Yi Jiang, Xiaochen Liu, Yan Shang, Jitao Li, Baoquan Gao, Yichao Ren, Xianliang Meng
{"title":"Physiological and Transcriptomic Analyses Provide Insights into Nitrite Stress Responses of the Swimming Crab Portunus trituberculatus","authors":"Yi Jiang, Xiaochen Liu, Yan Shang, Jitao Li, Baoquan Gao, Yichao Ren, Xianliang Meng","doi":"10.1007/s10126-024-10353-5","DOIUrl":"10.1007/s10126-024-10353-5","url":null,"abstract":"<div><p>Nitrite is a common environmental pollutant in intensive aquaculture systems. In this study, physiological and transcriptomic analyses were performed to investigate nitrite stress responses in the swimming crab <i>Portunus trituberculatus</i>, an important aquaculture species in China. The results revealed that nitrite can affect neurotransmitter signaling via the expression of neurotransmitter receptors such as <i>octopamine receptor</i> (<i>OAR</i>) and <i>5-hydroxytryptamine receptor</i> (<i>5-HTR</i>), and depress ecdysteroid signaling by downregulating <i>ecdysteroid receptor</i> (<i>EcR</i>) as well as its downstream transcription factors in hepatopancreas. In addition, nitrite suppressed the expression of <i>hemocyanins</i>, the oxygen-transporting protein, which at least partly contributed to tissue hypoxia, resulting in a switchover of energy metabolism from aerobic to anaerobic pathway. To meet the energy demand, glycogens and lipids were mobilized and transported to the hemolymph, and the catabolism of amino acids and fatty acids was enhanced to provide energy for hepatopancreas. β-oxidation of fatty acids, the major process by which fatty acids are oxidized to generate energy, seems to occur mainly not in mitochondria but in peroxisomes. Although the cellular protective mechanisms, including antioxidant defense, heat shock response (HSR), unfolded protein response (UPR), and autophagy, were activated, nitrite-induced cellular stress overwhelmed the repairing capacity and caused significant increase in the levels of apoptosis. These results indicated that nitrite stress influences neurotransmitter and endocrine signaling, disturbs energy metabolism, damages cellular components, and induces apoptosis in <i>P. trituberculatus</i>. The findings of this study provide new insights into nitrite stress response in the swimming crab and provide valuable information for aquaculture management of this species.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"1040 - 1052"},"PeriodicalIF":2.6,"publicationDate":"2024-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141900551","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Transcriptome Profiling of Gene Expression in Atlantic Salmon (Salmo salar) at Early Stage of Development","authors":"Najib Abdellaoui, Min Sun Kim","doi":"10.1007/s10126-024-10354-4","DOIUrl":"10.1007/s10126-024-10354-4","url":null,"abstract":"<div><p>For Atlantic salmon development, the most critical phase is the early development stage from egg to fry through alevin. However, the studies investigating the early development of Atlantic salmon based on RNA-seq are scarce and focus only on one stage of development. Therefore, using the RNA-seq technology, the assessment of different gene expressions of various early development stages (egg, alevin, and fry) was performed on a global scale. Over 22 GB of clean data was generated from 9 libraries with three replicates for each stage with over 90% mapping efficiency. A total of 5534 genes were differentially expressed, among which 19, 606, and 826 genes were specifically expressed in each stage, respectively. The transcriptome analysis showed that the number of differentially expressed genes (DEGs) increased as the Atlantic salmon progressed in development from egg to fry stage. In addition, gene ontology enrichment demonstrated that egg and alevin stages are characterized by upregulation of genes involved in spinal cord development, neuron projection morphogenesis, axonogenesis, and cytoplasmic translation. At the fry stage, upregulated genes were enriched in the muscle development process (muscle cell development, striated muscle cell differentiation, and muscle tissue development), immune system (defense response and canonical NF-kappaB signal transduction), as well as epidermis development. These results suggest that the early development of Atlantic salmon is characterized by a dynamic shift in gene expression and DEGs between different stages, which provided a solid foundation for the investigation of Atlantic salmon development.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"964 - 974"},"PeriodicalIF":2.6,"publicationDate":"2024-08-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141896431","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Ontogenetic, Sexual, and Monthly Niche Segregation of Sepia esculenta in the Northern East China Sea Revealed by Stable Carbon and Nitrogen Isotopes","authors":"Zhenfang Zhao, Guanyu Hu, Long Chen, Yingcong Chen, Fang Guo, Zhou Fang","doi":"10.1007/s10126-024-10352-6","DOIUrl":"10.1007/s10126-024-10352-6","url":null,"abstract":"<div><p>Golden cuttlefish play a significant role in the food web of the East and Yellow Seas and are a valuable fishery resource in Chinese coastal waters. Samples of golden cuttlefish were obtained from the northern East China Sea between September 2021 and March 2022, and stable isotope methods were utilized in this study to examine the variations in the forage ecology of golden cuttlefish. Our findings reveal dynamic shifts in carbon and nitrogen stable isotopes (δ<sup>13</sup>C and δ<sup>15</sup>N), highlighting intricate foraging strategies tailored to growth and environmental changes. A notable trend emerges: an initial growth-linked rise in δ<sup>13</sup>C and δ<sup>15</sup>N enrichment, followed by seasonal fluctuations mirroring seasonal food availability. The ontogenetic niche evolution displays striking habitat shifts and trophic level escalation in small mantle length stages, transitioning to niche overlap and subtle trophic shifts later on. Sex-specific differences emerge, with females occupying higher trophic levels than males in most samples. This comprehensive study underscores the complexity and adaptability of golden cuttlefish feeding ecology, inviting further inquiry into their intricate relationships within the marine ecosystem.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"1030 - 1039"},"PeriodicalIF":2.6,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141888166","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Metagenomic Insights Reveal Unrecognized Diversity of Entotheonella in Japanese Theonella Sponges","authors":"Sota Yamabe, Kazutoshi Yoshitake, Akihiro Ninomiya, Jörn Piel, Haruko Takeyama, Shigeki Matsunaga, Kentaro Takada","doi":"10.1007/s10126-024-10350-8","DOIUrl":"10.1007/s10126-024-10350-8","url":null,"abstract":"<div><p>Numerous biologically active natural products have been discovered from marine sponges, particularly from <i>Theonella swinhoei</i>, which is known to be a prolific source of natural products such as polyketides and peptides. Recent studies have revealed that many of these natural products are biosynthesized by <i>Candidatus</i> Entotheonella phylotypes, which are uncultivated symbionts within <i>T. swinhoei.</i> Consequently, Entotheonella is considered an untapped biochemical resource. In this study, we conducted metagenomic analyses to assess the diversity of Entotheonella in two <i>T. swinhoei</i> Y and two <i>T. swinhoei</i> W (Y and W referring to the yellow and white interior of the sponge, respectively), after separating filamentous bacteria using density gradient centrifugation. We obtained five Entotheonella metagenome-assembled genomes (MAGs) from filamentous bacteria-enriched fractions. Notably, one of these MAGs is significantly different from previously reported Entotheonella variants. Additionally, we identified closely related Entotheonella members present across different chemotypes of <i>T. swinhoei</i>. Thus, our metagenomic insights reveal that the diversity of Entotheonella within <i>Theonella</i> sponges is greater than previously recognized.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"1009 - 1016"},"PeriodicalIF":2.6,"publicationDate":"2024-08-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141892542","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Characterization of piRNAs in Diploid and Triploid Pacific Oyster Gonads: Exploring Their Potential Roles in Triploid Sterility","authors":"Yaru Zhou, Hong Yu, Qi Li, Lingfeng Kong, Shikai Liu, Chengxun Xu","doi":"10.1007/s10126-024-10351-7","DOIUrl":"10.1007/s10126-024-10351-7","url":null,"abstract":"<div><p>PIWI-interacting RNAs (piRNAs) are crucial for silencing transposable elements, germ cell development, and gametogenesis. Triploid Pacific oysters (<i>Crassostrea gigas</i>) are vital in the oyster aquaculture industry due to reduced fertility and rapid growth. This study integrates piRNA and mRNA expression analyses to elucidate their potential contributions to the sterility of triploid <i>C. gigas</i>. Bioinformatics analysis reveals a distinct U-bias at the 5′ terminal of oyster piRNAs. The abundance of piRNA clusters is reduced in triploid gonads compared to diploid gonads, particularly in sterile gonads, with a significant decrease in piRNA numbers. A specific piRNA cluster is annotated with the <i>PPP4R1</i> gene, which is downregulated in infertile female triploids and exhibits a negative correlation with three piRNAs within the cluster. Differential expression analysis identified 46 and 88 piRNAs in female and male comparison groups, respectively. In female sterile triploids, the expression of three target genes of differentially expressed piRNAs associated with cell division showed downregulation, suggesting the potential roles of piRNAs in the regulation of cell division-related genes, contributing to the gonad arrest observed in female triploid oysters. In male triploid oysters, piRNAs potentially interact with the target genes associated with spermatogenesis, including <i>TSSK4</i>, <i>SPAG17</i>, and <i>CCDC81</i>. This study provides a concise overview of piRNAs expression in oyster gonads, offering insights into the regulatory role of piRNAs in triploid sterility.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"1017 - 1029"},"PeriodicalIF":2.6,"publicationDate":"2024-07-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141787026","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Mo Aqib Raza Khan, Bo-Wei Wang, Hsiu-Chin Lin, Yu-Liang Yang, Chih-Chuang Liaw
{"title":"Structure-Functional Activity of Pyrone Derivatives for Inhibition of Barnacle Settlement and Biofilm Formation","authors":"Mo Aqib Raza Khan, Bo-Wei Wang, Hsiu-Chin Lin, Yu-Liang Yang, Chih-Chuang Liaw","doi":"10.1007/s10126-024-10349-1","DOIUrl":"10.1007/s10126-024-10349-1","url":null,"abstract":"<div><p>Naturally occurring 6-pentyl-2<i>H</i>-pyran-2-one and its synthetic analogues greatly inhibit the settlement of <i>Amphibalanus amphitrite</i> cyprids and the growth and biofilm formation of marine bacteria. To optimize the antifouling activities of pyrone derivatives, this study designed pyrone analogues by modifying functional groups, such as the benzyl group, cyclopentane, and halides, substituted on both sides of a pyrone. The antifouling effects of the synthesized pyrone derivatives were subsequently evaluated against five marine biofilm–forming bacteria, <i>Loktanella hongkongensis</i>, <i>Staphylococcus cohnii</i>, <i>S. saprophyticus</i>, <i>Photobacterium angustum</i>, and <i>Alteromonas macleodii</i>, along with barnacle cyprids of <i>Amphibalanus amphitrite</i>. Substituting nonpolar parts—such as the aliphatic, cyclopentyl, or phenyl moieties on C-5 or the furan moieties on C-3—not only increased antibacterial activity and inhibited biofilm formation but also inhibited barnacle cyprid settlement when compared to 6-pentyl-2<i>H</i>-pyran-2-one.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 5","pages":"1000 - 1008"},"PeriodicalIF":2.6,"publicationDate":"2024-07-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141772415","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Activin Signaling Pathway Specialization During Embryonic and Skeletal Muscle Development in Rainbow Trout (Oncorhynchus mykiss)","authors":"Jasmine Richman, Michael Phelps","doi":"10.1007/s10126-024-10345-5","DOIUrl":"10.1007/s10126-024-10345-5","url":null,"abstract":"<div><p>Activin signaling is essential for proper embryonic, skeletal muscle, and reproductive development. Duplication of the pathway in teleost fish has enabled diversification of gene function across the pathway but how gene duplication influences the function of activin signaling in non-mammalian species is poorly understood. Full characterization of activin receptor signaling pathway expression was performed across embryonic development and during early skeletal muscle growth in rainbow trout (RBT, <i>Oncorhynchus mykiss</i>). Rainbow trout are a model salmonid species that have undergone two additional rounds of whole genome duplication. A small number of genes were expressed early in development and most genes increased expression throughout development. There was limited expression of activin Ab in RBT embryos despite these genes exhibiting significantly elevated expression in post-hatch skeletal muscle. CRISPR editing of the activin Aa1 ohnolog and subsequent production of meiotic gynogenetic offspring revealed that biallelic disruption of activin Aa1 did not result in developmental defects, as occurs with knockout of activin A in mammals. The majority of gynogenetic offspring exhibited homozygous activin Aa1 genotypes (wild type, in-frame, or frameshift) derived from the mosaic founder female. The research identifies mechanisms of specialization among the duplicated activin ohnologs across embryonic development and during periods of high muscle growth in larval and juvenile fish. The knowledge gained provides insights into potential viable gene-targeting approaches for engineering the activin receptor signaling pathway and establishes the feasibility of employing meiotic gynogenesis as a tool for producing homozygous F1 genome-edited fish for species with long-generation times, such as salmonids.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 4","pages":"766 - 775"},"PeriodicalIF":2.6,"publicationDate":"2024-07-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141756478","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Exploring the Heat-Responsive miRNAs and their Target Gene Regulation in Ruditapes philippinarum Under Acute Heat Stress","authors":"Changsheng Gao, Hongtao Nie","doi":"10.1007/s10126-024-10348-2","DOIUrl":"10.1007/s10126-024-10348-2","url":null,"abstract":"<div><p>This study aimed to investigate the inherent molecular regulatory mechanisms of <i>Ruditapes philippinarum</i> in response to extremely high-temperature environments and to enhance the sustainable development of the <i>R. philippinarum</i> aquaculture industry. In this study, we established a differential expression profile of miRNA under acute heat stress and identified a total of 46 known miRNAs and 80 novel miRNAs, three of which were detected to be significantly differentially expressed. We analyzed the functions of target genes regulated by differentially expressed miRNAs (DEMs) of <i>R. philippinarum</i>. The findings of the KEGG enrichment analysis revealed that 29 enriched pathways in the group were subjected to acute heat stress. Notably, fatty acid metabolism, <i>FoxO</i> signaling pathway, <i>TGF-β</i> signaling pathway, and ubiquitin-mediated proteolysis were found to play significant roles in response to acute heat stress. We established a regulatory map of DEMs and their target genes in response to heat stress and constructed the miRNA-mRNA regulation network. This study provides valuable insights into the response of <i>R. philippinarum</i> to high temperature, helping to understand its underlying molecular regulatory mechanisms under high-temperature stress.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 4","pages":"810 - 826"},"PeriodicalIF":2.6,"publicationDate":"2024-07-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141750809","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Fei Wang, Zi-Rou Zhong, Qing Xie, Jie Ou, Ning-Xia Xiong, Ming-Zhu Huang, Shi-Yun Li, Gang Hu, Zi-Le Qin, Sheng-Wei Luo
{"title":"Multiomics Analyses Explore the Immunometabolic Interplay in the Liver of White Crucian Carp (Carassius cuvieri) After Aeromonas veronii Challenge","authors":"Fei Wang, Zi-Rou Zhong, Qing Xie, Jie Ou, Ning-Xia Xiong, Ming-Zhu Huang, Shi-Yun Li, Gang Hu, Zi-Le Qin, Sheng-Wei Luo","doi":"10.1007/s10126-024-10347-3","DOIUrl":"10.1007/s10126-024-10347-3","url":null,"abstract":"<div><p><i>Aeromonas veronii</i> is one of the predominant pathogenic species that can imperil the survival of farmed fish. However, the interactive networks of immune regulation and metabolic response in <i>A</i>. <i>veronii</i>–infected fish are still unclear. In this investigation, we aimed to explore immunometabolic interplay in white crucian carp (WCC) after the <i>A</i>. <i>veronii</i> challenge. Elevated levels of immune-related genes were observed in various tissues after <i>A</i>. <i>veronii</i> infection, along with the sharp alteration of disease-related enzymatic activities. Besides, decreased levels of antioxidant status were observed in the liver, but most metabolic gene expressions increased dramatically. Multiomics analyses revealed that metabolic products of amino acids, such as formiminoglutamic acid (FIGLU), L-glutamate (L-Glu), and 4-hydroxyhippuric acid, were considered the crucial liver biomarkers in<i> A</i>. <i>veronii</i>–infected WCC. In addition, <i>A</i>. <i>veronii</i> infection may dysregulate endoplasmic reticulum (ER) function to affect the metabolic process of lipids, carbohydrates, and amino acids in the liver of WCC. These results may have a comprehensive implication for understanding immunometabolic response in WCC upon <i>A</i>. <i>veronii</i> infection.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 4","pages":"790 - 809"},"PeriodicalIF":2.6,"publicationDate":"2024-07-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141747117","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
K. Shasti Risha, Kiran D. Rasal, Dhalongsaih Reang, Mir Asif Iquebal, Arvind Sonwane, Manoj Brahmane, Aparna Chaudhari, Naresh Nagpure
{"title":"DNA Methylation Profiling in Genetically Selected Clarias magur (Hamilton, 1822) Provides Insights into the Epigenetic Regulation of Growth and Development","authors":"K. Shasti Risha, Kiran D. Rasal, Dhalongsaih Reang, Mir Asif Iquebal, Arvind Sonwane, Manoj Brahmane, Aparna Chaudhari, Naresh Nagpure","doi":"10.1007/s10126-024-10346-4","DOIUrl":"10.1007/s10126-024-10346-4","url":null,"abstract":"<div><p>DNA methylation is an epigenetic alteration that impacts gene expression without changing the DNA sequence affecting an organism’s phenotype. This study utilized a reduced representation bisulfite sequencing (RRBS) approach to investigate the patterns of DNA methylation in genetically selected <i>Clarias magur</i> stocks. RRBS generated 249.22 million reads, with an average of 490,120 methylation sites detected in various parts of genes, including exons, introns, and intergenic regions. A total of 896 differentially methylated regions (DMRs) were identified; 356 and 540 were detected as hyper-methylated and hypo-methylated regions, respectively. The DMRs and their association with overlapping genes were explored using whole genome data of magur, which revealed 205 genes in exonic, 210 in intronic, and 480 in intergenic regions. The analysis identified the maximum number of genes enriched in biological processes such as RNA biosynthetic process, response to growth factors, nervous system development, neurogenesis, and anatomical structure morphogenesis. Differentially methylated genes (DMGs) such as <i>myrip</i>, <i>mylk3</i>, <i>mafb</i>, <i>egr3</i>, <i>ndnf</i>, <i>meis2a</i>, <i>foxn3</i>, <i>bmp1a</i>, <i>plxna3</i>, <i>fgf6</i>, <i>sipa1l1</i>, <i>mcu</i>, <i>cnot8</i>, <i>trim55b</i>, and <i>myof</i> were associated with growth and development. The selected DMGs were analyzed using real-time PCR, which showed altered mRNA expression levels. This work offers insights into the epigenetic mechanisms governing growth performance regulation in magur stocks. This work provides a valuable resource of epigenetic data that could be integrated into breeding programs to select high-performing individuals.</p></div>","PeriodicalId":690,"journal":{"name":"Marine Biotechnology","volume":"26 4","pages":"776 - 789"},"PeriodicalIF":2.6,"publicationDate":"2024-07-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141733158","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}