MycorrhizaPub Date : 2024-07-01Epub Date: 2024-06-08DOI: 10.1007/s00572-024-01156-6
Damilola Olanipon, Margaux Boeraeve, Hans Jacquemyn
{"title":"Arbuscular mycorrhizal fungal diversity and potential association networks among African tropical forest trees.","authors":"Damilola Olanipon, Margaux Boeraeve, Hans Jacquemyn","doi":"10.1007/s00572-024-01156-6","DOIUrl":"10.1007/s00572-024-01156-6","url":null,"abstract":"<p><p>Tropical forests represent one of the most diverse and productive ecosystems on Earth. High productivity is sustained by efficient and rapid cycling of nutrients, which is in large part made possible by symbiotic associations between plants and mycorrhizal fungi. In these associations, an individual plant typically associates simultaneously with multiple fungi and the fungi associate with multiple plants, creating complex networks among fungi and plants. However, there are few studies that have investigated mycorrhizal fungal composition and diversity in tropical forest trees, particularly in Africa, or that assessed the structure of the network of associations among fungi and trees. In this study, we collected root and soil samples from Ise Forest Reserve (Southwest Nigeria) and used a metabarcoding approach to identify the dominant arbuscular mycorrhizal (AM) fungal taxa in the soil and associating with ten co-occurring tree species to assess variation in AM communities. Network analysis was used to elucidate the architecture of the network of associations between fungi and tree species. A total of 194 Operational Taxonomic Units (OTUs) belonging to six AM fungal families were identified, with 68% of all OTUs belonging to Glomeraceae. While AM fungal diversity did not differ among tree species, AM fungal community composition did. Network analyses showed that the network of associations was not significantly nested and showed a relatively low level of specialization (H<sub>2</sub> = 0.43) and modularity (M = 0.44). We conclude that, although there were some differences in AM fungal community composition, the studied tree species associate with a large number of AM fungi. Similarly, most AM fungi had great host breadth and were detected in most tree species, thereby potentially working as interaction network hubs.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"271-282"},"PeriodicalIF":3.3,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141293543","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}
MycorrhizaPub Date : 2024-07-01Epub Date: 2024-06-25DOI: 10.1007/s00572-024-01158-4
Ren-Cheng Liu, Wan-Rou Lin, Pi-Han Wang
{"title":"Exploring mycorrhizal diversity in sympatric mycoheterotrophic plants: a comparative study of Monotropastrum humile var. humile and M. humile var. glaberrimum.","authors":"Ren-Cheng Liu, Wan-Rou Lin, Pi-Han Wang","doi":"10.1007/s00572-024-01158-4","DOIUrl":"10.1007/s00572-024-01158-4","url":null,"abstract":"<p><p>Mycoheterotrophic plants (MHPs) rely on their mycorrhizal fungus for carbon and nutrient supply, thus a shift in mycobionts may play a crucial role in speciation. This study aims to explore the mycorrhizal diversity of two closely related and sympatric fully MHPs, Monotropastrum humile var. humile (Mhh) and M. humile var. glaberrimum (Mhg), and determine their mycorrhizal associations. A total of 1,108,710 and 1,119,071 ectomycorrhizal fungal reads were obtained from 31 Mhh and 31 Mhg, and these were finally assigned to 227 and 202 operational taxonomic units, respectively. Results show that sympatric Mhh and Mhg are predominantly associated with different fungal genera in Russulaceae. Mhh is consistently associated with members of Russula, whereas Mhg is associated with members of Lactarius. Associating with different mycobionts and limited sharing of fungal partners might reduce the competition and contribute to their coexistence. The ectomycorrhizal fungal communities are significantly different among the five forests in both Mhh and Mhg. The distinct mycorrhizal specificity between Mhh and Mhg suggests the possibility of different mycobionts triggered ecological speciation between sympatric species.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"283-292"},"PeriodicalIF":3.3,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141450932","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}
MycorrhizaPub Date : 2024-07-01Epub Date: 2024-06-29DOI: 10.1007/s00572-024-01159-3
Camille S Delavaux, Robert J Ramos, Sidney L Stürmer, James D Bever
{"title":"An updated LSU database and pipeline for environmental DNA identification of arbuscular mycorrhizal fungi.","authors":"Camille S Delavaux, Robert J Ramos, Sidney L Stürmer, James D Bever","doi":"10.1007/s00572-024-01159-3","DOIUrl":"10.1007/s00572-024-01159-3","url":null,"abstract":"<p><p>Recent work established a backbone reference tree and phylogenetic placement pipeline for identification of arbuscular mycorrhizal fungal (AMF) large subunit (LSU) rDNA environmental sequences. Our previously published pipeline allowed any environmental sequence to be identified as putative AMF or within one of the major families. Despite this contribution, difficulties in implementation of the pipeline remain. Here, we present an updated database and pipeline with (1) an expanded backbone tree to include four newly described genera and (2) several changes to improve ease and consistency of implementation. In particular, packages required for the pipeline are now installed as a single folder (conda environment) and the pipeline has been tested across three university computing clusters. This updated backbone tree and pipeline will enable broadened adoption by the community, advancing our understanding of these ubiquitous and ecologically important fungi.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"369-373"},"PeriodicalIF":3.3,"publicationDate":"2024-07-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11283431/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141476995","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
MycorrhizaPub Date : 2024-06-01Epub Date: 2024-05-03DOI: 10.1007/s00572-024-01146-8
Khalfallah F, Bon L, El Mazlouzi M, Bakker M R, Fanin N, Bellanger R, Bernier F, De Schrijver A, Ducatillon C, Fotelli M N, Gateble G, Gundale M J, Larsson M, Legout A, Mason W L, Nordin A, Smolander A, Spyroglou G, Vanguelova E I, Verheyen K, Vesterdal L, Zeller B, Augusto L, Derrien D, Buée M
{"title":"\"Ectomycorrhizal exploration type\" could be a functional trait explaining the spatial distribution of tree symbiotic fungi as a function of forest humus forms.","authors":"Khalfallah F, Bon L, El Mazlouzi M, Bakker M R, Fanin N, Bellanger R, Bernier F, De Schrijver A, Ducatillon C, Fotelli M N, Gateble G, Gundale M J, Larsson M, Legout A, Mason W L, Nordin A, Smolander A, Spyroglou G, Vanguelova E I, Verheyen K, Vesterdal L, Zeller B, Augusto L, Derrien D, Buée M","doi":"10.1007/s00572-024-01146-8","DOIUrl":"10.1007/s00572-024-01146-8","url":null,"abstract":"<p><p>In European forests, most tree species form symbioses with ectomycorrhizal (EM) and arbuscular mycorrhizal (AM) fungi. The EM fungi are classified into different morphological types based on the development and structure of their extraradical mycelium. These structures could be root extensions that help trees to acquire nutrients. However, the relationship between these morphological traits and functions involved in soil nutrient foraging is still under debate.We described the composition of mycorrhizal fungal communities under 23 tree species in a wide range of climates and humus forms in Europe and investigated the exploratory types of EM fungi. We assessed the response of this tree extended phenotype to humus forms, as an indicator of the functioning and quality of forest soils. We found a significant relationship between the relative proportion of the two broad categories of EM exploration types (short- or long-distance) and the humus form, showing a greater proportion of long-distance types in the least dynamic soils. As past land-use and host tree species are significant factors structuring fungal communities, we showed this relationship was modulated by host trait (gymnosperms versus angiosperms), soil depth and past land use (farmland or forest).We propose that this potential functional trait of EM fungi be used in future studies to improve predictive models of forest soil functioning and tree adaptation to environmental nutrient conditions.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"203-216"},"PeriodicalIF":3.9,"publicationDate":"2024-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140863519","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}
MycorrhizaPub Date : 2024-06-01Epub Date: 2024-05-18DOI: 10.1007/s00572-024-01151-x
Lior Herol, Mor Avidar, Shahar Yirmiahu, Yair Yehoshua Zach, Tamir Klein, Hagai Shemesh, Stav Livne-Luzon
{"title":"Context-dependent benefits of forest soil addition on Aleppo pine seedling performance under drought and grass competition.","authors":"Lior Herol, Mor Avidar, Shahar Yirmiahu, Yair Yehoshua Zach, Tamir Klein, Hagai Shemesh, Stav Livne-Luzon","doi":"10.1007/s00572-024-01151-x","DOIUrl":"10.1007/s00572-024-01151-x","url":null,"abstract":"<p><p>Seedling establishment under natural conditions is limited by numerous interacting factors. Here, we tested the combined effects of drought, herbaceous competition, and ectomycorrhizal inoculation on the performance of Aleppo pine seedlings grown in a net-house. The roots of all pine seedlings were strongly dominated by Geopora, a fungal genus known to colonize seedlings in dry habitats. Ectomycorrhizal fungi (EMF) inoculum significantly increased seedling height, biomass, and the number of side branches. However, under either competition or drought, the positive effect of EMF on seedling biomass and height was greatly reduced, while the effect on shoot branching was maintained. Further, under a combination of drought and competition, EMF had no influence on either plant growth or shape. The discrepancy in pine performance across treatments highlights the complexity of benefits provided to seedlings by EMF under ecologically relevant settings.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"217-227"},"PeriodicalIF":3.9,"publicationDate":"2024-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11166812/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140958547","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
MycorrhizaPub Date : 2024-06-01Epub Date: 2024-05-17DOI: 10.1007/s00572-024-01149-5
Patrick Neuberger, Carlos Romero, Keunbae Kim, Xiying Hao, Tim A McAllister, Skyler Ngo, Chunli Li, Monika A Gorzelak
{"title":"Biochar is colonized by select arbuscular mycorrhizal fungi in agricultural soils.","authors":"Patrick Neuberger, Carlos Romero, Keunbae Kim, Xiying Hao, Tim A McAllister, Skyler Ngo, Chunli Li, Monika A Gorzelak","doi":"10.1007/s00572-024-01149-5","DOIUrl":"10.1007/s00572-024-01149-5","url":null,"abstract":"<p><p>Arbuscular mycorrhizal fungi (AMF) colonize biochar in soils, yet the processes governing their colonization and growth in biochar are not well characterized. Biochar amendment improves soil health by increasing soil carbon, decreasing bulk density, and improving soil water retention, all of which can increase yield and alleviate environmental stress on crops. Biochar is often applied with nutrient addition, impacting mycorrhizal communities. To understand how mycorrhizas explore soils containing biochar, we buried packets of non-activated biochar in root exclusion mesh bags in contrasting agricultural soils. In this greenhouse experiment, with quinoa (Chenopodium quinoa) as the host plant, we tested impacts of mineral nutrient (as manure and fertilizer) and biochar addition on mycorrhizal colonization of biochar. Paraglomus appeared to dominate the biochar packets, and the community of AMF found in the biochar was a subset (12 of 18) of the virtual taxa detected in soil communities. We saw differences in AMF community composition between soils with different edaphic properties, and while nutrient addition shifted those communities, the shifts were inconsistent between soil types and did not significantly influence the observation that Paraglomus appeared to selectively colonize biochar. This observation may reflect differences in AMF traits, with Paraglomus previously identified only in soils (not in roots) pointing to predominately soil exploratory traits. Conversely, the absence of some AMF from the biochar implies either a reduced tendency to explore soils or an ability to avoid recalcitrant nutrient sources. Our results point to a selective colonization of biochar in agricultural soils.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"191-201"},"PeriodicalIF":3.9,"publicationDate":"2024-06-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11166811/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140958540","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
MycorrhizaPub Date : 2024-04-21DOI: 10.1007/s00572-024-01148-6
Neha Sharma, Ashwani Tapwal
{"title":"Mycorrhizal symbiosis in Taxus: a review","authors":"Neha Sharma, Ashwani Tapwal","doi":"10.1007/s00572-024-01148-6","DOIUrl":"https://doi.org/10.1007/s00572-024-01148-6","url":null,"abstract":"<p><i>Taxus</i>, a genus of conifers known for its medicinal significance, faces various conservation challenges with several species classified under different threat categories by the IUCN. The overharvesting of bark and leaves for the well-known chemotherapy drug paclitaxel has resulted in its population decline. Exploring the mycorrhizal relationship in <i>Taxus</i> is of utmost importance, as mycorrhizal fungi play pivotal roles in nutrition, growth, and ecological resilience. <i>Taxus</i> predominantly associates with arbuscular mycorrhizal fungi (AM), and reports suggest ectomycorrhizal (EM) or dual mycorrhizal associations as well. This review consolidates existing literature on mycorrhizal associations in <i>Taxus</i> species, focusing on structural, physiological, and molecular aspects. AM associations are well-documented in <i>Taxus</i>, influencing plant physiology and propagation. Conversely, EM associations remain relatively understudied, with limited evidence suggesting their occurrence. The review highlights the importance of further research to elucidate dual mycorrhizal associations in <i>Taxus</i>, emphasizing the need for detailed structural and physiological examinations to understand their impact on growth and survival.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":"120 1","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-04-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140636929","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}
MycorrhizaPub Date : 2024-04-17DOI: 10.1007/s00572-024-01145-9
Ryota Kusakabe, Moe Sasuga, Masahide Yamato
{"title":"Ubiquitous arbuscular mycorrhizal fungi in the roots of herbaceous understory plants with hyphal degeneration in Colchicaceae and Gentianaceae","authors":"Ryota Kusakabe, Moe Sasuga, Masahide Yamato","doi":"10.1007/s00572-024-01145-9","DOIUrl":"https://doi.org/10.1007/s00572-024-01145-9","url":null,"abstract":"<p>Due to the loss of photosynthetic ability during evolution, some plant species rely on mycorrhizal fungi for their carbon source, and this nutritional strategy is known as mycoheterotrophy. Mycoheterotrophic plants forming <i>Paris</i>-type arbuscular mycorrhizas (AM) exhibit two distinctive mycorrhizal features: degeneration of fungal materials and specialization towards particular fungal lineages. To explore the possibility that some understory AM plants show partial mycoheterotrophy, i.e., both photosynthetic and mycoheterotrophic nutritional strategies, we investigated 13 green herbaceous plant species collected from five Japanese temperate forests. Following microscopic observation, degenerated hyphal coils were observed in four species: two Colchicaceae species, <i>Disporum sessile</i> and <i>Disporum smilacinum</i>, and two Gentianaceae species, <i>Gentiana scabra</i> and <i>Swertia japonica</i>. Through amplicon sequencing, however, we found that all examined plant species exhibited no specificity toward AM fungi. Several AM fungi were consistently found across most sites and all plant species studied. Because previous studies reported the detection of these AM fungi from various tree species in Japanese temperate forests, our findings suggest the presence of ubiquitous AM fungi in forest ecosystems. If the understory plants showing fungal degeneration exhibit partial mycoheterotrophy, they may obtain carbon compounds indirectly from a wide range of surrounding plants utilizing such ubiquitous AM fungi.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":"69 1 1","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-04-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140612301","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}
{"title":"Bioprospecting for plant resilience to climate change: mycorrhizal symbionts of European and American beachgrass (Ammophila arenaria and Ammophila breviligulata) from maritime sand dunes","authors":"Arianna Grassi, Irene Pagliarani, Luciano Avio, Caterina Cristani, Federico Rossi, Alessandra Turrini, Manuela Giovannetti, Monica Agnolucci","doi":"10.1007/s00572-024-01144-w","DOIUrl":"https://doi.org/10.1007/s00572-024-01144-w","url":null,"abstract":"<p>Climate change and global warming have contributed to increase terrestrial drought, causing negative impacts on agricultural production. Drought stress may be addressed using novel agronomic practices and beneficial soil microorganisms, such as arbuscular mycorrhizal fungi (AMF), able to enhance plant use efficiency of soil resources and water and increase plant antioxidant defence systems. Specific traits functional to plant resilience improvement in dry conditions could have developed in AMF growing in association with xerophytic plants in maritime sand dunes, a drought-stressed and low-fertility environment. The most studied of such plants are European beachgrass (<i>Ammophila arenaria</i> Link), native to Europe and the Mediterranean basin, and American beachgrass (<i>Ammophila breviligulata</i> Fern.), found in North America. Given the critical role of AMF for the survival of these beachgrasses, knowledge of the composition of AMF communities colonizing their roots and rhizospheres and their distribution worldwide is fundamental for the location and isolation of native AMF as potential candidates to be tested for promoting crop growth and resilience under climate change. This review provides quantitative and qualitative data on the occurrence of AMF communities of <i>A. arenaria</i> and <i>A. breviligulata</i> growing in European, Mediterranean basin and North American maritime sand dunes, as detected by morphological studies, trap culture isolation and molecular methods, and reports on their symbiotic performance. Moreover, the review indicates the dominant AMF species associated with the two <i>Ammophila</i> species and the common species to be further studied to assess possible specific traits increasing their host plants resilience toward drought stress under climate change.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":"55 1","pages":""},"PeriodicalIF":3.9,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140603112","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}
MycorrhizaPub Date : 2024-04-01Epub Date: 2024-02-21DOI: 10.1007/s00572-024-01138-8
Takahiro Yagame, Tomáš Figura, Eiji Tanaka, Marc-André Selosse, Tomohisa Yukawa
{"title":"Mycobiont identity and light conditions affect belowground morphology and physiology of a mixotrophic orchid Cremastra variabilis (Orchidaceae).","authors":"Takahiro Yagame, Tomáš Figura, Eiji Tanaka, Marc-André Selosse, Tomohisa Yukawa","doi":"10.1007/s00572-024-01138-8","DOIUrl":"10.1007/s00572-024-01138-8","url":null,"abstract":"<p><p>We have investigated whether mycobiont identity and environmental conditions affect morphology and physiology of the chlorophyllous orchid: Cremastra variabilis. This species grows in a broad range of environmental conditions and associates with saprotrophic rhizoctonias including Tulasnellaceae and saprotrophic non-rhizoctonian fungi from the family Psathyrellaceae. We cultured the orchid from seeds under aseptic culture conditions and subsequently inoculated the individuals with either a Tulasnellaceae or a Psathyrellaceae isolate. We observed underground organ development of the inoculated C. variabilis plants and estimated their nutritional dependency on fungi using stable isotope abundance. Coralloid rhizome development was observed in all individuals inoculated with the Psathyrellaceae isolate, and 1-5 shoots per seedling grew from the tip of the coralloid rhizome. In contrast, individuals associated with the Tulasnellaceae isolate did not develop coralloid rhizomes, and only one shoot emerged per plantlet. In darkness, δ<sup>13</sup>C enrichment was significantly higher with both fungal isolates, whereas δ<sup>15</sup>N values were only significantly higher in plants associated with the Psathyrellaceae isolate. We conclude that C. variabilis changes its nutritional dependency on fungal symbionts depending on light availability and secondly that the identity of fungal symbiont influences the morphology of underground organs.</p>","PeriodicalId":18965,"journal":{"name":"Mycorrhiza","volume":" ","pages":"19-31"},"PeriodicalIF":3.9,"publicationDate":"2024-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139913054","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}