Background: Staphylococcus aureus (S. aureus) mastitis results in economic losses during dairy production. Understanding the biological progression of bovine S. aureus mastitis is vital for its prevention. Lipoteichoic acid is a key virulence factor of S. aureus (aLTA), but the main biological pathways involved in its effect on bovine mammary epithetionallial cells (Mac-T) apoptosis and necrosis have not been fully explored. Folic acid (FA) has anti-inflammatory and anti-apoptotic effects. However, the role of FA in mediating the effects of aLTA on apoptosis and necrosis remains unknown.
Results: We found that low concentration of aLTA inhibited apoptosis and necrosis and that high concentration promoted the apoptosis and necrosis of Mac-T. FA pretreatment alleviated high concentration of aLTA induced apoptosis. Through transcriptomic analysis, we found that nuclear receptor subfamily 4 group A (NR4A), which alters the expression of downstream genes involved in apoptosis, proliferation, and inflammation, decreased under stimulation with a low concentration of aLTA and increased under stimulation with a high concentration of aLTA. Under stimulation with a high concentration of aLTA, the expression of the NR4A subfamily could be inhibited by FA. The results showed that aLTA may affect apoptosis and necrosis through the NR4A subfamily by targeting genes involved in bacterial invasion of epithelial cells, the IL-17 signaling pathway, DNA replication, longevity regulation, the cell cycle, and tight junction pathways. We further found that the expression trends of NR4A1 and the target genes of the NR4A subfamily (PTGS2, ESPL1, MCM5, and BUB1B) in the blood of healthy cows (Healthy), subclinical mastitis cows (SCM), and SCM supplemented with FA (SCM_FA) were consistent with those observed at the cellular level in this study.
Conclusions: Our study revealed that low and high concentrations of aLTA have opposite effects on apoptosis and necrosis of Mac-T and that FA can alleviate the apoptosis induced by high concentration of aLTA. Transcriptome analysis revealed that the NR4A subfamily play a role in the ability of FA to alleviate the apoptosis and necrosis induced by high concentration of aLTA.
背景:金黄色葡萄球菌(S. aureus)乳腺炎会给奶牛生产造成经济损失。了解牛金黄色葡萄球菌乳腺炎的生物学发展过程对预防乳腺炎至关重要。脂联素是金黄色葡萄球菌(aLTA)的关键毒力因子,但其影响牛乳腺上皮细胞(Mac-T)凋亡和坏死的主要生物学途径尚未完全探明。叶酸(FA)具有抗炎和抗细胞凋亡的作用。然而,叶酸在介导 aLTA 对细胞凋亡和坏死的影响中的作用仍然未知:结果:我们发现低浓度的 aLTA 可抑制 Mac-T 的细胞凋亡和坏死,而高浓度的 aLTA 则可促进 Mac-T 的细胞凋亡和坏死。FA预处理减轻了高浓度aLTA诱导的细胞凋亡。通过转录组分析,我们发现核受体 4 亚家族 A 组(NR4A)会改变参与凋亡、增殖和炎症的下游基因的表达,在低浓度 aLTA 的刺激下,NR4A 的表达减少,而在高浓度 aLTA 的刺激下,NR4A 的表达增加。在高浓度 aLTA 的刺激下,FA 可抑制 NR4A 亚家族的表达。结果表明,aLTA 可能通过 NR4A 亚家族靶向参与细菌入侵上皮细胞、IL-17 信号通路、DNA 复制、长寿调节、细胞周期和紧密连接通路的基因,从而影响细胞凋亡和坏死。我们进一步发现,健康奶牛(Healthy)、亚临床乳腺炎奶牛(SCM)和补充了 FA 的 SCM(SCM_FA)血液中 NR4A1 和 NR4A 亚家族靶基因(PTGS2、ESPL1、MCM5 和 BUB1B)的表达趋势与本研究在细胞水平观察到的趋势一致:我们的研究表明,低浓度和高浓度的 aLTA 对 Mac-T 的凋亡和坏死具有相反的影响,而 FA 可以缓解高浓度 aLTA 诱导的凋亡。转录组分析显示,NR4A亚家族在FA缓解高浓度aLTA诱导的凋亡和坏死的能力中发挥了作用。
{"title":"Transcriptome analysis identifies the NR4A subfamily involved in the alleviating effect of folic acid on mastitis induced by high concentration of Staphylococcus aureus lipoteichoic acid.","authors":"Quanzhen Chen, Siyuan Mi, Yue Xing, Songyan An, Siqian Chen, Yongjie Tang, Yajing Wang, Ying Yu","doi":"10.1186/s12864-024-10895-x","DOIUrl":"10.1186/s12864-024-10895-x","url":null,"abstract":"<p><strong>Background: </strong>Staphylococcus aureus (S. aureus) mastitis results in economic losses during dairy production. Understanding the biological progression of bovine S. aureus mastitis is vital for its prevention. Lipoteichoic acid is a key virulence factor of S. aureus (aLTA), but the main biological pathways involved in its effect on bovine mammary epithetionallial cells (Mac-T) apoptosis and necrosis have not been fully explored. Folic acid (FA) has anti-inflammatory and anti-apoptotic effects. However, the role of FA in mediating the effects of aLTA on apoptosis and necrosis remains unknown.</p><p><strong>Results: </strong>We found that low concentration of aLTA inhibited apoptosis and necrosis and that high concentration promoted the apoptosis and necrosis of Mac-T. FA pretreatment alleviated high concentration of aLTA induced apoptosis. Through transcriptomic analysis, we found that nuclear receptor subfamily 4 group A (NR4A), which alters the expression of downstream genes involved in apoptosis, proliferation, and inflammation, decreased under stimulation with a low concentration of aLTA and increased under stimulation with a high concentration of aLTA. Under stimulation with a high concentration of aLTA, the expression of the NR4A subfamily could be inhibited by FA. The results showed that aLTA may affect apoptosis and necrosis through the NR4A subfamily by targeting genes involved in bacterial invasion of epithelial cells, the IL-17 signaling pathway, DNA replication, longevity regulation, the cell cycle, and tight junction pathways. We further found that the expression trends of NR4A1 and the target genes of the NR4A subfamily (PTGS2, ESPL1, MCM5, and BUB1B) in the blood of healthy cows (Healthy), subclinical mastitis cows (SCM), and SCM supplemented with FA (SCM_FA) were consistent with those observed at the cellular level in this study.</p><p><strong>Conclusions: </strong>Our study revealed that low and high concentrations of aLTA have opposite effects on apoptosis and necrosis of Mac-T and that FA can alleviate the apoptosis induced by high concentration of aLTA. Transcriptome analysis revealed that the NR4A subfamily play a role in the ability of FA to alleviate the apoptosis and necrosis induced by high concentration of aLTA.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1051"},"PeriodicalIF":3.5,"publicationDate":"2024-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11542246/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589388","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 : 2024-11-07DOI: 10.1186/s12864-024-10980-1
Shuilian He, Yinqi Siman, Gengyun Li, Junheng Lv, Kai Zhao, Minghua Deng
Background: Capsicum (Solanaceae) is a globally important vegetable crop and is also used therapeutically in traditional medicine systems. However, little is known of the genetic variation within the commonly grown cultivars, the evolutionary relationships and differences in the chloroplast (cp.) genomes between Capsicum species remain unclear.
Results: The cp. genomes of 32 Capsicum varieties in three species from 6 countries were investigated. The cp. genome of Capsicum was found to be ~ 156 kb in length and to contain 113 unique genes, of which 79 encoded proteins, 30 encoded transfer tRNAs, and 4 were for ribosomal RNAs. The 32 varieties that we chose for study represented 13 genotypes, containing a total of 608 indels, 83 SNPs, 47 SSRs and 281-306 repeat sequences. We then included several previously sequenced Capsicum cp. genomes, and found that the nine investigated species showed a number of differences in the characteristics of the four IR boundaries, and it was the non-coding regions that contained the most variable regions. We conducted a phylogenetic reconstruction using the cp. genomes of 43 representative species of Solanaceae, and the resulting phylogeny generally reflected the currently accepted classification, with the species of the pungent group having close relationship with one another.
Conclusions: This study provides a comprehensive analysis of Capsicum chloroplast genomes, revealing significant variations in IR boundaries and other genomic features. These findings enhance our understanding of Capsicum evolution and genetic diversity.
{"title":"Chloroplast genome characteristic, comparative and phylogenetic analyses in Capsicum (Solanaceae).","authors":"Shuilian He, Yinqi Siman, Gengyun Li, Junheng Lv, Kai Zhao, Minghua Deng","doi":"10.1186/s12864-024-10980-1","DOIUrl":"10.1186/s12864-024-10980-1","url":null,"abstract":"<p><strong>Background: </strong>Capsicum (Solanaceae) is a globally important vegetable crop and is also used therapeutically in traditional medicine systems. However, little is known of the genetic variation within the commonly grown cultivars, the evolutionary relationships and differences in the chloroplast (cp.) genomes between Capsicum species remain unclear.</p><p><strong>Results: </strong>The cp. genomes of 32 Capsicum varieties in three species from 6 countries were investigated. The cp. genome of Capsicum was found to be ~ 156 kb in length and to contain 113 unique genes, of which 79 encoded proteins, 30 encoded transfer tRNAs, and 4 were for ribosomal RNAs. The 32 varieties that we chose for study represented 13 genotypes, containing a total of 608 indels, 83 SNPs, 47 SSRs and 281-306 repeat sequences. We then included several previously sequenced Capsicum cp. genomes, and found that the nine investigated species showed a number of differences in the characteristics of the four IR boundaries, and it was the non-coding regions that contained the most variable regions. We conducted a phylogenetic reconstruction using the cp. genomes of 43 representative species of Solanaceae, and the resulting phylogeny generally reflected the currently accepted classification, with the species of the pungent group having close relationship with one another.</p><p><strong>Conclusions: </strong>This study provides a comprehensive analysis of Capsicum chloroplast genomes, revealing significant variations in IR boundaries and other genomic features. These findings enhance our understanding of Capsicum evolution and genetic diversity.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1052"},"PeriodicalIF":4.3,"publicationDate":"2024-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11542203/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142603073","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 : 2024-11-06DOI: 10.1186/s12864-024-10896-w
Martine Devic, Louis Dennu, Jean-Claude Lozano, Cédric Mariac, Valérie Vergé, Philippe Schatt, François-Yves Bouget, François Sabot
Background: Although metabarcoding and metagenomic approaches have generated large datasets on worldwide phytoplankton species diversity, the intraspecific genetic diversity underlying the genetic adaptation of marine phytoplankton to specific environmental niches remains largely unexplored. This is mainly due to the lack of biological resources and tools for monitoring the dynamics of this diversity in space and time.
Results: To gain insight into population diversity, a novel method based on INDEL markers was developed on Bathycoccus prasinos (Mamiellophyceae), an abundant and cosmopolitan species with strong seasonal patterns. Long read sequencing was first used to characterize structural variants among the genomes of six B. prasinos strains sampled from geographically distinct regions in the world ocean. Markers derived from identified insertions/deletions were validated by PCR then used to genotype 55 B. prasinos strains isolated during the winter bloom 2018-2019 in the bay of Banyuls-sur-Mer (Mediterranean Sea, France). This led to their classification into eight multi-loci genotypes and the sequencing of strains representative of local diversity, further improving the available genetic diversity of B. prasinos. Finally, selected markers were directly tracked on environmental DNA sampled during 3 successive blooms from 2018 to 2021, showcasing a fast and cost-effective approach to follow local population dynamics.
Conclusions: This method, which involves (i) pre-identifying the genetic diversity of B. prasinos in environmental samples by PCR, (ii) isolating cells from selected environmental samples and (iii) identifying genotypes representative of B. prasinos diversity for sequencing, can be used to comprehensively describe the diversity and population dynamics not only in B. prasinos but also potentially in other generalist phytoplankton species.
背景:尽管代谢编码和元基因组学方法已经产生了有关全球浮游植物物种多样性的大量数据集,但海洋浮游植物对特定环境生态位的遗传适应所依赖的种内遗传多样性在很大程度上仍未得到探索。这主要是由于缺乏生物资源和工具来监测这种多样性在空间和时间上的动态变化:为了深入了解种群多样性,研究人员开发了一种基于 INDEL 标记的新方法,该方法适用于 Bathycoccus prasinos(Mamiellophyceae),这是一种丰富的世界性物种,具有很强的季节性。首先使用长读数测序来描述从世界海洋不同地理区域采样的六个 B. prasinos 菌株基因组的结构变异特征。通过 PCR 验证了从已识别的插入/缺失中提取的标记,然后用于对 2018-2019 年冬季水华期间在 Banyuls-sur-Mer 海湾(法国地中海)分离的 55 株 B. prasinos 菌株进行基因分型。这使得它们被划分为八个多基因型,并对代表当地多样性的菌株进行了测序,进一步提高了普拉西诺斯蚕的现有遗传多样性。最后,在 2018 年至 2021 年连续 3 次水华期间,对环境 DNA 取样直接跟踪所选标记,展示了一种快速、经济有效的方法来跟踪当地种群动态:该方法包括:(i)通过 PCR 预先确定环境样本中棱皮藻的遗传多样性;(ii)从选定的环境样本中分离细胞;(iii)确定代表棱皮藻多样性的基因型进行测序。
{"title":"An INDEL genomic approach to explore population diversity of phytoplankton.","authors":"Martine Devic, Louis Dennu, Jean-Claude Lozano, Cédric Mariac, Valérie Vergé, Philippe Schatt, François-Yves Bouget, François Sabot","doi":"10.1186/s12864-024-10896-w","DOIUrl":"10.1186/s12864-024-10896-w","url":null,"abstract":"<p><strong>Background: </strong>Although metabarcoding and metagenomic approaches have generated large datasets on worldwide phytoplankton species diversity, the intraspecific genetic diversity underlying the genetic adaptation of marine phytoplankton to specific environmental niches remains largely unexplored. This is mainly due to the lack of biological resources and tools for monitoring the dynamics of this diversity in space and time.</p><p><strong>Results: </strong>To gain insight into population diversity, a novel method based on INDEL markers was developed on Bathycoccus prasinos (Mamiellophyceae), an abundant and cosmopolitan species with strong seasonal patterns. Long read sequencing was first used to characterize structural variants among the genomes of six B. prasinos strains sampled from geographically distinct regions in the world ocean. Markers derived from identified insertions/deletions were validated by PCR then used to genotype 55 B. prasinos strains isolated during the winter bloom 2018-2019 in the bay of Banyuls-sur-Mer (Mediterranean Sea, France). This led to their classification into eight multi-loci genotypes and the sequencing of strains representative of local diversity, further improving the available genetic diversity of B. prasinos. Finally, selected markers were directly tracked on environmental DNA sampled during 3 successive blooms from 2018 to 2021, showcasing a fast and cost-effective approach to follow local population dynamics.</p><p><strong>Conclusions: </strong>This method, which involves (i) pre-identifying the genetic diversity of B. prasinos in environmental samples by PCR, (ii) isolating cells from selected environmental samples and (iii) identifying genotypes representative of B. prasinos diversity for sequencing, can be used to comprehensively describe the diversity and population dynamics not only in B. prasinos but also potentially in other generalist phytoplankton species.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1045"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539686/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589320","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}
Background: The placenta is essential for nutrient exchange and hormone production between the mother and the developing fetus and serves as an invaluable model for epigenetic research. Most epigenetic studies of the human placenta have used whole placentas from term pregnancies and have identified the presence of partially methylated domains (PMDs). However, the origin of these domains, which are typically absent in most somatic cells, remains unclear in the placental context.
Results: Using whole-genome bisulfite sequencing and analysis of histone H3 modifications, we generated epigenetic profiles of human cytotrophoblasts during the first trimester and at term, as well as human trophoblast stem cells. Our study focused specifically on PMDs. We found that genomic regions likely to form PMDs are resistant to global DNA demethylation during trophectoderm reprogramming, and that PMDs arise through a slow methylation process within condensed chromatin near the nuclear lamina. In addition, we found significant differences in histone H3 modifications between PMDs in cytotrophoblasts and trophoblast stem cells.
Conclusions: Our findings suggest that spatiotemporal genomic features shape megabase-scale DNA methylation patterns, including PMDs, in the human placenta and highlight distinct differences in PMDs between human cytotrophoblasts and trophoblast stem cells. These findings advance our understanding of placental biology and provide a basis for further research into human development and related diseases.
背景:胎盘对母体和发育中胎儿之间的营养交换和激素分泌至关重要,是表观遗传学研究的宝贵模型。对人类胎盘进行的大多数表观遗传学研究都使用了足月妊娠的整个胎盘,并发现了部分甲基化结构域(PMDs)的存在。然而,这些在大多数体细胞中通常不存在的结构域在胎盘中的起源仍不清楚:结果:通过全基因组亚硫酸氢盐测序和组蛋白 H3 修饰分析,我们生成了妊娠头三个月和足月人类细胞滋养层母细胞以及人类滋养层母细胞干细胞的表观遗传学图谱。我们的研究特别关注 PMD。我们发现,在滋养层外胚层重编程过程中,可能形成 PMD 的基因组区域对全局 DNA 去甲基化具有抵抗力,而 PMD 是通过核薄层附近凝聚染色质内的缓慢甲基化过程产生的。此外,我们还发现细胞滋养层细胞和滋养层干细胞中的PMDs在组蛋白H3修饰方面存在显著差异:我们的研究结果表明,时空基因组特征塑造了人类胎盘的巨碱基DNA甲基化模式,包括PMDs,并强调了人类细胞滋养层母细胞和滋养层干细胞之间在PMDs上的明显差异。这些发现增进了我们对胎盘生物学的了解,为进一步研究人类发育和相关疾病提供了基础。
{"title":"Epigenetic dynamics of partially methylated domains in human placenta and trophoblast stem cells.","authors":"Hidehiro Toh, Hiroaki Okae, Kenjiro Shirane, Tetsuya Sato, Hirotaka Hamada, Chie Kikutake, Daisuke Saito, Takahiro Arima, Hiroyuki Sasaki, Mikita Suyama","doi":"10.1186/s12864-024-10986-9","DOIUrl":"10.1186/s12864-024-10986-9","url":null,"abstract":"<p><strong>Background: </strong>The placenta is essential for nutrient exchange and hormone production between the mother and the developing fetus and serves as an invaluable model for epigenetic research. Most epigenetic studies of the human placenta have used whole placentas from term pregnancies and have identified the presence of partially methylated domains (PMDs). However, the origin of these domains, which are typically absent in most somatic cells, remains unclear in the placental context.</p><p><strong>Results: </strong>Using whole-genome bisulfite sequencing and analysis of histone H3 modifications, we generated epigenetic profiles of human cytotrophoblasts during the first trimester and at term, as well as human trophoblast stem cells. Our study focused specifically on PMDs. We found that genomic regions likely to form PMDs are resistant to global DNA demethylation during trophectoderm reprogramming, and that PMDs arise through a slow methylation process within condensed chromatin near the nuclear lamina. In addition, we found significant differences in histone H3 modifications between PMDs in cytotrophoblasts and trophoblast stem cells.</p><p><strong>Conclusions: </strong>Our findings suggest that spatiotemporal genomic features shape megabase-scale DNA methylation patterns, including PMDs, in the human placenta and highlight distinct differences in PMDs between human cytotrophoblasts and trophoblast stem cells. These findings advance our understanding of placental biology and provide a basis for further research into human development and related diseases.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1050"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11542204/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589341","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 : 2024-11-06DOI: 10.1186/s12864-024-10910-1
L Magpali, E Ramos, A Picorelli, L Freitas, M F Nery
Background: Echolocation was a key development in toothed whale evolution, enabling their adaptation and diversification across various environments. Previous bioacoustic and morphological studies suggest that environmental pressures have influenced the evolution of echolocation in toothed whales. This hypothesis demands further investigation, especially regarding the molecular mechanisms involved in the adaptive radiation of toothed whales across multiple habitats. Here we show that the coding sequences of four hearing genes involved in echolocation (CDH23, prestin, TMC1, and CLDN14) have different signatures of molecular evolution among riverine, coastal, and oceanic dolphins, suggesting that the evolutionary constraints of these habitats shaped the underlying genetic diversity of the toothed whale sonar.
Results: Our comparative analysis across 37 odontocete species revealed patterns of accelerated evolution within coastal and riverine lineages, supporting the hypothesis that shallow habitats pose specific selective pressures to sonar propagation, which are not found in the deep ocean. All toothed whales with genes evolving under positive selection are shallow coastal species, including three species that have recently diverged from freshwater lineages (Cephalorhynchus commersonii, Sotalia guianensis, and Orcaella heinsohni - CDH23), and three species that operate specialized Narrow Band High Frequency (NBHF) Sonars (Phocoena sinus - prestin, Neophocaena phocaenoides - TMC1 and Cephalorhynchus commersonii - CDH23). For river dolphins and deep-diving toothed whales, we found signatures of positive selection and molecular convergence affecting specific sites on CDH23, TMC1, and prestin. Positively selected sites (PSS) were different in number, identity, and substitution rates (dN/dS) across riverine, coastal, and oceanic toothed whales.
Conclusion: Here we shed light on potential molecular mechanisms underlying the diversification of toothed whale echolocation. Our results suggest that toothed whale hearing genes changed under different selective pressures in coastal, riverine, and oceanic environments.
{"title":"Molecular evolution of toothed whale genes reveals adaptations to echolocating in different environments.","authors":"L Magpali, E Ramos, A Picorelli, L Freitas, M F Nery","doi":"10.1186/s12864-024-10910-1","DOIUrl":"10.1186/s12864-024-10910-1","url":null,"abstract":"<p><strong>Background: </strong>Echolocation was a key development in toothed whale evolution, enabling their adaptation and diversification across various environments. Previous bioacoustic and morphological studies suggest that environmental pressures have influenced the evolution of echolocation in toothed whales. This hypothesis demands further investigation, especially regarding the molecular mechanisms involved in the adaptive radiation of toothed whales across multiple habitats. Here we show that the coding sequences of four hearing genes involved in echolocation (CDH23, prestin, TMC1, and CLDN14) have different signatures of molecular evolution among riverine, coastal, and oceanic dolphins, suggesting that the evolutionary constraints of these habitats shaped the underlying genetic diversity of the toothed whale sonar.</p><p><strong>Results: </strong>Our comparative analysis across 37 odontocete species revealed patterns of accelerated evolution within coastal and riverine lineages, supporting the hypothesis that shallow habitats pose specific selective pressures to sonar propagation, which are not found in the deep ocean. All toothed whales with genes evolving under positive selection are shallow coastal species, including three species that have recently diverged from freshwater lineages (Cephalorhynchus commersonii, Sotalia guianensis, and Orcaella heinsohni - CDH23), and three species that operate specialized Narrow Band High Frequency (NBHF) Sonars (Phocoena sinus - prestin, Neophocaena phocaenoides - TMC1 and Cephalorhynchus commersonii - CDH23). For river dolphins and deep-diving toothed whales, we found signatures of positive selection and molecular convergence affecting specific sites on CDH23, TMC1, and prestin. Positively selected sites (PSS) were different in number, identity, and substitution rates (dN/dS) across riverine, coastal, and oceanic toothed whales.</p><p><strong>Conclusion: </strong>Here we shed light on potential molecular mechanisms underlying the diversification of toothed whale echolocation. Our results suggest that toothed whale hearing genes changed under different selective pressures in coastal, riverine, and oceanic environments.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1049"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11542384/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589384","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 : 2024-11-06DOI: 10.1186/s12864-024-10966-z
Juntao Song, Jie Tan, Tao Long, Yuanshuai Shi, Xu Luo, Yang Liu
Brassinosteroids (BRs), one of the major classes of phytohormones are essential for various processes of plant growth, development, and adaptations to biotic and abiotic stresses. In Arabidopsis, AtCYP90D1 acts as a bifunctional cytochrome P450 monooxygenase, catalyzing C-23 hydroxylation in the brassinolide biosynthetic pathway. The present study reports the functional characterizations of PtoCYP90D1, one of the AtCYP90D1 homologous genes from Populus tomentosa. The qRT-PCR analysis showed that PtoCYP90D1 was highly expressed in roots and old leaves. Overexpression of PtoCYP90D1 (PtoCYP90D1-OE) in poplar promoted growth and biomass yield, as well as increased xylem area and cell layers. Transgenic plants exhibited a significant increase in plant height and stem diameter as compared to the wild type. In contrast, the CRISPR/Cas9-generated mutation of PtoCYP90D1 (PtoCYP90D1-KO) resulted in significantly decreased biomass production in transgenic plants. Further studies revealed that cell wall components increased significantly in PtoCYP90D1-OE lines but not in PtoCYP90D1-KO lines, as compared to wild-type plants. Overall, the findings indicate a positive role of PtoCYP90D1 in improving growth rate and elevating biomass production in poplar, which will have positive implications for its versatile industrial or agricultural applications.
{"title":"Molecular cloning and characterization of a brassinosteriod biosynthesis-related gene PtoCYP90D1 from Populus tomentosa.","authors":"Juntao Song, Jie Tan, Tao Long, Yuanshuai Shi, Xu Luo, Yang Liu","doi":"10.1186/s12864-024-10966-z","DOIUrl":"10.1186/s12864-024-10966-z","url":null,"abstract":"<p><p>Brassinosteroids (BRs), one of the major classes of phytohormones are essential for various processes of plant growth, development, and adaptations to biotic and abiotic stresses. In Arabidopsis, AtCYP90D1 acts as a bifunctional cytochrome P450 monooxygenase, catalyzing C-23 hydroxylation in the brassinolide biosynthetic pathway. The present study reports the functional characterizations of PtoCYP90D1, one of the AtCYP90D1 homologous genes from Populus tomentosa. The qRT-PCR analysis showed that PtoCYP90D1 was highly expressed in roots and old leaves. Overexpression of PtoCYP90D1 (PtoCYP90D1-OE) in poplar promoted growth and biomass yield, as well as increased xylem area and cell layers. Transgenic plants exhibited a significant increase in plant height and stem diameter as compared to the wild type. In contrast, the CRISPR/Cas9-generated mutation of PtoCYP90D1 (PtoCYP90D1-KO) resulted in significantly decreased biomass production in transgenic plants. Further studies revealed that cell wall components increased significantly in PtoCYP90D1-OE lines but not in PtoCYP90D1-KO lines, as compared to wild-type plants. Overall, the findings indicate a positive role of PtoCYP90D1 in improving growth rate and elevating biomass production in poplar, which will have positive implications for its versatile industrial or agricultural applications.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1047"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539751/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589371","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 : 2024-11-06DOI: 10.1186/s12864-024-10958-z
Muhammad Sarmad Iftikhar, Hafiza Masooma Naseer Cheema, Asif Ali Khan, Ian Henson DeLacy, Kaye Enid Basford
Genetic profiling of the biodiversity in cultivated crop plants is necessary to preserve important genes and utilize them in a breeding program. Cucumber is used as a model plant to study various characteristics of Cucurbitaceae. Its adaptation to a wide range of climatic conditions suggested analyzing the landraces. The present study was conducted to evaluate the differences, at the genetic level, among landraces spanning five continents. DNA extracted from fifty-six landraces selected from USDA germplasm bank to cover a global representative sample of world cucumber landraces was used for polymerase chain reaction using twenty-eight polymorphic expressed sequence tags simple sequence repeat (EST-SSR) markers. Twenty-eight EST-SSR markers covering all seven chromosomes yielded 98 bands with an average of 3.42 bands per marker. Polymorphic information content ranged from 0.00 (EC35) to 0.74 (EC17) with an average of 0.34. Six clusters provided an appropriate summary of the variation among the landraces, with the two largest groups including 32 (Asiatic) and 17 (European and American) landraces, respectively. Four small groups, three with two members, and one with one member (PI 525155-Egypt) were dissimilar to the two main groups. Landraces from the same region were often clustered together. Genetic similarity of the landraces was revealed by marker banding patterns. The locations of genetic diversity for cucumber landraces can be identified from this study.
{"title":"Genetic diversity assessment of cucumber landraces using molecular signatures.","authors":"Muhammad Sarmad Iftikhar, Hafiza Masooma Naseer Cheema, Asif Ali Khan, Ian Henson DeLacy, Kaye Enid Basford","doi":"10.1186/s12864-024-10958-z","DOIUrl":"10.1186/s12864-024-10958-z","url":null,"abstract":"<p><p>Genetic profiling of the biodiversity in cultivated crop plants is necessary to preserve important genes and utilize them in a breeding program. Cucumber is used as a model plant to study various characteristics of Cucurbitaceae. Its adaptation to a wide range of climatic conditions suggested analyzing the landraces. The present study was conducted to evaluate the differences, at the genetic level, among landraces spanning five continents. DNA extracted from fifty-six landraces selected from USDA germplasm bank to cover a global representative sample of world cucumber landraces was used for polymerase chain reaction using twenty-eight polymorphic expressed sequence tags simple sequence repeat (EST-SSR) markers. Twenty-eight EST-SSR markers covering all seven chromosomes yielded 98 bands with an average of 3.42 bands per marker. Polymorphic information content ranged from 0.00 (EC35) to 0.74 (EC17) with an average of 0.34. Six clusters provided an appropriate summary of the variation among the landraces, with the two largest groups including 32 (Asiatic) and 17 (European and American) landraces, respectively. Four small groups, three with two members, and one with one member (PI 525155-Egypt) were dissimilar to the two main groups. Landraces from the same region were often clustered together. Genetic similarity of the landraces was revealed by marker banding patterns. The locations of genetic diversity for cucumber landraces can be identified from this study.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1046"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539674/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589345","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 : 2024-11-06DOI: 10.1186/s12864-024-10955-2
Zhiqiang Wang, Mingyu Wang, Yujingyun Zhou, Kai Feng, Fang Tang
Background: Odontotermes formosanus (Shiraki) is a highly damaging agroforestry pest. Serratia marcescens is a broad-spectrum insecticidal pathogen and is highly lethal to O. formosanus. However, little is known about the mechanism between them. To improve the biological control of pests, a more in-depth analysis of the interactions between the pests and the pathogens is essential.
Results: We used RNA-seq, enzyme activity assays and real-time fluorescent quantitative PCR (qPCR) to explore the defense responses of O. formosanus against SM1. RNA-seq results showed that 1,160, 2,531 and 4,536 genes were differentially expressed at 3, 6 and 12 h after SM1 infection, and Kyoto Encyclopedia of Genes and Genomes (KEGG) results indicated that immune response and energy metabolism were involved in the defense of O. formosanus against SM1. Reactive oxygen species (ROS) levels and ROS synthesis genes were significantly elevated, and the antioxidant system were induced in O. formosanus after SM1 infection. In addition, the cellular immune genes were affected, and the Toll, immune deficiency (Imd), Janus kinase/signal transducer and activator of transcription (JAK/STAT), c-Jun N-terminal Kinase (JNK) and melanization pathways were activated. In vitro, Oftermicin, an antimicrobial peptide, had a significantly inhibitory effect on SM1. Furthermore, the expression levels and enzyme activities of phosphofructokinase (PFK), lactate dehydrogenase (LDH), succinate dehydrogenase (SDH) and isocitrate dehydrogenase (IDH) in glycolysis and tricarboxylic acid (TCA) cycles were increased.
Conclusions: Our results clearly demonstrated that O. formosanus defended against SM1 by activating the antioxidant system, innate immunity and energy metabolism. This study would provide useful information for the development of biological controls of O. formosanus.
{"title":"A comprehensive analysis of the defense responses of Odontotermes formosanus (Shiraki) provides insights into the changes during Serratia marcescens infection.","authors":"Zhiqiang Wang, Mingyu Wang, Yujingyun Zhou, Kai Feng, Fang Tang","doi":"10.1186/s12864-024-10955-2","DOIUrl":"10.1186/s12864-024-10955-2","url":null,"abstract":"<p><strong>Background: </strong>Odontotermes formosanus (Shiraki) is a highly damaging agroforestry pest. Serratia marcescens is a broad-spectrum insecticidal pathogen and is highly lethal to O. formosanus. However, little is known about the mechanism between them. To improve the biological control of pests, a more in-depth analysis of the interactions between the pests and the pathogens is essential.</p><p><strong>Results: </strong>We used RNA-seq, enzyme activity assays and real-time fluorescent quantitative PCR (qPCR) to explore the defense responses of O. formosanus against SM1. RNA-seq results showed that 1,160, 2,531 and 4,536 genes were differentially expressed at 3, 6 and 12 h after SM1 infection, and Kyoto Encyclopedia of Genes and Genomes (KEGG) results indicated that immune response and energy metabolism were involved in the defense of O. formosanus against SM1. Reactive oxygen species (ROS) levels and ROS synthesis genes were significantly elevated, and the antioxidant system were induced in O. formosanus after SM1 infection. In addition, the cellular immune genes were affected, and the Toll, immune deficiency (Imd), Janus kinase/signal transducer and activator of transcription (JAK/STAT), c-Jun N-terminal Kinase (JNK) and melanization pathways were activated. In vitro, Oftermicin, an antimicrobial peptide, had a significantly inhibitory effect on SM1. Furthermore, the expression levels and enzyme activities of phosphofructokinase (PFK), lactate dehydrogenase (LDH), succinate dehydrogenase (SDH) and isocitrate dehydrogenase (IDH) in glycolysis and tricarboxylic acid (TCA) cycles were increased.</p><p><strong>Conclusions: </strong>Our results clearly demonstrated that O. formosanus defended against SM1 by activating the antioxidant system, innate immunity and energy metabolism. This study would provide useful information for the development of biological controls of O. formosanus.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1044"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539531/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589302","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 : 2024-11-06DOI: 10.1186/s12864-024-10969-w
Barış Yaşar, Nina Boskovic, Marilin Ivask, Jere Weltner, Eeva-Mari Jouhilahti, Piibe Vill, Tiina Skoog, Ülle Jaakma, Juha Kere, Thomas R Bürglin, Shintaro Katayama, Tõnis Org, Ants Kurg
Background: Embryonic genome activation (EGA) is a critical step in early embryonic development, as it marks the transition from relying on maternal factors to the initiation of transcription from embryo's own genome. The factors associated with EGA are not well understood and need further investigation. PRD-like (PRDL) homeodomain transcription factors (TFs) are considered to play crucial roles in this early event during development but these TFs have evolved differently, even within mammalian lineages. Different numbers of PRDL TFs have been predicted in bovine (Bos taurus); however, their divergent evolution requires species-specific confirmation and functional investigations.
Results: In this study, we conducted molecular cloning of mRNAs for the PRDL TFs ARGFX, DUXA, LEUTX, NOBOX, TPRX1, TPRX2, and TPRX3 in bovine oocytes or in vitro fertilized (IVF) preimplantation embryos. Our results confirmed the expression of PRDL TF genes in early bovine development at the cDNA level and uncovered their structures. For each investigated PRDL TF gene, we isolated at least one homeodomain-encoding cDNA fragment, indicative of DNA binding and thus potential role in transcriptional regulation in developing bovine embryos. Additionally, our cDNA cloning approach allowed us to reveal breed-related differences in bovine, as evidenced by the identification of a high number of single nucleotide variants (SNVs) across the PRDL class homeobox genes. Subsequently, we observed the prediction of the 9aa transactivation domain (9aaTAD) motif in the putative protein sequence of TPRX3 leading us to conduct functional analysis of this gene. We demonstrated that the TPRX3 overexpression in bovine fibroblast induces not only protein-coding genes but also short noncoding RNAs involved in splicing and RNA editing. We supported this finding by identifying a shared set of genes between our and published bovine early embryo development datasets.
Conclusions: Providing full-length cDNA evidence for previously predicted homeobox genes that belong to PRDL class improves the annotation of the bovine genome. Updating the annotation with seven developmentally-important genes will enhance the accuracy of RNAseq analysis with datasets derived from bovine preimplantation embryos. In addition, the absence of TPRX3 in humans highlights the species-specific and TF-specific regulation of biological processes during early embryo development.
{"title":"Molecular cloning of PRD-like homeobox genes expressed in bovine oocytes and early IVF embryos.","authors":"Barış Yaşar, Nina Boskovic, Marilin Ivask, Jere Weltner, Eeva-Mari Jouhilahti, Piibe Vill, Tiina Skoog, Ülle Jaakma, Juha Kere, Thomas R Bürglin, Shintaro Katayama, Tõnis Org, Ants Kurg","doi":"10.1186/s12864-024-10969-w","DOIUrl":"10.1186/s12864-024-10969-w","url":null,"abstract":"<p><strong>Background: </strong>Embryonic genome activation (EGA) is a critical step in early embryonic development, as it marks the transition from relying on maternal factors to the initiation of transcription from embryo's own genome. The factors associated with EGA are not well understood and need further investigation. PRD-like (PRDL) homeodomain transcription factors (TFs) are considered to play crucial roles in this early event during development but these TFs have evolved differently, even within mammalian lineages. Different numbers of PRDL TFs have been predicted in bovine (Bos taurus); however, their divergent evolution requires species-specific confirmation and functional investigations.</p><p><strong>Results: </strong>In this study, we conducted molecular cloning of mRNAs for the PRDL TFs ARGFX, DUXA, LEUTX, NOBOX, TPRX1, TPRX2, and TPRX3 in bovine oocytes or in vitro fertilized (IVF) preimplantation embryos. Our results confirmed the expression of PRDL TF genes in early bovine development at the cDNA level and uncovered their structures. For each investigated PRDL TF gene, we isolated at least one homeodomain-encoding cDNA fragment, indicative of DNA binding and thus potential role in transcriptional regulation in developing bovine embryos. Additionally, our cDNA cloning approach allowed us to reveal breed-related differences in bovine, as evidenced by the identification of a high number of single nucleotide variants (SNVs) across the PRDL class homeobox genes. Subsequently, we observed the prediction of the 9aa transactivation domain (9aaTAD) motif in the putative protein sequence of TPRX3 leading us to conduct functional analysis of this gene. We demonstrated that the TPRX3 overexpression in bovine fibroblast induces not only protein-coding genes but also short noncoding RNAs involved in splicing and RNA editing. We supported this finding by identifying a shared set of genes between our and published bovine early embryo development datasets.</p><p><strong>Conclusions: </strong>Providing full-length cDNA evidence for previously predicted homeobox genes that belong to PRDL class improves the annotation of the bovine genome. Updating the annotation with seven developmentally-important genes will enhance the accuracy of RNAseq analysis with datasets derived from bovine preimplantation embryos. In addition, the absence of TPRX3 in humans highlights the species-specific and TF-specific regulation of biological processes during early embryo development.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1048"},"PeriodicalIF":3.5,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11542365/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142589379","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}
Background: The Japanese cedar (Cryptomeria japonica D. Don) is one of the most important Japanese forest trees, occupying approximately 44% of artificial forests and planted in East Asia, the Azores Archipelago, and certain islands in the Indian Ocean. Although the huge genome of the species (ca. 9 Gbp) with abundant repeat elements may have represented an obstacle for genetic analysis, this species is easily propagated by cutting, flowered by gibberellic acid, transformed by Agrobacterium, and edited by CRISPR/Cas9. These characteristics of C. japonica recommend it as a model conifer species for which reference genome sequences are necessary.
Results: Herein, we report the first chromosome-level assembly of C. japonica (2n = 22) using third-generation selfed progeny (estimated homozygosity rate = 0.96). Young leaf tissue was used to extract high molecular weight DNA (> 50 kb) for HiFi PacBio long-read sequencing and to construct an Hi-C/Omni-C library for Illumina short-read sequencing. The 29× and 26× genome coverage of HiFi and Illumina reads, respectively, for de novo assembly yielded 2,651 contigs (9.1 Gbp, N50 contig size 12.0 Mbp). Hi-C analysis mapped 97% of the nucleotides on 11 chromosomes. The assembly was verified through comparison with a consensus linkage map comprising 7,781 markers. BUSCO analysis identified ∼ 91% conserved genes.
Conclusions: Annotations of genes and comparisons of repeat elements with other Cupressaceae and Pinaceae species provide a fundamental resource for conifer research.
{"title":"A chromosome-level genome assembly of a model conifer plant, the Japanese cedar, Cryptomeria japonica D. Don.","authors":"Takeshi Fujino, Katsushi Yamaguchi, Toshiyuki T Yokoyama, Toshiya Hamanaka, Yoritaka Harazono, Hiroaki Kamada, Wataru Kobayashi, Tokuko Ujino-Ihara, Kentaro Uchiyama, Asako Matsumoto, Ayako Izuno, Yoshihiko Tsumura, Atsushi Toyoda, Shuji Shigenobu, Yoshinari Moriguchi, Saneyoshi Ueno, Masahiro Kasahara","doi":"10.1186/s12864-024-10929-4","DOIUrl":"10.1186/s12864-024-10929-4","url":null,"abstract":"<p><strong>Background: </strong>The Japanese cedar (Cryptomeria japonica D. Don) is one of the most important Japanese forest trees, occupying approximately 44% of artificial forests and planted in East Asia, the Azores Archipelago, and certain islands in the Indian Ocean. Although the huge genome of the species (ca. 9 Gbp) with abundant repeat elements may have represented an obstacle for genetic analysis, this species is easily propagated by cutting, flowered by gibberellic acid, transformed by Agrobacterium, and edited by CRISPR/Cas9. These characteristics of C. japonica recommend it as a model conifer species for which reference genome sequences are necessary.</p><p><strong>Results: </strong>Herein, we report the first chromosome-level assembly of C. japonica (2n = 22) using third-generation selfed progeny (estimated homozygosity rate = 0.96). Young leaf tissue was used to extract high molecular weight DNA (> 50 kb) for HiFi PacBio long-read sequencing and to construct an Hi-C/Omni-C library for Illumina short-read sequencing. The 29× and 26× genome coverage of HiFi and Illumina reads, respectively, for de novo assembly yielded 2,651 contigs (9.1 Gbp, N50 contig size 12.0 Mbp). Hi-C analysis mapped 97% of the nucleotides on 11 chromosomes. The assembly was verified through comparison with a consensus linkage map comprising 7,781 markers. BUSCO analysis identified ∼ 91% conserved genes.</p><p><strong>Conclusions: </strong>Annotations of genes and comparisons of repeat elements with other Cupressaceae and Pinaceae species provide a fundamental resource for conifer research.</p>","PeriodicalId":9030,"journal":{"name":"BMC Genomics","volume":"25 1","pages":"1039"},"PeriodicalIF":3.5,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11539532/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142581971","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}