Aquatic BotanyPub Date : 2024-09-04DOI: 10.1016/j.aquabot.2024.103811
Ye Liu , Yu Cao , Wei Li , Hongsheng Jiang , Jiwen Ge , Charity Mangoi , Qingxiang Han
{"title":"Integrated transcriptomic and metabolomic analysis reveals weak anti-feeding capability from submerged plant Ottelia alismoides to freshwater snails","authors":"Ye Liu , Yu Cao , Wei Li , Hongsheng Jiang , Jiwen Ge , Charity Mangoi , Qingxiang Han","doi":"10.1016/j.aquabot.2024.103811","DOIUrl":"10.1016/j.aquabot.2024.103811","url":null,"abstract":"<div><p>The direct grazing of herbivores on submerged macrophytes has long been recognized as an important contributor to macrophyte loss in shallow lakes. The defense mechanism of aquatic plants against grazing laid a theoretical basis for the conservation of endangered submerged macrophytes against habitat change. Here, we aim to explore the response of the endangered macrophyte <em>Ottelia alismoides</em> to direct grazing by the freshwater snails <em>Radix swinhoei</em> by using physiological, transcriptomic and metabolomic analyses. Based on field observation, we hypothesize that <em>O. alismoides</em> may not have an effective grazing resistance mechanism. Our 48-h microcosm study revealed 739 differentially expressed genes (DEGs) between the grazed treatment and the control. GO annotation analysis identified DEGs with molecular functions such as signaling receptor activity and various enzyme activities, as well as biological processes including auxin signaling, responses to oxidative stress, and salicylic acid. DEGs related to phytohormones (especially jasmonic acid, JA) and antioxidant enzymes were significantly up-regulated. In addition, the 20 metabolites changed significantly after being grazed. For example, the up-regulation of the JA biosynthetic pathway led to a marginal increase of the JA content in leaves, and its signal transduction pathway was also up-regulated, consistent with that the precursor of secondary metabolism of flavonoids was up-regulated and that the transcriptome biosynthesis pathway of flavonoids was also up-regulated. Though evident defensive steps were found at the aspects of transcriptome and metabolome, leaf intactness and the photosynthetic parameters in the leaves were strongly negatively affected by snail grazing. We argued that the efficiency of those defensive strategies has probably been compromised due to the degenerative secondary metabolism in submerged leaves. Thus, to protect endangered submerged macrophytes, countermeasures for herbivory should be considered along with other important policies.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"196 ","pages":"Article 103811"},"PeriodicalIF":1.9,"publicationDate":"2024-09-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0304377024000639/pdfft?md5=87782e44edce278ad38f041a101ecc42&pid=1-s2.0-S0304377024000639-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142150506","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-08-24DOI: 10.1016/j.aquabot.2024.103809
Hélène Groffier , Mohamed A. Mahdjoub , Simon Devin , Elisabeth M. Gross
{"title":"Impact of dye treatment as management strategy on available light may favour a highly invasive alien aquatic plant","authors":"Hélène Groffier , Mohamed A. Mahdjoub , Simon Devin , Elisabeth M. Gross","doi":"10.1016/j.aquabot.2024.103809","DOIUrl":"10.1016/j.aquabot.2024.103809","url":null,"abstract":"<div><p>Attempts to control massive proliferations of invasive alien aquatic plants (IAAP) are often ineffective. A renewed interest for dye treatment is emerging aiming to control the submerged macrophyte <em>Myriophyllum heterophyllum</em> in France. We aimed to understand the effects of dye on this plant knowing about its adaptation to low light. In a 2 × 2 factorial design experiment, we assessed the effect of a dye mixture based on Brilliant Blue (E133) and Allura Red (E129) at high and low light intensities on light quantity and quality and how this might affect the plant’s performance by measuring morphological and physiological traits. A multivariate analysis identified three groups – high light (HL) plants, plants in high light with dye (HLD) or low light (LL), and low light with dye (LLD) plants. HL plants performed well but showed stress signs, with a reduced main shoot length, a higher leaf dry matter content (LDMC) and a lower nitrogen content (N), not observed in plants grown in HLD or LL. HLD and LL plants exhibited a comparable total length growth rate to those in HL, but had lower LDMC and higher N contents. LLD plants performed poorly with the lowest growth and signs of physiological stress. Dye-induced changes in light quality only marginally affected the absorbance range of chlorophyll <em>b</em>, which apparently did not affect photosynthesis. Commercially available dyes currently used to control nuisance aquatic plants thus seem to have little or no effect on submerged macrophytes. The presence of dye may exacerbate negative effects of very low light intensities on the plant’s growth. However, these very low intensities would only be reached during high-water levels or in winter, periods where the dye would rapidly be diluted. During summer, however, the application of dye may protect the plant from damaging light intensities and thus not be a good management strategy to control low light adapted invasive submerged macrophytes.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103809"},"PeriodicalIF":1.9,"publicationDate":"2024-08-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0304377024000615/pdfft?md5=4aa6d89575bdffbfb26528c65361c1b4&pid=1-s2.0-S0304377024000615-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142089490","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Molecular evidence for the origin of the little-known hybrid Potamogeton ×vilnensis","authors":"Zofija Sinkevičienė , Donatas Naugžemys , Jurgita Butkuvienė","doi":"10.1016/j.aquabot.2024.103808","DOIUrl":"10.1016/j.aquabot.2024.103808","url":null,"abstract":"<div><p>A combined study of morphology, stem anatomy, and the genetic markers (ITS1-ITS4 region of nuclear ribosomal DNA and <em>rpl</em>20-<em>rps</em>12 intergenic spacer of chloroplast DNA) was used to verify the identity of hybrid <em>Potamogeton</em> ×<em>vilnensis</em> Galinis previously recognized as <em>P. gramineus</em> × <em>P. praelongus</em>. Authentic herbarium material and newly collected specimens morphologically similar to the hybrid from the locus classicus (SE Lithuania) were used for comparative morphological, anatomical and molecular analyses. The study proved the paternity of <em>P. lucens</em> and <em>P. praelongus</em> and excluded the involvement of <em>P. gramineus</em> in hybridization and identity with <em>P.</em> ×<em>angustifolius</em>. This hybrid formula is shared with plants recorded in the Czech Republic and Denmark under the name <em>P.</em> ×<em>jutlandicus</em> Zalewska-Galosz. The site in Lithuania, known since 1961, is the first natural habitat of long-lived hybrid between <em>P. lucens</em> and <em>P. praelongus</em> whose origin has been confirmed by molecular markers. The scarce records of this taxon indicate that the knowledge of the hybrid species of <em>Potamogeton</em> and their distribution is insufficient and that more extensive regional studies, including molecular methods, are needed.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103808"},"PeriodicalIF":1.9,"publicationDate":"2024-08-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142083160","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-08-22DOI: 10.1016/j.aquabot.2024.103810
Yutong He , Lizhi Zhu , Jiayu Sun , Yuxin Chen , Yu Cao
{"title":"High density promotes the germination of the recalcitrant seeds of submerged macrophyte Vallisneria natans","authors":"Yutong He , Lizhi Zhu , Jiayu Sun , Yuxin Chen , Yu Cao","doi":"10.1016/j.aquabot.2024.103810","DOIUrl":"10.1016/j.aquabot.2024.103810","url":null,"abstract":"<div><p>Seed germination is a critical process in the seed life cycle, especially for annual submerged macrophytes <em>Vallisneria natans</em> which is a model species for the restoration of degraded shallow lakes. Fresh seeds of <em>V. natans</em> have a very high germination rate but with no significant responses to the aggregation effect; meanwhile, these recalcitrant seeds quickly lose seed viability under dry storage. This study aims to explore the response of seed germination of <em>V. natans</em> after dry storage to aggregation effect by several microcosm experiments. We observed that seed aggregation has a significant positive effect on germination, and among the seven experimental densities between 10 ∼ 640 seeds, higher seed densities resulted in significantly enhanced germination. In contrast, daily removal of germinated seeds led to a significant decrease in the overall germination rate, suggesting that germinated seeds may secrete chemicals that promote the germination of ungerminated seeds. However, further experiments indicated that ethylene and gibberellins had no noticeable impact on seed germination, which was consistent with additional experiment results from spectrophotometer and high-throughput targeted metabolomics. We concluded that the promoting effect of aggregation on the seed germination of <em>V. natans</em> may be an adaptation of this species to its natural habitat but detailed mechanisms warranted further study.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103810"},"PeriodicalIF":1.9,"publicationDate":"2024-08-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142048391","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"First record of Ruppia brevipedunculata in Indonesia","authors":"Fery Kurniawan , Akbar Ario Digdo , Robba Fahrisy Darus , Nurlita Putri Anggraini , Meutia Samira Ismet , Pramaditya Wicaksono , Wawan Kiswara","doi":"10.1016/j.aquabot.2024.103806","DOIUrl":"10.1016/j.aquabot.2024.103806","url":null,"abstract":"<div><p>This paper presents the first records of the seagrass species <em>Ruppia brevipedunculata</em> Shuo Yu & den Hartog in Indonesia, which has never been reported before. <em>R. brevipedunculata</em> from a coastal lagoon was identified based on morphological characters and phylogenetics. Indonesian <em>R. brevipedunculata</em> had four carpels and a short peduncle. These differentiated from <em>R. maritima</em>. A phylogenetic analysis of ITS and matK demonstrated the same cluster as <em>R. brevipedunculata.</em> That was clearly shown by the matK gene-marker. Biodiversity exploration and conservation efforts are needed to protect and preserve <em>R. brevipedunculata</em> and its habitat.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103806"},"PeriodicalIF":1.9,"publicationDate":"2024-08-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142041285","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-08-08DOI: 10.1016/j.aquabot.2024.103805
Alyson Lowell , Claudia E.L. Hill , Sam Dupont , Eduardo Infantes , Kirti Ramesh , Bradley Peterson , Laura L. Govers , T. Erin Cox
{"title":"Low pH enhances germination of eelgrass (Zostera marina L.) seeds despite ubiquitous presence of Phytophthora gemini","authors":"Alyson Lowell , Claudia E.L. Hill , Sam Dupont , Eduardo Infantes , Kirti Ramesh , Bradley Peterson , Laura L. Govers , T. Erin Cox","doi":"10.1016/j.aquabot.2024.103805","DOIUrl":"10.1016/j.aquabot.2024.103805","url":null,"abstract":"<div><p>Seagrasses are foundation species in coastal ecosystems promoting biodiversity and community structure. Future marine carbonate chemistry under ocean acidification may enhance seagrass physiology, but little is known about how reproductive ecology and disease will integrate into future ocean conditions. A novel pathogen, <em>Phytophthora gemini</em>, infects >90 % of eelgrass, <em>Zostera marina,</em> surveyed in Northern Atlantic and Mediterranean populations reducing annual germination 6-fold<em>.</em> Our study investigated the combined effects of ocean acidification and <em>P. gemini</em> infection on germination of eelgrass seeds. We conducted a two-level factorial experiment crossing four pH levels (∆0, - ∆0.3, - ∆0.6, -∆0.9; relative to the average pH at the sampling site) with three infection levels (infected, non-infected, exposed) to determine germination rate and infection response. Prior to experimentation, flowering shoots were collected and held in flow-through seawater tanks where seeds ripened naturally. Once collected, seeds were held in copper sulfate solution (27.37 ± 1.57 ppt) and stored in darkness to mimic winter dormancy (4 °C). Before the start of the experiment, viable seeds were cultured on oomycete selective growth media to determine infection status. By the end of the experiment, 100 % of tested seeds, regardless of treatment, contained <em>P. gemini</em>. Germination rate significantly increased with decreased pH. Our findings indicate that <em>P. gemini</em> is not inhibited by ecologically relevant changes to carbonate chemistry and standard handling practices can result in effective and highly virulent disease transmission. These results confirm perennial populations of eelgrass are susceptible to infection and alerts conservationists to additional considerations necessary for successful eelgrass restoration.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103805"},"PeriodicalIF":1.9,"publicationDate":"2024-08-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141998153","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-07-26DOI: 10.1016/j.aquabot.2024.103803
Nathan E. Harms , Matthew Purcell , Sun-hee Hong , Sonja Stutz , Jialiang Zhang , Megann Harlow , Chenxi Liu , Nicholas P. Tippery
{"title":"Native and invaded-range surveys provide mixed support for enemy-release of Nymphoides peltata in the invaded range","authors":"Nathan E. Harms , Matthew Purcell , Sun-hee Hong , Sonja Stutz , Jialiang Zhang , Megann Harlow , Chenxi Liu , Nicholas P. Tippery","doi":"10.1016/j.aquabot.2024.103803","DOIUrl":"10.1016/j.aquabot.2024.103803","url":null,"abstract":"<div><p>Natural or anthropogenic movement of plant species outside their historical ranges may result in exposure to new environmental conditions and a lack of natural enemies, thus promoting their establishment and spread into new areas. A biogeographical comparison of native and invasive populations can provide insight into the mechanisms of successful invasions and guide effective management strategies, such as biological control, by targeting plant traits that promote invasiveness. We studied the Eurasian aquatic plant, <em>Nymphoides peltata</em>, <em>in situ</em> in the native (China, Korea) and invaded (USA) ranges to determine whether there were differences in natural enemy attack rates (percent leaf damage, frequency of leaf herbivory or disease), productivity (plant cover, reproduction), and leaf traits (leaf elemental content, leaf toughness, dry matter content, specific leaf area) between areas. We also investigated whether there was evidence of a tradeoff between natural enemy attack and growth or reproduction, as would be predicted by invasion theory. Plant cover (23–29 % higher) and reproductive output (eight times more seeds / m<sup>2</sup>) were consistently higher in the invaded range. Leaf traits consistently differed between ranges, which we would expect if plants in the invaded range had fewer herbivores or other pests. The amount of leaf damage present was similar between ranges, but the frequency of herbivory was 50 % greater, on average, in the native than invaded range. Although we did not quantify suppression of <em>N. peltata</em> by natural enemies, we found evidence of more frequent herbivory in Asia and reduced reproduction and plant cover compared to the USA, which supports further investigation into viability of biological controls.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103803"},"PeriodicalIF":1.9,"publicationDate":"2024-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141935488","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-07-26DOI: 10.1016/j.aquabot.2024.103804
Xiaolong Huang , Jing Lu , Hu He , Baohua Guan , Jing Luo , Jinlei Yu , Zhigang Mao , Kuanyi Li , Erik Jeppesen
{"title":"Eurasian watermilfoil (Myriophyllum spicatum) alters its root topology but conserves its root branching in response to freshwater cultural eutrophication","authors":"Xiaolong Huang , Jing Lu , Hu He , Baohua Guan , Jing Luo , Jinlei Yu , Zhigang Mao , Kuanyi Li , Erik Jeppesen","doi":"10.1016/j.aquabot.2024.103804","DOIUrl":"10.1016/j.aquabot.2024.103804","url":null,"abstract":"<div><p>Cultural eutrophication is the main cause of the decline of submerged plants in freshwater ecosystems. While many studies have focused on the nutrient uptake by the roots of these plants, less attention has been given to the effects of eutrophication on root structure. We designed a mesocosm experiment with Eurasian watermilfoil (<em>Myriophyllum spicatum</em>), a submerged plant indigenous to the Eurasian continent. The responses of plant functional traits, including growth traits, morphological traits and root topological indices, to different nitrogen (N) and phosphorus (P) concentrations were elucidated. We found that high P concentrations suppressed all the morphological traits and reduced the root topological traits, whereas N concentrations had a comparatively minor effect. Although the root branching of <em>M. spicatum</em> did not change, its root topology became more dichotomous with fewer exterior root links being formed in nutrient-rich habitats, and the root form changed from deep and thin to shallow and dense with increasing P concentrations. The root nutrient absorption ability of <em>M. spicatum</em> may decrease with cultural eutrophication, and this change most likely reduces its anchoring ability and increases its sensitivity to dislodge from the sediment if disturbed by hydraulic forces.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103804"},"PeriodicalIF":1.9,"publicationDate":"2024-07-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141935489","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-07-20DOI: 10.1016/j.aquabot.2024.103793
Teresa Cerqueira , Artur M.L. Oliveira , Marco F.L. Lemos
{"title":"DNA barcoding and phylogenetic relationships of ecologically and commercially important seaweed species from the Azores (NE Atlantic)","authors":"Teresa Cerqueira , Artur M.L. Oliveira , Marco F.L. Lemos","doi":"10.1016/j.aquabot.2024.103793","DOIUrl":"10.1016/j.aquabot.2024.103793","url":null,"abstract":"<div><p>Marine natural resources are increasingly demanded to support the livelihoods and wellbeing of humans facing multiple and simultaneous crises across the planet. Seaweeds, in particular, are renowned sources of bioactive marine compounds used for various purposes, including human and animal nutrition, soil fertilization, and healthcare markets. DNA-based tools are being adopted in integrative taxonomy and ecological research, as well as to monitor the supply chain of commercially important species. This research provides novel insights into the population genetics, phylogenetic relationships, and haplotype network of six commercially significant seaweed species that are abundant in the Azores archipelago and currently traded for industrial applications. This study provides a detailed assessment of the genetic diversity of the red seaweeds <em>Asparagopsis armata, Asparagopsis taxiformis,</em> and <em>Pterocladiella capillacea</em>, and the brown seaweeds <em>Halopteris scoparia, Zonaria tournefortii,</em> and <em>Cystoseira pustulata,</em> contributing with 17 newly generated barcodes of COI, <em>rbc</em>L, and 28 S rDNA gene records from the Azores region to the reference databases. Understanding the species identification and population dynamics is critical for understanding species composition in biodiversity hotspots. This knowledge supports taxonomy, conservation, environmental protection, and the sustainable use of marine resources.</p></div>","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103793"},"PeriodicalIF":1.9,"publicationDate":"2024-07-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S0304377024000457/pdfft?md5=77c4fefb89e9f14e0864f2264a5a8701&pid=1-s2.0-S0304377024000457-main.pdf","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141843630","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Aquatic BotanyPub Date : 2024-07-14DOI: 10.1016/j.aquabot.2024.103795
John S. Cassell
{"title":"A Letter to the Editor regarding the 2022 article “Range expansion of Marinomyxa marina, a phytomyxid parasite of the invasive seagrass Halophila stipulacea, to the Caribbean”","authors":"John S. Cassell","doi":"10.1016/j.aquabot.2024.103795","DOIUrl":"10.1016/j.aquabot.2024.103795","url":null,"abstract":"","PeriodicalId":8273,"journal":{"name":"Aquatic Botany","volume":"195 ","pages":"Article 103795"},"PeriodicalIF":1.9,"publicationDate":"2024-07-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141692035","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}