{"title":"ATBS1-INTERACTING FACTOR 2 Positively Regulates Freezing Tolerance via INDUCER OF CBF EXPRESSION 1/C-REPEAT BINDING FACTOR-Induced Cold Acclimation Pathway.","authors":"Yoon Kim, Sun-Ho Kim, Jun Lim, Soo-Hwan Kim","doi":"10.1093/pcp/pcae072","DOIUrl":"10.1093/pcp/pcae072","url":null,"abstract":"<p><p>The INDUCER OF CBF EXPRESSION 1/C-REPEAT BINDING FACTOR (ICE1/CBF) pathway plays a crucial role in plant responses to cold stress, impacting growth and development. Here, we demonstrated that ATBS1-INTERACTING FACTOR 2 (AIF2), a non-DNA-binding basic helix-loop-helix transcription factor, positively regulates freezing tolerance through the ICE1/CBF-induced cold tolerance pathway in Arabidopsis. Cold stress transcriptionally upregulated AIF2 expression and induced AIF2 phosphorylation, thereby stabilizing the AIF2 protein during early stages of cold acclimation. The AIF2 loss-of-function mutant, aif2-1, exhibited heightened sensitivity to freezing before and after cold acclimation. In contrast, ectopic expression of AIF2, but not the C-terminal-deleted AIF2 variant, restored freezing tolerance. AIF2 enhanced ICE1 stability during cold acclimation and promoted the transcriptional expression of CBFs and downstream cold-responsive genes, ultimately enhancing plant tolerance to freezing stress. MITOGEN-ACTIVATED PROTEIN KINASES 3 and 6 (MPK3/6), known negative regulators of freezing tolerance, interacted with and phosphorylated AIF2, subjecting it to protein degradation. Furthermore, transient co-expression of MPK3/6 with AIF2 and ICE1 downregulated AIF2/ICE1-induced transactivation of CBF2 expression. AIF2 interacted preferentially with BRASSINOSTEROID-INSENSITIVE 2 (BIN2) and MPK3/6 during the early and later stages of cold acclimation, respectively, thereby differentially regulating AIF2 activity in a cold acclimation time-dependent manner. Moreover, AIF2 acted additively in a gain-of-function mutant of BRASSINAZOLE-RESISTANT 1 (BZR1; bzr1-1D) and a triple knockout mutant of BIN2 and its homologs (bin2bil1bil2) to induce CBFs-mediated freezing tolerance. This suggests that cold-induced AIF2 coordinates freezing tolerance along with BZR1 and BIN2, key positive and negative components, respectively, of brassinosteroid signaling pathways.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1363-1376"},"PeriodicalIF":3.9,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141493142","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"PCIS1, Encoded by a Pentatricopeptide Protein Co-expressed Gene, Is Required for Splicing of Three Mitochondrial nad Transcripts in Angiosperms.","authors":"Brody Frink, Matthias Burger, Maya Yarkoni, Sofia Shevtsov-Tal, Hagit Zer, Shohei Yamaoka, Oren Ostersetzer-Biran, Mizuki Takenaka","doi":"10.1093/pcp/pcae086","DOIUrl":"10.1093/pcp/pcae086","url":null,"abstract":"<p><p>Group II introns are large catalytic RNAs, which reside mainly within genes encoding respiratory complex I (CI) subunits in angiosperms' mitochondria. Genetic and biochemical analyses led to the identification of many nuclear-encoded factors that facilitate the splicing of the degenerated organellar introns in plants. Here, we describe the analysis of the pentatricopeptide repeat (PPR) co-expressed intron splicing-1 (PCIS1) factor, which was identified in silico by its co-expression pattern with many PPR proteins. PCIS1 is well conserved in land plants but has no sequence similarity with any known protein motifs. PCIS1 mutant lines are arrested in embryogenesis and can be maintained by the temporal expression of the gene under the embryo-specific ABI3 promoter. The pABI3::PCIS1 mutant plants display low germination and stunted growth phenotypes. RNA-sequencing and quantitative RT-PCR analyses of wild-type and mutant plants indicated that PCIS1 is a novel splicing cofactor that is pivotal for the maturation of several nad transcripts in Arabidopsis mitochondria. These phenotypes are tightly associated with respiratory CI defects and altered plant growth. Our data further emphasize the key roles of nuclear-encoded cofactors that regulate the maturation and expression of mitochondrial transcripts for the biogenesis of the oxidative phosphorylation system, and hence for plant physiology. The discovery of novel splicing factors other than typical RNA-binding proteins suggests further complexity of splicing mechanisms in plant mitochondria.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1474-1485"},"PeriodicalIF":3.9,"publicationDate":"2024-10-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141875770","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Rapid Genetic Isolation Among Four Lineages Of Silene nutans.","authors":"Zoé Postel, Hélène Martin, Camille Roux, Cécile Godé, Mathieu Genete, Éric Schmitt, François Monnet, Xavier Vekemans, Pascal Touzet","doi":"10.1093/pcp/pcae110","DOIUrl":"https://doi.org/10.1093/pcp/pcae110","url":null,"abstract":"<p><p>Speciation is the process leading to the emergence of new species. While being usually progressive, it can sometimes be fast with rapid emergence of reproductive barriers leading to high level of reproductive isolation. Some reproductive barriers might leave signatures in the genome, through elevated level of genetic differentiation at specific loci. Similar signatures might also be the results of linked selection acting in low recombination regions. Nottingham catchfly (Silene nutans) is a Caryophyllaceae species composed of four genetically differentiated lineages for which strong and asymmetric levels of reproductive isolation have been identified. Using population transcriptomic data from several individuals of the four lineages, we inferred the best evo-demographic scenario leading to the current reproductive isolation of these four lineages. We also tested whether loci exhibiting high level of genetic differentiation represented barrier loci or were located in low recombination regions, evolving under strong influence of linked selection. Overall, the four lineages of S. nutans have diverged in strict isolation, likely during the different glacial period, through migration in distinct glacial refugia. Speciation between these four lineages appeared to be particularly fast, likely due to fast evolving plastid genome accelerating plastid-nuclear co-evolution and the probability of plastid-nuclear incompatibilities in inter-lineage hybrids.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142352647","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Engineering of Phycourobilin Synthase: PubS to a Two-Electron Reductase.","authors":"Keita Miyake, Saya Iwata, Rei Narikawa","doi":"10.1093/pcp/pcae098","DOIUrl":"https://doi.org/10.1093/pcp/pcae098","url":null,"abstract":"<p><p>Phycourobilin:ferredoxin oxidoreductase (PubS) belongs to the ferredoxin-dependent bilin reductase (FDBR) family and catalyzes the reduction of the C15=C16 double bond, followed by the C4=C5 double bond of biliverdin IXα to produce phycourobilin. Among the diverse FDBR enzymes that catalyze site-specific reduction reactions of bilins, PubS lineage is the only one that reduces the C4=C5 double bond. This family can be broadly divided into four-electron reduction enzymes, which catalyze two successive two-electron reductions, such as PubS, and two-electron reduction enzymes, which catalyze a single two-electron reduction. The crystal structures of diverse FDBRs, excluding PubS, have unraveled that there are two distinct binding modes in the substrate-binding pocket. In this study, we focused on the arginine (Arg) residues that is considered crucial for substrate-binding mode in two-electron reduction enzymes. Through sequence alignment and comparison with the predicted structure of PubS, we identified a residue in PubS that corresponds to the Arg residue in the two-electron reduction enzymes. We further introduced mutations to avoid the steric hindrance associated with changes in the binding mode. Biochemical characterization of these variants showed that we successfully modified PubS from a four-electron reduction enzyme to a two-electron reduction enzyme with the accumulation of radicals. Our results provide insight into the molecular mechanisms of the chromophore binding mode and proton donation from acidic residues.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142352645","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sze Wai Tse, Davide Annese, Facundo Romani, Fernando Guzman-Chavez, Ignacy Bonter, Edith Forestier, Eftychios Frangedakis, Jim Haseloff
{"title":"Optimizing Promoters and Subcellular Localization for Constitutive Transgene Expression in Marchantia polymorpha.","authors":"Sze Wai Tse, Davide Annese, Facundo Romani, Fernando Guzman-Chavez, Ignacy Bonter, Edith Forestier, Eftychios Frangedakis, Jim Haseloff","doi":"10.1093/pcp/pcae063","DOIUrl":"10.1093/pcp/pcae063","url":null,"abstract":"<p><p>Marchantia polymorpha has become an important model system for comparative studies and synthetic biology. The systematic characterization of genetic elements would make heterologous gene expression more predictable in this test bed for gene circuit assembly and bioproduction. Yet, the toolbox of genetic parts for Marchantia includes only a few constitutive promoters that need benchmarking to assess their utility. We compared the expression patterns of previously characterized and new constitutive promoters. We found that driving expression with the double enhancer version of the cauliflower mosaic virus 35S promoter (pro35S × 2) provided the highest yield of proteins, although it also inhibits the growth of transformants. In contrast, promoters derived from the Marchantia genes for ETHYLENE RESPONSE FACTOR 1 and the CLASS II HOMEODOMAIN-LEUCINE ZIPPER protein drove expression to higher levels across all tissues without a growth penalty and can provide intermediate levels of gene expression. In addition, we showed that the cytosol is the best subcellular compartment to target heterologous proteins for higher levels of expression without a significant growth burden. To demonstrate the potential of these promoters in Marchantia, we expressed RUBY, a polycistronic betalain synthesis cassette linked by P2A sequences, to demonstrate coordinated expression of metabolic enzymes. A heat-shock-inducible promoter was used to further mitigate growth burdens associated with high amounts of betalain accumulation. We have expanded the existing tool kit for gene expression in Marchantia and provided new resources for the Marchantia research community.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1298-1309"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369823/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141186683","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}
{"title":"Chromosome-Scale Genome Assembly and Characterization of Top-Quality Japanese Green Tea Cultivar 'Seimei'.","authors":"Yoshihiro Kawahara, Junichi Tanaka, Kazuhiro Takayama, Toshiyuki Wako, Akiko Ogino, Shuya Yamashita, Fumiya Taniguchi","doi":"10.1093/pcp/pcae060","DOIUrl":"10.1093/pcp/pcae060","url":null,"abstract":"<p><p>Japanese green tea, an essential beverage in Japanese culture, is characterized by the initial steaming of freshly harvested leaves during production. This process efficiently inactivates endogenous enzymes such as polyphenol oxidases, resulting in the production of sencha, gyokuro and matcha that preserves the vibrant green color of young leaves. Although genome sequences of several tea cultivars and germplasms have been published, no reference genome sequences are available for Japanese green tea cultivars. Here, we constructed a reference genome sequence of the cultivar 'Seimei', which is used to produce high-quality Japanese green tea. Using the PacBio HiFi and Hi-C technologies for chromosome-scale genome assembly, we obtained 15 chromosome sequences with a total genome size of 3.1 Gb and an N50 of 214.9 Mb. By analyzing the genomic diversity of 23 Japanese tea cultivars and lines, including the leading green tea cultivars 'Yabukita' and 'Saemidori', it was revealed that several candidate genes could be related to the characteristics of Japanese green tea. The reference genome of 'Seimei' and information on genomic diversity of Japanese green tea cultivars should provide crucial information for effective breeding of such cultivars in the future.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1271-1284"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369818/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141162311","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}
{"title":"Characterization of the Arabidopsis Mutant oligocellula6-D Reveals the Importance of Leaf Initiation in Determining the Final Leaf Size.","authors":"Risa Takeda, Shoki Sato, Takumi Ui, Hirokazu Tsukaya, Gorou Horiguchi","doi":"10.1093/pcp/pcae067","DOIUrl":"10.1093/pcp/pcae067","url":null,"abstract":"<p><p>The leaf is a determinate organ with a final size under genetic control. Numerous factors that regulate the final leaf size have been identified in Arabidopsis thaliana; although most of these factors play their roles during the growth of leaf primordia, much less is known about leaf initiation and its effects on the final leaf size. In this study, we characterized oligocellula6-D (oli6-D), a semidominant mutant of A. thaliana with smaller leaves than the wild type (WT) due to its reduced leaf cell numbers. A time-course analysis showed that oli6-D had approximately 50% fewer leaf cells even immediately after leaf initiation; this difference was maintained throughout leaf development. Next-generation sequencing showed that oli6-D had chromosomal duplications involving 2-kb and 3-Mb regions of chromosomes 2 and 4, respectively. Several duplicated genes examined had approximately 2-fold higher expression levels, and at least one gene acquired a new intron/exon structure due to a chromosome fusion event. oli6-D showed reduced auxin responses in leaf primordia, primary roots and embryos, as well as reduced apical dominance and partial auxin-resistant root growth. CRISPR-associated protein-9-mediated genome editing enabled the removal of a 3-Mb duplicated segment, the largest targeted deletion in plants thus far. As a result, oli6-D restored the WT leaf phenotypes, demonstrating that oli6-D is a gain-of-function mutant. Our results suggest a new regulatory point of leaf size determination that functions at a very early stage of leaf development and is negatively regulated by one or more genes located in the duplicated chromosomal segments.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1310-1327"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141327792","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Secret Weapon of Insects: The Oral Secretion Cocktail and Its Modulation of Host Immunity.","authors":"Vinod Kumar Prajapati, Vishakh Vijayan, Jyothilakshmi Vadassery","doi":"10.1093/pcp/pcae059","DOIUrl":"10.1093/pcp/pcae059","url":null,"abstract":"<p><p>Plants and insects have co-existed for almost 400 million years and their interactions can be beneficial or harmful, thus reflecting their intricate co-evolutionary dynamics. Many herbivorous arthropods cause tremendous crop loss, impacting the agro-economy worldwide. Plants possess an arsenal of chemical defenses that comprise diverse secondary metabolites that help protect against harmful herbivorous arthropods. In response, the strategies that herbivores use to cope with plant defenses can be behavioral, or molecular and/or biochemical of which salivary secretions are a key determinant. Insect salivary secretions/oral secretions (OSs) play a crucial role in plant immunity as they contain several biologically active elicitors and effector proteins that modulate plants' defense responses. Using this oral secretion cocktail, insects overcome plant natural defenses to allow successful feeding. However, a lack of knowledge of the nature of the signals present in oral secretion cocktails has resulted in reduced mechanistic knowledge of their cellular perception. In this review, we discuss the latest knowledge on herbivore oral secretion derived elicitors and effectors and various mechanisms involved in plant defense modulation. Identification of novel herbivore-released molecules and their plant targets should pave the way for understanding the intricate strategies employed by both herbivorous arthropods and plants in their interactions.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1213-1223"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141327794","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Micromorphological and Chemical Characterization of Drimys winteri Leaf Surfaces: The Secondary Alcohols Forming Epicuticular Wax Crystals Are Accompanied by Alkanediol, Alkanetriol and Ketol Derivatives.","authors":"Zhonghang Zhang, Dwiti Mistry, Reinhard Jetter","doi":"10.1093/pcp/pcae053","DOIUrl":"10.1093/pcp/pcae053","url":null,"abstract":"<p><p>The cuticle is a hydrophobic coating of most aerial plant surfaces crucial for limiting non-stomatal water loss. Plant cuticles consist of the lipid polyester cutin and associated waxes with compositions varying widely between plant species and organs. Here, we aimed to provide a comparative analysis of the dark-glossy adaxial and pale-glaucous abaxial sides of Drimys winteri (Winteraceae) leaves. Scanning electron microscopy showed nanotubular wax crystals lining the entire abaxial side of the leaf (including stomatal pores), while the adaxial side had patches of mixed platelet/tubule crystals and smooth areas between them. Consecutive treatments for wax removal and cutin depolymerization revealed that the waxes were deposited on a cutin network with micron-scale cavities across the entire abaxial surface including the stomata pores, and on a microscopically smooth cutin surface on the adaxial side of the leaf. Gas chromatography coupled to mass spectrometry and flame ionization detection showed that the wax mixtures on both sides of the leaf were complex mixtures of very-long-chain compounds dominated by the secondary alcohol nonacosan-10-ol and alkanediols with one hydroxyl on C-10. It is therefore very likely that the characteristic tubular wax crystals of both leaf sides are formed by these alcohols and diols. Further secondary alcohols and alkanediols, as well as ketols and alkanetriols with one functional group on C-10, were identified based on mass spectral fragmentation patterns. The similarities between all these mid-chain-functionalized compounds suggest that they are derived from nonacosan-10-ol via regio-specific hydroxylation reactions, likely catalyzed by three P450-dependent monooxygenases with different regio-specificities.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1245-1260"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11369817/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140959099","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}
{"title":"The PLETHORA Homolog in Marchantia polymorpha is Essential for Meristem Maintenance, Developmental Progression, and Redox Homeostasis.","authors":"Jing Fu, Congye Zhou, Fei Ma, Jing Zhao, Fei Yu, Hongchang Cui","doi":"10.1093/pcp/pcae055","DOIUrl":"10.1093/pcp/pcae055","url":null,"abstract":"<p><p>To adapt to a terrestrial habitat, the ancestors of land plants must have made several morphological and physiological modifications, such as a meristem allowing for three-dimensional growth, rhizoids for water and nutrient uptake, air pore complexes or stomata that permit air exchange, and a defense system to cope with oxidative stress that occurs frequently in a terrestrial habitat. To understand how the meristem was determined during land plant evolution, we characterized the function of the closest PLETHORA homolog in the liverwort Marchantia polymorpha, which we named MpPLT. Through a transgenic approach, we showed that MpPLT is expressed not only in the stem cells at the apical notch but also in the proliferation zone of the meristem, as well as in cells that form the air-pore complex and rhizoids. Using the CRISPR method we then created mutants for MpPLT and found that the mutants are not only defective in meristem maintenance but also compromised in air-pore complex and rhizoid development. Strikingly, at later developmental stages, numerous gemma-like structures were formed in Mpplt mutants, suggesting developmental arrest. Further experiments indicated that MpPLT promotes plant growth by regulating MpWOX, which shared a similar expression pattern to MpPLT, and genes involved in auxin and cytokinin signaling pathways. Through transcriptome analyses, we found that MpPLT also has a role in redox homeostasis and that this role is essential for plant growth. Taken together, these results suggest that MpPLT has a crucial role in liverwort growth and development and hence may have played a crucial role in early land plant evolution.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1231-1244"},"PeriodicalIF":3.9,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140959101","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}