{"title":"Insights into the Differences in Polysaccharide and Alkaloid Biosynthesis in the Medicinal Orchids Dendrobium nobile and D. officinale.","authors":"Yu-Wen Zhang, Yu-Cen Shi, Wei Huang, Shi-Bao Zhang","doi":"10.1111/ppl.14575","DOIUrl":"https://doi.org/10.1111/ppl.14575","url":null,"abstract":"<p><p>Both Dendrobium nobile and D. officinale are widely used medicinal plants in China and their major medicinal components are alkaloids and polysaccharides, respectively. It is still unclear why these two closely related orchids synthesize and accumulate different chemical components. Here, we investigated the molecular mechanisms underlying polysaccharide and alkaloid biosynthesis in D. nobile and D. officinale through transcriptome and metabolomic analysis at different growth stages. A total of 1267 metabolites were identified in the juvenile and mature stages of the two species. D. nobile accumulated a large number of alkaloids, benzenoids/phenylpropanoids, flavonoids, and terpenoids during the transition from juvenile to mature plants. In contrast, D. officinale accumulated a small number of those metabolites and an absence of flavonoids. The correlation analysis of polysaccharide contents with the differentially expressed genes suggested that the differential expression of GH1, GH3, and GH9 might be related to the difference in polysaccharide contents between the two Dendrobium species. Meanwhile, the difference in the biosynthesis of dendrobine, the main component of alkaloids in D. nobile, was involved in the differential expression of HMGCR, DXR, DXS, ISPH and eight CYP450s. These findings provided new insights into understanding the biosynthetic mechanisms of the main medicinal components in Dendrobium species.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14575"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472480","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":"Elucidation of AsANS controlling pigment biosynthesis in Angelica sinensis through hormonal and transcriptomic analysis.","authors":"Khadija Tehseen Arshad, Chunfan Xiang, Chengxiao Yuan, Lesong Li, Juan Wang, Pinhan Zhou, Nazer Manzoor, Shengchao Yang, Mengfei Li, Yanli Liang, Junwen Chen, Yan Zhao","doi":"10.1111/ppl.14500","DOIUrl":"10.1111/ppl.14500","url":null,"abstract":"<p><p>Angelica sinensis, a traditional Chinese medicinal plant, has been primarily reported due to its nutritional value. Pigmentation in this plant is an important appearance trait that directly affects its commercial value. To understand the mechanism controlling purpleness in A. sinensis, hormonal and transcriptomic analyses were performed in three different tissues (leave, root and stem), using two cultivars with contrasting colors. The two-dimensional data set provides dynamic hormonal and gene expression networks underpinning purpleness in A. sinensis. We found abscisic acid as a crucial hormone modulating anthocyanin biosynthesis in A. sinensis. We further identified and validated 7 key genes involved in the anthocyanin biosynthesis pathway and found a specific module containing ANS as a hub gene in WGCNA. Overexpression of a candidate pigment regulatory gene, AsANS (AS08G02092), in transgenic calli of A. sinensis resulted in increased anthocyanin production and caused purpleness. Together, these analyses provide an important understanding of the molecular networks underlying A. sinensis anthocyanin production and its correlation with plant hormones, which can provide an important source for breeding.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14500"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142110903","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":"Enhancing wheat growth and nutrient content through integrated microbial and non-microbial biostimulants.","authors":"Devashish Pathak, Archna Suman, Anchal Dass, Pushpendra Sharma, Aswini Krishnan, Shrikant Gond","doi":"10.1111/ppl.14485","DOIUrl":"https://doi.org/10.1111/ppl.14485","url":null,"abstract":"<p><p>This study focused on two aspects: to develop a selected functionally competent bacterial community, and its integrated with biostimulant humic acid and seaweed extract which was validated to enhance wheat growth and nutrient content. Wheat and maize-associated bacterial isolates (92) were screened for Plant Growth-Promoting traits (PGPts-72) and Community-Forming traits (CFts-66). 46 isolates possessed both kinds of traits, of which 20 isolates were chosen based on high Bonitur scale ratings. Based on metabolic diversity, growth rate, and compatibility, 11 isolates were grouped to make a synthetic microbial community (SM). Non-microbial biostimulants, humic acid (HA) and seaweed extract (SWE) were used, and 0.2% HA and 1% SWE were found to be optimal for bacterial and plant growth. SM integrated each with 0.2% HA and 1% SWE, leading to products SynBio1 (SM + HA) and SynBio2 (SM + SWE). Under microcosm study, SynBio1 and SynBio2 improved germination by 90.10% and 83.80%, respectively. SynBio1 increased chlorophyll content by 40.5 SPAD units, root length by 15.7%, and shoot length by 18.4%. Field level validations revealed that SynBio1 increased plant height by 15.76%, root length by 27.16%, and flag leaf length by 21.35% compared to the control. The grain yield with SynBio1 was 40.41% higher than that of the control. Macro and micronutrient analysis of seeds treated with SynBio1 showed significant improvements. These findings demonstrate the potential of integrating microbial communities with biostimulants, and they pave the way for developing novel bioinoculants for sustainable agriculture and promoting a healthier environment.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14485"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142140805","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}
Sara Álvarez-Rodríguez, Biancamaria Senizza, Fabrizio Araniti, Luigi Lucini, Giorgio Lucchini, Adela M Sánchez-Moreiras
{"title":"Evaluating the effects of azelaic acid in the metabolism of Arabidopsis thaliana seedlings through untargeted metabolomics and ionomics approaches.","authors":"Sara Álvarez-Rodríguez, Biancamaria Senizza, Fabrizio Araniti, Luigi Lucini, Giorgio Lucchini, Adela M Sánchez-Moreiras","doi":"10.1111/ppl.14550","DOIUrl":"https://doi.org/10.1111/ppl.14550","url":null,"abstract":"<p><p>The present study demonstrates that low concentrations of azelaic acid (AZA) significantly impact the metabolism of Arabidopsis thaliana seedlings, leading to imbalances in numerous minerals and metabolites due to AZA-induced stress. Untargeted metabolomic analyses were conducted on untreated and AZA-treated seedlings at two time points: 7 and 14 days after treatment initiation. The results revealed a general accumulation of sugars (e.g., glucose, mannose, xylose), amino acids (e.g., lysine, GABA, threonine, glutamine), and organic acids (e.g., glutaric acid, shikimic acid, succinic acid) in AZA treated-seedlings, suggesting that AZA triggers stress responses in Arabidopsis. Ionomic analysis revealed that AZA induces phosphorus deficiency, which plants compensate by increasing malate content in the roots. Additionally, AZA treatment induced putrescine accumulation within the root, a metabolic biomarker of potassium deficiency and plant stress. The metabolomic profile showed elevated levels of different specialized metabolites, such as nitrogen- and sulphur-containing compounds, and altered levels of various phytohormones, including jasmonates and brassinosteroids, implicated in plant protection under biotic and/or abiotic stresses. These findings support the hypothesis that AZA's mode of action is associated with an auxin imbalance, suggesting its function as an auxinic herbicide. The observed increases in starch and jasmonates, coupled with the disruptions in potassium homeostasis, are linked to the previously reported alterations in the auxin transport, root architecture and gravitropic root response. Statistical analyses were applied, including Kruskal-Wallis tests for ionomic data, as well as multifactor analysis, Principal Component Analysis, Orthogonal Partial Least Squares-Discriminant Analysis, and enrichment pathway analysis for metabolomic data, ensuring the robustness and validity of these findings.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14550"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142352050","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":"Accelerating wheat improvement through trait characterization: advances and perspectives.","authors":"Rajib Roychowdhury, Arindam Ghatak, Manoj Kumar, Kajal Samantara, Wolfram Weckwerth, Palak Chaturvedi","doi":"10.1111/ppl.14544","DOIUrl":"https://doi.org/10.1111/ppl.14544","url":null,"abstract":"<p><p>Wheat (Triticum spp.) is a primary dietary staple food for humanity. Many wheat genetic resources with variable genomes have a record of domestication history and are widespread throughout the world. To develop elite wheat varieties, agronomical and stress-responsive trait characterization is foremost for evaluating existing germplasm to promote breeding. However, genomic complexity is one of the primary impediments to trait mining and characterization. Multiple reference genomes and cutting-edge technologies like haplotype mapping, genomic selection, precise gene editing tools, high-throughput phenotyping platforms, high-efficiency genetic transformation systems, and speed-breeding facilities are transforming wheat functional genomics research to understand the genomic diversity of polyploidy. This review focuses on the research achievements in wheat genomics, the available omics approaches, and bioinformatic resources developed in the past decades. Advances in genomics and system biology approaches are highlighted to circumvent bottlenecks in genomic and phenotypic selection, as well as gene transfer. In addition, we propose conducting precise functional genomic studies and developing sustainable breeding strategies for wheat. These developments in understanding wheat traits have speed up the creation of high-yielding, stress-resistant, and nutritionally enhanced wheat varieties, which will help in addressing global food security and agricultural sustainability in the era of climate change.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14544"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142368194","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":"Evidence for the translocation of fixed N in the N<sub>2</sub>-fixing lichen Stereocaulon vesuvianum.","authors":"Peter D Crittenden, Barry Thornton","doi":"10.1111/ppl.14555","DOIUrl":"https://doi.org/10.1111/ppl.14555","url":null,"abstract":"<p><p>The fruticose lichen Stereocaulon vesuvianum is among the most abundant and widespread lichens in upland Britain. It typically produces cephalodia (nodules) that contain the cyanobacterium Stigonema, which can fix atmospheric nitrogen. However, over much of England, Wales, and southern Scotland S. vesuvianum no longer produces cephalodia and does not fix nitrogen, a morphological change linked to elevated atmospheric nitrogen deposition. This provided a unique opportunity to compare the <sup>15</sup>N natural abundance signatures in N<sub>2</sub>-fixing and non-N<sub>2</sub>-fixing lichen populations, keeping in mind that fixed nitrogen has a <sup>15</sup>N content close to that of atmospheric N<sub>2</sub> while, in comparison, several components of atmospheric combined N (e.g. nitrate and ammonium in precipitation) tend to be <sup>15</sup>N depleted. We found that in N<sub>2</sub>-fixing samples, there was a steep gradient in <sup>15</sup>N relative abundance in the terminal 15 mm of thallus branches (pseudopodetia), changing from <sup>15</sup>N depleted tissues at 10-15 mm below the tips to values close to that of atmospheric N<sub>2</sub> at the apices while in non-N<sub>2</sub>-fixing samples thallus branches were uniformly <sup>15</sup>N depleted. The <sup>15</sup>N gradient in N<sub>2</sub>-fixing material could not be explained by the presence of cephalodia since these are more abundant towards branch bases. The data provide the first evidence in lichens of translocation of recently fixed N to sink regions of active growth and production of asexual reproductive propagules, bringing lichens into line with N source-sink relationships in N<sub>2</sub>-fixing plant symbioses.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14555"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142392497","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":"Instantaneous growth: a compact measure of efficient carbon and nitrogen allocation in leaves and roots of C<sub>3</sub> and C<sub>4</sub> plants.","authors":"Chandra Bellasio","doi":"10.1111/ppl.14535","DOIUrl":"https://doi.org/10.1111/ppl.14535","url":null,"abstract":"<p><p>Elucidating plant functions and identifying crop productivity bottlenecks requires the accurate quantification of their performance. This task has been attained through photosynthetic models. However, their traditional focus on the leaf's capacity to uptake CO<sub>2</sub> is becoming increasingly restrictive. Advanced bioengineering of C<sub>3</sub> plants has made it possible to increase rates of CO<sub>2</sub> assimilation by packing photosynthetic structures more densely within leaves. The operation of mechanisms that concentrate CO<sub>2</sub> inside leaves can boost rates of assimilation while requiring a lower investment in carboxylating enzymes. Therefore, whether in the context of spontaneous plants or modern manipulation, considering trade-offs in resource utilization efficiency emerges as a critical necessity. I've developed a concise and versatile analytical model that simulates concurrent leaf and root growth by balancing instantaneous fluxes of carbon and nitrogen. Carbon is made available by leaf photosynthesis, encompassing all types of biochemistries, while nitrogen is either taken up by roots or remobilized after senescence. The allocation of leaf nitrogen between light or carbon reactions was determined using a fitting algorithm: growth maximisation was the only reliable fitting goal. Both the leaf nitrogen pool and the root-to-leaf ratio responded realistically to various environmental drivers (CO<sub>2</sub> concentration, light intensity, soil nitrogen), replicating trends typically observed in plants. Furthermore, modifying the strength of CO<sub>2</sub> concentrating mechanisms proved sufficient to alter the root-to-leaf ratio between C<sub>3</sub> and C<sub>4</sub> types. This direct and mechanistic one-to-one link convincingly demonstrates, for the first time, the functional dependence of a morphological trait on a single biochemical property.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14535"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142472481","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":"Chromatic acclimation in cyanobacteria renders robust photosynthesis and fitness in dynamic light environment: Recent advances and future perspectives.","authors":"Soumila Mondal, Deepa Pandey, Shailendra P Singh","doi":"10.1111/ppl.14536","DOIUrl":"https://doi.org/10.1111/ppl.14536","url":null,"abstract":"<p><p>Cyanobacteria are photoautotrophic organisms that use light and water as a source of energy and electrons, respectively, to fix atmospheric carbon dioxide and release oxygen as a by-product during photosynthesis. However, photosynthesis and fitness of organisms are challenged by seasonal and diurnal fluctuations in light environments. Also, the distribution of cyanobacteria in a water column is subject to changes in the light regime. The quality and quantity of light change significantly in low and bright light environments that either limit photochemistry or result in photoinhibition due to an excess amount of light reaching reaction centers. Therefore, cyanobacteria have to adjust their light-harvesting machinery and cell morphology for the optimal harvesting of light. This adjustment of light-harvesting involves remodeling of the light-harvesting complex called phycobilisome or incorporation of chlorophyll molecules such as chlorophyll d and f into their light-harvesting machinery. Thus, photoacclimation responses of cyanobacteria at the level of pigment composition and cell morphology maximize their photosynthetic ability and fitness under a dynamic light environment. Cyanobacteria exhibit different types of photoacclimation responses that are commonly known as chromatic acclimation (CA). In this work, we discuss different types of CA reported in cyanobacteria and present a molecular mechanism of well-known type 3 CA where phycoerythrin and phycocyanin of phycobilisome changes according to light signals. We also include other aspects of type 3 CA that have been recently studied at a molecular level and highlight the importance of morphogenes, cytoskeleton, and carboxysome proteins. In summary, CA gives a unique competitive benefit to cyanobacteria by increasing their resource utilization ability and fitness.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14536"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142352049","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":"Network analysis of metabolomics, transcriptome and hormones reveals propionic acid-mediated novel survival strategy against drought in wheat.","authors":"Zongzhen Li, Yanhao Lian, Hui Guo, Chenxi Li, Yongzhe Ren, Zeyu Xin, Tongbao Lin, Zhiqiang Wang","doi":"10.1111/ppl.14551","DOIUrl":"https://doi.org/10.1111/ppl.14551","url":null,"abstract":"<p><p>Propionic acid (PA), a low-molecular-weight organic acid, is crucial to plant life metabolism. However, the regulatory mechanism of PA-mediated drought resistance in wheat remains largely unknown. Herein, we reported on a regulatory network of PA-mediated drought resistance in wheat using integrated transcriptome and metabolomics analysis and verified genes associated with drought resistance. Compared to the water-treated group, the application of PA alleviated the damage of drought by increasing plant water content, antioxidant enzyme activities and decreasing the malondialdehyde level (MDA). Transcriptome and metabolomics analysis revealed that PA triggered upregulation of key genes and metabolites, including TaBCAT, TaALDH6A1, TaALDH7A1, TaCHI, TaFLS, chrysin, and galangin, which were involved in valine, leucine and isoleucine degradation or flavonoid biosynthesis, respectively. In addition, the expression of genes encoding auxin-related transcription factors (TFs) strikingly increased, such as auxin/indoleacetic acid (AUX/IAA) and auxin response factor (ARF). Moreover, PA activated abscisic acid (ABA) and indole-3-acetic acid (IAA) signalling pathways. Taken together, our findings suggest that PA promotes energy metabolism and antioxidant activities to confer wheat drought resistance by introducing comprehensive and systemic effects of valine, leucine and isoleucine degradation flavonoid biosynthesis. Furthermore, activated AUX/IAA and ARF TFs might serve vital roles in drought resistance via modulating IAA signalling. This study provides novel insights into PA-mediated crop resistance and the improvement of the agroecological environment.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14551"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142352053","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}
María Ancín, David Soba, Pedro J Picazo, Angie L Gámez, Jean-François Le Page, Diane Houdusse, Iker Aranjuelo
{"title":"Optimizing oilseed rape growth: Exploring the effect of foliar biostimulants on the interplay among metabolism, phenology, and yield.","authors":"María Ancín, David Soba, Pedro J Picazo, Angie L Gámez, Jean-François Le Page, Diane Houdusse, Iker Aranjuelo","doi":"10.1111/ppl.14561","DOIUrl":"https://doi.org/10.1111/ppl.14561","url":null,"abstract":"<p><p>The current agricultural system is in search of new strategies to achieve a more sustainable production while keeping or even increasing crop yield and quality. In this scenario, the application of biostimulants constitutes a potent solution. In the current study, the impact of a blue-green microalgal extract (MB) and a pig tissue hydrolysate (PTH) on rapeseed plants' development was characterized. Obtained results revealed a positive effect on yield parameters of plants treated with MB and, especially, PTH; this was associated to an improvement on the photosynthetic performance. Moreover, this study remarked the effects of biostimulants on plant phenology through their pivotal role in modulating developmental processes. More specifically, proteomic, metabolomic, and hormone content analyses revealed distinct alterations associated with the acceleration of phenology induced by biostimulant application. Additionally, some antioxidant enzymes and stress-related compounds were up-regulated upon MB and PTH treatments, indicating enhanced plant defense mechanisms in response to accelerated phenological transitions. Such findings highlight the intricate interplay between biostimulants and plant physiology, wherein biostimulants orchestrate rapid developmental changes, ultimately influencing growth dynamics. Altogether, the current study reveals that the application of both MB and PTH biostimulants promoted rapeseed plant phenology and productivity associated with an improvement in the photosynthetic machinery while boosting other physiological and molecular mechanisms.</p>","PeriodicalId":20164,"journal":{"name":"Physiologia plantarum","volume":"176 5","pages":"e14561"},"PeriodicalIF":5.4,"publicationDate":"2024-09-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142372584","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}