Biochemistry Biochemistry最新文献

{"title":"The Effect of Phosphoserine-Containing Membranes on Electrostatic Fields at the Protein-Protein Interface Measured through Vibrational Stark Effect Spectroscopy.","authors":"Jackson C Fink, Lauren J Webb","doi":"10.1021/acs.biochem.5c00028","DOIUrl":"10.1021/acs.biochem.5c00028","url":null,"abstract":"<p><p>In the cell, Ras GTPases function as membrane-bound molecular switches for a variety of cell signaling pathways. Ras isoforms have long been of interest because of the connection between amino acid mutations and tumorigenesis. Much research focused on Ras has used truncated, solubilized constructs, which exclude the membrane-binding domain and therefore ignore the effects of membrane binding on Ras function. Since the membrane is a highly charged surface, it could have a significant impact on the electrostatic environment at or near the protein-protein interface. Here, we use a thiocyanate probe chemically inserted into the Ras-binding domain of RalGDS to investigate the effect of membrane binding at the Ras active site. Changes in the electric field caused by the membrane were measured by the probe as vibrational energy shifts in the infrared (IR) spectrum. For a selection of mutants which caused large shifts at this interface on the soluble H-Ras construct, binding to a 30% phosphatidylserine (PS)/70% phosphatidylcholine (PC) nanodisc caused reduced shifts compared to the solubilized counterparts. Additionally, the vibrational probe bonded to the wildtype (WT) Ras construct demonstrated a shift of 0.7 cm^-1 as a PC nanodisc was doped from 0% to 30% PS, but mutations introduced to the Ras active site caused the probe to show no shift across these PS concentrations. These results indicate that the local membrane environment has an effect on the electrostatics at the Ras active site and needs to be considered when investigating the effect of oncogenic mutations on Ras function.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":" ","pages":"2280-2290"},"PeriodicalIF":2.9,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143952193","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":"Redox Homeostasis within the Drug-Resistant Malarial Parasite Digestive Vacuole.","authors":"Andreas Willems, Therese Oertel, Paul D Roepe","doi":"10.1021/acs.biochem.4c00750","DOIUrl":"10.1021/acs.biochem.4c00750","url":null,"abstract":"<p><p>We have developed a cost-effective strategy for the complete synthesis of azetidinyl coumarin fluorophore derivatives that report changes in physiologic levels of glutathione (GSH), which includes a more cost- effective synthesis of the probe precursor hydroxyl derivative and its subsequent derivatization to promote subcellular localization. We functionalize coumarin derivatives with a cyano side chain similar to a previous strategy (Jiang X. et al., <i>Nature Communications</i> <b>2017,</b> 8; 16087) and validate the 7-azetidinyl conformation as an explanation for enhanced GSH-dependent coumarin fluorescence. We couple the azetidinyl probe to different mass dextrans using either no linker or a 6C linker and also synthesize a morpholino derivative. We titrate the fluorescence of the different functionalized probes vs [GSH] <i>in vitro</i>. We load one dextran-conjugated probe within the digestive vacuole (DV) of live intraerythrocytic <i>P. falciparum</i> malarial parasites and also measure cytosolic localization of the morpholino probe. Using significantly improved single-cell photometry (SCP) methods, we show that the morpholino probe faithfully reports [GSH] from the live parasite cytosol, while the 70 kDa dextran-conjugated probe reports DV redox homeostasis for control chloroquine-sensitive (CQS) and artemisinin-sensitive (ARTS) transfectant parasites vs their genetically matched chloroquine-resistant (CQR)/artemisinin-sensitive (CQR/ARTS) and CQR artemisinin-resistant (CQR/ARTR) strains, respectively. We quantify rapid changes in DV redox homeostasis for these parasites ± drug pulses under live-cell perfusion conditions. The results are important for understanding the pharmacology of antimalarial drugs and the molecular mechanisms underlying CQR and ARTR phenomena.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":" ","pages":"2247-2261"},"PeriodicalIF":2.9,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12096432/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143953400","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Identification and Functional Characterization of the Polymerizing Glycosyltransferase Required for the Transfer of d-Ribose to the d-Gal<i>f</i>NAc Moiety of the Capsular Polysaccharide of <i>Campylobacter jejuni</i>.","authors":"Dao Feng Xiang, Tamari Narindoshvili, Frank M Raushel","doi":"10.1021/acs.biochem.5c00052","DOIUrl":"10.1021/acs.biochem.5c00052","url":null,"abstract":"<p><p><i>Campylobacter jejuni</i> is the leading cause of food poisoning in the United States. The exterior surface of this bacterium is coated with a capsular polysaccharide (CPS) that helps protect the organism from the host immune system. In the HS:2 serotype of strain <i>C. jejuni</i> NCTC 11168, the minimal repeating trisaccharide consist of d-ribose, <i>N</i>-acetyl-d-galactosamine (GalNAc) and the serinol amide of d-glucuronic acid. Here we demonstrate that the C-terminal domain of Cj1432 (residues 574-914) is responsible for the transfer of d-ribose-5-P from phosphoribosyl pyrophosphate (PRPP) to C5 of the d-Gal<i>f</i>NAc moiety of the growing polysaccharide chain. In the next step the middle domain of Cj1432 (residues 357-573) catalyzes the hydrolysis of phosphate from this product. The N-terminal domain of Cj1432 (residues 1-356) catalyzes the transfer of d-GlcA from UDP-d-GlcA to C2 of the d-ribose moiety and thus Cj1432 catalyzes three consecutive reactions during the biosynthesis of the capsular polysaccharide of <i>C. jejuni</i>. We have previously shown that the remaining three reactions required for the polymerization of the CPS are catalyzed by the bifunctional enzyme Cj1438 and Cj1435. We have now demonstrated that the minimal repeating trisaccharide of the CPS of <i>C. jejuni</i> NCTC 11168 requires six enzyme-catalyzed reactions with six intermediate structures. This accomplishment will now enable the large-scale cell-free enzyme-catalyzed synthesis of well-defined oligomers of the CPS that can potentially be used in the production of glycoconjugate vaccines for the prevention of infections by <i>C. jejuni</i>.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":" ","pages":"2226-2236"},"PeriodicalIF":2.9,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12096443/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143955680","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"An Alkaliphilic Chitinase Unveils Environment-Dependent Variation in the Canonical Catalytic Machinery of Family-18 Glycoside Hydrolases.","authors":"Jogi Madhuprakash, Bjørn Dalhus, Bastien Bissaro, Lal Duhsaki, Gustav Vaaje-Kolstad, Morten Sørlie, Åsmund K Røhr, Vincent G H Eijsink","doi":"10.1021/acs.biochem.5c00082","DOIUrl":"10.1021/acs.biochem.5c00082","url":null,"abstract":"<p><p>Chitinases belonging to glycoside hydrolase family-18 (GH18) employ substrate-assisted catalysis and typically have neutral/acidic pH-optima. We describe the structural and functional analysis of <i>Ca</i>ChiA, a chitinase from the anaerobic alkaliphilic bacterium <i>Chitinivibrio alkaliphilus</i> with an alkaline pH optimum (8.8) and unique active site features, including a noncanonical catalytic H<i>xx</i>E<i>x</i>D<i>x</i>E motif, which is D<i>xx</i>D<i>x</i>D<i>x</i>E in other chitinases. Propka calculations indicated a significantly higher p<i>K</i>_a for the catalytic acid/base, Glu148, in <i>Ca</i>GH18, compared to other GH18 enzymes, aligning with its alkaline pH optimum. Both Propka calculations and functional studies of enzyme variants with mutations in the catalytic center suggested that not the change in the catalytic motif, but rather a unique glutamine, Gln57, modulating the properties of this motif, enables activity at alkaline pH. Further characterization of <i>Ca</i>ChiA unveiled additional peculiar enzyme properties, such as a unique ability to convert chitin to chitotriose. Thus, <i>Ca</i>ChiA adds novel catalytic capabilities to the widespread family of GH18 chitinases, made possible by adaptation of an intricate catalytic center.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":" ","pages":"2291-2305"},"PeriodicalIF":2.9,"publicationDate":"2025-05-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143954047","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":"Emergent and Convergent Features in the Laboratory Evolution of Polymerase Ribozymes","authors":"David P. Horning*,&nbsp;","doi":"10.1021/acs.biochem.5c0016010.1021/acs.biochem.5c00160","DOIUrl":"https://doi.org/10.1021/acs.biochem.5c00160https://doi.org/10.1021/acs.biochem.5c00160","url":null,"abstract":"<p >In modern biology, molecular heredity is established by polymerase proteins that copy genetic information encoded in the sequence of nucleic acids. Prior to the emergence of coded protein synthesis, this role may have been filled by RNA polymerase ribozymes. Although such enzymes can no longer be found in extant life, ribozymes first evolved from random sequence populations have been progressively engineered in the laboratory to function as general RNA-dependent RNA polymerases. Polymerase ribozymes discovered in the past ten years can catalyze hundreds of sequential RNA synthesis reactions, match the complexity and catalytic sophistication of biological RNA enzymes, and employ many of the same strategies used by polymerase proteins to copy nucleic acids. This review describes the approaches to directed <i>in vitro</i> evolution that have led to the discovery of RNA enzymes that copy RNA molecules processively and accurately, and surveys how laboratory evolution has shaped biochemical and structural adaptations in these enzymes. The review then considers the challenges and opportunities that remain in the effort to propagate and evolve RNA genes with RNA catalysts alone.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2364–2375 2364–2375"},"PeriodicalIF":2.9,"publicationDate":"2025-05-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194231","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":"Predicting Protein Function in the AI and Big Data Era","authors":"Riccardo Percudani*,&nbsp; and ,&nbsp;Carlo De Rito,&nbsp;","doi":"10.1021/acs.biochem.5c0018610.1021/acs.biochem.5c00186","DOIUrl":"https://doi.org/10.1021/acs.biochem.5c00186https://doi.org/10.1021/acs.biochem.5c00186","url":null,"abstract":"<p >It is an exciting time for researchers working to link proteins to their functions. Most techniques for extracting functional information from genomic sequences were developed several years ago, with major progress driven by the availability of big data. Now, groundbreaking advances in deep-learning and AI-based methods have enriched protein databases with three-dimensional information and offer the potential to predict biochemical properties and biomolecular interactions, providing key functional insights. This progress is expected to increase the proportion of functionally bright proteins in databases and deepen our understanding of life at the molecular level.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2345–2352 2345–2352"},"PeriodicalIF":2.9,"publicationDate":"2025-05-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://pubs.acs.org/doi/epdf/10.1021/acs.biochem.5c00186","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194396","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Mu Opioid Receptor Positive Allosteric Modulator BMS-986122 Confers Agonist-Dependent G Protein Subtype Signaling Bias","authors":"Grant M. Grieble,&nbsp;Brian I. Knapp and Jean M. Bidlack*,&nbsp;","doi":"10.1021/acs.biochem.5c0002210.1021/acs.biochem.5c00022","DOIUrl":"https://doi.org/10.1021/acs.biochem.5c00022https://doi.org/10.1021/acs.biochem.5c00022","url":null,"abstract":"<p >The mu opioid receptor (MOR) is a G protein-coupled receptor (GPCR) and is responsible for the effects of all medically used opioids. Most opioids activate all inhibitory Gαi/o/z proteins through MOR, initiating signaling events that culminate in a variety of physiological effects such as analgesia, euphoria, and respiratory depression. Gaining a better understanding of how the chemical structure of opioids influences the functional activation profiles of G protein subtypes by MOR is critical for disentangling the multitude of opioid effects and the development of safer analgesics. A recent development in opioid pharmacology has been the discovery of positive allosteric modulators (PAMs) for opioid receptors, such as BMS-986122, which act at the MOR to increase the potency of full agonists and the efficacy of partial agonists. Here, we utilized a nanoBRET-based functional assay system in live HEK 293T cells to study how the pharmacological properties of opioids were uniquely affected by BMS-986122 when the MOR signaled through specific inhibitory Gα subunits. We report that BMS-986122 differentially enhanced opioid activity when the MOR signaled through different Gα subunits with the greatest difference observed with partial agonists. Additionally, the binding affinity of BMS-986122 to the MOR was significantly altered by the co-binding Gα subunit. Site-directed mutagenesis experiments revealed key amino acid residue differences on Gαi/o subunits involved in the differential effects observed. This study sheds light on the molecular features of biased signaling for both opioid ligands and G proteins, which may prove useful for the further development of biased agonists or allosteric modulators at the MOR.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2376–2393 2376–2393"},"PeriodicalIF":2.9,"publicationDate":"2025-05-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://pubs.acs.org/doi/epdf/10.1021/acs.biochem.5c00022","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194279","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Expanding the Riboglow-FLIM Toolbox with Different Fluorescence Lifetime-Producing RNA Tags","authors":"Zachary Stickelman,&nbsp;Nadia Sarfraz,&nbsp;Morgan K. Rice,&nbsp;Ben J. Lambeck,&nbsp;Sonja Milkovich and Esther Braselmann*,&nbsp;","doi":"10.1021/acs.biochem.4c0056710.1021/acs.biochem.4c00567","DOIUrl":"https://doi.org/10.1021/acs.biochem.4c00567https://doi.org/10.1021/acs.biochem.4c00567","url":null,"abstract":"<p >RNAs are essential elements of biology with subcellular localizations critical for function. Genetically tagging fluorescent RNA reporters to an RNA of interest allows for investigating RNA spatiotemporal dynamics. We previously developed a fluorescence lifetime imaging microscopy (FLIM)-based RNA-tagging platform, Riboglow-FLIM. Here, a genetically encoded RNA tag binds a fluorescent probe, causing an increase in both fluorescence intensity and fluorescence lifetime. Importantly, the Riboglow platform is derived from a bacterial riboswitch RNA family and different riboswitch sequences from nature may build the basis for multiplexing capabilities. We previously observed fluorescence lifetime differences for two RNA tags <i>in vitro</i> and in live mammalian cells as a proof-of-concept demonstration. As an in-depth expansion for multiplexing capabilities, here we evaluate the performance of different RNA sequences <i>in vitro</i> for systematically expanding the RNA tag sequence space of Riboglow-FLIM. We use two methods of varying the genetic tag to evaluate multiplexing capabilities, a literature-guided and a rational design approach. The literature-guided approach includes riboswitch sequences with both indirect and direct evidence of probe binding. For this, a phylogenetic tree of riboswitch-derived tags from indirect binding results was constructed, and RNA members from different branches were characterized. We also designed RNA mutations rationally based on insights from established Riboglow RNA tags. Together, nine different RNA tags yielded a wide range of fluorescence lifetimes for the Riboglow-FLIM platform, building the foundation to tag and track several different RNAs simultaneously. These findings will serve as the basis for achieving multiplexed RNA imaging in live cells using a fluorescence lifetime sensor.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2429–2438 2429–2438"},"PeriodicalIF":2.9,"publicationDate":"2025-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://pubs.acs.org/doi/epdf/10.1021/acs.biochem.4c00567","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194149","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Not Once, not Twice, but Thrice: Structure and Catalytic Mechanisms of the Dihydroorotate Dehydrogenases","authors":"Corine O. Smith,&nbsp; and ,&nbsp;Graham R. Moran*,&nbsp;","doi":"10.1021/acs.biochem.5c0017010.1021/acs.biochem.5c00170","DOIUrl":"https://doi.org/10.1021/acs.biochem.5c00170https://doi.org/10.1021/acs.biochem.5c00170","url":null,"abstract":"<p >Dihydroorotate dehydrogenases (DHODs) are common to all life and catalyze the oxidation of dihydroorotate (DHO) to orotate the precursor of all pyrimidine nucleotides. The core structure of all DHODs has a TIM-barrel topology (the PyrD subunit or domain) that harbors an FMN cofactor that interacts with DHO. There are two classes of DHOD enzymes. Each has unique structures and oxidant substrates that conserve part of the energy available by coupling the reaction to ATP synthesis. The class 1 enzymes are soluble and divided into classes 1A and 1B. Class 1A has fumarate as the electron acceptor forming succinate and is the simplest form of DHOD, successively binding DHO and fumarate at the same active site locale. Class 1B uses NAD⁺ as the oxidant and this form of DHOD is heterodimeric having, in addition to the PyrD subunit, a subunit (PyrK) whose structure is like those of ferredoxin reductases. PyrK adds a second active site with a bound FAD that interacts with the NAD⁺ substrate and includes an Fe₂S₂ center that resides at the interface of the subunits, forming a conduit for electrons. Class 2 DHODs have ubiquinone (UQ) as the electron acceptor. This form of DHOD is membrane associated via an N-terminal domain that also forms a quinone binding site end-on to the FMN xylene moiety. This arrangement uses the flavin to mediate between the substrates and as a redox partition between water-soluble NAD⁺ and lipid soluble UQ₁₀. In this review, we summarize the structure and mechanism of DHOD enzymes.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2353–2363 2353–2363"},"PeriodicalIF":2.9,"publicationDate":"2025-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194154","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":"Abundance of Glycine-mediated O···C=O, N–H···N, and Cα–H···O Interactions in Homo- and Hetero-oligomeric Protein Complexes","authors":"Surbhi Vilas Tajane,&nbsp;Sanjeevani Pohane,&nbsp;Pinak Chakrabarti and Sucharita Dey*,&nbsp;","doi":"10.1021/acs.biochem.4c0062010.1021/acs.biochem.4c00620","DOIUrl":"https://doi.org/10.1021/acs.biochem.4c00620https://doi.org/10.1021/acs.biochem.4c00620","url":null,"abstract":"<p >Glycines are considered the most flexible among all residues, can fit anywhere, and are typically found in short loops and turns. Their specific roles in protein folding and binding have been largely overlooked. Here, we investigate the presence of key noncovalent interactions, O···C=O and N–H···N, that are mediated by Gly between two peptide groups at the interface of oligomeric proteins. These are put in context relative to another weak interaction, viz., C^α–H···O. Also, these include interactions where both of the interacting residues are Gly or where either of them is a Gly. We found an enrichment of all of the Gly···Gly-mediated interactions at the interfaces, irrespective of the nature of the complex, whether obligate, transient, or a heterodimer. Comparatively, a higher propensity of Gly<b>···</b>Gly O···C=O interactions is found at the obligate homodimer interfaces. We also noted that 10% of the Gly residues at the obligate homodimer interfaces are involved in the O···C=O interactions, 1% is involved in the N–H···N, and 22% are involved in C^α–H···O interactions. Interestingly, in the weakly associated transient dimers too, 40% of the total interface Gly residues are involved in any of the three interactions. We noted a secondary structure preference for the Gly···Gly-mediated O···C=O interactions in obligate dimers, which are predominantly from helical segments. These nonclassical interactions may contribute to the function of Gly-rich regions in proteins.</p>","PeriodicalId":28,"journal":{"name":"Biochemistry Biochemistry","volume":"64 11","pages":"2394–2400 2394–2400"},"PeriodicalIF":2.9,"publicationDate":"2025-05-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144194211","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}