Henrik Mihály Szaker,Radhika Verma,István Szádeczky-Kardoss,Nóra Gál,Syed Hussam Abbas,Éva Darkó,Aladár Pettkó-Szandtner,Dániel Silhavy,Tibor Csorba
Transcriptional quality control is essential to maintain the integrity of genetic information. Although well characterized in yeast and metazoans, the regulation of transcriptional fidelity in plants remains elusive. We explored transcriptional fidelity and alternative splicing control in Arabidopsis thaliana using genetic, molecular biology, and deep sequencing tools. Using circle-sequencing assays, we analyzed the error landscape of the transcriptome at single-nucleotide depth under ambient and heat-stress conditions in wild-type and different quality control mutant plants. We found that the frequency of nucleotide misincorporations and insertions is significantly elevated under heat stress, and that nucleotide imbalance also leads to error-prone transcription. We demonstrate that the RNA polymerase II-associated elongation cofactor TFIIS is a fidelity factor for both transcription and alternative splicing, as its absence reduces the accuracy of both processes. Moreover, we found that the nonsense-mediated mRNA decay (NMD) cytoplasmic surveillance system is also required for heat-stress tolerance: NMD degrades transcripts containing premature termination codons, generated by 1-2 nucleotide indels of erroneous transcription and by alternative splicing during heat stress. In conclusion, the interplay between these RNA surveillance systems safeguards the correct genetic information flow and is critical for developmental regulation and heat-stress adaptation in plants.
{"title":"Transcription fidelity and control of alternative splicing contribute to heat stress survival in Arabidopsis.","authors":"Henrik Mihály Szaker,Radhika Verma,István Szádeczky-Kardoss,Nóra Gál,Syed Hussam Abbas,Éva Darkó,Aladár Pettkó-Szandtner,Dániel Silhavy,Tibor Csorba","doi":"10.1093/plcell/koaf256","DOIUrl":"https://doi.org/10.1093/plcell/koaf256","url":null,"abstract":"Transcriptional quality control is essential to maintain the integrity of genetic information. Although well characterized in yeast and metazoans, the regulation of transcriptional fidelity in plants remains elusive. We explored transcriptional fidelity and alternative splicing control in Arabidopsis thaliana using genetic, molecular biology, and deep sequencing tools. Using circle-sequencing assays, we analyzed the error landscape of the transcriptome at single-nucleotide depth under ambient and heat-stress conditions in wild-type and different quality control mutant plants. We found that the frequency of nucleotide misincorporations and insertions is significantly elevated under heat stress, and that nucleotide imbalance also leads to error-prone transcription. We demonstrate that the RNA polymerase II-associated elongation cofactor TFIIS is a fidelity factor for both transcription and alternative splicing, as its absence reduces the accuracy of both processes. Moreover, we found that the nonsense-mediated mRNA decay (NMD) cytoplasmic surveillance system is also required for heat-stress tolerance: NMD degrades transcripts containing premature termination codons, generated by 1-2 nucleotide indels of erroneous transcription and by alternative splicing during heat stress. In conclusion, the interplay between these RNA surveillance systems safeguards the correct genetic information flow and is critical for developmental regulation and heat-stress adaptation in plants.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"77 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145380915","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Rory J Craig,Marco A Dueñas,Dimitrios J Camacho,Sean D Gallaher,Maria Clara Avendaño-Monsalve,Yang-Tsung Lin,Crysten E Blaby-Haas,Jeffrey L Moseley,Sabeeha S Merchant
Auxenochlorella spp. are diploid oleaginous green algae whose streamlined genomes can be readily manipulated by homologous recombination, making them highly amenable to discovery research and bioengineering. Vegetatively diploid organisms experience specific evolutionary phenomena, including allodiploid hybridization, mitotic recombination, loss-of-heterozygosity and aneuploidy; however, studies of these forces have largely focused on yeasts. Here, we present a telomere-to-telomere phased diploid genome assembly of Auxenochlorella UTEX 250-A (haploid length 22 Mb) and introduce a genetic toolkit for site-specific manipulation of the nuclear genome in multiple strains, featuring several selectable markers, inducible promoters, and fluorescent reporters for protein localization. UTEX 250-A is an allodiploid hybrid of Auxenochlorella protothecoides and Auxenochlorella symbiontica, two species differentiated by extensive chromosomal rearrangements. UTEX 250-A haplotypes are a mosaic of each parental species following mitotic recombination, and two chromosomes are trisomic. Loss-of-heterozygosity events are pervasive across Auxenochlorella and can evolve rapidly in the laboratory. High-quality structural annotation yielded ∼7,500 genes per haplotype. Auxenochlorella have experienced gene family loss and reduction, including core photosynthesis genes, and exhibit periodic adenine and cytosine methylation at promoters and gene bodies, respectively. Approximately 10% of genes, especially those involved in DNA repair and sex, overlap antisense long noncoding RNAs, which may participate in a regulatory mechanism. We demonstrate the utility of Auxenochlorella for fundamental research by knockout of a chlorophyll biosynthesis enzyme, and confirm one trisomy by allele-specific transformation. These results demonstrate the generality of several evolutionary forces associated with vegetative diploidy and provide a foundation for use of Auxenochlorella as a reference organism.
{"title":"Targeted genetic manipulation and yeast-like evolutionary genomics in the green alga Auxenochlorella.","authors":"Rory J Craig,Marco A Dueñas,Dimitrios J Camacho,Sean D Gallaher,Maria Clara Avendaño-Monsalve,Yang-Tsung Lin,Crysten E Blaby-Haas,Jeffrey L Moseley,Sabeeha S Merchant","doi":"10.1093/plcell/koaf259","DOIUrl":"https://doi.org/10.1093/plcell/koaf259","url":null,"abstract":"Auxenochlorella spp. are diploid oleaginous green algae whose streamlined genomes can be readily manipulated by homologous recombination, making them highly amenable to discovery research and bioengineering. Vegetatively diploid organisms experience specific evolutionary phenomena, including allodiploid hybridization, mitotic recombination, loss-of-heterozygosity and aneuploidy; however, studies of these forces have largely focused on yeasts. Here, we present a telomere-to-telomere phased diploid genome assembly of Auxenochlorella UTEX 250-A (haploid length 22 Mb) and introduce a genetic toolkit for site-specific manipulation of the nuclear genome in multiple strains, featuring several selectable markers, inducible promoters, and fluorescent reporters for protein localization. UTEX 250-A is an allodiploid hybrid of Auxenochlorella protothecoides and Auxenochlorella symbiontica, two species differentiated by extensive chromosomal rearrangements. UTEX 250-A haplotypes are a mosaic of each parental species following mitotic recombination, and two chromosomes are trisomic. Loss-of-heterozygosity events are pervasive across Auxenochlorella and can evolve rapidly in the laboratory. High-quality structural annotation yielded ∼7,500 genes per haplotype. Auxenochlorella have experienced gene family loss and reduction, including core photosynthesis genes, and exhibit periodic adenine and cytosine methylation at promoters and gene bodies, respectively. Approximately 10% of genes, especially those involved in DNA repair and sex, overlap antisense long noncoding RNAs, which may participate in a regulatory mechanism. We demonstrate the utility of Auxenochlorella for fundamental research by knockout of a chlorophyll biosynthesis enzyme, and confirm one trisomy by allele-specific transformation. These results demonstrate the generality of several evolutionary forces associated with vegetative diploidy and provide a foundation for use of Auxenochlorella as a reference organism.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"1 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145370619","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In plants, responses to hypoxia include activation of fermentation pathways, cytosolic acidification, and other metabolic shifts. In Arabidopsis (Arabidopsis thaliana), the transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) contributes to regulating cellular responses to low-oxygen stress; however, the underlying mechanism remains largely unknown. Here, we showed that transgenic lines overexpressing STOP1 exhibited improved tolerance of hypoxia and submergence, whereas knockout of STOP1 reduced tolerance. STOP1 accumulated during hypoxia and was degraded during post-hypoxia reoxygenation via ubiquitination by PLANT U-BOX-TYPE UBIQUITIN LIGASE 24 (PUB24). Under hypoxia, MITOGEN-ACTIVATED PROTEIN KINASE 3 (MPK3) and MPK6 interacted with and phosphorylated STOP1 to compete with its PUB24-mediated ubiquitination, thus stabilizing STOP1 in the nucleus, where it activated the transcription of GLUTAMATE DEHYDROGENASE 1 (GDH1) and GDH2 for cellular homeostasis of acidic metabolism during hypoxia. Mutating three phosphorylated residues in STOP1 to alanine attenuated its nuclear accumulation and diminished STOP1-mediated hypoxia tolerance. Moreover, we identified the lipid phosphatidic acid as a critical modulator of the MPK3/6-STOP1 association. Overall, these findings uncover an antagonistic biochemical mechanism in which MPK3/6-dependent phosphorylation and PUB24-dependent ubiquitination of STOP1 modulate its nuclear accumulation to control hypoxia responses in Arabidopsis.
{"title":"MPK3- and MPK6-mediated phosphorylation of STOP1 triggers its nuclear stabilization to modulate hypoxia responses in Arabidopsis.","authors":"Jian-Hong Wang,Ying Zhou,Guo-Zhen Su,Qi-Qi Song,Gao-Fan Lin,Ying Xing,Qin-Fang Chen,Lu-Jun Yu,Shi-Hao Su,Ruo-Han Xie,Shi Xiao","doi":"10.1093/plcell/koaf257","DOIUrl":"https://doi.org/10.1093/plcell/koaf257","url":null,"abstract":"In plants, responses to hypoxia include activation of fermentation pathways, cytosolic acidification, and other metabolic shifts. In Arabidopsis (Arabidopsis thaliana), the transcription factor SENSITIVE TO PROTON RHIZOTOXICITY 1 (STOP1) contributes to regulating cellular responses to low-oxygen stress; however, the underlying mechanism remains largely unknown. Here, we showed that transgenic lines overexpressing STOP1 exhibited improved tolerance of hypoxia and submergence, whereas knockout of STOP1 reduced tolerance. STOP1 accumulated during hypoxia and was degraded during post-hypoxia reoxygenation via ubiquitination by PLANT U-BOX-TYPE UBIQUITIN LIGASE 24 (PUB24). Under hypoxia, MITOGEN-ACTIVATED PROTEIN KINASE 3 (MPK3) and MPK6 interacted with and phosphorylated STOP1 to compete with its PUB24-mediated ubiquitination, thus stabilizing STOP1 in the nucleus, where it activated the transcription of GLUTAMATE DEHYDROGENASE 1 (GDH1) and GDH2 for cellular homeostasis of acidic metabolism during hypoxia. Mutating three phosphorylated residues in STOP1 to alanine attenuated its nuclear accumulation and diminished STOP1-mediated hypoxia tolerance. Moreover, we identified the lipid phosphatidic acid as a critical modulator of the MPK3/6-STOP1 association. Overall, these findings uncover an antagonistic biochemical mechanism in which MPK3/6-dependent phosphorylation and PUB24-dependent ubiquitination of STOP1 modulate its nuclear accumulation to control hypoxia responses in Arabidopsis.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"39 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145357950","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gray mold caused by the fungal pathogen Botrytis cinerea is a major disease of vegetable and fruit crops. This study elucidates mechanism that fine-tunes B. cinerea resistance mediated by the transcription factor SlMYC2 in tomato (Solanum lycopersicum), characterized by a dynamic balance between "active braking" and "brake release". The Lateral Organ Boundaries Domain (LBD) transcription factor family members SlLBD40 and SlLBD42 repress transcription and form homodimers or heterodimers, with heterodimers demonstrating higher activity. SlLBD40 and SlLBD42 are transcriptionally up-regulated by SlMYC2, but SlLBD40 and SlLBD42 attenuate SlMYC2-orchestrated defenses against B. cinerea, thereby safeguarding the plant from immune over-activation. Moreover, the BTB/POZ-MATH (BPM) protein family member SlBPM4 targets and degrades SlLBD40 and SlLBD42, releasing the defense response and enhancing B. cinerea resistance. Genetic analyses demonstrated that SlLBD40 and SlLBD42 are epistatic to SlBPM4. Additionally, SlLBD40 and SlLBD42 play dual roles in fruit development and B. cinerea defense, and SlBPM4 functions as a protective factor under pathogen attack. Our study uncovered a MYC2-LBD40/42-CRL3BPM4 module in tomato that allocates growth and defense resources by finely regulating gene expression and balancing immune response activation levels. This module also provides potential targets for optimizing the balance between plant growth and defense through gene-editing technologies.
{"title":"Fine-tuning of MYC2-mediated Botrytis defense response by the LBD40/42-CRL3BPM4 module in tomato.","authors":"Jialong Zhang,Danhui Dong,Congyang Jia,Hongxin Li,Lun Liu,Jiayi Xu,Hao Cui,Na Zhang,Yang-Dong Guo","doi":"10.1093/plcell/koaf258","DOIUrl":"https://doi.org/10.1093/plcell/koaf258","url":null,"abstract":"Gray mold caused by the fungal pathogen Botrytis cinerea is a major disease of vegetable and fruit crops. This study elucidates mechanism that fine-tunes B. cinerea resistance mediated by the transcription factor SlMYC2 in tomato (Solanum lycopersicum), characterized by a dynamic balance between \"active braking\" and \"brake release\". The Lateral Organ Boundaries Domain (LBD) transcription factor family members SlLBD40 and SlLBD42 repress transcription and form homodimers or heterodimers, with heterodimers demonstrating higher activity. SlLBD40 and SlLBD42 are transcriptionally up-regulated by SlMYC2, but SlLBD40 and SlLBD42 attenuate SlMYC2-orchestrated defenses against B. cinerea, thereby safeguarding the plant from immune over-activation. Moreover, the BTB/POZ-MATH (BPM) protein family member SlBPM4 targets and degrades SlLBD40 and SlLBD42, releasing the defense response and enhancing B. cinerea resistance. Genetic analyses demonstrated that SlLBD40 and SlLBD42 are epistatic to SlBPM4. Additionally, SlLBD40 and SlLBD42 play dual roles in fruit development and B. cinerea defense, and SlBPM4 functions as a protective factor under pathogen attack. Our study uncovered a MYC2-LBD40/42-CRL3BPM4 module in tomato that allocates growth and defense resources by finely regulating gene expression and balancing immune response activation levels. This module also provides potential targets for optimizing the balance between plant growth and defense through gene-editing technologies.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"19 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145357951","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jana Wittmer, Menno Pijnenburg, Tristan Wijsman, Sieme Pelzer, Kelvin Adema, Merijn Kerstens, An-Nikol Kutevska, Joke Fierens, Hugo Hofhuis, Robert Sevenier, Bjorn Kloosterman, Michiel de Both, Wouter Kohlen, Harm Nijveen, Ben Scheres, Renze Heidstra
Plants have a remarkable regenerative capacity, but this varies widely among species and tissue types. Important crop cultivars show regenerative recalcitrance, which is a major obstacle for the application of modern plant propagation and breeding techniques. Regeneration generally involves empirically determined tissue culture methods that are based on the principle of inducing totipotency. Cells are first persuaded to change fate towards root stem cell-like identity and then are reprogrammed to acquire shoot fate. Alternatively, pluri- or totipotent cells can lead to the formation of a complete plantlet through somatic embryogenesis. We applied our knowledge of root stem cell niche biology to directly use the implicated stem cell factors, including RETINOBLASTOMA (RBR), SCARECROW (SCR), SHORT ROOT (SHR) and members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) and WUSCHEL-related homeobox (WOX) gene families, as a tool to induce regeneration in a way similar to the principle of induced pluripotent stem cells in the animal field. We show that stem cell factors synergistically induce regeneration involving the somatic embryogenesis pathway and can break recalcitrance in Arabidopsis (Arabidopsis thaliana) and pepper (Capsicum annuum).
{"title":"Rational design of induced regeneration via somatic embryogenesis in the absence of exogenous phytohormones","authors":"Jana Wittmer, Menno Pijnenburg, Tristan Wijsman, Sieme Pelzer, Kelvin Adema, Merijn Kerstens, An-Nikol Kutevska, Joke Fierens, Hugo Hofhuis, Robert Sevenier, Bjorn Kloosterman, Michiel de Both, Wouter Kohlen, Harm Nijveen, Ben Scheres, Renze Heidstra","doi":"10.1093/plcell/koaf252","DOIUrl":"https://doi.org/10.1093/plcell/koaf252","url":null,"abstract":"Plants have a remarkable regenerative capacity, but this varies widely among species and tissue types. Important crop cultivars show regenerative recalcitrance, which is a major obstacle for the application of modern plant propagation and breeding techniques. Regeneration generally involves empirically determined tissue culture methods that are based on the principle of inducing totipotency. Cells are first persuaded to change fate towards root stem cell-like identity and then are reprogrammed to acquire shoot fate. Alternatively, pluri- or totipotent cells can lead to the formation of a complete plantlet through somatic embryogenesis. We applied our knowledge of root stem cell niche biology to directly use the implicated stem cell factors, including RETINOBLASTOMA (RBR), SCARECROW (SCR), SHORT ROOT (SHR) and members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) and WUSCHEL-related homeobox (WOX) gene families, as a tool to induce regeneration in a way similar to the principle of induced pluripotent stem cells in the animal field. We show that stem cell factors synergistically induce regeneration involving the somatic embryogenesis pathway and can break recalcitrance in Arabidopsis (Arabidopsis thaliana) and pepper (Capsicum annuum).","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"15 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145314588","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Peng Shuai, Jo-Wei Allison Hsieh, Chung-Ting Kao, Chen-Wei Hu, Ray Wang, Shang-Che Kuo, Ming-Ren Yen, Pin-Chien Liou, Yi-Chi Ho, Chia-Chen Chu, Shuotian Huang, Jiao Liu, Lixia Zhang, Chia-Chen Wu, Yi-Jyun Luo, Quanzi Li, Chuan-Chih Hsu, Chao-Li Huang, Jung-Chen Su, Mei-Chun Tseng, Ying-Lan Chen, Te-Lun Mai, Ying-Chung Jimmy Lin
Secondary growth is a key characteristic evolved from seed plants and generates secondary xylem—the most abundant tissue on Earth. Recent studies have uncovered xylem developmental lineages in eudicots and magnoliids of angiosperms. However, xylem development in gymnosperms, the other representative clade of seed plants, remained elusive. We performed single-cell transcriptomics for xylem cells of conifers (Cunninghamia lanceolata), the major clade in gymnosperms. Using Seurat and scVI-based cross-species integration, we reconstructed the xylem differentiation trajectories and revealed that the radial system is conserved across seed plants, while the axial system in C. lanceolata exhibits a composite lineage architecture resembling both eudicots and magnoliids. To validate these trajectories, we established a multi-modal spatial framework incorporating spatial transcriptomics, spatial proteomics, and spatial metabolomics. These three spatial layers provided orthogonal evidence confirming cell-type identities and trajectory inference. Additionally, we identified a xylem cell population unique to gymnosperms, suggesting a lineage-specific specialization. Together, our findings uncover a more complex ancestral xylem architecture in gymnosperms and propose a progressive simplification of axial developmental programs from gymnosperms to angiosperms, highlighting a trajectory of reductive evolution in seed plant vascular development.
{"title":"Single-cell and spatial omics reveal progressive loss of xylem developmental complexity across seed plants","authors":"Peng Shuai, Jo-Wei Allison Hsieh, Chung-Ting Kao, Chen-Wei Hu, Ray Wang, Shang-Che Kuo, Ming-Ren Yen, Pin-Chien Liou, Yi-Chi Ho, Chia-Chen Chu, Shuotian Huang, Jiao Liu, Lixia Zhang, Chia-Chen Wu, Yi-Jyun Luo, Quanzi Li, Chuan-Chih Hsu, Chao-Li Huang, Jung-Chen Su, Mei-Chun Tseng, Ying-Lan Chen, Te-Lun Mai, Ying-Chung Jimmy Lin","doi":"10.1093/plcell/koaf253","DOIUrl":"https://doi.org/10.1093/plcell/koaf253","url":null,"abstract":"Secondary growth is a key characteristic evolved from seed plants and generates secondary xylem—the most abundant tissue on Earth. Recent studies have uncovered xylem developmental lineages in eudicots and magnoliids of angiosperms. However, xylem development in gymnosperms, the other representative clade of seed plants, remained elusive. We performed single-cell transcriptomics for xylem cells of conifers (Cunninghamia lanceolata), the major clade in gymnosperms. Using Seurat and scVI-based cross-species integration, we reconstructed the xylem differentiation trajectories and revealed that the radial system is conserved across seed plants, while the axial system in C. lanceolata exhibits a composite lineage architecture resembling both eudicots and magnoliids. To validate these trajectories, we established a multi-modal spatial framework incorporating spatial transcriptomics, spatial proteomics, and spatial metabolomics. These three spatial layers provided orthogonal evidence confirming cell-type identities and trajectory inference. Additionally, we identified a xylem cell population unique to gymnosperms, suggesting a lineage-specific specialization. Together, our findings uncover a more complex ancestral xylem architecture in gymnosperms and propose a progressive simplification of axial developmental programs from gymnosperms to angiosperms, highlighting a trajectory of reductive evolution in seed plant vascular development.","PeriodicalId":501012,"journal":{"name":"The Plant Cell","volume":"45 1","pages":""},"PeriodicalIF":0.0,"publicationDate":"2025-10-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145314589","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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