{"title":"Multi-omics signatures of diverse plant callus cultures.","authors":"June-Sik Kim, Muneo Sato, Mikiko Kojima, Muchamad Imam Asrori, Yukiko Uehara-Yamaguchi, Yumiko Takebayashi, Thi Nhung Do, Thi Yen Do, Kieu Oanh Nguyen Thi, Hitoshi Sakakibara, Keiichi Mochida, Shijiro Ogita, Masami Yokota Hirai","doi":"10.5511/plantbiotechnology.24.0719a","DOIUrl":"10.5511/plantbiotechnology.24.0719a","url":null,"abstract":"<p><p>Callus cultures are fundamental for plant propagation, genetic transformation, and emerging biotechnological applications that use cellular factories to produce high-value metabolites like plant-based drugs. These applications exploit the diverse metabolic capabilities of various plant species. However, optimizing culture conditions for specific applications necessitates a deep understanding of the transcriptome, metabolome, and phytohormone profiles of different species. Comprehensive comparative studies of callus characteristics across species are limited. Here, we analyzed the transcriptome, metabolome, and phytohormone profiles of callus cultures from tobacco (<i>Nicotiana tabacum</i>), rice (<i>Oryza sativa</i>), and two bamboo species (<i>Phyllostachys nigra</i> and <i>P. bambusoides</i>). Multivariate analyses of metabolome data revealed similar metabolic trends in these diverse callus cultures and identified metabolites that differ between species. Hormone profiling showed distinct species-specific patterns and notable cytokinin diversity, even between the bamboo species. Moreover, a comparative analysis of 8,256 pairs of syntenic genes between rice and bamboo revealed that 84.7% of these orthologs showed differential expression, indicating significant transcriptomic diversity despite phylogenomic relatedness. Transcriptional regulation of developing organs often involves conserved gene expression patterns across species; however, our findings suggest that callus formation may relax evolutionary constraints on these regulatory programs. These results illustrate the molecular diversity in callus cultures from multiple plant species, emphasizing the need to map this variability comprehensively to fully exploit the biotechnological potential of plant callus cultures.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"309-314"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921129/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670336","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Synthetic biology in plants.","authors":"Takahiko Hayakawa, Hayato Suzuki, Hiroshi Yamamoto, Nobutaka Mitsuda","doi":"10.5511/plantbiotechnology.24.0630b","DOIUrl":"10.5511/plantbiotechnology.24.0630b","url":null,"abstract":"<p><p>Synthetic biology, an interdisciplinary field at the intersection of engineering and biology, has garnered considerable attention for its potential applications in plant science. By exploiting engineering principles, synthetic biology enables the redesign and construction of biological systems to manipulate plant traits, metabolic pathways, and responses to environmental stressors. This review explores the evolution and current state of synthetic biology in plants, highlighting key achievements and emerging trends. Synthetic biology offers innovative solutions to longstanding challenges in agriculture and biotechnology for improvement of nutrition and photosynthetic efficiency, useful secondary metabolite production, engineering biosensors, and conferring stress tolerance. Recent advances, such as genome editing technologies, have facilitated precise manipulation of plant genomes, creating new possibilities for crop improvement and sustainable agriculture. Despite its transformative potential, ethical and biosafety considerations underscore the need for responsible deployment of synthetic biology tools in plant research and development. This review provides insights into the burgeoning field of plant synthetic biology, offering a glimpse into its future implications for food security, environmental sustainability, and human health.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"173-193"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921130/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670343","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant BiotechnologyPub Date : 2024-09-25DOI: 10.5511/plantbiotechnology.24.0717b
Hayato Suzuki, Shigeo S Sugano, Toshiya Muranaka, Hikaru Seki
{"title":"Ectopic expression of BpbHLH9 suggested the presence of a self-activating loop mechanism of clade Ia bHLHs to enhance betulinic acid biosynthesis in <i>Lotus japonicus</i> hairy roots.","authors":"Hayato Suzuki, Shigeo S Sugano, Toshiya Muranaka, Hikaru Seki","doi":"10.5511/plantbiotechnology.24.0717b","DOIUrl":"10.5511/plantbiotechnology.24.0717b","url":null,"abstract":"<p><p>For the optimal production of specialized (secondary) metabolites in plant hosts, a comprehensive understanding of their regulatory mechanisms is imperative. Bioactive C-28-oxidized triterpenes, such as oleanolic, ursolic, and betulinic acids, are metabolites ubiquitously found across the plant kingdom; however the precise regulatory mechanisms governing their biosynthesis remain elusive. Previously, we demonstrated that the clade Ia bHLH transcription factor, LjbHLH50, plays a pivotal role in the upregulation of betulinic acid biosynthesis in <i>Lotus japonicus</i>. However, inconsistent outcomes have been observed in transient effector-reporter assays, which are commonly employed in transcription factor studies. Thus, in the present study, we sought to further characterize LjbHLH50 by examining the ectopic expression of <i>BpbHLH9</i>, a homolog of <i>LjbHLH50</i> in <i>Betula platyphylla</i>, in <i>L. japonicus</i> hairy roots. Remarkably, <i>BpbHLH9</i> expression elicited metabolic and transcriptomic alterations almost similar to those induced by <i>LjbHLH50</i> overexpression, highlighting the conserved function of clade Ia bHLHs. Through RNA-sequencing analysis, we found that <i>LjbHLH50</i> was upregulated by ectopic BpbHLH9 expression, implying the existence of a self-activating loop in clade Ia bHLHs that facilitates enhanced betulinic acid biosynthesis. Notably, among the clade Ia bHLHs homologous to <i>BpbHLH9</i>, <i>LjbHLH50</i> and two <i>LjbHLH50</i> paralogs were upregulated upon BpbHLH9 induction, underscoring the central role of these clade Ia bHLHs in betulinic acid biosynthesis regulatory networks in <i>L. japonicus</i> hairy roots.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"319-323"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11962628/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143773138","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Tracer experiment revealed that (<i>E</i>)-3″-hydroxygeranylhydroquinone is not an intermediate of the shikonin/alkannin and shikonofuran biosynthetic pathways in <i>Lithospermum erythrorhizon</i>.","authors":"Misaki Manabe, Bunta Watanabe, Haruka Oshikiri, Kojiro Takanashi","doi":"10.5511/plantbiotechnology.24.0303a","DOIUrl":"10.5511/plantbiotechnology.24.0303a","url":null,"abstract":"<p><p><i>Lithospermum erythrorhizon</i> (Boraginaceae) produces shikonin/alkannin, an enantiomeric pair of red naphthoquinone pigments with diverse biological activities. For the industrial production of shikonin/alkannin derivatives, a cell suspension culture system of <i>L. erythrorhizon</i> has been established. To produce shikonin/alkannin derivatives more efficiently in cultured cells, it is essential to understand the shikonin/alkannin biosynthetic pathway, which has not been fully elucidated. A previous study suggested that a conversion of (<i>Z</i>)- to (<i>E</i>)-3″-hydroxygeranylhydroquinone (3″-OH-GHQ) is a branching point of the shikonin/alkannin biosynthetic pathway and the shikonofuran biosynthetic pathway in <i>L. erythrorhizon</i> cell cultures. However, it is not clear whether (<i>E</i>)-3″-OH-GHQ is an intermediate of both pathways. This study performed a feeding assay with three deuterium-labeled compounds including (<i>E</i>)-3″-OH-GHQ and its (<i>Z</i>)-isomer, and showed that (<i>E</i>)-3″-OH-GHQ was not involved in the shikonin/alkannin and shikonofuran biosynthetic pathways.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"315-317"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921126/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670347","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Distribution, biosynthesis, and synthetic biology of phenylethanoid glycosides in the order Lamiales.","authors":"Yushiro Fuji, Hiroshi Matsufuji, Masami Yokota Hirai","doi":"10.5511/plantbiotechnology.24.0720a","DOIUrl":"10.5511/plantbiotechnology.24.0720a","url":null,"abstract":"<p><p>Phenylethanoid glycosides (PhGs), with a C<sub>6</sub>-C<sub>2</sub> glucoside unit as the basic skeleton, are specialized (secondary) metabolites found in several medicinal plants. As PhGs exhibit various pharmacological activities, they are expected to be used as lead compounds in drug discovery. However, mass-production systems have not yet been established even for acteoside, a typical PhG that is widely distributed in nature (more than 150 species). This review focuses on recent studies on the accumulation and distribution of PhGs in plants, biosynthetic pathways of PhGs, and the bioproduction of PhGs.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"231-241"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921133/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670908","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant BiotechnologyPub Date : 2024-09-25DOI: 10.5511/plantbiotechnology.24.0601a
Ko Tahara, Carsten Milkowski, Chihiro Oda-Yamamizo
{"title":"Elucidation and reconstitution of hydrolyzable tannin biosynthesis.","authors":"Ko Tahara, Carsten Milkowski, Chihiro Oda-Yamamizo","doi":"10.5511/plantbiotechnology.24.0601a","DOIUrl":"10.5511/plantbiotechnology.24.0601a","url":null,"abstract":"<p><p>Hydrolyzable tannins (HTs) are a class of polyphenols produced mostly in core eudicot plants. They accumulate in various plant tissues and are considered to function as defense compounds that protect against herbivory, infections, and toxic metals (specifically aluminum ions). Moreover, HTs have industrial and pharmaceutical uses that benefit humans. Elucidating and reconstituting the biosynthesis of HTs is necessary for genetically engineering in planta functions and for efficiently producing HTs for human use. The biosynthesis of HTs is initiated by the formation of gallic acid from the shikimate pathway intermediate 3-dehydroshikimic acid, which is catalyzed by bifunctional dehydroquinate dehydratase/shikimate dehydrogenases (DQD/SDHs). In the second step, UDP glycosyltransferases (UGTs) esterify gallic acid with glucose to form β-glucogallin (1-<i>O</i>-galloyl-β-D-glucose). β-glucogallin is then converted to 1,2,3,4,6-penta-<i>O</i>-galloyl-β-D-glucose through a series of galloylation steps that are catalyzed by galloyltransferases, using β-glucogallin as a galloyl donor. Laccases subsequently catalyze the oxidative coupling between adjacent galloyl groups to form hexahydroxydiphenoyl (HHDP) groups, which are characteristic components of ellagitannins. Furthermore, monomeric ellagitannins can undergo oligomerization via intermolecular oxidative coupling, which is also catalyzed by laccases. To reconstitute the HT biosynthetic pathway in HT-non-accumulating plants, <i>DQD</i>/<i>SDH</i>s and <i>UGT</i>s from <i>Eucalyptus camaldulensis</i> were heterologously co-expressed in <i>Nicotiana benthamiana</i> leaves, which resulted in the production of gallic acid and β-glucogallin. In future studies, this transgenic system will be used to identify genes encoding galloyltransferases and laccases to further elucidate and reconstitute the HT biosynthetic pathway.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"203-212"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921145/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670909","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant BiotechnologyPub Date : 2024-09-25DOI: 10.5511/plantbiotechnology.24.0716a
Noriho Fukuzawa, Kouki Matsuo, Go Atsumi, Yasushi Tasaka, Nobutaka Mitsuda
{"title":"Plant-made pharmaceuticals.","authors":"Noriho Fukuzawa, Kouki Matsuo, Go Atsumi, Yasushi Tasaka, Nobutaka Mitsuda","doi":"10.5511/plantbiotechnology.24.0716a","DOIUrl":"10.5511/plantbiotechnology.24.0716a","url":null,"abstract":"<p><p>Plant-made pharmaceuticals (PMP) have great potential in terms of production costs, scalability, safety, environmental protection, and consumer acceptability. The first PMP were antibodies and antigens produced in stably transformed transgenic plants in the around 90s. Even though the effort using stable transgenic plants is still going on, the mainstream of PMP production has shifted to transient expression in <i>Nicotiana benthamiana</i>. This system involves the expression vectors by <i>Agrobacterium</i>, and its efficiency has been improved by the development of new vector systems and host engineering. The COVID-19 outbreak accelerated this trend through efforts to produce vaccines in plants. Transient expression systems have been improved and diversified by the development of plant virus vectors, which can be classified as full and deconstructed vectors. Full virus vectors spread systemically, allowing for protein production in the entire plant. Compared with conventional agroinfiltration vectors, excellent virus vectors result in higher protein production. Engineering of host plants has included knocking out gene-silencing systems to increase protein production, and the introduction of glycan modification enzymes so that plant-made proteins more resemble animal-made proteins. Hydroponic cultivation systems in plant factories and environmental controls have contributed to efficient protein production in plants. Considering their advantages and small environmental impact, PMP should be more widely adopted for pharmaceuticals' production. However, the initial investment and running costs of plant factories are higher than open filed cultivation. The next objectives are to develop next-generation low-cost plant factories that use renewable energy and recycle materials based on the idea of circular economy.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"243-260"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11962629/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143773146","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant BiotechnologyPub Date : 2024-09-25DOI: 10.5511/plantbiotechnology.24.0312b
Yasuyuki Yamada, Miya Urui, Nobukazu Shitan
{"title":"Integration of co-culture and transport engineering for enhanced metabolite production.","authors":"Yasuyuki Yamada, Miya Urui, Nobukazu Shitan","doi":"10.5511/plantbiotechnology.24.0312b","DOIUrl":"10.5511/plantbiotechnology.24.0312b","url":null,"abstract":"<p><p>Microbial production of valuable plant metabolites is feasible. However, constructing all pathways in a single cell is a formidable challenge, and the extended biosynthetic pathways within cells often result in reduced productivity. To address these challenges, a co-culture system that divides biosynthetic pathways into several host cells and co-cultures has been developed. Various combinations of host cells, along with the optimal conditions for each co-culture, have been documented, leading to the successful production of valuable metabolites. In addition, efficient biosynthesis frequently involves metabolite movement, encompassing substrate uptake, intracellular intermediate transport, and end-product efflux. Recent advances in plant transporters of specialized metabolites have enhanced productivity by harnessing these transporters. This review summarizes the latest findings on co-culture systems and transport engineering and provides insights into the future of valuable metabolite production through the integration of co-culture and transport engineering.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"195-202"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921134/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670080","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Plant BiotechnologyPub Date : 2024-09-25DOI: 10.5511/plantbiotechnology.24.0312c
Keita Tamura, Hirokazu Chiba, Hidemasa Bono
{"title":"Triterpene RDF: Developing a database of plant enzymes and transcription factors involved in triterpene biosynthesis using the Resource Description Framework.","authors":"Keita Tamura, Hirokazu Chiba, Hidemasa Bono","doi":"10.5511/plantbiotechnology.24.0312c","DOIUrl":"10.5511/plantbiotechnology.24.0312c","url":null,"abstract":"<p><p>Plants produce structurally diverse triterpenes (triterpenoids and steroids). Their biosynthesis occurs from a common precursor, namely 2,3-oxidosqualene, followed by cyclization catalyzed by oxidosqualene cyclases (OSCs) to yield various triterpene skeletons. Steroids, which are biosynthesized from cycloartenol or lanosterol, are essential primary metabolites in most plant species, along with lineage-specific steroids, such as steroidal glycoalkaloids found in the <i>Solanum</i> species. Other diverse triterpene skeletons are converted into triterpenoids, often classified as specialized compounds that are biosynthesized only in a limited number of plant species with tissue- or cell-type-specific accumulation in plants. Recent studies have identified various tailoring enzymes involved in the structural diversification of triterpenes as well as transcription factors that regulate the expression of these enzymes. However, the coverage of these proteins is scarce in publicly available databases for curated proteins or enzymes, which complicates the functional annotation of newly assembled genomes or transcriptome sequences. Here, we created the Triterpene RDF, a manually curated database of enzymes and transcription factors involved in plant triterpene biosynthesis. The database (https://github.com/ktamura2021/triterpene_rdf/) contains 532 proteins, with links to the UniProt Knowledgebase or NCBI protein database, and it enables direct download of a set of protein sequences filtered by protein type or taxonomy. Triterpene RDF will enhance the functional annotation of enzymes and regulatory elements for triterpene biosynthesis, in a current expansion of availability of genomic information on various plant species.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"303-308"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921141/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670349","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Disruption of <i>CYP88B1</i> by transcription activator-like effector nuclease in potato and potential use to produce useful saponins.","authors":"Shuhei Yasumoto, Hyoung Jae Lee, Ryota Akiyama, Satoru Sawai, Masaharu Mizutani, Naoyuki Umemoto, Kazuki Saito, Toshiya Muranaka","doi":"10.5511/plantbiotechnology.24.0614a","DOIUrl":"10.5511/plantbiotechnology.24.0614a","url":null,"abstract":"<p><p>Potatoes produce steroidal glycoalkaloids (SGAs), toxic secondary metabolites associated with food poisoning. SGAs are synthesized by multiple biosynthetic enzymes. Knockdown of the <i>CYP88B1</i> gene, also known as <i>PGA3</i> or <i>GAME4</i>, is predicted to reduce toxic SGAs and accumulate steroidal saponins. These saponins not only serve as a source of steroidal drugs but are also anticipated to confer disease resistance to potatoes. In this study, we employed transcription activator-like effector nucleases (TALENs) for genome editing to disrupt <i>CYP88B1</i>. We introduced the TALEN expression vector via <i>Agrobacterium</i>-mediated transformation into seven potato lines. In six of these lines, disruption of the <i>CYP88B1</i> gene was confirmed. Liquid chromatography-mass spectrometry analysis revealed that SGAs were reduced to undetectable levels, corroborating the accumulation of steroidal saponins observed in previous knockdown studies. Our findings demonstrate the feasibility of generating low-toxicity potato lines through <i>CYP88B1</i> gene disruption using genome editing techniques.</p>","PeriodicalId":20411,"journal":{"name":"Plant Biotechnology","volume":"41 3","pages":"289-293"},"PeriodicalIF":1.4,"publicationDate":"2024-09-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11921144/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143670907","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}