Frontiers in fungal biology最新文献

{"title":"Metal tolerance of Río Tinto fungi.","authors":"Monike Oggerin, Catalina Del Moral, Nuria Rodriguez, Nuria Fernandez-Gonzalez, José Manuel Martínez, Iván Lorca, Ricardo Amils","doi":"10.3389/ffunb.2024.1446674","DOIUrl":"10.3389/ffunb.2024.1446674","url":null,"abstract":"<p><p>Southwest Spain's Río Tinto is a stressful acidic microbial habitat with a noticeably high concentration of toxic heavy metals. Nevertheless, it has an unexpected degree of eukaryotic diversity in its basin, with a high diversity of fungal saprotrophs. Although some studies on the eukaryotic diversity in Rio Tinto have been published, none of them used molecular methodologies to describe the fungal diversity and taxonomic affiliations that emerge along the river in different seasons. The aim of the present study was to isolate and describe the seasonal diversity of the fungal community in the Río Tinto basin and its correlation with the physicochemical parameters existing along the river's course. The taxonomic affiliation of 359 fungal isolates, based on the complete internal transcribed spacer DNA sequences, revealed a high degree of diversity, identifying species belonging primarily to the phylum Ascomycota, but representatives of the Basidiomycota and Mucoromycota phyla were also present. In total, 40 representative isolates along the river were evaluated for their tolerance to toxic heavy metals. Some of the isolates were able to grow in the presence of 1000 mM of Cu²⁺, 750 mM of As⁵⁺ and Cd²⁺, and 100 mM of Co²⁺, Ni²⁺, and Pb²⁺.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11521807/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142549255","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"What lies behind the large genome of <i>Colletotrichum lindemuthianum</i>.","authors":"Leandro Lopes da Silva, Hilberty Lucas Nunes Correia, Osiel Silva Gonçalves, Pedro Marcus Pereira Vidigal, Rafael Oliveira Rosa, Mateus Ferreira Santana, Marisa Vieira de Queiroz","doi":"10.3389/ffunb.2024.1459229","DOIUrl":"https://doi.org/10.3389/ffunb.2024.1459229","url":null,"abstract":"<p><p><i>Colletotrichum lindemuthianum</i> is the etiological agent of anthracnose disease in common bean (<i>Phaseolus vulgaris</i> L.), noted for its ability to cause serious damage and significant pathogenic variability. This study reveals the features of the high-quality genome of <i>C. lindemuthianum</i>. Analysis showed improvements over the first assembly, with the refined genome having 119 scaffolds, ten times fewer than the first, and a 19% increase in gene number. The effector candidates increased by nearly 1.5 times. More than 40% of the amino acid sequences with homologs in the Pathogen-Host Interactions (PHI-base) database are linked to pathogenicity. Of 18 putative proteins identified as Chitinase-like Protein, six have a mutation in the enzyme catalytic motif, and three showed gene expression in the biotrophic phase, indicating they can act as effectors. Comparative genomic analyses with 30 other fungal species revealed that <i>C. lindemuthianum</i> is among the top three fungi encoding transport proteins. Seven Necrosis and Ethylene-Inducing Peptide 1 (Nep1)-Like Proteins (NLPs) are present in the <i>C. lindemuthianum</i> genome, but none had complete identity with the GHRHDWE conserved motif of NLPs; two were grouped with proteins that induce necrosis and may retain the capability to induce host necrosis. <i>Colletotrichum</i> species show a high number of secondary metabolite (SM) clusters, with <i>C. lindemuthianum</i> having 47 SM clusters. Approximately 60% of the <i>C. lindemuthianum</i> genome is composed of repetitive elements, a significantly higher proportion than in other fungi. These differences in transposable element (TE) numbers may explain why <i>C. lindemuthianum</i> has one of the largest genomes among the fungi analyzed. A significant portion of its genome comprises retroelements, particularly the <i>Ty1/Copia</i> superfamily, which accounts for 22% of the genome and represents 40% of the repetitive elements. The genomic profile features a remarkably high RIP-affected genomic proportion of 54.77%, indicating substantial RIP activity within this species. This high-quality genome of <i>C. lindemuthianum</i>, a significant pathogen in common bean cultivation, will support future research into this pathosystem, fostering a deeper understanding of the interaction between the fungus and its host.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11518743/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142549256","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Conserved perception of host and non-host signals via the a-pheromone receptor Ste3 in <i>Colletotrichum graminicola</i>.","authors":"Anina Yasmin Rudolph, Carolin Schunke, Daniela Elisabeth Nordzieke","doi":"10.3389/ffunb.2024.1454633","DOIUrl":"10.3389/ffunb.2024.1454633","url":null,"abstract":"<p><p>Understanding the interactions between fungal plant pathogens and host roots is crucial for developing effective disease management strategies. This study investigates the molecular mechanisms underpinning the chemotropic responses of the maize anthracnose fungus <i>Colletotrichum graminicola</i> to maize root exudates. Combining the generation of a deletion mutant with monitoring of disease symptom development and detailed analysis of chemotropic growth using a 3D-printed device, we identify the 7-transmembrane G-protein coupled receptor (GPCR) CgSte3 as a key player in sensing both plant-derived class III peroxidases and diterpenoids. Activation of CgSte3 initiates signaling through CgSo, a homolog to the Cell Wall Integrity Mitogen-Activated Protein Kinase (CWI MAPK) pathway scaffold protein identified in other filamentous fungi, facilitating the pathogen's growth towards plant defense molecules. The NADPH oxidase CgNox2 is crucial for peroxidase sensing but not for diterpenoid detection. These findings reveal that CgSte3 and CWI MAPK pathways are central to <i>C. graminicola's</i> ability to hijack plant defense signals, highlighting potential targets for controlling maize anthracnose.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-10-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11491335/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142482331","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The yeast <i>Wickerhamomyces anomalus</i> acts as a predator of the olive anthracnose-causing fungi, <i>Colletotrichum nymphaeae</i>, <i>C. godetiae</i>, and <i>C. gloeosporioides</i>.","authors":"Mariana Amorim-Rodrigues, Rogélio Lopes Brandão, Fernanda Cássio, Cândida Lucas","doi":"10.3389/ffunb.2024.1463860","DOIUrl":"10.3389/ffunb.2024.1463860","url":null,"abstract":"<p><p>Olive tree anthracnose is caused by infection with <i>Colletotrichum</i> fungi, which in Portugal are mostly <i>C. nymphaeae</i>, <i>C. godetiae</i>, and <i>C. gloeosporioides</i> s.s. Severe economic losses are caused by this disease that would benefit from a greener and more efficient alternative to the present agrochemical methods. Yeasts are serious candidates for pre-harvest/in field biocontrol of fungal infections. This work identified the yeast <i>Wickerhamomyces anomalus</i> as a strong antagonizer of the three fungi and studied <i>in vitro</i> this ability and its associated mechanisms. Antagonism was shown to not depend on the secretion of volatile compounds (VOCs), or siderophores or any other agar-diffusible compound, including hydrolytic enzymes. Rather, it occurred mostly in a cell-to-cell contact dependent manner. This was devised through detailed microscopic assessment of yeast-fungus cocultures. This showed that <i>W. anomalus</i> antagonism of the three <i>Colletotrichum</i> proceeded through (i) the adhesion of yeast cells to the phytopathogen hyphae, (ii) the secretion of a viscous extracellular matrix, and (iii) the emptying of the hyphae. Yeasts ultimately putatively feed on hyphal contents, which is supported by light microscopy observation of MB and PI co-culture-stained samples. Accordingly, numerous <i>W. anomalus</i> cells were observed packing inside <i>C. godetiae</i> emptied hyphae. This behaviour can be considered microbial predation and classified as necrotrophic mycoparasitism, more explicitly in the case of <i>C. godetiae</i>. The results support the prospect of future application of <i>W. anomalus</i> as a living biofungicide/BCA in the preharvest control of olive anthracnose.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11443700/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142360723","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Editorial: Co-morbidity of COVID 19 and fungal infections.","authors":"Ramendra Pati Pandey, Ruby Dhiman, Vivek Mishra, V Samuel Raj, Chung-Ming Chang","doi":"10.3389/ffunb.2024.1462172","DOIUrl":"10.3389/ffunb.2024.1462172","url":null,"abstract":"","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11439790/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333826","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Fungi of Great Salt Lake, Utah, USA: a spatial survey.","authors":"David L Parrott, Bonnie K Baxter","doi":"10.3389/ffunb.2024.1438347","DOIUrl":"https://doi.org/10.3389/ffunb.2024.1438347","url":null,"abstract":"<p><p>The natural system at Great Salt Lake, Utah, USA was augmented by the construction of a rock-filled railroad causeway in 1960, creating two lakes at one site. The north arm is sequestered from the mountain snowmelt inputs and thus became saturated with salts (250-340 g/L). The south arm is a flourishing ecosystem with moderate salinity (90-190 g/L) and a significant body of water for ten million birds on the avian flyways of the western US who engorge themselves on the large biomass of brine flies and shrimp. The sediments around the lake shores include calcium carbonate oolitic sand and clay, and further away from the saltwater margins, a zone with less saline soil. Here a small number of plants can thrive, including <i>Salicornia</i> and <i>Sueda</i> species. At the north arm at Rozel Point, halite crystals precipitate in the salt-saturated lake water, calcium sulfate precipitates to form gypsum crystals embedded in the clay, and high molecular weight asphalt seeps from the ground. It is an ecosystem with gradients and extremes, and fungi are up to the challenge. We have collected data on Great Salt Lake fungi from a variety of studies and present them here in a spatial survey. Combining knowledge of cultivation studies as well as environmental DNA work, we discuss the genera prevalent in and around this unique ecosystem. A wide diversity of taxa were found in multiple microniches of the lake, suggesting significant roles for these genera: <i>Acremonium, Alternaria</i>, <i>Aspergillus</i>, <i>Cladosporium</i>, <i>Clydae</i>, <i>Coniochaeta</i>, <i>Cryptococcus</i>, <i>Malassezia</i>, <i>Nectria</i>, <i>Penicillium</i>, <i>Powellomyces</i>, <i>Rhizophlyctis</i>, and <i>Wallemia</i>. Considering the species present and the features of Great Salt Lake as a terminal basin, we discuss of the possible roles of the fungi. These include not only nutrient cycling, toxin mediation, and predation for the ecosystem, but also roles that would enable other life to thrive in the water and on the shore. Many genera that we discovered may help other organisms in alleviating salinity stress, promoting growth, or affording protection from dehydration. The diverse taxa of Great Salt Lake fungi provide important benefits for the ecosystem.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11427377/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333828","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Editorial: Fungal toxic secondary metabolites in foods and feeds: recent sustainable analytical techniques and innovative preventative and remediation strategies for their formation and toxicity.","authors":"Dikabo Mogopodi, Olubukola Oluranti Babalola, Titus A M Msagati","doi":"10.3389/ffunb.2024.1442327","DOIUrl":"https://doi.org/10.3389/ffunb.2024.1442327","url":null,"abstract":"","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11424511/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333827","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"In <i>Rhodotorula mucilaginosa</i>, active oxidative metabolism increases carotenoids to inactivate excess reactive oxygen species.","authors":"Edson Mosqueda-Martínez, Natalia Chiquete-Félix, Paulina Castañeda-Tamez, Carolina Ricardez-García, Manuel Gutiérrez-Aguilar, Salvador Uribe-Carvajal, Ofelia Mendez-Romero","doi":"10.3389/ffunb.2024.1378590","DOIUrl":"10.3389/ffunb.2024.1378590","url":null,"abstract":"<p><p>Carotenoids produced by bacteria, yeasts, algae and plants inactivate Free Radicals (FR). However, FR may inactivate carotenoids and even turn them into free radicals. Oxidative metabolism is a source of the highly motile Reactive Oxygen Species (ROS). To evaluate carotenoid interactions with ROS, the yeast <i>Rhodotorula mucilaginosa</i> was grown in dextrose (YPD), a fermentative substrate where low rates of oxygen consumption and low carotenoid expression were observed, or in lactate (YPLac), a mitochondrial oxidative-phosphorylation (OxPhos) substrate, which supports high respiratory activity and carotenoid production. ROS were high in YPLac-grown cells and these were unmasked by the carotenoid production-inhibitor diphenylamine (DPA). In contrast, in YPD-grown cells ROS were almost absent. It is proposed that YPLac cells are under oxidative stress. In addition, YPLac-grown cells were more sensitive than YPD-grown cells to menadione (MD), a FR-releasing agent. To test whether carotenoids from cells grown in YPLac had been modified by ROS, carotenoids from each, YPD- and YPLac-grown cells were isolated and added back to cells, evaluating protection from MD. Remarkably, carotenoids extracted from cells grown in YPLac medium inhibited growth, while in contrast extracts from YPD-grown cells were innocuous or mildly protective. Results suggest that carotenoid-synthesis in YPLac-cells is a response to OxPhos-produced ROS. However, upon reacting with FR, carotenoids themselves may be inactivated or even become prooxidant themselves.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11412819/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302512","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Comparative genomics of the extremophile <i>Cryomyces antarcticus</i> and other psychrophilic Dothideomycetes.","authors":"Sandra V Gomez-Gutierrrez, Wily R Sic-Hernandez, Sajeet Haridas, Kurt LaButti, Joanne Eichenberger, Navneet Kaur, Anna Lipzen, Kerrie Barry, Stephen B Goodwin, Michael Gribskov, Igor V Grigoriev","doi":"10.3389/ffunb.2024.1418145","DOIUrl":"10.3389/ffunb.2024.1418145","url":null,"abstract":"<p><p>Over a billion years of fungal evolution has enabled representatives of this kingdom to populate almost all parts of planet Earth and to adapt to some of its most uninhabitable environments including extremes of temperature, salinity, pH, water, light, or other sources of radiation. <i>Cryomyces antarcticus</i> is an endolithic fungus that inhabits rock outcrops in Antarctica. It survives extremes of cold, humidity and solar radiation in one of the least habitable environments on Earth. This fungus is unusual because it produces heavily melanized, meristematic growth and is thought to be haploid and asexual. Due to its growth in the most extreme environment, it has been suggested as an organism that could survive on Mars. However, the mechanisms it uses to achieve its extremophilic nature are not known. Comparative genomics can provide clues to the processes underlying biological diversity, evolution, and adaptation. This effort has been greatly facilitated by the 1000 Fungal Genomes project and the JGI MycoCosm portal where sequenced genomes have been assembled into phylogenetic and ecological groups representing different projects, lifestyles, ecologies, and evolutionary histories. Comparative genomics within and between these groups provides insights into fungal adaptations, for example to extreme environmental conditions. Here, we analyze two <i>Cryomyces</i> genomes in the context of additional psychrophilic fungi, as well as non-psychrophilic fungi with diverse lifestyles selected from the MycoCosm database. This analysis identifies families of genes that are expanded and contracted in <i>Cryomyces</i> and other psychrophiles and may explain their extremophilic lifestyle. Higher GC contents of genes and of bases in the third positions of codons may help to stabilize DNA under extreme conditions. Numerous smaller contigs in <i>C. antarcticus</i> suggest the presence of an alternative haplotype that could indicate the sequenced isolate is diploid or dikaryotic. These analyses provide a first step to unraveling the secrets of the extreme lifestyle of <i>C. antarcticus</i>.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11412873/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142302511","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Navigating the fungal battlefield: cysteine-rich antifungal proteins and peptides from Eurotiales.","authors":"Jeanett Holzknecht, Florentine Marx","doi":"10.3389/ffunb.2024.1451455","DOIUrl":"https://doi.org/10.3389/ffunb.2024.1451455","url":null,"abstract":"<p><p>Fungi are ubiquitous in the environment and play a key role in the decomposition and recycling of nutrients. On the one hand, their special properties are a great asset for the agricultural and industrial sector, as they are used as source of nutrients, producers of enzymes, pigments, flavorings, and biocontrol agents, and in food processing, bio-remediation and plant growth promotion. On the other hand, they pose a serious challenge to our lives and the environment, as they are responsible for fungal infections in plants, animals and humans. Although host immunity opposes invading pathogens, certain factors favor the manifestation of fungal diseases. The prevalence of fungal infections is on the rise, and there is an alarming increase in the resistance of fungal pathogens to approved drugs. The limited number of antimycotics, the obstacles encountered in the development of new drugs due to the poor tolerability of antifungal agents in patients, the limited number of unique antifungal targets, and the low species specificity contribute to the gradual depletion of the antifungal pipeline and newly discovered antifungal drugs are rare. Promising candidates as next-generation therapeutics are antimicrobial proteins and peptides (AMPs) produced by numerous prokaryotic and eukaryotic organisms belonging to all kingdom classes. Importantly, filamentous fungi from the order Eurotiales have been shown to be a rich source of AMPs with specific antifungal activity. A growing number of published studies reflects the efforts made in the search for new antifungal proteins and peptides (AFPs), their efficacy, species specificity and applicability. In this review, we discuss important aspects related to fungi, their impact on our life and issues involved in treating fungal infections in plants, animals and humans. We specifically highlight the potential of AFPs from Eurotiales as promising alternative antifungal therapeutics. This article provides insight into the structural features, mode of action, and progress made toward their potential application in a clinical and agricultural setting. It also identifies the challenges that must be overcome in order to develop AFPs into therapeutics.</p>","PeriodicalId":73084,"journal":{"name":"Frontiers in fungal biology","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11423270/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142333830","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}