Symbiosis最新文献

{"title":"Fungal community structure in bees: influence of biome and host species","authors":"Wellington Fava Roque, James Moraes de Moura, Lorhaine Santos-Silva, Gilvan Ferreira da Silva, Lucas Amoroso Lopes de Carvalho, Daniel Guariz Pinheiro, Carmen Wobeto, Marcos Antônio Soares","doi":"10.1007/s13199-024-01012-3","DOIUrl":"https://doi.org/10.1007/s13199-024-01012-3","url":null,"abstract":"<p>Understanding the ecological relationship between fungi and insects is essential for elucidating interactions in biodiverse regions such as South American biomes. This study aimed to evaluate the influence of biome, host species, and microhabitat on the community structure of yeasts (using culture-dependent methods) and fungi (culture-independent methods) in bees and to identify the functional characteristics of isolated strains. Samples were collected from the body, hive, honey, and beebread of bees from the genera <i>Trigona</i>, <i>Scaptotrigona</i>, <i>Tetragona</i>, <i>Apis</i>, <i>Meliponas</i>, and <i>Tetragonisca</i> in the Pantanal, Amazon, and Cerrado biomes. We isolated 176 strains representing 46 yeast species, predominantly from the genera <i>Starmerella</i> (44.32%), <i>Hanseniaspora</i> (5.16%), and <i>Wickerhamiella</i> (4.38%). <i>Starmerella etchellsii</i> (32%) was the most abundant species, while <i>Aureobasidium leucospermi</i> (&lt; 0.01%) was the least abundant. Only <i>S. etchellsii</i> and <i>S. apicola</i> (11%) were present in all bee species. The composition and abundance of yeasts were significantly influenced by biome and host species (PERMANOVA, <i>p</i> &lt; 0.05). Alpha diversity varied significantly among microhabitats (Dunn’s <i>p</i> &lt; 0.05), bee species, and biomes (Duncan <i>p</i> &lt; 0.05). Culture-independent methods identified 234 Ascomycota ASVs, 18 Basidiomycota ASVs, and 1 Mucoromycete ASV across 90 genera and 108 species. Saccharomycetales accounted for approximately 72% of the fungal abundance, with <i>S. apicola</i> (14.64%) and <i>S. meliponinorum</i> (11.21%) being the most abundant. Additionally, barcoding identified 100 ASVs of plants associated with bees, grouped into 22 families and 24 species, predominantly Asteraceae, Anacardiacea, Elaeocarpaceae, and Solanaceae. The functional characteristics of the yeasts showed potential for industrial applications, varying according to the strain.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142256968","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The monodominant species Spirotropis longifolia is mainly nodulated by strains of the genus Bradyrhizobium outside the B. japonicum and B. elkanii superclades","authors":"Christine Le Roux, Emile Fonty, Laurent Brottier, Mathilde Bernard, Yves Prin, Daniel Sabatier","doi":"10.1007/s13199-024-01010-5","DOIUrl":"https://doi.org/10.1007/s13199-024-01010-5","url":null,"abstract":"<p><i>Spirotropis longifolia </i>(DC.) Baill. is organized in monodominant forest patches in French Guiana. <i>S. longifolia</i> root nodules and forest soil samples were collected in three monodominant populations of <i>S. longifolia</i> and in four zones, from the <i>S. longifolia</i> core dominance to the adjacent mixed forest where this species was absent. <i>S. longifolia</i> roots presented arbuscular mycorrhizal fungus (AMF) structures, but no ectomycorrhizae. The presence of myconodule-like structures was only noted once. Isolates of <i>S. longifolia</i> and of diverse French Guianese legume trees were 95% identified as <i>Bradyrhizobium</i> spp. and rarely as <i>Rhizobium</i> spp. On a partial 16S rDNA phylogenetic tree, <i>S. longifolia-</i>associated bradyrhizobia were positioned in a separate cluster including the <i>Bradyrhizobium</i> sp. Tv2a-2 strain isolated from <i>Tachigali versicolor</i> in Panama. Bradyrhizobia of other forest legume trees were positioned identically, or differently, in various clusters. A partial 16S-23S rDNA internal transcribed spacer (ITS) phylogenetic tree confirmed that the main cluster accounting for 82% of the direct or trapped bradyrhizobia associated with <i>S. longifolia</i> was situated outside the <i>B. japonicum</i> and <i>B. elkanii</i> superclades, in the Tv2a-2 superclade/Kakadu supergroup. In this cluster, other bradyrhizobia appeared that were associated with legumes from the tribes Ormosieae, Brongniartieae and Dalbergieae, suggesting the possibility of a shared pool of the most ancestral symbionts that are bradyrhizobia with the Caesalpinoid legumes and the early-branching Papilionoid legumes. Curiously, the seven monodominant Fabaceae of the Amazonian forests were exclusively part of these subfamilies. The link between ancestral symbiosis and monodominance still remains to be studied.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142256969","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The soil legacy produced by grass-endophyte-mycorrhizae fungi interaction increases legume establishment","authors":"A. Minás, P. A. García-Parisi, M. Omacini","doi":"10.1007/s13199-024-01009-y","DOIUrl":"https://doi.org/10.1007/s13199-024-01009-y","url":null,"abstract":"<h3 data-test=\"abstract-sub-heading\">Aims</h3><p>Plants alter the performance of other plants by changing soil conditions. These plant-soil feedback (PSF) can be shaped by plant interactions with other organisms and may be crucial for understanding plant coexistence. Here, we analyse how specialist and generalist symbionts change the legacy left in the soil by conspecific and heterospecific plants in the absence of pathogens and litter inputs.</p><h3 data-test=\"abstract-sub-heading\">Methods</h3><p>We conducted a two-phase experiment to evaluate <i>Trifolium repens</i> establishment and its ability to form symbiotic associations with AMF and rhizobia in soils conditioned by <i>Lolium multiflorum</i> plants with contrasting levels of endophyte infection (heterospecific soils: Lm⁺ or Lm⁻) and inoculated or not with AMF (M⁺ or M⁻). We also conditioned the soils with <i>T. repens</i> plants inoculated with rhizobia on M⁺ and M⁻ soils (conspecific soils: Tr).</p><h3 data-test=\"abstract-sub-heading\">Results</h3><p>In M- treatments, the number of established seedlings showed no difference between conspecific and heterospecific soils. In M + treatments, conditioned soils by Tr and Lm⁺ increased legume establishment by 64% compared to soils conditioned with Lm⁻. AMF colonization was higher in Tr and Lm + soils compared to Lm⁻. Regardless of AMF inoculation, legume biomass was higher in conspecific soils than in heterospecific ones, consistent with nodulation changes.</p><h3 data-test=\"abstract-sub-heading\">Conclusions</h3><p>We found that legume establishment depended significantly on the previous presence of heterospecific soils only when <i>L. multiflorum</i> was associated with <i>Epichloë</i> endophyte and AMF. The strength of PSF was determined by AMF inoculum, while the positive or negative nature of this effect was given by the level of endophyte infection. These findings unveil a new pathway by which these symbionts modulate the coexistence between legumes and grasses.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-08-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142226887","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Are the symbiont faunas of the venomous echinoids Toxopneustes pileolus and Tripneustes gratilla (Echinoidea, Toxopneustidae) similar?","authors":"P. Yu. Dgebuadze, O. A. Bratova, V. N. Ivanenko, N. T. H. Thanh, T. A. Britayev","doi":"10.1007/s13199-024-01008-z","DOIUrl":"https://doi.org/10.1007/s13199-024-01008-z","url":null,"abstract":"<p>The coexistence of taxonomically related hosts often leads to their infestation by the same symbiont species. This study tested the hypothesis that, despite the taxonomic proximity of the hosts, morphological differences have a predominant effect on the composition of their symbiont faunas. For this purpose, we studied the species composition, species richness and abundance of symbiont communities, associated with two tropical venomous echinoids <i>Toxopneustes pileolus</i> and <i>Tripneustes gratilla</i> (Toxopneustidae) and analyzed their symbiont specificity. Our results showed that 65.5% of <i>T. gratilla</i> and 91.0% of <i>T. pileolus</i> individuals were inhabited by symbionts. Both hosts harbored eleven species of obligate symbionts (polychaetes, gastropods, copepods, decapods and ophiuroids) all of them first recorded off the coast of Vietnam. Mean species richness was similar in both species, mean intensity were higher in <i>T. gratilla</i> than in <i>T. pileolus</i>, while the level of dominance was higher in <i>T. pileolus</i>. We find out that toxicity per se did not affect the composition of symbiont faunas; the symbiont fauna of <i>T. gratilla</i> is similar to that of taxonomically unrelated regular echinoids; whereas the symbiont fauna of <i>T. pileolus</i> is less diverse and more specific. We concluded that the depleted composition and specificity of of <i>T. pileolus</i> symbiont fauna are associated with its unique morphological feature – a cavity between the surface of the test and the canopy of pedicellariae, preventing the penetration of invaders onto the surface of the test and protecting their symbionts from predators.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-08-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141941634","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Microbiome diversity and composition across development stages of the Blue Orchard Bee, Osmia lignaria (Megachilidae)","authors":"Bailey L. Crowley, Robert N. Schaeffer","doi":"10.1007/s13199-024-01006-1","DOIUrl":"https://doi.org/10.1007/s13199-024-01006-1","url":null,"abstract":"<p>Host-associated microbes are increasingly recognized as important drivers of bee health. Surveys of bee microbiomes have primarily sampled social bees, yet non-social bees constitute the majority of species. We employed 16S and ITS amplicon sequencing to describe the diversity and composition of bacterial and fungal communities across multiple developmental stages of <i>Osmia lignaria</i>, an important native and managed solitary mason bee. Bacterial and fungal diversity were not significantly different across bee development. However, the composition of bacteria and fungi significantly changed between larval and fully pigmented adult stages, in agreement with dramatic changes in host morphology during metamorphosis. Many of the microbial taxa found in provisions were also present in larvae, indicating that immature bees likely acquire their microbiome from food. Notably, the most prevalent bacterial genus was <i>Arsenophonus</i>, a symbiont with many recorded phenotypes, ranging from reproductive parasitism to beneficial endosymbiont. <i>Arsenophonus</i> was found in samples from provisions and eggs, yet reached higher read counts in larvae and fully pigmented adults. The <i>Arsenophonus</i> amplicon sequencing variants (ASVs) detected in this study had high sequence similarity with a symbiont that displays the son-killing phenotype, suggesting that the ASVs in <i>O. lignaria</i> are also reproductive parasites. The causative agent of chalkbrood disease in bees, <i>Ascosphaera</i>, was also detected in provisions and larvae. Most other taxa present were plant pathogens or commonly found in soil. This study highlights that <i>O. lignaria</i> may harbor horizontally and vertically transmitted microbial taxa with diverse consequences for bee fitness.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-07-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141775717","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Microbial symbionts of hymenopteran parasitoids: an effective tool for next-generation crop protection","authors":"C. Deepak, H. C. Patel, H. K. Patel","doi":"10.1007/s13199-024-01002-5","DOIUrl":"https://doi.org/10.1007/s13199-024-01002-5","url":null,"abstract":"<p>Parasitoids, a distinct group of insects, rely on other insects for their offspring’s development, depositing their eggs within or atop a host insect, which is then consumed during the juvenile phase. These insects possess a wide array of microbial symbionts, including viruses, bacteria, and fungi. Unlike the symbionts in herbivorous and blood-feeding insects that supply nutrients, those associated with parasitoids are crucial for the reproduction of the parasitoid, the suppression of the host’s immune system, and the alteration of the host’s behaviour, including disrupting metamorphosis and affecting the metabolism of fats in herbivorous hosts. Additionally, recent research has shown that interactions between herbivores and parasitoids within plant-associated communities at different trophic levels can be influenced by parasitoid symbionts such polydnaviruses. This suggests that the role of these symbionts is significantly broader than previously understood. This review examines the influence of parasitoid symbionts on both direct and indirect interactions among species and its implications for the dynamics of ecological communities, particularly in terms of evolutionary processes and species interactions.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-07-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141718885","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Exploring the cooperation between nitrogen-fixing and non-fixing alfalfa rhizobia","authors":"S. Brambilla, K. Liebrenz, A. Odorizzi, V. Arolfo, Vanina Maguire, Valeria Moreno, Oscar Ruiz, Margarita Stritzler, Laura Serantes, Gabriela Soto, N. Ayub","doi":"10.1007/s13199-024-01007-0","DOIUrl":"https://doi.org/10.1007/s13199-024-01007-0","url":null,"abstract":"","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2024-07-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141647758","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Emerging diseases: trend research and omics-based analysis reveals mechanisms of endophytes modulate Chilli plant resilience","authors":"Wiwiek Harsonowati, Evy Latifah, Arinal Haq Izzawati Nurrahma, Jati Purwani, Rashid Iqbal, Javid Ahmad Parray, Ashish D. Patel","doi":"10.1007/s13199-024-01005-2","DOIUrl":"https://doi.org/10.1007/s13199-024-01005-2","url":null,"abstract":"<p>Chili pepper, widely recognized as a popular spice and an important cash crop worldwide, faces significant threats from climate change-related stress, particularly plant disease outbreaks. Emerging global diseases like Phytophthora blight, anthracnose fruit rot, and Ralstonia bacterial wilt threaten chili-producing countries, causing substantial annual yield losses. These major threatening diseases are difficult to control due to their widespread, extensive, and long-lived survival structures. Disease management practices rely on agrochemicals, leading to resistance to phytopathogens and environmental issues. Current research focuses on developing innovative, effective, chemical-free, and sustainable biosecurity strategies to address these challenges. Endophytes are plant endosymbionts that provide new insights for scientists due to their remarkable genome regulation to host plants. This review highlights the current state of emerging global diseases affecting chili pepper crops based on bibliometric analysis. We also focus on endophytes-mediated plant defense response as a sustainable solution for chemical pesticides. This review discusses the importance of omics-based technologies in deciphering the biochemical and molecular mechanisms of endophytes-mediated chili plant tolerance to various pathogens. A holistic approach of plant endophytes and multi-omics technologies can help develop effective mitigation strategies to prevent disease outbreaks for sustainable crop production and environmental restoration in the modern era of Agriculture 4.0 ‒ a green agricultural revolution.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-07-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141576799","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Bacterial consortia among Bradyrhizobium species, Azospirillum baldaniorum and Bacillus pumilus promote plant growth and efficient symbiotic nitrogen fixation in mung bean","authors":"Vicente Paulo da Costa Neto, Ana Raquel Pereira de Melo, Carla Elisa Sousa Alencar, Victor Breno Campelo de Lima, Jerri Edson Zilli, Artenisa Cerqueira Rodrigues, Aurenivia Bonifacio","doi":"10.1007/s13199-024-01003-4","DOIUrl":"https://doi.org/10.1007/s13199-024-01003-4","url":null,"abstract":"<p>The use of nitrogen-fixing bacteria in leguminous plants is a widespread approach, and the exploration of symbiotic bacteria that are efficient in biological nitrogen fixation (BNF) continues to be explored. The aim of the present study was to evaluate the effect of inoculation and coinoculation of mung bean plants with different combinations of <i>Bradyrhizobium</i> (<i>B. elkanii</i> BR 2003, <i>B. pachyrhizi</i> BR 3262, <i>B. yuanmingense</i> BR 3267, <i>B. paxllaeri</i> BR 10398 and <i>B. icense</i> BR 10399), <i>Azospirillum baldaniorum</i> (Sp245) and <i>Bacillus pumilus</i> (UFPEDA 472) on the contribution of biomass, the concentration of nitrogen (N) compounds and BNF. The experiment was carried out under greenhouse conditions with pots containing washed and autoclaved sand. Mung bean seeds were inoculated or coinoculated (double or triple) with <i>Bradyrhizobium</i>, <i>A. baldaniorum</i> and/or <i>Bacillus pumilus</i>, and one absolute control (not inoculated) was used. The experimental design was a completely randomized design with 21 treatments harvested in two different periods (flowering and pod maturation). Inoculation and coinoculation positively influenced the number of nodules, shoot dry weight, N accumulated, total N content and inorganic and organic compounds (free ammonia, nitrate, ureides and leghemoglobin), indicating that there was efficiency in BNF and synergistic interaction between the bacteria used and the mung bean plants. Inoculation with <i>Bradyrhizobium</i> species and the combination of these strains with <i>A. baldaniorum</i> and <i>Bacillus pumilus</i> positively influenced N fixation and metabolism in mung bean plants, especially when <i>B. elkanii</i> BR 2003 and <i>B. pachyrhizi</i> BR 3262 were used.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-07-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141576794","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Inoculation with native bacterial endophytes promote adventitious rooting and plant growth in Piper longum L.","authors":"Laccy Phurailatpam, Amrita Gupta, Pramod Kumar Sahu, Sushma Mishra","doi":"10.1007/s13199-024-01001-6","DOIUrl":"https://doi.org/10.1007/s13199-024-01001-6","url":null,"abstract":"<p><i>Piper longum</i>, the Indian long pepper, is widely used in Ayurvedic medicine system to cure respiratory and digestive disorders. In a previous study, we reported the isolation and characterization of plant growth promoting (PGP) endophytic bacteria from <i>P. longum.</i> Here, we have tested the effect of two native endophytic bacteria, <i>Acinetobacter soli</i> PlS14 and <i>Enterobacter hormaechei</i> PlR15, on growth attributes, adventitious root development and reactive oxygen species levels in <i>P. longum</i> PlR15. Our results indicate that stem cuttings treated with <i>A. soli</i> PlS14 and <i>E. hormaechei</i> PlR15 exhibited rooting in &gt; 50% of stem cuttings, when none of the Control cuttings did. Further, the endophyte-inoculated plants showed better vegetative growth (in terms of shoot growth and leaf number); higher levels of chlorophyll, proline and phenylalanine ammonia lyase; and lesser accumulation of reactive oxygen species than Control plants. The improved growth performance of endophyte-inoculated plants could be corelated with results of localization studies that indicate higher bacterial population in roots of endophyte-inoculated plants. To our knowledge, this is the first report of use of native endophytic strains as bioinoculants for growth of <i>P. longum</i>. Altogether, our results highlight the (often neglected) role of PGP native endophytes for cultivation of plants including medicinal plant species.</p>","PeriodicalId":22123,"journal":{"name":"Symbiosis","volume":null,"pages":null},"PeriodicalIF":2.5,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141502219","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}