Pub Date : 2024-10-26DOI: 10.1186/s12864-024-10927-6
Hongyan Zhu, Xiaohan Li, Jie Wang, Haoming Wang, Song Zhao, Yumin Tian, Yuhong Su
Background: With the improvement of living standards, the quality of chicken has become a significant concern. Chinese Dagu Chicken (dual-purpose type) and Arbor Acres plus broiler (AA+ broiler) (meat-type) were selected as the research subjects in this study, the meat quality of the breast and leg muscles were measured. However, the molecular mechanism(s) underlying regulation of muscle development are not yet fully elucidated. Therefore, finding molecular markers or major genes that regulate muscle quality has become a crucial breakthrough in chicken breeding. Unraveling the molecular mechanism behind meat traits in chicken and other domestic fowl is facilitated by identifying the key genes associated with these developmental events. Here, a comparative transcriptomic analysis of chicken meat was conducted on breast muscles (BM) and leg muscles (LM) in AA+ broilers (AA) and Dagu chicken (DG) to explore the differences in their meat traits employing RNA-seq.
Results: Twelve cDNA libraries of BM and LM from AA and DG were constructed from four experimental groups, yielding 14,464 genes. Among them, Dagu chicken breast muscles (DGB) vs AA+ broilers breast muscles (AAB) showed 415 upregulated genes and 449 downregulated genes, Dagu chicken leg muscles (DGL) vs AA+ broilers leg muscles (AAL) exhibited 237 upregulated genes and 278 downregulated genes, DGL vs DGB demonstrated 391 upregulated genes and 594 downregulated genes, and AAL vs AAB displayed 122 upregulated genes and 154 downregulated genes. 13 genes, including nine upregulated genes (COX5A, COX7C, NDUFV1, UQCRFS1, UQCR11, BRT-1, FGF14, TMOD1, MYOZ2) and four downregulated genes (MYBPC3, MYO7B, MTMR7, and TNNC1), were found to be associated with the oxidative phosphorylation signaling pathway. Further analysis revealed that the differentially expressed genes (DEGs) from muscle were enriched in various pathways, such as metabolic pathways, oxidative phosphorylation, carbon metabolism, glycolysis, extracellular matrix-receptor interaction, biosynthesis of amino acids, focal adhesion, vascular smooth muscle contraction, and cardiac muscle contraction, all of which are involved in muscle development and metabolism. This study also measured the meat quality of the breast and leg muscles from the two breeds, which demonstrated superior overall meat quality in Chinese Dagu Chicken compared to the AA+ broiler.
Conclusions: Our findings show that the meat quality of dual-purpose breeds (Chinese Dagu chicken) is higher than meat-type (AA+ broiler), which may be related to the DEGs regulating muscle development and metabolism. Our findings also provide transcriptomic insights for a comparative analysis of molecular mechanisms underlying muscle development between the two breeds, and have practical implications for the improvement of chicken breeding practices.
{"title":"Transcriptomic analysis reveals differentially expressed genes associated with meat quality in Chinese Dagu chicken and AA<sup>+</sup> broiler roosters.","authors":"Hongyan Zhu, Xiaohan Li, Jie Wang, Haoming Wang, Song Zhao, Yumin Tian, Yuhong Su","doi":"10.1186/s12864-024-10927-6","DOIUrl":"10.1186/s12864-024-10927-6","url":null,"abstract":"<p><strong>Background: </strong>With the improvement of living standards, the quality of chicken has become a significant concern. Chinese Dagu Chicken (dual-purpose type) and Arbor Acres plus broiler (AA<sup>+</sup> broiler) (meat-type) were selected as the research subjects in this study, the meat quality of the breast and leg muscles were measured. However, the molecular mechanism(s) underlying regulation of muscle development are not yet fully elucidated. Therefore, finding molecular markers or major genes that regulate muscle quality has become a crucial breakthrough in chicken breeding. Unraveling the molecular mechanism behind meat traits in chicken and other domestic fowl is facilitated by identifying the key genes associated with these developmental events. Here, a comparative transcriptomic analysis of chicken meat was conducted on breast muscles (BM) and leg muscles (LM) in AA<sup>+</sup> broilers (AA) and Dagu chicken (DG) to explore the differences in their meat traits employing RNA-seq.</p><p><strong>Results: </strong>Twelve cDNA libraries of BM and LM from AA and DG were constructed from four experimental groups, yielding 14,464 genes. Among them, Dagu chicken breast muscles (DGB) vs AA<sup>+</sup> broilers breast muscles (AAB) showed 415 upregulated genes and 449 downregulated genes, Dagu chicken leg muscles (DGL) vs AA<sup>+</sup> broilers leg muscles (AAL) exhibited 237 upregulated genes and 278 downregulated genes, DGL vs DGB demonstrated 391 upregulated genes and 594 downregulated genes, and AAL vs AAB displayed 122 upregulated genes and 154 downregulated genes. 13 genes, including nine upregulated genes (COX5A, COX7C, NDUFV1, UQCRFS1, UQCR11, BRT-1, FGF14, TMOD1, MYOZ2) and four downregulated genes (MYBPC3, MYO7B, MTMR7, and TNNC1), were found to be associated with the oxidative phosphorylation signaling pathway. Further analysis revealed that the differentially expressed genes (DEGs) from muscle were enriched in various pathways, such as metabolic pathways, oxidative phosphorylation, carbon metabolism, glycolysis, extracellular matrix-receptor interaction, biosynthesis of amino acids, focal adhesion, vascular smooth muscle contraction, and cardiac muscle contraction, all of which are involved in muscle development and metabolism. This study also measured the meat quality of the breast and leg muscles from the two breeds, which demonstrated superior overall meat quality in Chinese Dagu Chicken compared to the AA<sup>+</sup> broiler.</p><p><strong>Conclusions: </strong>Our findings show that the meat quality of dual-purpose breeds (Chinese Dagu chicken) is higher than meat-type (AA<sup>+</sup> broiler), which may be related to the DEGs regulating muscle development and metabolism. Our findings also provide transcriptomic insights for a comparative analysis of molecular mechanisms underlying muscle development between the two breeds, and have practical implications for the improvement of chicken breeding practices.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515088/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494743","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-25DOI: 10.1186/s12864-024-10913-y
Zhiduan Chi, Qiong Jia, Haoyu Yang, Hongrui Ren, Congli Jin, Jinxin He, Nile Wuri, Ze Sui, Junzhen Zhang, Bayier Mengke, Lixian Zhu, Ge Qiqi, Sarengaowa Aierqing, Ji Wuli, Dong Ai, Ruiwen Fan, Muren Herrid
Background: Mongolian cattle are local breeds in northern China with excellent adaptability to harsh environmental conditions. Adipose tissues play essential roles in tolerance to cold and disease, but the associated cellular and molecular mechanisms are unclear.
Methods: Single-nucleus RNA sequencing (snRNA-seq) was performed on the adipose tissues from the subcutaneous (SAT), greater omentum (OAT) and perirenal (PAT) of 3 healthy cattle. The adipogenic trajectory was analyzed, and the functional roles of gene of interest were verified in vitro.
Results: There were different cell subpopulations in adipose tissues. The lipid-deposition adipocytes identified by the PTGER3 marker exhibited outstanding characteristics in SAT. In PAT and OAT, aldosterone was expressed to provide clues for the differential brown adipocytes. Among the DEGs by comparing OAT with SAT and PAT with OAT, C3 was significantly expressed in most of the cell populations in SAT. G0S2, LIPE, LPIN1, PTGER3 and RGCC took part in the adipogenic trajectory from preadipocyte commitment to mature adipocytes. S100A4 expression affected Ca2+ signaling and the expression of UCP1 ~ 3, FABP4 and PTGER3.
Conclusion: The cell heterogeneity and genes expressed in adipose tissues of Mongolian cattle not only determine the endocrine and energy storage, but contribute to adapt to cold and disease resistance.
背景:蒙古牛是中国北方的地方品种,对恶劣的环境条件具有极强的适应性。脂肪组织在耐寒和抗病方面发挥着重要作用,但相关的细胞和分子机制尚不清楚:方法:对 3 头健康牛的皮下(SAT)、大网膜(OAT)和肾周(PAT)脂肪组织进行了单核 RNA 测序(snRNA-seq)。分析了脂肪形成的轨迹,并在体外验证了相关基因的功能作用:结果:脂肪组织中有不同的细胞亚群。结果:脂肪组织中存在不同的细胞亚群。在 SAT 中,通过 PTGER3 标记鉴定的脂质沉积脂肪细胞表现出突出的特征。在 PAT 和 OAT 中,醛固酮的表达为棕色脂肪细胞的差异提供了线索。通过比较 OAT 与 SAT 和 PAT 与 OAT 的 DEGs,发现 C3 在 SAT 的大多数细胞群中都有显著表达。G0S2、LIPE、LPIN1、PTGER3和RGCC参与了前脂肪细胞到成熟脂肪细胞的成脂过程。S100A4 的表达影响了 Ca2+ 信号转导以及 UCP1 ~ 3、FABP4 和 PTGER3 的表达:结论:蒙古牛脂肪组织的细胞异质性和基因表达不仅决定了其内分泌和能量储存,而且有助于适应寒冷和抗病。
{"title":"snRNA-seq of adipose tissues reveals the potential cellular and molecular mechanisms of cold and disease resistance in Mongolian cattle.","authors":"Zhiduan Chi, Qiong Jia, Haoyu Yang, Hongrui Ren, Congli Jin, Jinxin He, Nile Wuri, Ze Sui, Junzhen Zhang, Bayier Mengke, Lixian Zhu, Ge Qiqi, Sarengaowa Aierqing, Ji Wuli, Dong Ai, Ruiwen Fan, Muren Herrid","doi":"10.1186/s12864-024-10913-y","DOIUrl":"10.1186/s12864-024-10913-y","url":null,"abstract":"<p><strong>Background: </strong>Mongolian cattle are local breeds in northern China with excellent adaptability to harsh environmental conditions. Adipose tissues play essential roles in tolerance to cold and disease, but the associated cellular and molecular mechanisms are unclear.</p><p><strong>Methods: </strong>Single-nucleus RNA sequencing (snRNA-seq) was performed on the adipose tissues from the subcutaneous (SAT), greater omentum (OAT) and perirenal (PAT) of 3 healthy cattle. The adipogenic trajectory was analyzed, and the functional roles of gene of interest were verified in vitro.</p><p><strong>Results: </strong>There were different cell subpopulations in adipose tissues. The lipid-deposition adipocytes identified by the PTGER3 marker exhibited outstanding characteristics in SAT. In PAT and OAT, aldosterone was expressed to provide clues for the differential brown adipocytes. Among the DEGs by comparing OAT with SAT and PAT with OAT, C3 was significantly expressed in most of the cell populations in SAT. G0S2, LIPE, LPIN1, PTGER3 and RGCC took part in the adipogenic trajectory from preadipocyte commitment to mature adipocytes. S100A4 expression affected Ca<sup>2+</sup> signaling and the expression of UCP1 ~ 3, FABP4 and PTGER3.</p><p><strong>Conclusion: </strong>The cell heterogeneity and genes expressed in adipose tissues of Mongolian cattle not only determine the endocrine and energy storage, but contribute to adapt to cold and disease resistance.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11520132/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494741","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-25DOI: 10.1186/s12864-024-10922-x
Lei Li, Zijuan Zhao, Zihao Liu, Yuquan Tang, Tan Yang, Nailin Gong, Bing Liao, Yang Long, Yongmei Nie, Fengxu Yu
Background: Atrial fibrillation (AF) stands as a prevalent and detrimental arrhythmic disorder, characterized by intricate pathophysiological mechanisms. The availability of reliable and reproducible AF models is pivotal in unraveling the underlying mechanisms of this complex condition. Unfortunately, the researchers are still confronted with the absence of consistent in vitro AF models, hindering progress in this crucial area of research.
Methods: Human induced pluripotent stem cells derived atrial myocytes (hiPSC-AMs) were generated based on the GiWi methods and were verified by whole-cell patch clamp, immunofluorescent staining, and flow cytometry. Then hiPSC-AMs were employed to establish the AF model by HS. Whole-cell patch clamp technique and calcium imaging were used to identify the AF model. The stability of 29 reference genes was evaluated using delta-Ct, GeNorm, NormFinder, and BestKeeper algorithms; RESULTS: HiPSC-AMs displayed atrial myocyte action potentials and expressed the atrial-specific protein MLC-2 A and NR2F2, about 70% of the cardiomyocytes were MLC-2 A positive. After HS, hiPSC-AMs showed a significant increase in beating frequency, a shortened action potential duration, and increased calcium transient frequency. Of the 29 candidate genes, the top five most stably ranked genes were ABL1, RPL37A, POP4, RPL30, and EIF2B1. After normalization using ABL1, KCNJ2 was significantly upregulated in the AF model; Conclusions: In the hiPSC-AMs AF model established by HS, ABL1 provides greater normalization efficiency than commonly used GAPDH.
{"title":"Identification of the optimal reference genes for atrial fibrillation model established by iPSC-derived atrial myocytes.","authors":"Lei Li, Zijuan Zhao, Zihao Liu, Yuquan Tang, Tan Yang, Nailin Gong, Bing Liao, Yang Long, Yongmei Nie, Fengxu Yu","doi":"10.1186/s12864-024-10922-x","DOIUrl":"10.1186/s12864-024-10922-x","url":null,"abstract":"<p><strong>Background: </strong>Atrial fibrillation (AF) stands as a prevalent and detrimental arrhythmic disorder, characterized by intricate pathophysiological mechanisms. The availability of reliable and reproducible AF models is pivotal in unraveling the underlying mechanisms of this complex condition. Unfortunately, the researchers are still confronted with the absence of consistent in vitro AF models, hindering progress in this crucial area of research.</p><p><strong>Methods: </strong>Human induced pluripotent stem cells derived atrial myocytes (hiPSC-AMs) were generated based on the GiWi methods and were verified by whole-cell patch clamp, immunofluorescent staining, and flow cytometry. Then hiPSC-AMs were employed to establish the AF model by HS. Whole-cell patch clamp technique and calcium imaging were used to identify the AF model. The stability of 29 reference genes was evaluated using delta-Ct, GeNorm, NormFinder, and BestKeeper algorithms; RESULTS: HiPSC-AMs displayed atrial myocyte action potentials and expressed the atrial-specific protein MLC-2 A and NR2F2, about 70% of the cardiomyocytes were MLC-2 A positive. After HS, hiPSC-AMs showed a significant increase in beating frequency, a shortened action potential duration, and increased calcium transient frequency. Of the 29 candidate genes, the top five most stably ranked genes were ABL1, RPL37A, POP4, RPL30, and EIF2B1. After normalization using ABL1, KCNJ2 was significantly upregulated in the AF model; Conclusions: In the hiPSC-AMs AF model established by HS, ABL1 provides greater normalization efficiency than commonly used GAPDH.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515253/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494728","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-24DOI: 10.1186/s12864-024-10879-x
Rajindra Napit, Annie Elong Ngono, Kathie A Mihindukulasuriya, Aunji Pradhan, Binod Khadka, Smita Shrestha, Lindsay Droit, Anne Paredes, Lata Karki, Rabindra Khatiwada, Mamata Tamang, Bimal Sharma Chalise, Manisha Rawal, Bimalesh Kumar Jha, David Wang, Scott A Handley, Sujan Shresta, Krishna Das Manandhar
Background: The 4 serotypes of dengue virus (DENV1-4) can each cause potentially deadly dengue disease, and are spreading globally from tropical and subtropical areas to more temperate ones. Nepal provides a microcosm of this global phenomenon, having met each of these grim benchmarks. To better understand DENV transmission dynamics and spread into new areas, we chose to study dengue in Nepal and, in so doing, to build the onsite infrastructure needed to manage future, larger studies.
Methods and results: During the 2022 dengue season, we enrolled 384 patients presenting at a hospital in Kathmandu with dengue-like symptoms; 79% of the study participants had active or recent DENV infection (NS1 antigen and IgM). To identify circulating serotypes, we screened serum from 50 of the NS1+ participants by RT-PCR and identified DENV1, 2, and 3 - with DENV1 and 3 codominant. We also performed whole-genome sequencing of DENV, for the first time in Nepal, using our new on-site capacity. Sequencing analysis demonstrated the DENV1 and 3 genomes clustered with sequences reported from India in 2019, and the DENV2 genome clustered with a sequence reported from China in 2018.
Conclusion: These findings highlight DENV's geographic expansion from neighboring countries, identify China and India as the likely origin of the 2022 DENV cases in Nepal, and demonstrate the feasibility of building onsite capacity for more rapid genomic surveillance of circulating DENV. These ongoing efforts promise to protect populations in Nepal and beyond by informing the development and deployment of DENV drugs and vaccines in real time.
{"title":"Dengue virus surveillance in Nepal yields the first on-site whole genome sequences of isolates from the 2022 outbreak.","authors":"Rajindra Napit, Annie Elong Ngono, Kathie A Mihindukulasuriya, Aunji Pradhan, Binod Khadka, Smita Shrestha, Lindsay Droit, Anne Paredes, Lata Karki, Rabindra Khatiwada, Mamata Tamang, Bimal Sharma Chalise, Manisha Rawal, Bimalesh Kumar Jha, David Wang, Scott A Handley, Sujan Shresta, Krishna Das Manandhar","doi":"10.1186/s12864-024-10879-x","DOIUrl":"10.1186/s12864-024-10879-x","url":null,"abstract":"<p><strong>Background: </strong>The 4 serotypes of dengue virus (DENV1-4) can each cause potentially deadly dengue disease, and are spreading globally from tropical and subtropical areas to more temperate ones. Nepal provides a microcosm of this global phenomenon, having met each of these grim benchmarks. To better understand DENV transmission dynamics and spread into new areas, we chose to study dengue in Nepal and, in so doing, to build the onsite infrastructure needed to manage future, larger studies.</p><p><strong>Methods and results: </strong>During the 2022 dengue season, we enrolled 384 patients presenting at a hospital in Kathmandu with dengue-like symptoms; 79% of the study participants had active or recent DENV infection (NS1 antigen and IgM). To identify circulating serotypes, we screened serum from 50 of the NS1<sup>+</sup> participants by RT-PCR and identified DENV1, 2, and 3 - with DENV1 and 3 codominant. We also performed whole-genome sequencing of DENV, for the first time in Nepal, using our new on-site capacity. Sequencing analysis demonstrated the DENV1 and 3 genomes clustered with sequences reported from India in 2019, and the DENV2 genome clustered with a sequence reported from China in 2018.</p><p><strong>Conclusion: </strong>These findings highlight DENV's geographic expansion from neighboring countries, identify China and India as the likely origin of the 2022 DENV cases in Nepal, and demonstrate the feasibility of building onsite capacity for more rapid genomic surveillance of circulating DENV. These ongoing efforts promise to protect populations in Nepal and beyond by informing the development and deployment of DENV drugs and vaccines in real time.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515306/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494711","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-24DOI: 10.1186/s12864-024-10905-y
Stephen Lu, Lucas C de Sousa-Paula, Jose M C Ribeiro, Lucas Tirloni
Background: Female ticks remain attached to their host for multiple days to complete a blood meal. This prolonged feeding period is accompanied by a significant increase in the tick's size and body weight, paralleled by noteworthy changes to the tick midgut. While the midgut is recognized for its established role in blood storage and processing, its importance extends to playing a crucial role in the acquisition, survival, and proliferation of pathogens. Despite this, our overall understanding of tick midgut biology is limited.
Results: Our transcriptome analysis identified 15,599 putative DNA coding sequences (CDS), which were classified into 26 functional groups. Dimensional and differential expression analyses revealed four primary transcriptional profiles corresponding to unfed, slow-feeding, transitory (from slow- to rapid-feeding), and rapid-feeding stages. Additionally, comparing the current dataset with previously deposited transcriptome from other tick species allowed the identification of commonly expressed transcripts across different feeding stages.
Conclusion: Our findings provide a detailed temporal resolution of numerous metabolic pathways in the midgut of A. americanum adult females throughout the feeding process, highlighting the dynamic transcriptional regulation of the tick's midgut as feeding progresses. Furthermore, we identified conserved transcripts across three different tick species that exhibit similar expression patterns. This knowledge not only enhances our understanding of the physiological processes within the tick midgut but also opens up potential avenues for developing control methods that target multiple tick species.
背景:雌性蜱会在宿主身上停留多日,以完成一次血食。伴随着这一漫长的进食期,蜱的体型和体重会显著增加,同时蜱的中肠也会发生显著变化。虽然中肠在血液储存和处理方面的作用已得到公认,但它在病原体的获取、存活和增殖方面也发挥着至关重要的作用。尽管如此,我们对蜱中肠生物学的总体了解仍然有限:我们的转录组分析确定了 15,599 个假定 DNA 编码序列 (CDS),并将其分为 26 个功能组。维度和差异表达分析揭示了四种主要的转录谱,分别对应未进食、慢速进食、过渡阶段(从慢速进食到快速进食)和快速进食阶段。此外,将目前的数据集与以前保存的其他蜱物种的转录组进行比较,可以确定不同摄食阶段的常见表达转录本:我们的研究结果提供了雌性成年蜱中肠在整个摄食过程中许多代谢途径的详细时间分辨率,突出了蜱中肠在摄食过程中的动态转录调控。此外,我们还发现了三个不同蜱物种中表现出相似表达模式的保守转录本。这些知识不仅加深了我们对蜱中肠生理过程的了解,还为开发针对多种蜱的控制方法开辟了潜在的途径。
{"title":"Exploring the longitudinal expression dynamics of midguts in adult female Amblyomma americanum ticks.","authors":"Stephen Lu, Lucas C de Sousa-Paula, Jose M C Ribeiro, Lucas Tirloni","doi":"10.1186/s12864-024-10905-y","DOIUrl":"10.1186/s12864-024-10905-y","url":null,"abstract":"<p><strong>Background: </strong>Female ticks remain attached to their host for multiple days to complete a blood meal. This prolonged feeding period is accompanied by a significant increase in the tick's size and body weight, paralleled by noteworthy changes to the tick midgut. While the midgut is recognized for its established role in blood storage and processing, its importance extends to playing a crucial role in the acquisition, survival, and proliferation of pathogens. Despite this, our overall understanding of tick midgut biology is limited.</p><p><strong>Results: </strong>Our transcriptome analysis identified 15,599 putative DNA coding sequences (CDS), which were classified into 26 functional groups. Dimensional and differential expression analyses revealed four primary transcriptional profiles corresponding to unfed, slow-feeding, transitory (from slow- to rapid-feeding), and rapid-feeding stages. Additionally, comparing the current dataset with previously deposited transcriptome from other tick species allowed the identification of commonly expressed transcripts across different feeding stages.</p><p><strong>Conclusion: </strong>Our findings provide a detailed temporal resolution of numerous metabolic pathways in the midgut of A. americanum adult females throughout the feeding process, highlighting the dynamic transcriptional regulation of the tick's midgut as feeding progresses. Furthermore, we identified conserved transcripts across three different tick species that exhibit similar expression patterns. This knowledge not only enhances our understanding of the physiological processes within the tick midgut but also opens up potential avenues for developing control methods that target multiple tick species.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515579/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494722","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The nutritional quality and yield of oats (Avena sativa) are often compromised by plant diseases such as red leaf, powdery mildew, and leaf spot. Sugars Will Eventually be Exported Transporters (SWEETs) are newly identified sugar transporters involved in regulating plant growth and stress responses. However, the roles of SWEET genes in biotic stress responses remain uncharacterized in oats. In this study, 13 AsSWEET genes were identified across nine chromosomes of the oat genome, all of which were predicted to contain seven transmembrane regions. Phylogenetic analysis revealed four clades of AsSWEET proteins, with high homology to SWEET proteins in the Poaceae family. Collinearity analysis demonstrated strong relationships between oat and Zea mays SWEETs. Using subcellular localization prediction tools, AsSWEET proteins were predicted to localize to the plasma membrane. Promoter analysis revealed cis-acting elements associated with light response, growth, and stress regulation. Six AsSWEET proteins were predicted to interact in a network centered on AsSWEET1a and AsSWEET11. Gene expression analysis of two oat varieties, 'ForagePlus' and 'Molasses', indicated significant expression differences in several AsSWEET genes following infection with powdery mildew or leaf spot, including AsSWEET1a, AsSWEET1b, AsSWEET2b, AsSWEET3a, AsSWEET11, and AsSWEET16. These SWEET genes are potential candidates for disease resistance in oats. This study provides a foundation for understanding the regulatory mechanisms of AsSWEET genes, particularly in response to powdery mildew and leaf spot, and offers insights for enhancing oat molecular breeding.
{"title":"Genome-wide analysis of the SWEET gene family and its response to powdery mildew and leaf spot infection in the common oat (Avena sativa L.).","authors":"Yuanbo Pan, Kuiju Niu, Peiqin Miao, Guiqin Zhao, Yuehua Zhang, Zeliang Ju, Jikuan Chai, Juanjuan Yang, Xiaoning Cui, Ran Zhang","doi":"10.1186/s12864-024-10933-8","DOIUrl":"10.1186/s12864-024-10933-8","url":null,"abstract":"<p><p>The nutritional quality and yield of oats (Avena sativa) are often compromised by plant diseases such as red leaf, powdery mildew, and leaf spot. Sugars Will Eventually be Exported Transporters (SWEETs) are newly identified sugar transporters involved in regulating plant growth and stress responses. However, the roles of SWEET genes in biotic stress responses remain uncharacterized in oats. In this study, 13 AsSWEET genes were identified across nine chromosomes of the oat genome, all of which were predicted to contain seven transmembrane regions. Phylogenetic analysis revealed four clades of AsSWEET proteins, with high homology to SWEET proteins in the Poaceae family. Collinearity analysis demonstrated strong relationships between oat and Zea mays SWEETs. Using subcellular localization prediction tools, AsSWEET proteins were predicted to localize to the plasma membrane. Promoter analysis revealed cis-acting elements associated with light response, growth, and stress regulation. Six AsSWEET proteins were predicted to interact in a network centered on AsSWEET1a and AsSWEET11. Gene expression analysis of two oat varieties, 'ForagePlus' and 'Molasses', indicated significant expression differences in several AsSWEET genes following infection with powdery mildew or leaf spot, including AsSWEET1a, AsSWEET1b, AsSWEET2b, AsSWEET3a, AsSWEET11, and AsSWEET16. These SWEET genes are potential candidates for disease resistance in oats. This study provides a foundation for understanding the regulatory mechanisms of AsSWEET genes, particularly in response to powdery mildew and leaf spot, and offers insights for enhancing oat molecular breeding.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515518/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494724","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-24DOI: 10.1186/s12864-024-10889-9
Lina Tan, Lijuan Lu, Wen Sun, Xinyuan Zhang, Yanglin Liu, Yan Xiang, Hanwei Yan
Background: Grapes are highly valued for their nutritional and economic benefits, and have been widely studied for their biological attributes such as fruit development, quality formation, and stress resistance. One significant threat to grape quality is gray mold, caused by Botrytis cinerea, which can infect the flowers, fruits, leaves, and stems. The quantitative real-time PCR (qRT-PCR), known for its high sensitivity and quantitative accuracy, is an essential tool for analyzing gene expression related to the pathogenesis of gray mold, thereby providing deeper insights into the disease.
Result: In this study, we aim to identify stable internal reference genes crucial for accurate gene expression analysis via qRT-PCR. Utilizing transcriptome data from grapes under various disease stresses, we identified twelve candidate reference genes with consistently high expression levels. The stability of these genes was assessed through delta-CT, geNorm, NormFinder, BestKeeper, and RefFinder analyses after establishing the cycling thresholds (Ct) in different grape varieties treated with Botrytis cinerea.
Conclusions: Our findings reveal that VIT-17s0000g02750 and VIT-06s0004g04280 exhibit stable expression and are suitable as new reference genes. This foundational work supports further research into the molecular mechanisms of grape biological processes.
{"title":"Identification and validation of qRT-PCR reference genes for analyzing grape infection with gray mold.","authors":"Lina Tan, Lijuan Lu, Wen Sun, Xinyuan Zhang, Yanglin Liu, Yan Xiang, Hanwei Yan","doi":"10.1186/s12864-024-10889-9","DOIUrl":"10.1186/s12864-024-10889-9","url":null,"abstract":"<p><strong>Background: </strong>Grapes are highly valued for their nutritional and economic benefits, and have been widely studied for their biological attributes such as fruit development, quality formation, and stress resistance. One significant threat to grape quality is gray mold, caused by Botrytis cinerea, which can infect the flowers, fruits, leaves, and stems. The quantitative real-time PCR (qRT-PCR), known for its high sensitivity and quantitative accuracy, is an essential tool for analyzing gene expression related to the pathogenesis of gray mold, thereby providing deeper insights into the disease.</p><p><strong>Result: </strong>In this study, we aim to identify stable internal reference genes crucial for accurate gene expression analysis via qRT-PCR. Utilizing transcriptome data from grapes under various disease stresses, we identified twelve candidate reference genes with consistently high expression levels. The stability of these genes was assessed through delta-CT, geNorm, NormFinder, BestKeeper, and RefFinder analyses after establishing the cycling thresholds (Ct) in different grape varieties treated with Botrytis cinerea.</p><p><strong>Conclusions: </strong>Our findings reveal that VIT-17s0000g02750 and VIT-06s0004g04280 exhibit stable expression and are suitable as new reference genes. This foundational work supports further research into the molecular mechanisms of grape biological processes.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515470/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494727","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-23DOI: 10.1186/s12864-024-10914-x
Yi Xiong, Xiong Lei, Yanli Xiong, Yingjie Liu, Zhixiao Dong, Junming Zhao, Qingqing Yu, Xiao Ma
The use of complete organelle genomes, including chloroplast and mitochondrial genomes, is a powerful molecular method for studying biological evolution and gene transfer. However, in the case of Polygonaceae, an important family with numerous edible, medicinal, and ornamental species, the mitochondrial genomes of only three species have been sequenced and analyzed. In this study, we present the mitochondrial and chloroplast genomes of two important Tibetan medicinal plants, Bistorta viviparum and B. macrophyllum. All the organelle genomes are assembled into a single circular structure and contain a common set of 32 protein-coding genes (PCGs). Some genes such as rps2 and ndhF were found to have high nucleotide polymorphism (Pi) in the chloroplast genomes, while cox1, mttB and rps12 showed pronounced Pi values in the mitochondrial genomes. Furthermore, our analysis revealed that most chloroplast genes and mitochondrial PCGs in Polygonaceae plants are under purifying selection. However, a few genes, including the chloroplast gene psaJ and the mitochondrial genes ccmFc, atp8 and nad4, showed positive selection in certain Polygonaceae plants, as indicated by a Ka/Ks ratio greater than one. Structural variation analysis revealed a wealth of differences between the mitochondrial genomes of five Polygonaceae species, with a particularly notable large-scale inversion observed between Reynoutria japonica and Fallopia aubertii. Furthermore, an analysis of the homologous sequences in the chloroplast and mitochondrial genomes revealed that the rps7 has been transferred from the chloroplast to the mitochondrial genome in all five Polygonaceae species. Finally, ecological niche models were constructed for B. viviparum and B. macrophyllum, indicating that mean annual temperature and altitude are the main climatic factors influencing the distribution of both species. Although the current distribution of B. viviparum is significantly wider than that of B. macrophyllum, projections suggest that the optimal growth ranges of both species will expand in the future, with B. macrophyllum potentially exceeding B. viviparum. This study not only contributes to the plastid genome database for Polygonaceae plants, but also provides theoretical insights into the adaptive evolution of these plants.
{"title":"Factors contributing to organelle genomes size variation and the intracellular DNA transfer in Polygonaceae.","authors":"Yi Xiong, Xiong Lei, Yanli Xiong, Yingjie Liu, Zhixiao Dong, Junming Zhao, Qingqing Yu, Xiao Ma","doi":"10.1186/s12864-024-10914-x","DOIUrl":"10.1186/s12864-024-10914-x","url":null,"abstract":"<p><p>The use of complete organelle genomes, including chloroplast and mitochondrial genomes, is a powerful molecular method for studying biological evolution and gene transfer. However, in the case of Polygonaceae, an important family with numerous edible, medicinal, and ornamental species, the mitochondrial genomes of only three species have been sequenced and analyzed. In this study, we present the mitochondrial and chloroplast genomes of two important Tibetan medicinal plants, Bistorta viviparum and B. macrophyllum. All the organelle genomes are assembled into a single circular structure and contain a common set of 32 protein-coding genes (PCGs). Some genes such as rps2 and ndhF were found to have high nucleotide polymorphism (Pi) in the chloroplast genomes, while cox1, mttB and rps12 showed pronounced Pi values in the mitochondrial genomes. Furthermore, our analysis revealed that most chloroplast genes and mitochondrial PCGs in Polygonaceae plants are under purifying selection. However, a few genes, including the chloroplast gene psaJ and the mitochondrial genes ccmFc, atp8 and nad4, showed positive selection in certain Polygonaceae plants, as indicated by a Ka/Ks ratio greater than one. Structural variation analysis revealed a wealth of differences between the mitochondrial genomes of five Polygonaceae species, with a particularly notable large-scale inversion observed between Reynoutria japonica and Fallopia aubertii. Furthermore, an analysis of the homologous sequences in the chloroplast and mitochondrial genomes revealed that the rps7 has been transferred from the chloroplast to the mitochondrial genome in all five Polygonaceae species. Finally, ecological niche models were constructed for B. viviparum and B. macrophyllum, indicating that mean annual temperature and altitude are the main climatic factors influencing the distribution of both species. Although the current distribution of B. viviparum is significantly wider than that of B. macrophyllum, projections suggest that the optimal growth ranges of both species will expand in the future, with B. macrophyllum potentially exceeding B. viviparum. This study not only contributes to the plastid genome database for Polygonaceae plants, but also provides theoretical insights into the adaptive evolution of these plants.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515532/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494723","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-23DOI: 10.1186/s12864-024-10917-8
Dongbo Zhu, Rui Rao, Yu Du, Chunmin Mao, Rong Chen, Liangliang Yue
BACKGROUND : Garuga Roxb. is a genus endemic to southwest China and other tropical regions in Southeast Asia facing risk of extinction due to the loss of tropical forests and changes in land use. Conducting a genome survey of G. forrestii contribute to a deeper understanding and conservation of the genus. RESULTS: This study utilized genome survey of G. forrestii generated approximately 54.56 GB of sequence data, with approximately 112 × coverage. K-mer analysis indicated a genome size of approximately 0.48 GB, smaller than 0.52GB estimated by flow cytometry. The heterozygosity is of about 0.54%, and a repeat rate of around 51.54%. All the shotgun data were assembled into 339,729 scaffolds, with an N50 of 17,344 bp. The average content of guanine and cytosine was approximately 35.16%. A total of 330,999 SSRs were detected, with mononucleotide repeats being the most abundant at 70.16%, followed by dinucleotide repeats at 20.40%. We conducted a preliminary ploidy assessment using Smudgeplot and observed a clear bimodal distribution in G. forrestii at 1/2 relative coverage depth and total coverage depth (2n), suggesting a potential diploid genome structure. A pseudo chromosome of G. forrestii and a gemone of Boswellia sacra were used as reference genome to perform a primer population resequencing analysis within three Garuga species. Principal component analysis (PCA) indicated three distinct groups, but genome wide phylogenetics represented conflicting both between the dataset of different reference genomes and between maternal and nuclear genome. CONCLUSION: In summary, the genome of G. forrestii is small, and the phylogenetic relationships within the Garuga genus are complex. The genetic data presented in this study holds significant value for comprehensive whole-genome analyses, the evaluation of population genetic diversity, investigations into adaptive evolution, the advancement of artificial breeding efforts, and the support of species conservation and restoration initiatives. Ultimately, this research contributes to reinforcing the conservation and management of natural ecosystems, promoting biodiversity conservation, and advancing sustainable development.
{"title":"A tip of the iceberg: genome survey indicated a complex evolutionary history of Garuga Roxb. species.","authors":"Dongbo Zhu, Rui Rao, Yu Du, Chunmin Mao, Rong Chen, Liangliang Yue","doi":"10.1186/s12864-024-10917-8","DOIUrl":"10.1186/s12864-024-10917-8","url":null,"abstract":"<p><p>BACKGROUND : Garuga Roxb. is a genus endemic to southwest China and other tropical regions in Southeast Asia facing risk of extinction due to the loss of tropical forests and changes in land use. Conducting a genome survey of G. forrestii contribute to a deeper understanding and conservation of the genus. RESULTS: This study utilized genome survey of G. forrestii generated approximately 54.56 GB of sequence data, with approximately 112 × coverage. K-mer analysis indicated a genome size of approximately 0.48 GB, smaller than 0.52GB estimated by flow cytometry. The heterozygosity is of about 0.54%, and a repeat rate of around 51.54%. All the shotgun data were assembled into 339,729 scaffolds, with an N50 of 17,344 bp. The average content of guanine and cytosine was approximately 35.16%. A total of 330,999 SSRs were detected, with mononucleotide repeats being the most abundant at 70.16%, followed by dinucleotide repeats at 20.40%. We conducted a preliminary ploidy assessment using Smudgeplot and observed a clear bimodal distribution in G. forrestii at 1/2 relative coverage depth and total coverage depth (2n), suggesting a potential diploid genome structure. A pseudo chromosome of G. forrestii and a gemone of Boswellia sacra were used as reference genome to perform a primer population resequencing analysis within three Garuga species. Principal component analysis (PCA) indicated three distinct groups, but genome wide phylogenetics represented conflicting both between the dataset of different reference genomes and between maternal and nuclear genome. CONCLUSION: In summary, the genome of G. forrestii is small, and the phylogenetic relationships within the Garuga genus are complex. The genetic data presented in this study holds significant value for comprehensive whole-genome analyses, the evaluation of population genetic diversity, investigations into adaptive evolution, the advancement of artificial breeding efforts, and the support of species conservation and restoration initiatives. Ultimately, this research contributes to reinforcing the conservation and management of natural ecosystems, promoting biodiversity conservation, and advancing sustainable development.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515747/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494709","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-23DOI: 10.1186/s12864-024-10893-z
Adhityo Wicaksono, Teerapong Buaboocha
Background: Calmodulin-binding transcription activator (CAMTA) is comprised of a group of transcription factors and plays an important role in the Ca2+ signaling pathway, mediating various molecular responses via interactions with other transcription factors and binding to the promoter region of specific genes. Mung beans (Vigna radiata) are one of the most commonly consumed commodities in Asia. To date, CAMTA proteins have not been characterized in this important crop plant.
Results: Eight paralogous VrCAMTA genes were identified and found to be distributed on five of the 11 chromosomes. The proteins possessed CG-1 DNA-binding domains with bipartite NLS signals, ankyrin domains, CaM-binding IQ motifs, and CaM-binding domain (CaMBD). The 2 kb upstream regions of VrCAMTA genes contained sequence motifs of abscisic acid-responsive elements (ABRE) and ethylene-responsive elements (ERE), and binding sites for transcription factors of the bZIP and bHLH domains. Analysis of RNA-seq data from a public repository revealed ubiquitous expression of the VrCAMTA genes, as VrCAMTA1 was expressed at the highest level in seedling leaves, whereas VrCAMTA8 was expressed at the lowest level, which agreed with the RT-qPCR analysis performed on the first true leaves. On day four after leaf emergence, all VrCAMTA genes were upregulated, with VrCAMTA1 exhibiting the highest degree of upregulation. In darkness on day 4, upregulation was not observed in most VrCAMTA genes, except VrCAMTA7, for which a low degree of upregulation was found, whereas no difference was found in VrCAMTA8 expression between light and dark conditions. Treatment with calcium ionophores enhanced VrCAMTA expression under light and/or dark conditions at different times after leaf emergence, suggesting that calcium signaling is involved in the light-induced upregulation of VrCAMTA gene expression.
Conclusions: The expression dependence of nearly all VrCAMTA genes on light and calcium signaling suggests their possible differential but likely complementary roles during the early stages of mung bean growth and development.
{"title":"Genome-wide identification of CAMTA genes and their expression dependence on light and calcium signaling during seedling growth and development in mung bean.","authors":"Adhityo Wicaksono, Teerapong Buaboocha","doi":"10.1186/s12864-024-10893-z","DOIUrl":"10.1186/s12864-024-10893-z","url":null,"abstract":"<p><strong>Background: </strong>Calmodulin-binding transcription activator (CAMTA) is comprised of a group of transcription factors and plays an important role in the Ca<sup>2+</sup> signaling pathway, mediating various molecular responses via interactions with other transcription factors and binding to the promoter region of specific genes. Mung beans (Vigna radiata) are one of the most commonly consumed commodities in Asia. To date, CAMTA proteins have not been characterized in this important crop plant.</p><p><strong>Results: </strong>Eight paralogous VrCAMTA genes were identified and found to be distributed on five of the 11 chromosomes. The proteins possessed CG-1 DNA-binding domains with bipartite NLS signals, ankyrin domains, CaM-binding IQ motifs, and CaM-binding domain (CaMBD). The 2 kb upstream regions of VrCAMTA genes contained sequence motifs of abscisic acid-responsive elements (ABRE) and ethylene-responsive elements (ERE), and binding sites for transcription factors of the bZIP and bHLH domains. Analysis of RNA-seq data from a public repository revealed ubiquitous expression of the VrCAMTA genes, as VrCAMTA1 was expressed at the highest level in seedling leaves, whereas VrCAMTA8 was expressed at the lowest level, which agreed with the RT-qPCR analysis performed on the first true leaves. On day four after leaf emergence, all VrCAMTA genes were upregulated, with VrCAMTA1 exhibiting the highest degree of upregulation. In darkness on day 4, upregulation was not observed in most VrCAMTA genes, except VrCAMTA7, for which a low degree of upregulation was found, whereas no difference was found in VrCAMTA8 expression between light and dark conditions. Treatment with calcium ionophores enhanced VrCAMTA expression under light and/or dark conditions at different times after leaf emergence, suggesting that calcium signaling is involved in the light-induced upregulation of VrCAMTA gene expression.</p><p><strong>Conclusions: </strong>The expression dependence of nearly all VrCAMTA genes on light and calcium signaling suggests their possible differential but likely complementary roles during the early stages of mung bean growth and development.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":null,"pages":null},"PeriodicalIF":3.5,"publicationDate":"2024-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11515718/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142494725","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}