Pub Date : 2024-11-25DOI: 10.1080/00275514.2024.2418784
Poppy Diver, Ben A Ward, Michael Cunliffe
Polymorphic yeasts can switch between unicellular division and multicellular filamentous growth. Although prevalent in aquatic ecosystems, such as the open ocean, we have a limited understanding of the controlling factors on their morphological variation in an aquatic ecology context. Here we show that substrate concentration regulates cell morphogenesis in a cosmopolitan polymorphic yeast, Aureobasidium pullulans, isolated from the pelagic open ocean and analyzed in liquid batch culture. Filamentous cell development was triggered only under high initial substrate conditions, suggesting that hyphal growth could be more advantageous under eutrophic conditions and may influence pelagic fungal interactions with particulate organic matter. Filamentous growth proportionally declined before the exhaustion of substrate and before budding yeast-type cell division entered stationary phase, possibly modulated by quorum sensing as previously evidenced in other polymorphic yeasts. We also found that budding yeast-type unicells decreased in size and became more elongated in shape in response to substrate depletion, resulting in higher cell surface area to volume ratios, which could affect yeast dispersal and/or provide a nutrient uptake advantage under oligotrophic conditions. Our results demonstrate resource-responsive morphological plasticity in a marine-derived polymorphic yeast, providing mechanistic insight into the ability of fungi to survive fluctuating environmental conditions such as in the open ocean.
{"title":"Cell morphological plasticity in response to substrate availability of a cosmopolitan polymorphic yeast from the open ocean.","authors":"Poppy Diver, Ben A Ward, Michael Cunliffe","doi":"10.1080/00275514.2024.2418784","DOIUrl":"https://doi.org/10.1080/00275514.2024.2418784","url":null,"abstract":"<p><p>Polymorphic yeasts can switch between unicellular division and multicellular filamentous growth. Although prevalent in aquatic ecosystems, such as the open ocean, we have a limited understanding of the controlling factors on their morphological variation in an aquatic ecology context. Here we show that substrate concentration regulates cell morphogenesis in a cosmopolitan polymorphic yeast, <i>Aureobasidium pullulans</i>, isolated from the pelagic open ocean and analyzed in liquid batch culture. Filamentous cell development was triggered only under high initial substrate conditions, suggesting that hyphal growth could be more advantageous under eutrophic conditions and may influence pelagic fungal interactions with particulate organic matter. Filamentous growth proportionally declined before the exhaustion of substrate and before budding yeast-type cell division entered stationary phase, possibly modulated by quorum sensing as previously evidenced in other polymorphic yeasts. We also found that budding yeast-type unicells decreased in size and became more elongated in shape in response to substrate depletion, resulting in higher cell surface area to volume ratios, which could affect yeast dispersal and/or provide a nutrient uptake advantage under oligotrophic conditions. Our results demonstrate resource-responsive morphological plasticity in a marine-derived polymorphic yeast, providing mechanistic insight into the ability of fungi to survive fluctuating environmental conditions such as in the open ocean.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-15"},"PeriodicalIF":2.6,"publicationDate":"2024-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142716581","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}
Pub Date : 2024-11-25DOI: 10.1080/00275514.2024.2418792
Hai D T Nguyen, Jeremy R Dettman, Scott A Redhead, Suzanne Gerdis, Kasia Dadej, Émilie D Tremblay, Julie Carey, Guillaume J Bilodeau, Sarah Hambleton
Some species of Tilletia are responsible for diseases in economically important crops, such as wheat and rice. In this study, we sequenced, assembled, and annotated 22 new genomes for Tilletia, with a focus on species causing dwarf bunt (DB; T. controversa), common bunt (CB; T. caries and T. laevis), and rice kernel smut (RKS; T. horrida). We present the first genomes for four other species (T. bromi, T. fusca, T. goloskokovii, and T. rugispora), resulting in the largest and most diverse sample of Tilletia genomes studied to date. Depending on the species and strain, the assembly size ranged from 24.3 to 30.5 Mb and gene prediction resulted in 7138 to 8261 gene models per genome. Phylogenomic analyses with hundreds to thousands of genes revealed significant support for the relationships among certain Tilletia taxa and validated findings of previous molecular studies that employed a small number of genes. Further population-level analyses showed two distinct populations of DB and CB: T. controversa (DB) as a single population and another intermixed population of T. caries and T. laevis (CB). No evidence of geographic isolation was observed within these populations. Our phylogenomic analyses also supported previous multigene hypotheses that multiple lineages of Tilletia may cause RKS. Collectively, our results suggest that taxonomic revisions are needed for the RKS-causing pathogens and provide convincing evidence for formally recognizing the CB-causing taxa as one species, named T. caries (synonym T. laevis). Overall, our study significantly enhances genomic resources for Tilletia, offers insights into phylogenetic relationships and population structure, and provides whole genome sequences for future studies.
一些 Tilletia 物种是小麦和水稻等重要经济作物的病害元凶。在这项研究中,我们对 22 个新的 Tilletia 基因组进行了测序、组装和注释,重点研究了导致矮花叶病(DB;T. controversa)、普通花叶病(CB;T. caries 和 T. laevis)和稻仁烟霉病(RKS;T. horrida)的物种。我们首次展示了其他四个物种(T. bromi、T. fusca、T. goloskokovii 和 T. rugispora)的基因组,这是迄今为止研究的最大、最多样化的 Tilletia 基因组样本。根据物种和品系的不同,组装大小从 24.3 到 30.5 Mb 不等,基因预测结果是每个基因组有 7138 到 8261 个基因模型。使用数百至数千个基因进行的系统发生组分析表明,某些 Tilletia 类群之间的关系得到了重要支持,并验证了之前使用少量基因进行的分子研究的结果。进一步的种群水平分析表明,DB 和 CB 有两个不同的种群:T. controversa(DB)是一个单一种群,另一个是 T. caries 和 T. laevis(CB)的混合种群。在这些种群中没有观察到地理隔离的证据。我们的系统发生组分析也支持之前的多基因假设,即 Tilletia 的多个品系可能会导致 RKS。总之,我们的研究结果表明,需要对引起 RKS 的病原体进行分类学修订,并为正式确认引起 CB 的类群为一个物种提供了令人信服的证据,该物种被命名为 T. caries(同义词 T. laevis)。总之,我们的研究极大地丰富了 Tilletia 的基因组资源,为系统发育关系和种群结构提供了见解,并为未来的研究提供了全基因组序列。
{"title":"Genome sequencing, phylogenomics, and population analyses of <i>Tilletia</i>, with recognition of one common bunt species, <i>T. caries</i> (synonym <i>T. laevis</i>), distinct from dwarf bunt, <i>T. controversa</i>.","authors":"Hai D T Nguyen, Jeremy R Dettman, Scott A Redhead, Suzanne Gerdis, Kasia Dadej, Émilie D Tremblay, Julie Carey, Guillaume J Bilodeau, Sarah Hambleton","doi":"10.1080/00275514.2024.2418792","DOIUrl":"https://doi.org/10.1080/00275514.2024.2418792","url":null,"abstract":"<p><p>Some species of <i>Tilletia</i> are responsible for diseases in economically important crops, such as wheat and rice. In this study, we sequenced, assembled, and annotated 22 new genomes for <i>Tilletia</i>, with a focus on species causing dwarf bunt (DB; <i>T. controversa</i>), common bunt (CB; <i>T. caries</i> and <i>T. laevis</i>), and rice kernel smut (RKS; <i>T. horrida</i>). We present the first genomes for four other species (<i>T. bromi, T. fusca, T. goloskokovii</i>, and <i>T. rugispora</i>), resulting in the largest and most diverse sample of <i>Tilletia</i> genomes studied to date. Depending on the species and strain, the assembly size ranged from 24.3 to 30.5 Mb and gene prediction resulted in 7138 to 8261 gene models per genome. Phylogenomic analyses with hundreds to thousands of genes revealed significant support for the relationships among certain <i>Tilletia</i> taxa and validated findings of previous molecular studies that employed a small number of genes. Further population-level analyses showed two distinct populations of DB and CB: <i>T. controversa</i> (DB) as a single population and another intermixed population of <i>T. caries</i> and <i>T. laevis</i> (CB). No evidence of geographic isolation was observed within these populations. Our phylogenomic analyses also supported previous multigene hypotheses that multiple lineages of <i>Tilletia</i> may cause RKS. Collectively, our results suggest that taxonomic revisions are needed for the RKS-causing pathogens and provide convincing evidence for formally recognizing the CB-causing taxa as one species, named <i>T. caries</i> (synonym <i>T. laevis</i>). Overall, our study significantly enhances genomic resources for <i>Tilletia</i>, offers insights into phylogenetic relationships and population structure, and provides whole genome sequences for future studies.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-16"},"PeriodicalIF":2.6,"publicationDate":"2024-11-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142716586","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}
Pub Date : 2024-11-11DOI: 10.1080/00275514.2024.2401320
Nourhene Grich, Thuan Huynh, Anna Kisiala, Daniel Palberg, R J Neil Emery
While a lot is known about cytokinins (CKs) and their actions at the molecular and cellular levels in plants, much less is known about the function of CKs in other kingdoms such as fungi. CKs have been detected in a wide range of fungal species where they play roles ranging from enhancing the virulence of phytopathogens to fortifying plant growth when secreted from fungal symbionts. However, the role of CKs where they concern fungal physiology, apart from plant associations, remains largely uncharacterized. Profiling by UHPLC-HRMS/MS (ultrahigh-performance liquid chromatography-high-resolution tandem mass spectrometry) revealed that Pleurotus ostreatus (oyster mushroom) produces CKs in vitro in both liquid and solid cultures. During fungal growth, CK profiling patterns were consistent with previous suggestions that tRNA degradation products might play a role in the physiological development of fungi. It confirms that those products are CKs that act as fungal growth regulators. Moreover, P. ostreatus was shown to respond to exogenous applications of aromatic and isoprenoid CKs, and their effects were dependent on the dose and CK type in a biphasic manner consistent with hormone action. N6-benzyladenine (BAP), kinetin (KIN), N6-isopentenyladenine (iP), and trans-zeatin (tZ) bioassays all revealed hormesis-type responses. Accordingly, at low doses, mycelium colony diameter, biomass accumulation, and changes in morphology were stimulated, whereas at high doses only inhibitory effects were observed. Thus, CKs may act as "mycohormones" and consequently have potential for applications in fungal agriculture and medicinal compound production.
虽然人们对细胞分裂素(CKs)及其在植物分子和细胞水平上的作用有很多了解,但对 CKs 在真菌等其他领域的功能却知之甚少。在多种真菌中都检测到了 CKs,它们的作用包括增强植物病原体的毒性,以及在真菌共生体分泌 CKs 时强化植物生长。然而,除了与植物的联系之外,CKs 在真菌生理方面的作用在很大程度上仍未得到描述。通过超高效液相色谱-高分辨串联质谱(UHPLC-HRMS/MS)分析发现,杏鲍菇在体外液体和固体培养物中都会产生 CKs。在真菌生长过程中,CK 分析模式与之前提出的 tRNA 降解产物可能在真菌生理发育过程中发挥作用的观点一致。研究证实,这些产物是作为真菌生长调节剂的 CK。此外,研究还表明,奥斯特真菌对外源芳香族和异戊烯类 CK 有反应,其作用与剂量和 CK 类型呈双相依赖,与激素作用一致。N6-苄基腺嘌呤(BAP)、激肽原(KIN)、N6-异戊烯基腺嘌呤(iP)和反式玉米素(tZ)生物测定均显示出激素类反应。因此,在低剂量时,菌丝菌落直径、生物量积累和形态变化都会受到刺激,而在高剂量时,只能观察到抑制作用。因此,CKs 可作为 "真菌激素 "发挥作用,从而有望应用于真菌农业和药用化合物生产。
{"title":"The biosynthesis and impacts of cytokinins on growth of the oyster mushroom, <i>Pleurotus ostreatus</i>.","authors":"Nourhene Grich, Thuan Huynh, Anna Kisiala, Daniel Palberg, R J Neil Emery","doi":"10.1080/00275514.2024.2401320","DOIUrl":"https://doi.org/10.1080/00275514.2024.2401320","url":null,"abstract":"<p><p>While a lot is known about cytokinins (CKs) and their actions at the molecular and cellular levels in plants, much less is known about the function of CKs in other kingdoms such as fungi. CKs have been detected in a wide range of fungal species where they play roles ranging from enhancing the virulence of phytopathogens to fortifying plant growth when secreted from fungal symbionts. However, the role of CKs where they concern fungal physiology, apart from plant associations, remains largely uncharacterized. Profiling by UHPLC-HRMS/MS (ultrahigh-performance liquid chromatography-high-resolution tandem mass spectrometry) revealed that <i>Pleurotus ostreatus</i> (oyster mushroom) produces CKs in vitro in both liquid and solid cultures. During fungal growth, CK profiling patterns were consistent with previous suggestions that tRNA degradation products might play a role in the physiological development of fungi. It confirms that those products are CKs that act as fungal growth regulators. Moreover, <i>P. ostreatus</i> was shown to respond to exogenous applications of aromatic and isoprenoid CKs, and their effects were dependent on the dose and CK type in a biphasic manner consistent with hormone action. <i>N</i><sup>6</sup>-benzyladenine (BAP), kinetin (KIN), <i>N</i><sup>6</sup>-isopentenyladenine (iP), and <i>trans</i>-zeatin (tZ) bioassays all revealed hormesis-type responses. Accordingly, at low doses, mycelium colony diameter, biomass accumulation, and changes in morphology were stimulated, whereas at high doses only inhibitory effects were observed. Thus, CKs may act as \"mycohormones\" and consequently have potential for applications in fungal agriculture and medicinal compound production.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-19"},"PeriodicalIF":2.6,"publicationDate":"2024-11-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142624093","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}
Pub Date : 2024-11-06DOI: 10.1080/00275514.2024.2399996
JinMei Ma, ZhiQin Wang, ZhiLi Yang, Tao Sun, ShiDao Yang, Hong Yu
Two species of Blackwellomyces (Clavicipitaceae, Hypocreales, Ascomycota) were discovered during an investigation of the diversity of entomopathogenic fungi. A new fungus and one known fungal species that were gathered from Yunnan Province were described in this study. Blackwellomyces changningensis, sp. nov. was described using morphology and phylogenetic evidence from 14 mitochondrial protein-coding gene (PCG) data sets (atp6, atp8, atp9, cob, cox1, cox2, cox3, nad1, nad2, nad3, nad4, nad5, nad6, and nad4L) and six nuclear genes (ITS [ITS4 and ITS5], 18S nuc rDNA [18S], 28S nuc rDNA [28S], tef1-α, rpb1, and rpb2). B. changningensis were found parasitic to Lepidoptera larvae and to produce filiform ascospores with septations. The asexual conidia were ovoid to ellipsoid in shape. Phylogenetic analysis and morphological observations concurred that the fungus belonged to a different species within the genus of Blackwellomyces. The foundation for further taxonomic, genetic, and evolutionary biological studies of the genus Blackwellomyces was laid by this work.
{"title":"Morphology, phylogeny, and mitogenomics reveal a new entomopathogenic fungus, <i>Blackwellomyces changningensis</i> (Hypocreales, Clavicipitaceae), from southwestern China.","authors":"JinMei Ma, ZhiQin Wang, ZhiLi Yang, Tao Sun, ShiDao Yang, Hong Yu","doi":"10.1080/00275514.2024.2399996","DOIUrl":"https://doi.org/10.1080/00275514.2024.2399996","url":null,"abstract":"<p><p>Two species of <i>Blackwellomyces</i> (Clavicipitaceae, Hypocreales, Ascomycota) were discovered during an investigation of the diversity of entomopathogenic fungi. A new fungus and one known fungal species that were gathered from Yunnan Province were described in this study. <i>Blackwellomyces changningensis</i>, sp. nov. was described using morphology and phylogenetic evidence from 14 mitochondrial protein-coding gene (PCG) data sets (<i>atp6, atp8, atp9, cob, cox1, cox2, cox3, nad1, nad2, nad3, nad4, nad5, nad6</i>, and <i>nad4L</i>) and six nuclear genes (ITS [ITS4 and ITS5], 18S nuc rDNA [18S], 28S nuc rDNA [28S], <i>tef1-α, rpb1</i>, and <i>rpb2</i>). <i>B. changningensis</i> were found parasitic to Lepidoptera larvae and to produce filiform ascospores with septations. The asexual conidia were ovoid to ellipsoid in shape. Phylogenetic analysis and morphological observations concurred that the fungus belonged to a different species within the genus of <i>Blackwellomyces</i>. The foundation for further taxonomic, genetic, and evolutionary biological studies of the genus <i>Blackwellomyces</i> was laid by this work.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-17"},"PeriodicalIF":2.6,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142591403","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}
Pub Date : 2024-11-05DOI: 10.1080/00275514.2024.2413343
Henrik F Gøtzsche, Bernard Woerly, Flavius Popa, Oleg N Shchepin, Ilya S Prikhodko, Ángela López-Villalba, Jan Woyzichovski, Lothar Krieglsteiner, Yuri K Novozhilov, Anja Klahr, Martin Schnittler
We describe a new species, Diacheopsis resinae (Myxomycetes), collected from a microhabitat new for myxomycetes: stem wounds of coniferous trees (Norway spruce) where the resin is overgrown with a community of resinicolous fungi. The 80 known collections come from the Vosges (France), the Black Forest (Germany), Swabian Alp (Germany), and several localities in Denmark and Norway. Observations, but as well as metabarcoding of substrate samples with fungal (ITS [internal transcribed spacer]), bacterial (16S rDNA), and myxomycete (18S nuc rDNA) primers from eight trunks, revealed the new myxomycete to co-occur with resin-degrading ascomycetes (Infundichalara microchona, Lophium arboricola, Zythia resinae). The gram-negative bacterial genera Endobacter and Sphingomonas were found to be abundant in the substrate and may be a food source for the myxomycete. Fruit bodies were found mostly during the more humid winter season, with a peak in January/February. Partial sequences of two independent molecular markers (18S nuc rDNA, EF1α [elongation factor 1-alpha] gene) were obtained for 41 accessions, which form a monophyletic cluster in a two-gene phylogeny of Stemonititidales but do not group with other species of Diacheopsis, thus rendering this genus paraphyletic. The new species, although exclusively developing sessile sporocarps and morphologically undoubtedly falling into the genus Diacheopsis, is most closely related to species of Lamproderma, especially L. album, L. zonatum, and L. zonatopulchellum. Within D. resinae, three groups can be differentiated, which show nearly complete reproductive isolation, as judged from a recombination analysis of the two unlinked markers and the allelic combinations of the EF1α gene.
{"title":"A new species of <i>Diacheopsis</i> (Myxomycetes) and a new habitat for myxomycetes.","authors":"Henrik F Gøtzsche, Bernard Woerly, Flavius Popa, Oleg N Shchepin, Ilya S Prikhodko, Ángela López-Villalba, Jan Woyzichovski, Lothar Krieglsteiner, Yuri K Novozhilov, Anja Klahr, Martin Schnittler","doi":"10.1080/00275514.2024.2413343","DOIUrl":"https://doi.org/10.1080/00275514.2024.2413343","url":null,"abstract":"<p><p>We describe a new species, <i>Diacheopsis resinae</i> (Myxomycetes), collected from a microhabitat new for myxomycetes: stem wounds of coniferous trees (Norway spruce) where the resin is overgrown with a community of resinicolous fungi. The 80 known collections come from the Vosges (France), the Black Forest (Germany), Swabian Alp (Germany), and several localities in Denmark and Norway. Observations, but as well as metabarcoding of substrate samples with fungal (ITS [internal transcribed spacer]), bacterial (16S rDNA), and myxomycete (18S nuc rDNA) primers from eight trunks, revealed the new myxomycete to co-occur with resin-degrading ascomycetes (<i>Infundichalara microchona, Lophium arboricola, Zythia resinae</i>). The gram-negative bacterial genera <i>Endobacter</i> and <i>Sphingomonas</i> were found to be abundant in the substrate and may be a food source for the myxomycete. Fruit bodies were found mostly during the more humid winter season, with a peak in January/February. Partial sequences of two independent molecular markers (18S nuc rDNA, <i>EF1α</i> [elongation factor 1-alpha] gene) were obtained for 41 accessions, which form a monophyletic cluster in a two-gene phylogeny of Stemonititidales but do not group with other species of <i>Diacheopsis</i>, thus rendering this genus paraphyletic. The new species, although exclusively developing sessile sporocarps and morphologically undoubtedly falling into the genus <i>Diacheopsis</i>, is most closely related to species of <i>Lamproderma</i>, especially <i>L. album, L. zonatum</i>, and <i>L. zonatopulchellum</i>. Within <i>D. resinae</i>, three groups can be differentiated, which show nearly complete reproductive isolation, as judged from a recombination analysis of the two unlinked markers and the allelic combinations of the <i>EF1α</i> gene.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-18"},"PeriodicalIF":2.6,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142583489","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}
Pub Date : 2024-11-04DOI: 10.1080/00275514.2024.2386230
Michael Bradshaw, Uwe Braun, James K Mitchell, Uma Crouch, Scott LaGreca, Donald H Pfister
This is the sixth contribution in a series devoted to the phylogeny and taxonomy of powdery mildews. This part includes our third treatment of the species of the genus Erysiphe. It continues the previous contribution on the phylogenetic-taxonomic assessment of the species belonging to the "Microsphaera lineage." Since this is a large lineage, we have split the treatment of the "Microsphaera lineage" into two parts. Phylogenetic trees based on rDNA are supplemented by sequences of additional markers (CAM, GAPDH, GS, RPB2, and TUB). The "Erysiphe trifoliorum complex" is a challenging group that belongs to the "Microsphaera lineage." Adequate clarification of this complex will be possible when additional worldwide multilocus sequence analyses are performed. The new species Erysiphe acetosae, E. acmisponis, E. lathyrina, E. salmoniana, and E. santalicola are described, and the new combinations E. biuncinata and E. pavoniae are introduced. Specimens of several species have been sequenced for the first time, particularly North American species, such as Erysiphe caryae, E. ceanothi, E. juglandis-nigrae, and E. ravenelii. Erysiphe syringae is lectotypified and 15 species names are epitypified in order to provide ex-epitype reference sequences. For other species, non-ex-type reference sequences are proposed for phylogenetic-taxonomic purposes. Ex-type sequences for Erysiphe baptisiicola, E. sesbaniae, Microsphaera sydowiana, M. umbilici, and Oidium pavoniae have been retrieved.
{"title":"Phylogeny and taxonomy of the genera of Erysiphaceae, part 6: <i>Erysiphe</i> (the \"<i>Microsphaera</i> lineage\" part 2).","authors":"Michael Bradshaw, Uwe Braun, James K Mitchell, Uma Crouch, Scott LaGreca, Donald H Pfister","doi":"10.1080/00275514.2024.2386230","DOIUrl":"https://doi.org/10.1080/00275514.2024.2386230","url":null,"abstract":"<p><p>This is the sixth contribution in a series devoted to the phylogeny and taxonomy of powdery mildews. This part includes our third treatment of the species of the genus <i>Erysiphe</i>. It continues the previous contribution on the phylogenetic-taxonomic assessment of the species belonging to the \"<i>Microsphaera</i> lineage.\" Since this is a large lineage, we have split the treatment of the \"<i>Microsphaera</i> lineage\" into two parts. Phylogenetic trees based on rDNA are supplemented by sequences of additional markers (<i>CAM, GAPDH, GS, RPB2</i>, and <i>TUB</i>). The \"<i>Erysiphe trifoliorum</i> complex\" is a challenging group that belongs to the \"<i>Microsphaera</i> lineage.\" Adequate clarification of this complex will be possible when additional worldwide multilocus sequence analyses are performed. The new species <i>Erysiphe acetosae, E. acmisponis, E. lathyrina, E. salmoniana</i>, and <i>E. santalicola</i> are described, and the new combinations <i>E. biuncinata</i> and <i>E. pavoniae</i> are introduced. Specimens of several species have been sequenced for the first time, particularly North American species, such as <i>Erysiphe caryae, E. ceanothi, E. juglandis-nigrae</i>, and <i>E. ravenelii. Erysiphe syringae</i> is lectotypified and 15 species names are epitypified in order to provide ex-epitype reference sequences. For other species, non-ex-type reference sequences are proposed for phylogenetic-taxonomic purposes. Ex-type sequences for <i>Erysiphe baptisiicola, E. sesbaniae, Microsphaera sydowiana, M. umbilici</i>, and <i>Oidium pavoniae</i> have been retrieved.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1-56"},"PeriodicalIF":2.6,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142575778","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}
Pub Date : 2024-11-01Epub Date: 2024-10-31DOI: 10.1080/00275514.2024.2407755
Alassane Sow, Benjamin Lemmond, Bryan Rennick, Judson Van Wyk, Lois Martin, Margaret Townsend, Arthur Grupe, Randolph Beaudry, Rosanne Healy, Matthew E Smith, Gregory Bonito
Ectomycorrhizal fungi in the genus Tuber form hypogeous fruiting bodies called truffles. Many Tuber species are highly prized due to their edible and aromatic ascomata. Historically, there has been attention on cultivating and selling European truffle species, but there is growing interest in cultivating, wild-harvesting, and selling species of truffles endemic to North America. North America has many endemic Tuber species that remain undescribed, including some that have favorable culinary qualities. Here, we describe two such Tuber species from eastern North America. Maximum likelihood and Bayesian phylogenetic analyses of ITS (internal transcribed spacer), tef1 (translation elongation factor 1-alpha), and rpb2 (second largest subunit of RNA polymerase II) sequences were used to place these species within a phylogenetic context. We coupled these data with morphological analyses and volatile analyses based on gas chromatography-mass spectrometry. Tuber cumberlandense, sp. nov. (previously referred to as Tuber sp. 66), is a member of the Rufum clade that has been opportunistically harvested for commercial sale from T. melanosporum orchards across eastern North America. Tuber canirevelatum, sp. nov. belongs in the Macrosporum clade and thus far is only known from eastern Tennessee, USA. Both new species were discovered with the assistance of trained truffle dogs. The volatile profiles of T. canirevelatum and T. cumberlandense were measured in order to characterize aromas based on the chemical compounds produced by these fungi. Ascomata from both species were enriched in acetone, dimethyl sulfide, 1-(methylthio)-1-propene, and 1-(methylthio)propane. In this work, we celebrate and encourage the use of trained truffle-hunting dogs for fungal biodiversity discovery and research.
块菌属的外生菌根真菌会形成被称为块菌的次生子实体。许多块菌物种因其可食用和芳香的子实体而备受推崇。历史上,人们一直关注欧洲松露品种的栽培和销售,但现在人们对北美特有松露品种的栽培、野生采摘和销售越来越感兴趣。北美洲有许多尚未被描述的特有块菌品种,包括一些具有良好烹饪品质的品种。在这里,我们描述了北美东部的两个这样的块菌物种。通过对 ITS(内部转录间隔)、tef1(翻译伸长因子 1-α)和 rpb2(RNA 聚合酶 II 的第二大亚基)序列进行最大似然法和贝叶斯系统发生学分析,将这些物种置于系统发生学背景中。我们将这些数据与形态分析和基于气相色谱-质谱法的挥发性分析相结合。Tuber cumberlandense,sp.nov.(以前称为 Tuber sp.66)是 Rufum 支系的一个成员,在北美东部的 T. melanosporum 果园中被伺机收获用于商业销售。Tuber canirevelatum,sp. nov.属于Macrosporum支系,目前仅产于美国田纳西州东部。这两个新物种都是在训练有素的松露犬的协助下发现的。对 T. canirevelatum 和 T. cumberlandense 的挥发性特征进行了测量,以便根据这些真菌产生的化学物质来确定香气的特征。这两种真菌的子囊都富含丙酮、二甲基硫醚、1-(甲硫基)-1-丙烯和 1-(甲硫基)丙烷。在这项工作中,我们赞扬并鼓励使用训练有素的松露猎犬来发现和研究真菌的生物多样性。
{"title":"<i>Tuber cumberlandense and T. canirevelatum</i>, two new edible <i>Tuber</i> species from eastern North America discovered by truffle-hunting dogs.","authors":"Alassane Sow, Benjamin Lemmond, Bryan Rennick, Judson Van Wyk, Lois Martin, Margaret Townsend, Arthur Grupe, Randolph Beaudry, Rosanne Healy, Matthew E Smith, Gregory Bonito","doi":"10.1080/00275514.2024.2407755","DOIUrl":"10.1080/00275514.2024.2407755","url":null,"abstract":"<p><p>Ectomycorrhizal fungi in the genus <i>Tuber</i> form hypogeous fruiting bodies called truffles. Many <i>Tuber</i> species are highly prized due to their edible and aromatic ascomata. Historically, there has been attention on cultivating and selling European truffle species, but there is growing interest in cultivating, wild-harvesting, and selling species of truffles endemic to North America. North America has many endemic <i>Tuber</i> species that remain undescribed, including some that have favorable culinary qualities. Here, we describe two such <i>Tuber</i> species from eastern North America. Maximum likelihood and Bayesian phylogenetic analyses of ITS (internal transcribed spacer), <i>tef1</i> (translation elongation factor 1-alpha), and <i>rpb2</i> (second largest subunit of RNA polymerase II) sequences were used to place these species within a phylogenetic context. We coupled these data with morphological analyses and volatile analyses based on gas chromatography-mass spectrometry. <i>Tuber cumberlandense</i>, sp. nov. (previously referred to as <i>Tuber</i> sp. 66), is a member of the Rufum clade that has been opportunistically harvested for commercial sale from <i>T. melanosporum</i> orchards across eastern North America. <i>Tuber canirevelatum</i>, sp. nov. belongs in the Macrosporum clade and thus far is only known from eastern Tennessee, USA. Both new species were discovered with the assistance of trained truffle dogs. The volatile profiles of <i>T. canirevelatum</i> and <i>T. cumberlandense</i> were measured in order to characterize aromas based on the chemical compounds produced by these fungi. Ascomata from both species were enriched in acetone, dimethyl sulfide, 1-(methylthio)-1-propene, and 1-(methylthio)propane. In this work, we celebrate and encourage the use of trained truffle-hunting dogs for fungal biodiversity discovery and research.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"949-964"},"PeriodicalIF":2.6,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142558273","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}
Pub Date : 2024-11-01Epub Date: 2024-10-18DOI: 10.1080/00275514.2024.2397932
Melissa Cravero, Gregory Bonito, Patrick S Chain, Saskia Bindschedler, Pilar Junier
Morchella helvetica, sp. nov. (Morchella sect. Distantes) is a new species of true morels discovered in Switzerland. It is formally described in the present study using an integrative approach based on micro- and macromorphological characteristics, multilocus phylogenetics, and a brief description of its habitat. Molecular analyses clearly indicated that Morchella helvetica is a sister species to M. eximioides, M. angusticeps, and M. confusa. It can be distinguished by the two phylogenetic markers RNA polymerase II subunit 2 (RPB2) and translation elongation factor-1 alpha (TEF1-α). In addition, M. helvetica exhibits particular morphological features, notably the presence of pale hairs on the pileus, a mealy stipe, and darkening ridges when aging.
Morchella helvetica,新种(Morchella sect.Distantes)是在瑞士发现的一种真正的羊肚菌新物种。本研究基于微观和宏观形态特征、多焦点系统发生学以及对其栖息地的简要描述,采用综合方法对其进行了正式描述。分子分析清楚地表明,Morchella helvetica 是 M. eximioides、M. angusticeps 和 M. confusa 的姐妹种。它可以通过 RNA 聚合酶 II 亚基 2(RPB2)和翻译延伸因子-1 α(TEF1-α)这两个系统发育标记来区分。此外,M. helvetica 还表现出特殊的形态特征,特别是绒毛上有浅色绒毛、蚧壳柄和老化时变黑的脊。
{"title":"A new species of true morel from Switzerland: <i>Morchella helvetica</i>, sp. nov.","authors":"Melissa Cravero, Gregory Bonito, Patrick S Chain, Saskia Bindschedler, Pilar Junier","doi":"10.1080/00275514.2024.2397932","DOIUrl":"10.1080/00275514.2024.2397932","url":null,"abstract":"<p><p><i>Morchella helvetica</i>, sp. nov. (<i>Morchella</i> sect. <i>Distantes</i>) is a new species of true morels discovered in Switzerland. It is formally described in the present study using an integrative approach based on micro- and macromorphological characteristics, multilocus phylogenetics, and a brief description of its habitat. Molecular analyses clearly indicated that <i>Morchella helvetica</i> is a sister species to <i>M. eximioides, M. angusticeps</i>, and <i>M. confusa</i>. It can be distinguished by the two phylogenetic markers RNA polymerase II subunit 2 (<i>RPB2</i>) and translation elongation factor-1 alpha <i>(TEF1-α</i>). In addition, <i>M. helvetica</i> exhibits particular morphological features, notably the presence of pale hairs on the pileus, a mealy stipe, and darkening ridges when aging.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1101-1109"},"PeriodicalIF":2.6,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142470220","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}
Pub Date : 2024-11-01Epub Date: 2024-08-19DOI: 10.1080/00275514.2024.2370198
Donald H Pfister, Katherine F LoBuglio, Michael Bradshaw, Renée Lebeuf, Andrus Voitk
Several members of the genus Peziza sensu stricto occur at the edge of melting snow. These nivicolous species have been widely reported in the Northern Hemisphere and are also known from Australia and New Zealand. We have used 16 specimens from North America and Australia to study morphology and to perform DNA sequencing. In sequence analyses, we have used ITS1 and ITS2 (internal transcribed spacers), 28S, RPB2 (RNA polymerase II gene), and two genes new to these studies, GAPDH (glyceraldehyde-3-phosphate dehydrogenase) and HSP90 (heat shock protein 90). Although not all regions are available for all samples, we have recognized the following species: Peziza heimii, P. nivalis, and P. nivis. Phylogenetic analyses were done using ITS alone; combined ITS1-5.8S-ITS2, 28S, and RPB2; ITS, and 28S, RPB2, GAPDH, and HSP90. Even with this augmented set of genes and despite their widespread occurrence in North America, Europe, Australia, and New Zealand, we have not definitively distinguished species within this group. To assess these results, pairwise homoplasy index (PHI) analysis was employed. This showed evidence of recombination among the samples of P. nivalis and further supports the view of P. nivalis as a monophyletic cosmopolitan species. As part of this study, we also examined the variation in ITS copies in P. echinospora, for which a genome is available.
严格意义上的 Peziza 属的几个成员出现在融雪边缘。这些裸子植物在北半球被广泛报道,在澳大利亚和新西兰也有发现。我们利用来自北美和澳大利亚的 16 个标本进行了形态学研究和 DNA 测序。在序列分析中,我们使用了 ITS1 和 ITS2(内部转录间隔)、28S、RPB2(RNA 聚合酶 II 基因)以及两个新基因,即 GAPDH(甘油醛-3-磷酸脱氢酶)和 HSP90(热休克蛋白 90)。虽然并非所有样本的所有区域都能找到,但我们已经确认了以下物种:Peziza heimii、P. nivalis 和 P. nivis。系统发育分析仅使用 ITS;联合使用 ITS1-5.8S-ITS2、28S 和 RPB2;ITS 以及 28S、RPB2、GAPDH 和 HSP90。即使使用了这组扩增基因,尽管它们广泛分布于北美、欧洲、澳大利亚和新西兰,我们仍未能明确区分出该类群中的物种。为了评估这些结果,我们采用了成对同源指数(PHI)分析。结果表明,在尼瓦尔河豚的样本中存在重组的证据,这进一步支持了尼瓦尔河豚作为单系世界性物种的观点。作为本研究的一部分,我们还研究了 P. echinospora 中 ITS 拷贝的变异情况,该物种的基因组已经获得。
{"title":"<i>Peziza nivalis</i> and relatives-spring fungi of wide distribution.","authors":"Donald H Pfister, Katherine F LoBuglio, Michael Bradshaw, Renée Lebeuf, Andrus Voitk","doi":"10.1080/00275514.2024.2370198","DOIUrl":"10.1080/00275514.2024.2370198","url":null,"abstract":"<p><p>Several members of the genus <i>Peziza</i> sensu stricto occur at the edge of melting snow. These nivicolous species have been widely reported in the Northern Hemisphere and are also known from Australia and New Zealand. We have used 16 specimens from North America and Australia to study morphology and to perform DNA sequencing. In sequence analyses, we have used ITS1 and ITS2 (internal transcribed spacers), 28S, <i>RPB2</i> (RNA polymerase II gene), and two genes new to these studies, <i>GAPDH</i> (glyceraldehyde-3-phosphate dehydrogenase) and <i>HSP90</i> (heat shock protein 90). Although not all regions are available for all samples, we have recognized the following species: <i>Peziza heimii, P. nivalis</i>, and <i>P. nivis</i>. Phylogenetic analyses were done using ITS alone; combined ITS1-5.8S-ITS2, 28S, and <i>RPB2</i>; ITS, and 28S, <i>RPB2, GAPDH</i>, and <i>HSP90</i>. Even with this augmented set of genes and despite their widespread occurrence in North America, Europe, Australia, and New Zealand, we have not definitively distinguished species within this group. To assess these results, pairwise homoplasy index (PHI) analysis was employed. This showed evidence of recombination among the samples of <i>P. nivalis</i> and further supports the view of <i>P. nivalis</i> as a monophyletic cosmopolitan species. As part of this study, we also examined the variation in ITS copies in <i>P. echinospora</i>, for which a genome is available.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"1019-1032"},"PeriodicalIF":2.6,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142004814","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}
Pub Date : 2024-11-01Epub Date: 2024-10-07DOI: 10.1080/00275514.2024.2395697
R Berndt, M A G Otálora, M Angulo, J C Zamora
This paper reports the South American rust fungi Puccinia modiolae and P. platyspora (Pucciniales/Uredinales) as new alien species of the European rust funga. Puccinia modiolae is presently known from Switzerland and Germany, P. platyspora from Switzerland, Germany, and France. The records of P. platyspora are the first ones from outside South America. The specimens were identified by teliospore characters and sequences of the nuclear ribosomal DNA (internal transcribed spacer 2 and domains D1-D2 of the nuclear ribosomal large subunit) and the mitochondrial CO3 (cytochrome c oxidase III) gene. Puccinia modiolae and P. platyspora have been recorded so far in Europe on members of the genera Alcea, predominantly on Alcea rosea, Althaea, and Malva of the Malvaceae, subfam. Malvoideae. Alcea rosea is host of both species and shared also with the common mallow rust, P. malvacearum, allowing for mixed infections. The plant is commonly grown as an ornamental and may play a major role for the spread of the alien Malvaceae rust fungi. It was observed for the first time that P. platyspora can produce spermogonia and aecidium-type aecia, suggesting phenotypic plasticity regarding the formation of spore states. The observed spermogonia mainly remained closed and did not liberate spermatia. They produced telio- and aeciospores besides spermatia in their cavity and eventually converted entirely into telia or, rarely, into aecidium-like sori. Small clusters of aeciospores and peridial cells were commonly found hidden in the telial plectenchyma, and well-developed aecidium-type aecia provided with a peridium developed rarely in the center of mature telia. Spermogonia belonging to group V type 4 were found in P. malvacearum, which is generally supposed to lack spermogonia. Some spermogonia produced only spermatia in their cavity; others formed spermatia and teliospores, and some eventually converted into telia.
本文报告了南美洲锈菌 Puccinia modiolae 和 P. platyspora(Pucciniales/Uredinales),它们是欧洲锈菌的外来新种。目前已知的 Puccinia modiolae 产自瑞士和德国,P. platyspora 产自瑞士、德国和法国。Platyspora 的记录是南美洲以外的首次记录。通过端孢子特征、核核糖体 DNA 序列(核核糖体大亚基内部转录间隔 2 和结构域 D1-D2)和线粒体 CO3(细胞色素 c 氧化酶 III)基因,对标本进行了鉴定。迄今为止,欧洲已记录到 Puccinia modiolae 和 P. platyspora 侵染茜草属植物,主要是蔷薇茜草属(Alcea rosea)、茜草属(Althaea)和锦葵亚科锦葵属(Malva)植物。Malvoideae.Alcea rosea 是这两个物种的寄主,也与常见的锦葵锈菌 P. malvacearum 共享,从而造成混合感染。这种植物通常作为观赏植物种植,可能对外来锦葵科锈菌的传播起到重要作用。首次观察到 P. platyspora 能产生精原细胞和纤毛虫型纤毛虫,这表明孢子的形成具有表型可塑性。观察到的精原细胞主要保持闭合状态,不释放精子。它们除了在腔内产生精子外,还产生端孢子和蜕皮孢子,并最终完全转化为端孢子,或在极少数情况下转化为水螅状的菌丝。在端孢子器的皮质中通常会发现小簇的无孢子细胞和包被细胞,而在成熟端孢子器的中心则很少发育出发育良好的带有包被的 "ecidium "型无孢子器。Malvacearum 中发现了属于第 V 组第 4 型的精原细胞,而一般认为它缺乏精原细胞。一些精原细胞在腔内只产生精子;其他精原细胞形成精子和端孢子,有些最终转化为端孢子。
{"title":"First European records of <i>Puccinia modiolae</i> and <i>P. platyspora</i>, two native South American rust fungi, and new observations on their life cycle and morphology.","authors":"R Berndt, M A G Otálora, M Angulo, J C Zamora","doi":"10.1080/00275514.2024.2395697","DOIUrl":"10.1080/00275514.2024.2395697","url":null,"abstract":"<p><p>This paper reports the South American rust fungi <i>Puccinia modiolae</i> and <i>P. platyspora</i> (Pucciniales/Uredinales) as new alien species of the European rust funga. <i>Puccinia modiolae</i> is presently known from Switzerland and Germany, <i>P. platyspora</i> from Switzerland, Germany, and France. The records of <i>P. platyspora</i> are the first ones from outside South America. The specimens were identified by teliospore characters and sequences of the nuclear ribosomal DNA (internal transcribed spacer 2 and domains D1-D2 of the nuclear ribosomal large subunit) and the mitochondrial <i>CO3</i> (cytochrome <i>c</i> oxidase III) gene. <i>Puccinia modiolae</i> and <i>P. platyspora</i> have been recorded so far in Europe on members of the genera <i>Alcea</i>, predominantly on <i>Alcea rosea, Althaea</i>, and <i>Malva</i> of the Malvaceae, subfam. Malvoideae. <i>Alcea rosea</i> is host of both species and shared also with the common mallow rust, <i>P. malvacearum</i>, allowing for mixed infections. The plant is commonly grown as an ornamental and may play a major role for the spread of the alien Malvaceae rust fungi. It was observed for the first time that <i>P. platyspora</i> can produce spermogonia and aecidium-type aecia, suggesting phenotypic plasticity regarding the formation of spore states. The observed spermogonia mainly remained closed and did not liberate spermatia. They produced telio- and aeciospores besides spermatia in their cavity and eventually converted entirely into telia or, rarely, into aecidium-like sori. Small clusters of aeciospores and peridial cells were commonly found hidden in the telial plectenchyma, and well-developed aecidium-type aecia provided with a peridium developed rarely in the center of mature telia. Spermogonia belonging to group V type 4 were found in <i>P. malvacearum</i>, which is generally supposed to lack spermogonia. Some spermogonia produced only spermatia in their cavity; others formed spermatia and teliospores, and some eventually converted into telia.</p>","PeriodicalId":18779,"journal":{"name":"Mycologia","volume":" ","pages":"915-935"},"PeriodicalIF":2.6,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142391851","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}