significantly higher, as did its enzymatic activity compared with the control. Subcellular localization revealed that AsWRKY9 is located in the nucleus. The promoter sequence of AsFMO1 was then obtained using genomee walking. Yeast one-hybrid (Y1H) and dual-luciferase assays (LUC) confirmed that AsWRKY9 interact with the AsFMO1 promoter. Further verification by electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation qPCR (ChIP-qPCR) confirmed that AsWRKY9 interacts by binding to the W-box site on the AsFMO1 promoter. Compared to the control, the alliin content in the transgenic callus overexpressing AsWRKY9 was significantly increased, thus confirming the activation of the alliin biosynthesis pathway and enhancing the accumulation of alliin in garlic.
Conclusions: Our study reveals the crucial role of AsWRKY9 in alliin biosynthesis, filling a gap in the complex transcriptional regulation of the alliin biosynthetic pathway. It provides a new molecular breeding strategy for developing garlic varieties with high alliin content.
{"title":"Identification and functional characterization of AsWRKY9, a WRKY transcription factor modulating alliin biosynthesis in garlic (Allium sativum L.).","authors":"Jiaying Wu, Min Li, Wanni Wang, Yiren Su, Jie Li, Jiaxin Gong, Xianfeng Meng, Chenyuan Lin, Qiantong Zhang, Yanyan Yang, Chunyan Xu, Limei Zeng, Jihong Jiang, Xuqin Yang","doi":"10.1186/s12915-025-02116-y","DOIUrl":"https://doi.org/10.1186/s12915-025-02116-y","url":null,"abstract":"<p><strong>Background: </strong>The variations in alliin content are a crucial criterion for evaluating garlic quality and is the sole precursor for allicin biosynthesis, which is significant for the growth, development, and stress response of garlic. WRKY transcription factors are essential for enhancing stress resistance by regulating the synthesis of plant secondary metabolites. However, the molecular mechanisms regulating alliin biosynthesis remain unexplored. Here, we report for the first time that a WRKY family transcription factor regulates the expression of a key enzyme gene in the alliin biosynthesis pathway, enhancing the accumulation of alliin.</p><p><strong>Results: </strong>AsWRKY9 was most highly expressed in garlic leaves, and its expression was significantly upregulated at various time points following leaf injury. Moreover, we established an improved garlic callus induction medium based on MS medium with 1.5 mg/L 2,4-D and 0.5 mg/L NAA, suitable for \"PiZi\" garlic bulbils. In transgenic callus overexpressing AsWRKY9, the transcription level of the key enzyme flavin-containing monooxygenase gene (AsFMO1) significantly higher, as did its enzymatic activity compared with the control. Subcellular localization revealed that AsWRKY9 is located in the nucleus. The promoter sequence of AsFMO1 was then obtained using genomee walking. Yeast one-hybrid (Y1H) and dual-luciferase assays (LUC) confirmed that AsWRKY9 interact with the AsFMO1 promoter. Further verification by electrophoretic mobility shift assay (EMSA) and chromatin immunoprecipitation qPCR (ChIP-qPCR) confirmed that AsWRKY9 interacts by binding to the W-box site on the AsFMO1 promoter. Compared to the control, the alliin content in the transgenic callus overexpressing AsWRKY9 was significantly increased, thus confirming the activation of the alliin biosynthesis pathway and enhancing the accumulation of alliin in garlic.</p><p><strong>Conclusions: </strong>Our study reveals the crucial role of AsWRKY9 in alliin biosynthesis, filling a gap in the complex transcriptional regulation of the alliin biosynthetic pathway. It provides a new molecular breeding strategy for developing garlic varieties with high alliin content.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"14"},"PeriodicalIF":4.4,"publicationDate":"2025-01-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11731438/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143055778","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}
Pub Date : 2025-01-10DOI: 10.1186/s12915-025-02115-z
Jiali Kong, Jie Wang, Liyun Nie, Luke R Tembrock, Changsong Zou, Shenglong Kan, Xiongfeng Ma, Jonathan F Wendel, Zhiqiang Wu
Background: Plant mitochondrial genomes (mitogenomes) exhibit extensive structural variation yet extremely low nucleotide mutation rates, phenomena that remain only partially understood. The genus Gossypium, a globally important source of cotton, offers a wealth of long-read sequencing resources to explore mitogenome and plastome variation and dynamics accompanying the evolutionary divergence of its approximately 50 diploid and allopolyploid species.
Results: Here, we assembled 19 mitogenomes from Gossypium species, representing all genome groups (diploids A through G, K, and the allopolyploids AD) based on a uniformly applied strategy. A graph-based mitogenome assembly method revealed more alternative structural conformations than previously recognized, some of which confirmed the mitogenome structure reported in earlier studies on cotton. Using long-read data, we quantified alternative conformations mediated by recombination events between repeats, and phylogenetically informative structural variants were noted. Nucleotide substitution rate comparisons between coding and non-coding regions revealed low mutation rates across the entire mitogenome. Genome-wide mapping of nuclear organellar DNA transfers (NUOTs) in Gossypium revealed a nonrandom distribution of transfers in the nuclear genome. In cotton, the fate of NUOT events varied, with mitochondrion-to-nucleus transfer (NUMT) predominantly retained as short fragments in the nuclear genome, with more plastid sequences integrated into the nucleus. Phylogenetic relationships inferred using different data sets highlighted distinct evolutionary histories among these cellular compartments, providing ancillary evidence relevant to the evolutionary history of Gossypium.
Conclusions: A comprehensive analysis of organellar genome variation demonstrates complex structural variation and low mutation rates across the entire mitogenome and reveals the history of organellar genome transfer among the three genomes throughout the cotton genus. The findings enhance our general understanding of mitogenome evolution, comparative organellar and nuclear evolutionary rates, and the history of inter-compartment genomic integration.
{"title":"Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species.","authors":"Jiali Kong, Jie Wang, Liyun Nie, Luke R Tembrock, Changsong Zou, Shenglong Kan, Xiongfeng Ma, Jonathan F Wendel, Zhiqiang Wu","doi":"10.1186/s12915-025-02115-z","DOIUrl":"10.1186/s12915-025-02115-z","url":null,"abstract":"<p><strong>Background: </strong>Plant mitochondrial genomes (mitogenomes) exhibit extensive structural variation yet extremely low nucleotide mutation rates, phenomena that remain only partially understood. The genus Gossypium, a globally important source of cotton, offers a wealth of long-read sequencing resources to explore mitogenome and plastome variation and dynamics accompanying the evolutionary divergence of its approximately 50 diploid and allopolyploid species.</p><p><strong>Results: </strong>Here, we assembled 19 mitogenomes from Gossypium species, representing all genome groups (diploids A through G, K, and the allopolyploids AD) based on a uniformly applied strategy. A graph-based mitogenome assembly method revealed more alternative structural conformations than previously recognized, some of which confirmed the mitogenome structure reported in earlier studies on cotton. Using long-read data, we quantified alternative conformations mediated by recombination events between repeats, and phylogenetically informative structural variants were noted. Nucleotide substitution rate comparisons between coding and non-coding regions revealed low mutation rates across the entire mitogenome. Genome-wide mapping of nuclear organellar DNA transfers (NUOTs) in Gossypium revealed a nonrandom distribution of transfers in the nuclear genome. In cotton, the fate of NUOT events varied, with mitochondrion-to-nucleus transfer (NUMT) predominantly retained as short fragments in the nuclear genome, with more plastid sequences integrated into the nucleus. Phylogenetic relationships inferred using different data sets highlighted distinct evolutionary histories among these cellular compartments, providing ancillary evidence relevant to the evolutionary history of Gossypium.</p><p><strong>Conclusions: </strong>A comprehensive analysis of organellar genome variation demonstrates complex structural variation and low mutation rates across the entire mitogenome and reveals the history of organellar genome transfer among the three genomes throughout the cotton genus. The findings enhance our general understanding of mitogenome evolution, comparative organellar and nuclear evolutionary rates, and the history of inter-compartment genomic integration.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"9"},"PeriodicalIF":4.4,"publicationDate":"2025-01-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11720916/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142963728","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}
Pub Date : 2025-01-09DOI: 10.1186/s12915-025-02113-1
Zhihui Wang, Wenbin Wang, Qing Luo, Guanbin Song
Background: Abundant research indicates that increased extracellular matrix (ECM) stiffness significantly enhances the malignant characteristics of hepatocellular carcinoma (HCC) cells. Plectin, an essential cytoskeletal linker protein, has recently emerged as a promoter of cancer progression, particularly in the context of cancer cell invasion and metastasis. However, the responsiveness of plectin to changes in ECM stiffness and its impact on HCC progression remain unclear. In this study, we aimed to investigate whether plectin responds to variations in ECM stiffness and to explore its involved molecular mechanisms in regulating HCC cell migration.
Results: Our results showed that, when compared with control group (7 kPa), high ECM stiffness (53 kPa) boosts HCC cell migration by upregulating plectin and integrin β1 expression and increasing F-actin polymerization. Knockdown of integrin β1 negated the high stiffness-upregulated plectin expression. Furthermore, reducing either plectin or integrin β1 levels, or using latrunculin A, effectively prevented the high ECM stiffness-induced F-actin polymerization and HCC cell migration.
Conclusions: These findings demonstrate that integrin β1-plectin-F-actin axis is necessary for high matrix stiffness-driven migration of HCC cells, and provide evidence for the critical role of plectin in mechanotransduction in HCC cells.
背景:大量研究表明,细胞外基质(ECM)硬度的增加显著增强了肝细胞癌(HCC)细胞的恶性特征。Plectin是一种重要的细胞骨架连接蛋白,最近被发现是癌症进展的促进因子,特别是在癌细胞侵袭和转移的背景下。然而,粘附素对ECM硬度变化的反应性及其对HCC进展的影响尚不清楚。在这项研究中,我们旨在研究粘附素是否对ECM硬度的变化作出反应,并探讨其调节HCC细胞迁移的相关分子机制。结果:我们的研究结果表明,与对照组(7 kPa)相比,高ECM刚度(53 kPa)通过上调凝集素和整合素β1的表达以及增加f -肌动蛋白的聚合来促进HCC细胞的迁移。整合素β1的敲低可抑制高刚度上调的plectin表达。此外,降低凝集素或整合素β1水平,或使用latrunculin A,都能有效阻止高ECM刚度诱导的F-actin聚合和HCC细胞迁移。结论:这些发现表明整合素β1-凝集素- f -肌动蛋白轴是HCC细胞高基质刚度驱动迁移所必需的,并为凝集素在HCC细胞机械转导中的关键作用提供了证据。
{"title":"High matrix stiffness accelerates migration of hepatocellular carcinoma cells through the integrin β1-Plectin-F-actin axis.","authors":"Zhihui Wang, Wenbin Wang, Qing Luo, Guanbin Song","doi":"10.1186/s12915-025-02113-1","DOIUrl":"10.1186/s12915-025-02113-1","url":null,"abstract":"<p><strong>Background: </strong>Abundant research indicates that increased extracellular matrix (ECM) stiffness significantly enhances the malignant characteristics of hepatocellular carcinoma (HCC) cells. Plectin, an essential cytoskeletal linker protein, has recently emerged as a promoter of cancer progression, particularly in the context of cancer cell invasion and metastasis. However, the responsiveness of plectin to changes in ECM stiffness and its impact on HCC progression remain unclear. In this study, we aimed to investigate whether plectin responds to variations in ECM stiffness and to explore its involved molecular mechanisms in regulating HCC cell migration.</p><p><strong>Results: </strong>Our results showed that, when compared with control group (7 kPa), high ECM stiffness (53 kPa) boosts HCC cell migration by upregulating plectin and integrin β1 expression and increasing F-actin polymerization. Knockdown of integrin β1 negated the high stiffness-upregulated plectin expression. Furthermore, reducing either plectin or integrin β1 levels, or using latrunculin A, effectively prevented the high ECM stiffness-induced F-actin polymerization and HCC cell migration.</p><p><strong>Conclusions: </strong>These findings demonstrate that integrin β1-plectin-F-actin axis is necessary for high matrix stiffness-driven migration of HCC cells, and provide evidence for the critical role of plectin in mechanotransduction in HCC cells.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"8"},"PeriodicalIF":4.4,"publicationDate":"2025-01-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11721467/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142944892","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}
Pub Date : 2025-01-08DOI: 10.1186/s12915-024-02108-4
Marta Pla-Díaz, Gülfirde Akgül, Martyna Molak, Louis du Plessis, Hanna Panagiotopoulou, Karolina Doan, Wiesław Bogdanowicz, Paweł Dąbrowski, Maciej Oziembłowski, Barbara Kwiatkowska, Jacek Szczurowski, Joanna Grzelak, Natasha Arora, Kerttu Majander, Fernando González-Candelas, Verena J Schuenemann
Background: Treponemal diseases are a significant global health risk, presenting challenges to public health and severe consequences to individuals if left untreated. Despite numerous genomic studies on Treponema pallidum and the known possible biases introduced by the choice of the reference genome used for mapping, few investigations have addressed how these biases affect phylogenetic and evolutionary analysis of these bacteria. In this study, we ascertain the importance of selecting an appropriate genomic reference on phylogenetic and evolutionary analyses of T. pallidum.
Results: We designed a multiple-reference-based (MRB) mapping strategy using four different reference genomes and compared it to traditional single-reference mapping. To conduct this comparison, we created a genomic dataset comprising 77 modern and ancient genomes from the three subspecies of T. pallidum, including a newly sequenced seventeenth century genome (35X mean coverage) of a syphilis-causing strain (designated as W86). Our findings show that recombination detection was consistent across different references, but the choice of reference significantly affected ancient genome reconstruction and phylogenetic inferences. The high-coverage W86 genome introduced in this study also provided a new calibration point for Bayesian molecular clock dating, improving the reconstruction of the evolutionary history of treponemal diseases. Additionally, we identified novel recombination events, positive selection targets, and refined dating estimates for key events in the species' history.
Conclusions: This study highlights the importance of considering methodological implications and reference genome bias in high-throughput sequencing-based whole-genome analysis of T. pallidum, especially of ancient or low-coverage samples, contributing to a deeper understanding of the treponemal pathogen and its subspecies.
{"title":"Insights into Treponema pallidum genomics from modern and ancient genomes using a novel mapping strategy.","authors":"Marta Pla-Díaz, Gülfirde Akgül, Martyna Molak, Louis du Plessis, Hanna Panagiotopoulou, Karolina Doan, Wiesław Bogdanowicz, Paweł Dąbrowski, Maciej Oziembłowski, Barbara Kwiatkowska, Jacek Szczurowski, Joanna Grzelak, Natasha Arora, Kerttu Majander, Fernando González-Candelas, Verena J Schuenemann","doi":"10.1186/s12915-024-02108-4","DOIUrl":"10.1186/s12915-024-02108-4","url":null,"abstract":"<p><strong>Background: </strong>Treponemal diseases are a significant global health risk, presenting challenges to public health and severe consequences to individuals if left untreated. Despite numerous genomic studies on Treponema pallidum and the known possible biases introduced by the choice of the reference genome used for mapping, few investigations have addressed how these biases affect phylogenetic and evolutionary analysis of these bacteria. In this study, we ascertain the importance of selecting an appropriate genomic reference on phylogenetic and evolutionary analyses of T. pallidum.</p><p><strong>Results: </strong>We designed a multiple-reference-based (MRB) mapping strategy using four different reference genomes and compared it to traditional single-reference mapping. To conduct this comparison, we created a genomic dataset comprising 77 modern and ancient genomes from the three subspecies of T. pallidum, including a newly sequenced seventeenth century genome (35X mean coverage) of a syphilis-causing strain (designated as W86). Our findings show that recombination detection was consistent across different references, but the choice of reference significantly affected ancient genome reconstruction and phylogenetic inferences. The high-coverage W86 genome introduced in this study also provided a new calibration point for Bayesian molecular clock dating, improving the reconstruction of the evolutionary history of treponemal diseases. Additionally, we identified novel recombination events, positive selection targets, and refined dating estimates for key events in the species' history.</p><p><strong>Conclusions: </strong>This study highlights the importance of considering methodological implications and reference genome bias in high-throughput sequencing-based whole-genome analysis of T. pallidum, especially of ancient or low-coverage samples, contributing to a deeper understanding of the treponemal pathogen and its subspecies.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"7"},"PeriodicalIF":4.4,"publicationDate":"2025-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11716147/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142944896","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}
Pub Date : 2025-01-08DOI: 10.1186/s12915-024-02111-9
Luthfi Nurhidayat, Vladimir Benes, Sira Blom, Inês Gomes, Nisrina Firdausi, Merijn A G de Bakker, Herman P Spaink, Michael K Richardson
Background: Regeneration is the replacement of lost or damaged tissue with a functional copy. In axolotls and zebrafish, regeneration involves stem cells produced by de-differentiation. These cells form a growth zone which expresses developmental patterning genes at its apex. This system resembles an embryonic developmental field where cells undergo pattern formation. Some lizards, including geckos, can regenerate their tails, but it is unclear whether they show a "development-like" regeneration pathway.
Results: Using the tokay gecko (Gekko gecko) model species, we examined seven stages of tail regeneration, and three stages of embryonic tail bud development, using transcriptomics, single-cell sequencing, and in situ hybridization. We find no apical growth zone in the regenerating tail. The transcriptomes of the regenerating vs. embryonic tails are quite different with respect to developmental patterning genes. Posterior HOXC genes were activated in a temporally collinear sequence in the regenerating tail. The major precursor populations were stromal cells (regenerating tail) vs. pluripotent stem cells (embryonic tail). Segmented skeletal muscles were regenerated with no expression of classical segmentation genes, but with the early activation of satellite cell markers.
Conclusions: Our study suggests that tail regeneration in the tokay gecko-unlike tail development-might rely on the activation of resident stem cells, guided by pre-existing positional information.
{"title":"Tokay gecko tail regeneration involves temporally collinear expression of HOXC genes and early expression of satellite cell markers.","authors":"Luthfi Nurhidayat, Vladimir Benes, Sira Blom, Inês Gomes, Nisrina Firdausi, Merijn A G de Bakker, Herman P Spaink, Michael K Richardson","doi":"10.1186/s12915-024-02111-9","DOIUrl":"10.1186/s12915-024-02111-9","url":null,"abstract":"<p><strong>Background: </strong>Regeneration is the replacement of lost or damaged tissue with a functional copy. In axolotls and zebrafish, regeneration involves stem cells produced by de-differentiation. These cells form a growth zone which expresses developmental patterning genes at its apex. This system resembles an embryonic developmental field where cells undergo pattern formation. Some lizards, including geckos, can regenerate their tails, but it is unclear whether they show a \"development-like\" regeneration pathway.</p><p><strong>Results: </strong>Using the tokay gecko (Gekko gecko) model species, we examined seven stages of tail regeneration, and three stages of embryonic tail bud development, using transcriptomics, single-cell sequencing, and in situ hybridization. We find no apical growth zone in the regenerating tail. The transcriptomes of the regenerating vs. embryonic tails are quite different with respect to developmental patterning genes. Posterior HOXC genes were activated in a temporally collinear sequence in the regenerating tail. The major precursor populations were stromal cells (regenerating tail) vs. pluripotent stem cells (embryonic tail). Segmented skeletal muscles were regenerated with no expression of classical segmentation genes, but with the early activation of satellite cell markers.</p><p><strong>Conclusions: </strong>Our study suggests that tail regeneration in the tokay gecko-unlike tail development-might rely on the activation of resident stem cells, guided by pre-existing positional information.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"6"},"PeriodicalIF":4.4,"publicationDate":"2025-01-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11715542/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142944900","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}
Pub Date : 2025-01-07DOI: 10.1186/s12915-024-02110-w
Jolyon Troscianko
Background: The spatial and spectral properties of the light environment underpin many aspects of animal behaviour, ecology and evolution, and quantifying this information is crucial in fields ranging from optical physics, agriculture/plant sciences, human psychophysics, food science, architecture and materials sciences. The escalating threat of artificial light at night (ALAN) presents unique challenges for measuring the visual impact of light pollution, requiring measurement at low light levels across the human-visible and ultraviolet ranges, across all viewing angles, and often with high within-scene contrast.
Results: Here, I present a hyperspectral open-source imager (HOSI), an innovative and low-cost solution for collecting full-field hyperspectral data. The system uses a Hamamatsu C12880MA micro spectrometer to take single-point measurements, together with a motorised gimbal for spatial control. The hardware uses off-the-shelf components and 3D printed parts, costing around £350 in total. The system can run directly from a computer or smartphone with a graphical user interface, making it highly portable and user-friendly. The HOSI system can take panoramic hyperspectral images that meet the difficult requirements of ALAN research, sensitive to low light around 0.001 cd.m-2, across 320-880 nm range with spectral resolution of ~ 9 nm (FWHM) and spatial resolution of ~ 2 cycles per degree. The independent exposure of each pixel also allows for an extremely wide dynamic range that can encompass typical natural and artificially illuminated scenes, with sample night-time scans achieving full-spectrum peak-to-peak dynamic ranges of > 50,000:1.
Conclusions: This system's adaptability, cost-effectiveness and open-source nature position it as a valuable tool for researchers investigating the complex relationships between light, environment, behaviour, ecology and biodiversity, with further potential uses in many other fields.
{"title":"A hyperspectral open-source imager (HOSI).","authors":"Jolyon Troscianko","doi":"10.1186/s12915-024-02110-w","DOIUrl":"https://doi.org/10.1186/s12915-024-02110-w","url":null,"abstract":"<p><strong>Background: </strong>The spatial and spectral properties of the light environment underpin many aspects of animal behaviour, ecology and evolution, and quantifying this information is crucial in fields ranging from optical physics, agriculture/plant sciences, human psychophysics, food science, architecture and materials sciences. The escalating threat of artificial light at night (ALAN) presents unique challenges for measuring the visual impact of light pollution, requiring measurement at low light levels across the human-visible and ultraviolet ranges, across all viewing angles, and often with high within-scene contrast.</p><p><strong>Results: </strong>Here, I present a hyperspectral open-source imager (HOSI), an innovative and low-cost solution for collecting full-field hyperspectral data. The system uses a Hamamatsu C12880MA micro spectrometer to take single-point measurements, together with a motorised gimbal for spatial control. The hardware uses off-the-shelf components and 3D printed parts, costing around £350 in total. The system can run directly from a computer or smartphone with a graphical user interface, making it highly portable and user-friendly. The HOSI system can take panoramic hyperspectral images that meet the difficult requirements of ALAN research, sensitive to low light around 0.001 cd.m<sup>-2</sup>, across 320-880 nm range with spectral resolution of ~ 9 nm (FWHM) and spatial resolution of ~ 2 cycles per degree. The independent exposure of each pixel also allows for an extremely wide dynamic range that can encompass typical natural and artificially illuminated scenes, with sample night-time scans achieving full-spectrum peak-to-peak dynamic ranges of > 50,000:1.</p><p><strong>Conclusions: </strong>This system's adaptability, cost-effectiveness and open-source nature position it as a valuable tool for researchers investigating the complex relationships between light, environment, behaviour, ecology and biodiversity, with further potential uses in many other fields.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"5"},"PeriodicalIF":4.4,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11708076/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142944884","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}
Pub Date : 2025-01-07DOI: 10.1186/s12915-024-02093-8
Ebru Karasu, Rebecca Halbgebauer, Lena Schütte, Johannes Greven, Felix M Bläsius, Johannes Zeller, Oscar Winninger, David Braig, David Alexander Christian Messerer, Bettina Berger, Hendrik Feuerstein, Anke Schultze, Karlheinz Peter, Uwe Knippschild, Klemens Horst, Frank Hildebrand, Steffen U Eisenhardt, Markus Huber-Lang
Background: C-reactive protein (CRP) represents a routine diagnostic marker of inflammation. Dissociation of native pentameric CRP (pCRP) into the monomeric structure (mCRP) liberates proinflammatory features, presumably contributing to excessive immune cell activation via unknown molecular mechanisms.
Results: In a multi-translational study of systemic inflammation, we found a time- and inflammation-dependent pCRP dissociation into mCRP. We were able to confirm that mCRP co-localizes with leukocytes at the site of injury after polytrauma and therefore assessed whether the CRP conformation potentiates neutrophil activation. We found mCRP-induced neutrophil-extracellular trap formation in vitro and ex vivo involving nicotinamide adenine dinucleotide phosphate oxidase activation, p38/mitogen-activated protein kinase signaling, and histone H3 citrullination. Mimicking the trauma milieu in a human ex vivo whole blood model, we found significant mCRP generation as well as NET formation, prevented by blocking pCRP conformational changes.
Conclusions: Our data provide novel molecular insights how CRP dissociation contributes to neutrophil activation as driver of various inflammatory disorders.
{"title":"A conformational change of C-reactive protein drives neutrophil extracellular trap formation in inflammation.","authors":"Ebru Karasu, Rebecca Halbgebauer, Lena Schütte, Johannes Greven, Felix M Bläsius, Johannes Zeller, Oscar Winninger, David Braig, David Alexander Christian Messerer, Bettina Berger, Hendrik Feuerstein, Anke Schultze, Karlheinz Peter, Uwe Knippschild, Klemens Horst, Frank Hildebrand, Steffen U Eisenhardt, Markus Huber-Lang","doi":"10.1186/s12915-024-02093-8","DOIUrl":"https://doi.org/10.1186/s12915-024-02093-8","url":null,"abstract":"<p><strong>Background: </strong>C-reactive protein (CRP) represents a routine diagnostic marker of inflammation. Dissociation of native pentameric CRP (pCRP) into the monomeric structure (mCRP) liberates proinflammatory features, presumably contributing to excessive immune cell activation via unknown molecular mechanisms.</p><p><strong>Results: </strong>In a multi-translational study of systemic inflammation, we found a time- and inflammation-dependent pCRP dissociation into mCRP. We were able to confirm that mCRP co-localizes with leukocytes at the site of injury after polytrauma and therefore assessed whether the CRP conformation potentiates neutrophil activation. We found mCRP-induced neutrophil-extracellular trap formation in vitro and ex vivo involving nicotinamide adenine dinucleotide phosphate oxidase activation, p38/mitogen-activated protein kinase signaling, and histone H3 citrullination. Mimicking the trauma milieu in a human ex vivo whole blood model, we found significant mCRP generation as well as NET formation, prevented by blocking pCRP conformational changes.</p><p><strong>Conclusions: </strong>Our data provide novel molecular insights how CRP dissociation contributes to neutrophil activation as driver of various inflammatory disorders.</p>","PeriodicalId":9339,"journal":{"name":"BMC Biology","volume":"23 1","pages":"4"},"PeriodicalIF":4.4,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11708171/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142944879","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}