Pub Date : 2025-02-14DOI: 10.1186/s12870-025-06173-x
Walaa A Abo-Shanab, Mostafa E Elshobary, Anna Czubacka, Rana H Diab
Background: This study investigated the effects of the different concentrations of CaCl2 (10 and 15 mol m-3) on the growth, physiology, and cytological characteristics of salt-stressed Vicia faba (L.) seedlings grown under greenhouse conditions.
Results: Salinity stress (150 mol m-3 NaCl) had detrimental effects on all measured growth parameters, increased the micronucleus count number (MCN) by 26.6 micronuclei/1000 cells, decreased the mitotic index (MI) by 66.6%, and caused various chromosomal aberrations, nuclear alterations, and chromatin bridges in salt-stressed seedlings compared to the untreated plant. Nevertheless, the seed priming with CaCl2 (10 and 15 mol m-3) significantly alleviated the toxic effects induced by salinity stress, improved growth parameters, total chlorophyll (TChl), proline, and total soluble sugar (TSS) contents in salt-stressed faba bean seedling compared with seedlings germinated from non-primed seeds. The antioxidative system of salt-stressed faba bean was highly stimulated by increasing the activity of catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) enzymes as well as phenolics and flavonoids were increased in all salt-stressed seedlings germinated from seeds primed with CaCl2 (10 and 15 mol m-3) indicating an improved tolerance of faba bean plant to salinity stress. Notably, the pretreatment with CaCl2 (10 mol m-3) reduced the micronuclei number per 1000 cells by 91.3% and decreased the abnormality index by 58.9% more effectively than CaCl2 (15 mol m-3). SDS-PAGE profiling revealed the presence of 16 proteins with different molecular weights, including two peptides, induced by CaCl2 (10 mol m-3) in response to salinity stress.
Conclusions: This study showed that 10 mol m-3 CaCl2 significantly improved salt tolerance in treated faba bean plants mitigating the antagonistic effects of salt stress on several physiological and cytological parameters.
{"title":"Improvement of salt tolerance in Vicia faba (L.) seedlings: a comprehensive investigation of the effects of exogenous calcium chloride.","authors":"Walaa A Abo-Shanab, Mostafa E Elshobary, Anna Czubacka, Rana H Diab","doi":"10.1186/s12870-025-06173-x","DOIUrl":"10.1186/s12870-025-06173-x","url":null,"abstract":"<p><strong>Background: </strong>This study investigated the effects of the different concentrations of CaCl<sub>2</sub> (10 and 15 mol m<sup>-3</sup>) on the growth, physiology, and cytological characteristics of salt-stressed Vicia faba (L.) seedlings grown under greenhouse conditions.</p><p><strong>Results: </strong>Salinity stress (150 mol m<sup>-3</sup> NaCl) had detrimental effects on all measured growth parameters, increased the micronucleus count number (MCN) by 26.6 micronuclei/1000 cells, decreased the mitotic index (MI) by 66.6%, and caused various chromosomal aberrations, nuclear alterations, and chromatin bridges in salt-stressed seedlings compared to the untreated plant. Nevertheless, the seed priming with CaCl<sub>2</sub> (10 and 15 mol m<sup>-3</sup>) significantly alleviated the toxic effects induced by salinity stress, improved growth parameters, total chlorophyll (TChl), proline, and total soluble sugar (TSS) contents in salt-stressed faba bean seedling compared with seedlings germinated from non-primed seeds. The antioxidative system of salt-stressed faba bean was highly stimulated by increasing the activity of catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) enzymes as well as phenolics and flavonoids were increased in all salt-stressed seedlings germinated from seeds primed with CaCl<sub>2</sub> (10 and 15 mol m<sup>-3</sup>) indicating an improved tolerance of faba bean plant to salinity stress. Notably, the pretreatment with CaCl<sub>2</sub> (10 mol m<sup>-3</sup>) reduced the micronuclei number per 1000 cells by 91.3% and decreased the abnormality index by 58.9% more effectively than CaCl<sub>2</sub> (15 mol m<sup>-3</sup>). SDS-PAGE profiling revealed the presence of 16 proteins with different molecular weights, including two peptides, induced by CaCl<sub>2</sub> (10 mol m<sup>-3</sup>) in response to salinity stress.</p><p><strong>Conclusions: </strong>This study showed that 10 mol m<sup>-3</sup> CaCl<sub>2</sub> significantly improved salt tolerance in treated faba bean plants mitigating the antagonistic effects of salt stress on several physiological and cytological parameters.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"200"},"PeriodicalIF":4.3,"publicationDate":"2025-02-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11827168/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143424988","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}
Background: The Colletotrichum fructicola (C. fructicola) is a hemibiotrophic fungus, which causes devastating anthracnose in strawberry. At present, the resistance mechanism to C. fructicola remains poorly understood.
Results: Here, we used RNA-sequencing and liquid chromatography-mass spectrometry (LC-MS) metabolomics to excavate the molecular mechanism of strawberry resistance to C. fructicola. The differentially accumulated metabolites (DAMs) and differentially expressed genes (DEGs) were screened at different stages after C. fructicola infection in the susceptible 'Benihoppe' and resistant cultivar 'Sweet Charlie'. The core common DEGs with high association of common DAMs were identified by multi-omics integration analysis, and showed convergence and divergence in the two strawberry cultivars. Strikingly, the phenylpropanoids biosynthesis was simultaneously enriched in a multi-level omics at different stages after C. fructicola infection in the resistant (R) and susceptible (S) strawberries. Furthermore, we constructed the DEGs-DAMs map of phenylpropanoid biosynthesis. More importantly, we showed that chloroplasts and starch and sugar metabolism related genes, such as chlorophyII A-B binding genes, glycosyl hydrolase (GH) family genes and so on, were differentially expressed.
Conclusions: Taken together, our study revealed major changes in genes and metabolites expression associated with C. fructicola resistance, and identified the multi-level regulatory network based on phenylpropanoid biosynthesis, useful for further mechanistic excavation of resistance to C. fructicola in strawberries.
背景:果核霉菌(Colletotrichum fructicola,C. fructicola)是一种半生营养真菌,可引起草莓毁灭性炭疽病。目前,人们对 C. fructicola 的抗性机理仍知之甚少:结果:我们利用 RNA 测序和液相色谱-质谱(LC-MS)代谢组学方法,研究了草莓对 C. fructicola 的抗性分子机制。研究人员筛选了易感品种 "Benihoppe "和抗性品种 "Sweet Charlie "在果蝇疫霉感染后不同阶段的差异积累代谢物(DAMs)和差异表达基因(DEGs)。通过多组学整合分析,确定了与共同 DAMs 高度相关的核心共同 DEGs,这些 DEGs 在两个草莓栽培品种中表现出趋同性和差异性。引人注目的是,在抗性草莓(R)和易感草莓(S)感染果蝇疫霉后的不同阶段,苯丙酮类生物合成在多级组学中同时富集。此外,我们还构建了苯丙酮生物合成的 DEGs-DAMs 图谱。更重要的是,我们发现叶绿体及淀粉和糖代谢相关基因,如叶绿体II A-B结合基因、糖基水解酶(GH)家族基因等,均有差异表达:综上所述,我们的研究揭示了与果蝇科细菌抗性相关的基因和代谢产物表达的主要变化,并确定了基于苯丙氨酸生物合成的多级调控网络,有助于进一步从机理上挖掘草莓对果蝇科细菌的抗性。
{"title":"Integrated transcriptomic and metabolomic analyses provide insights into defense against Colletotrichum fructicola in octoploid strawberries.","authors":"Xiaohua Zou, Yun Bai, Ying Ji, Liqing Zhang, Qinghua Gao, Xianping Fang","doi":"10.1186/s12870-025-06057-0","DOIUrl":"10.1186/s12870-025-06057-0","url":null,"abstract":"<p><strong>Background: </strong>The Colletotrichum fructicola (C. fructicola) is a hemibiotrophic fungus, which causes devastating anthracnose in strawberry. At present, the resistance mechanism to C. fructicola remains poorly understood.</p><p><strong>Results: </strong>Here, we used RNA-sequencing and liquid chromatography-mass spectrometry (LC-MS) metabolomics to excavate the molecular mechanism of strawberry resistance to C. fructicola. The differentially accumulated metabolites (DAMs) and differentially expressed genes (DEGs) were screened at different stages after C. fructicola infection in the susceptible 'Benihoppe' and resistant cultivar 'Sweet Charlie'. The core common DEGs with high association of common DAMs were identified by multi-omics integration analysis, and showed convergence and divergence in the two strawberry cultivars. Strikingly, the phenylpropanoids biosynthesis was simultaneously enriched in a multi-level omics at different stages after C. fructicola infection in the resistant (R) and susceptible (S) strawberries. Furthermore, we constructed the DEGs-DAMs map of phenylpropanoid biosynthesis. More importantly, we showed that chloroplasts and starch and sugar metabolism related genes, such as chlorophyII A-B binding genes, glycosyl hydrolase (GH) family genes and so on, were differentially expressed.</p><p><strong>Conclusions: </strong>Taken together, our study revealed major changes in genes and metabolites expression associated with C. fructicola resistance, and identified the multi-level regulatory network based on phenylpropanoid biosynthesis, useful for further mechanistic excavation of resistance to C. fructicola in strawberries.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"190"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823099/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413454","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06213-6
Sarasadat Abbasirad, Ali Akbar Ghotbi-Ravandi
Background: Over the years, nanoparticles have emerged as a promising approach for improving crop growth, yield, and overall agricultural sustainability. However, there has been growing concern about the potential adverse effects of nanoparticles in the agricultural sector and the environment. The present study aimed to investigate the detrimental effects of high (1000 mg L-1) concentrations of copper oxide nanoparticles (CuO NPs) on barley seedlings. The equivalent concentrations of CuO bulk and the ionic form of copper were also used in the experiments for comparative analysis. CuO NPs were characterized by Field Emission-Scanning Electron Microscopy, Dynamic Light Scattering, Zeta Potential analysis, and X-ray Diffraction prior to the application. Barley seedlings were subjected to the foliar application of CuO NP, CuO bulk, ionic Cu, and control group. The presence of CuO NPs in barley leaves was confirmed 72 hours after treatment by energy-dispersive X-ray analysis.
Results: The results showed a CuO NPs treatment led to an impairment of nutrient balance in barley leaves. An increase in hydrogen peroxide content followed by the higher specific activity of catalase and ascorbate peroxidase was also observed in response to CuO NPs, CuO bulk, and Cu2+ ions. The profile of phytohormones including auxins (IAA and IBA), Gibberellins (GA1, GA4, and GA9), abscisic acid (ABA), ethylene (ET), and jasmonic acid (JA) significantly affected by CuO NPs, CuO bulk, and Cu2+ ions. The transcripts of the PR1 gene involved in systemic acquired resistance (SAR) and LOX-1 and PAL involved in induced systemic resistance (ISR) were significantly upregulated in response to CuO NPs treatment.
Conclusion: Our findings suggest that the systemic resistances in barley seedlings were induced by higher accumulation of ABA, ET, and JA under CuO NPs treatment. The activation of systemic resistances indicated the involvement of both SAR and SAR pathways in the response to CuO NPs in barley.
{"title":"Toxicity of copper oxide nanoparticles in barley: induction of oxidative stress, hormonal imbalance, and systemic resistances.","authors":"Sarasadat Abbasirad, Ali Akbar Ghotbi-Ravandi","doi":"10.1186/s12870-025-06213-6","DOIUrl":"10.1186/s12870-025-06213-6","url":null,"abstract":"<p><strong>Background: </strong>Over the years, nanoparticles have emerged as a promising approach for improving crop growth, yield, and overall agricultural sustainability. However, there has been growing concern about the potential adverse effects of nanoparticles in the agricultural sector and the environment. The present study aimed to investigate the detrimental effects of high (1000 mg L<sup>-1</sup>) concentrations of copper oxide nanoparticles (CuO NPs) on barley seedlings. The equivalent concentrations of CuO bulk and the ionic form of copper were also used in the experiments for comparative analysis. CuO NPs were characterized by Field Emission-Scanning Electron Microscopy, Dynamic Light Scattering, Zeta Potential analysis, and X-ray Diffraction prior to the application. Barley seedlings were subjected to the foliar application of CuO NP, CuO bulk, ionic Cu, and control group. The presence of CuO NPs in barley leaves was confirmed 72 hours after treatment by energy-dispersive X-ray analysis.</p><p><strong>Results: </strong>The results showed a CuO NPs treatment led to an impairment of nutrient balance in barley leaves. An increase in hydrogen peroxide content followed by the higher specific activity of catalase and ascorbate peroxidase was also observed in response to CuO NPs, CuO bulk, and Cu<sup>2+</sup> ions. The profile of phytohormones including auxins (IAA and IBA), Gibberellins (GA<sub>1</sub>, GA<sub>4</sub>, and GA<sub>9</sub>), abscisic acid (ABA), ethylene (ET), and jasmonic acid (JA) significantly affected by CuO NPs, CuO bulk, and Cu<sup>2+</sup> ions. The transcripts of the PR1 gene involved in systemic acquired resistance (SAR) and LOX-1 and PAL involved in induced systemic resistance (ISR) were significantly upregulated in response to CuO NPs treatment.</p><p><strong>Conclusion: </strong>Our findings suggest that the systemic resistances in barley seedlings were induced by higher accumulation of ABA, ET, and JA under CuO NPs treatment. The activation of systemic resistances indicated the involvement of both SAR and SAR pathways in the response to CuO NPs in barley.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"187"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823089/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413458","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06210-9
Luiz Augusto Cauz-Santos, Zirlane Portugal da Costa, Mariela Analía Sader, Cássio van den Berg, Maria Lucia Carneiro Vieira
Chloroplasts are essential organelles in plants and eukaryotic algae, responsible for photosynthesis, fatty acid synthesis, amino acid production, and stress responses. The genus Passiflora, known for its species diversity and dynamic chloroplast (cp) genome evolution, serves as an excellent model for studying structural variations. This study investigates evolutionary relationships within Passiflora by sequencing 11 new chloroplast genomes, assessing selective pressures on cp genes, and comparing plastid and nuclear phylogenies. Passiflora cp genomes showed significant variations in size, gene content, and structure, ranging from 132,736 to 163,292 base pairs, especially in Decaloba. Structural rearrangements and species-specific repeat patterns were identified. Selective pressure tests revealed significant adaptive evolution in certain lineages, with several genes, including clpP and petL, under positive selection. Phylogenetic analyses confirmed the monophyly of subgenera Astrophea, Passiflora, and Decaloba, while Deidamioides appeared polyphyletic. Nuclear phylogenetic analysis based on 35S rDNA sequences supported the monophyly of Astrophea but showed inconsistencies within subgenus Passiflora compared to cp genome data. This study highlights the evolutionary complexity of Passiflora cp genomes, demonstrating significant structural variations and adaptive evolution. The findings underscore the effectiveness of plastid phylogenomics in resolving phylogenetic relationships and provide insights into adaptive mechanisms shaping cp genome diversity in angiosperms.
{"title":"Chloroplast genomic insights into adaptive evolution and rapid radiation in the genus Passiflora (Passifloraceae).","authors":"Luiz Augusto Cauz-Santos, Zirlane Portugal da Costa, Mariela Analía Sader, Cássio van den Berg, Maria Lucia Carneiro Vieira","doi":"10.1186/s12870-025-06210-9","DOIUrl":"10.1186/s12870-025-06210-9","url":null,"abstract":"<p><p>Chloroplasts are essential organelles in plants and eukaryotic algae, responsible for photosynthesis, fatty acid synthesis, amino acid production, and stress responses. The genus Passiflora, known for its species diversity and dynamic chloroplast (cp) genome evolution, serves as an excellent model for studying structural variations. This study investigates evolutionary relationships within Passiflora by sequencing 11 new chloroplast genomes, assessing selective pressures on cp genes, and comparing plastid and nuclear phylogenies. Passiflora cp genomes showed significant variations in size, gene content, and structure, ranging from 132,736 to 163,292 base pairs, especially in Decaloba. Structural rearrangements and species-specific repeat patterns were identified. Selective pressure tests revealed significant adaptive evolution in certain lineages, with several genes, including clpP and petL, under positive selection. Phylogenetic analyses confirmed the monophyly of subgenera Astrophea, Passiflora, and Decaloba, while Deidamioides appeared polyphyletic. Nuclear phylogenetic analysis based on 35S rDNA sequences supported the monophyly of Astrophea but showed inconsistencies within subgenus Passiflora compared to cp genome data. This study highlights the evolutionary complexity of Passiflora cp genomes, demonstrating significant structural variations and adaptive evolution. The findings underscore the effectiveness of plastid phylogenomics in resolving phylogenetic relationships and provide insights into adaptive mechanisms shaping cp genome diversity in angiosperms.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"192"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823247/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413440","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06193-7
Kamilla Kovács, Ádám Szierer, Enikő Mészáros, Árpád Molnár, Andrea Rónavári, Zoltán Kónya, Gábor Feigl
Background: Abiotic stressors such as heavy metals and nanoparticles pose significant challenges to sustainable agriculture, with copper oxide nanoparticles (CuO NPs) known to inhibit root growth and induce oxidative stress in plants. While silica nanoparticles (SiO2 NPs) have been shown to increase abiotic stress tolerance, their role in mitigating CuO NP-induced stress in crops, especially monocots, remains poorly understood. This study addresses this critical knowledge gap by investigating how SiO2 NP pretreatment modulates CuO NP-induced stress responses, with a particular focus on root growth inhibition and nitro-oxidative stress pathways.
Results: Using an in vitro semihydroponic system, seeds were pretreated with varying concentrations of SiO2 NPs (100-800 mg/L) before exposure to CuO NPs at levels known to inhibit root growth by 50%. SiO2 NP pretreatment alleviated CuO NP-induced root growth inhibition in sorghum, wheat, and rye but intensified it in triticale. These responses are associated with species-specific alterations in reactive signaling molecules, including a reduction in nitric oxide levels and an increase in hydrogen sulfide in sorghum, a decrease in superoxide anion levels in rye, and elevated hydrogen peroxide levels in wheat. Protein tyrosine nitration, a marker of nitro-oxidative stress, was reduced in most cases, further indicating the stress-mitigating role of SiO2 NPs. These signaling molecules were selected for their established roles in mediating oxidative and nitrosative stress responses under abiotic stress conditions.
Conclusions: SiO2 NP pretreatment modulates CuO NP-induced stress responses through species-specific regulation of reactive oxygen and nitrogen species, demonstrating its potential as a tool for enhancing crop resilience. These findings advance the understanding of nanoparticle‒plant interactions and provide a foundation for future applications of nanotechnology in sustainable agriculture.
Clinical trial number: Not applicable.
{"title":"Species-specific modulation of nitro-oxidative stress and root growth in monocots by silica nanoparticle pretreatment under copper oxide nanoparticle stress.","authors":"Kamilla Kovács, Ádám Szierer, Enikő Mészáros, Árpád Molnár, Andrea Rónavári, Zoltán Kónya, Gábor Feigl","doi":"10.1186/s12870-025-06193-7","DOIUrl":"10.1186/s12870-025-06193-7","url":null,"abstract":"<p><strong>Background: </strong>Abiotic stressors such as heavy metals and nanoparticles pose significant challenges to sustainable agriculture, with copper oxide nanoparticles (CuO NPs) known to inhibit root growth and induce oxidative stress in plants. While silica nanoparticles (SiO<sub>2</sub> NPs) have been shown to increase abiotic stress tolerance, their role in mitigating CuO NP-induced stress in crops, especially monocots, remains poorly understood. This study addresses this critical knowledge gap by investigating how SiO<sub>2</sub> NP pretreatment modulates CuO NP-induced stress responses, with a particular focus on root growth inhibition and nitro-oxidative stress pathways.</p><p><strong>Results: </strong>Using an in vitro semihydroponic system, seeds were pretreated with varying concentrations of SiO<sub>2</sub> NPs (100-800 mg/L) before exposure to CuO NPs at levels known to inhibit root growth by 50%. SiO<sub>2</sub> NP pretreatment alleviated CuO NP-induced root growth inhibition in sorghum, wheat, and rye but intensified it in triticale. These responses are associated with species-specific alterations in reactive signaling molecules, including a reduction in nitric oxide levels and an increase in hydrogen sulfide in sorghum, a decrease in superoxide anion levels in rye, and elevated hydrogen peroxide levels in wheat. Protein tyrosine nitration, a marker of nitro-oxidative stress, was reduced in most cases, further indicating the stress-mitigating role of SiO<sub>2</sub> NPs. These signaling molecules were selected for their established roles in mediating oxidative and nitrosative stress responses under abiotic stress conditions.</p><p><strong>Conclusions: </strong>SiO<sub>2</sub> NP pretreatment modulates CuO NP-induced stress responses through species-specific regulation of reactive oxygen and nitrogen species, demonstrating its potential as a tool for enhancing crop resilience. These findings advance the understanding of nanoparticle‒plant interactions and provide a foundation for future applications of nanotechnology in sustainable agriculture.</p><p><strong>Clinical trial number: </strong>Not applicable.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"188"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823027/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413457","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06174-w
Zishan Ahmad, Olga Babich, Stanislav Sukhikh, Vikas Yadav, Muthusamy Ramakrishnan, Fatima Firdaus, Anwar Shahzad
Decalepis arayapathra is an important medicinal plant known for several medicinal values, however, due to overharvesting, habitat destruction, and its limited geographical distribution, D. arayapathra faces severe threats of extinction. A synthetic seed protocol was developed for this plant, representing a novel approach in its propagation and conservation. Nodal segments (NS) were encapsulated in a sodium alginate (SA) matrix. 3% SA with 100 mM CaCl2 solutions was best to obtain ideal beads with fine texture. Murashige and Skoog (MS) medium consisting of BA 5.0 µM + NAA 0.5 µM + ADS 20.0 µM resulted in a maximum regrowth frequency of 71.26% with 3.13 shoots per bead and a shoot length of 4.10 cm after six weeks of culture. Rooting in the microshoots was better observed with half- strength MS + 2.5 µM NAA, resulting in 3.1 roots per microshoot and a root length of 3.0 cm after four weeks of culture, followed by successful acclimatization. The study investigated the effect of photosynthetic photon flux density (PPFD) levels of 50 and 300 PPFD on various physiological and biochemical parameters during the acclimatization of in vitro-derived plants. Results showed an increase in photosynthetic pigments, including chlorophyll and carotenoids, as well as an enhanced net photosynthetic rate (PN) and stomatal conductance (gs) with prolonged acclimatization, with higher PPFD being more effective. Antioxidant enzyme activities, including SOD, CAT, APX, and GR, increased over time, except for SOD, which began to decline after 21 days under both light conditions. Stress markers such as malondialdehyde (MDA) and electrolyte leakage decreased over time, indicating successful acclimatization. Genetic fidelity was confirmed through clear and monomorphic banding patterns obtained using RAPD and ISSR markers. Quantification of 2H4MB (2-hydroxy-4-methoxy benzaldehyde) in synseed-derived roots using HPLC revealed a concentration of 16.27 µg/ml. Metabolic profiling of the synseed-derived root tuber using GC-MS identified several major and minor metabolites. This study offers a breakthrough in the conservation of D. arayapathra through synthetic seed technology, enabling sustainable propagation while preserving genetic stability. It ensures a consistent supply of the bioactive compound 2H4MB, promoting medicinal research and commercial applications.
{"title":"Unlocking the biotechnological potential of Decalepis arayalpathra: exploring synthetic seed production, metabolic profiling, genetic stability, and the impact of photosynthetic photon flux density on acclimatization.","authors":"Zishan Ahmad, Olga Babich, Stanislav Sukhikh, Vikas Yadav, Muthusamy Ramakrishnan, Fatima Firdaus, Anwar Shahzad","doi":"10.1186/s12870-025-06174-w","DOIUrl":"10.1186/s12870-025-06174-w","url":null,"abstract":"<p><p>Decalepis arayapathra is an important medicinal plant known for several medicinal values, however, due to overharvesting, habitat destruction, and its limited geographical distribution, D. arayapathra faces severe threats of extinction. A synthetic seed protocol was developed for this plant, representing a novel approach in its propagation and conservation. Nodal segments (NS) were encapsulated in a sodium alginate (SA) matrix. 3% SA with 100 mM CaCl<sub>2</sub> solutions was best to obtain ideal beads with fine texture. Murashige and Skoog (MS) medium consisting of BA 5.0 µM + NAA 0.5 µM + ADS 20.0 µM resulted in a maximum regrowth frequency of 71.26% with 3.13 shoots per bead and a shoot length of 4.10 cm after six weeks of culture. Rooting in the microshoots was better observed with half- strength MS + 2.5 µM NAA, resulting in 3.1 roots per microshoot and a root length of 3.0 cm after four weeks of culture, followed by successful acclimatization. The study investigated the effect of photosynthetic photon flux density (PPFD) levels of 50 and 300 PPFD on various physiological and biochemical parameters during the acclimatization of in vitro-derived plants. Results showed an increase in photosynthetic pigments, including chlorophyll and carotenoids, as well as an enhanced net photosynthetic rate (P<sub>N</sub>) and stomatal conductance (gs) with prolonged acclimatization, with higher PPFD being more effective. Antioxidant enzyme activities, including SOD, CAT, APX, and GR, increased over time, except for SOD, which began to decline after 21 days under both light conditions. Stress markers such as malondialdehyde (MDA) and electrolyte leakage decreased over time, indicating successful acclimatization. Genetic fidelity was confirmed through clear and monomorphic banding patterns obtained using RAPD and ISSR markers. Quantification of 2H4MB (2-hydroxy-4-methoxy benzaldehyde) in synseed-derived roots using HPLC revealed a concentration of 16.27 µg/ml. Metabolic profiling of the synseed-derived root tuber using GC-MS identified several major and minor metabolites. This study offers a breakthrough in the conservation of D. arayapathra through synthetic seed technology, enabling sustainable propagation while preserving genetic stability. It ensures a consistent supply of the bioactive compound 2H4MB, promoting medicinal research and commercial applications.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"189"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823203/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413459","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06198-2
Paweł Sowiński, Katarzyna Wieliczko-Manowska, Marcin Grzybowski, Maciej Jończyk, Jakub Sowiński, Alicja Sobkowiak, Piotr Kowalec, Janusz Rogacki
Background: Maize cultivation has considerably expanded beyond its place of origin in Central America. The successful adaptation of maize to temperate climates can be achieved by selecting genotypes that demonstrate tolerance to low temperatures, especially in cold springs. In maize, cold tolerance at the early growth stages enables early sowing, a long growing season, and eventually high yields, even in temperate climates. Maize adaptation during early growth has not been thoroughly investigated; therefore, we tested the working hypothesis that several distinct and independent adaptation strategies may be involved in maize habituation to cool temperate climates during seedling establishment.
Results: We studied the effect of mild cold stress (day/night 16/12 °C) on early growth stage followed by regrowth at optimal daily temperatures (24/21 °C). Automated plant phenotyping was performed on 30 inbred lines selected from a diverse genetic pool during preliminary studies. As a result, we generated time series based on selected morphological parameters, spectral parameters, and spectral vegetation indices. These curves were clustered and four classes of maize with clearly contrasting growth modes and changes in their physiological status were distinguished at low temperatures and during regrowth. Two classes comprised either cold-sensitive (slow growth and poor physiological status in cold) or cold-tolerant (moderately fast growth and good physiological status in cold) lines. However, two other classes showed that growth rate and physiological status at low temperature is not necessarily related, for instance one class included lines with small seedlings but good physiological status and the other grouped seedlings with rapid growth despite poor physiological status. These classes clearly exhibited different modes of cold adaptation. Moreover, a class containing cold-sensitive inbred lines may represent a distinct and novel type of cold-adaptation strategy related to the arrest of coleoptile emerge related with ability to recover rapidly under favourable conditions.
Conclusions: Our results support the hypothesis that maize may have several adaptation strategies to cold environments at early growth stages based on independent mechanisms. These findings suggest that maize adaptability to adverse environments is likely more complex than previously understood.
{"title":"Diverse coping modes of maize in cool environment at early growth.","authors":"Paweł Sowiński, Katarzyna Wieliczko-Manowska, Marcin Grzybowski, Maciej Jończyk, Jakub Sowiński, Alicja Sobkowiak, Piotr Kowalec, Janusz Rogacki","doi":"10.1186/s12870-025-06198-2","DOIUrl":"10.1186/s12870-025-06198-2","url":null,"abstract":"<p><strong>Background: </strong>Maize cultivation has considerably expanded beyond its place of origin in Central America. The successful adaptation of maize to temperate climates can be achieved by selecting genotypes that demonstrate tolerance to low temperatures, especially in cold springs. In maize, cold tolerance at the early growth stages enables early sowing, a long growing season, and eventually high yields, even in temperate climates. Maize adaptation during early growth has not been thoroughly investigated; therefore, we tested the working hypothesis that several distinct and independent adaptation strategies may be involved in maize habituation to cool temperate climates during seedling establishment.</p><p><strong>Results: </strong>We studied the effect of mild cold stress (day/night 16/12 °C) on early growth stage followed by regrowth at optimal daily temperatures (24/21 °C). Automated plant phenotyping was performed on 30 inbred lines selected from a diverse genetic pool during preliminary studies. As a result, we generated time series based on selected morphological parameters, spectral parameters, and spectral vegetation indices. These curves were clustered and four classes of maize with clearly contrasting growth modes and changes in their physiological status were distinguished at low temperatures and during regrowth. Two classes comprised either cold-sensitive (slow growth and poor physiological status in cold) or cold-tolerant (moderately fast growth and good physiological status in cold) lines. However, two other classes showed that growth rate and physiological status at low temperature is not necessarily related, for instance one class included lines with small seedlings but good physiological status and the other grouped seedlings with rapid growth despite poor physiological status. These classes clearly exhibited different modes of cold adaptation. Moreover, a class containing cold-sensitive inbred lines may represent a distinct and novel type of cold-adaptation strategy related to the arrest of coleoptile emerge related with ability to recover rapidly under favourable conditions.</p><p><strong>Conclusions: </strong>Our results support the hypothesis that maize may have several adaptation strategies to cold environments at early growth stages based on independent mechanisms. These findings suggest that maize adaptability to adverse environments is likely more complex than previously understood.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"191"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823182/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413443","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}
Pub Date : 2025-02-13DOI: 10.1186/s12870-025-06191-9
Kun Yi, Luyan Gao, Yue Xu, Jiajia Yang, Peisheng Mao, Liru Dou, Manli Li
Background: The high fat content in oat seeds makes them susceptible to aging during storage, leading to reduced seed vigor, delayed germination, and even seed death. Much evidence suggests that lipid remodeling is closely associated with successful seed germination. However, the dynamic behavior and response mechanisms of lipids during the germination of aged oat seeds remain unclear. In this study, 'Monida' (aging-tolerant) and 'Haywire' (aging-sensitive), were used to investigate the lipid profiles in the embryo and endosperm and the dynamic transcriptomic differences in the embryo during the germination.
Results: The results demonstrate that phospholipid alterations during the germination of aged seeds are more significant compared to unaged seeds, indicating that aging affects lipid remodeling during germination, particularly in the 'Haywire'. Further analysis revealed that the most critical lipid response events occurred at the end of germination stage II (32 h) in embryo, primarily regulated through the PLC-DGK pathway to modulate phospholipid and glycerolipid molecules. Specifically, transcripts of PLC, DGK, and DGAT were upregulated, promoting the generation of diacylglycerol (DG) from various phospholipids, which further increased the monogalactosyldiacylglycerol/digalactosyldiacylglycerol (MGDG/DGDG) ratio, thereby influencing membrane repair. Additionally, at 6 h of germination in aged seeds, PC(3:0/0:0) levels significantly decreased. Compared to 'Monida,' the aging-sensitive 'Haywire' seeds exhibited substantial production of PE(19:0/0:0) and PC(15:0/0:0) at 32 h of germination, which may be key factors contributing to the seed's sensitivity to aging and the significant reduction in germination percentage after aging. Therefore, PC(3:0/0:0), PE(19:0/0:0), and PC(15:0/0:0) could serve as important lipid metabolic markers in future studies on the mechanisms of oat seed vigor.
Conclusions: The findings of this study provide insights into the specificity of lipid remodeling and its response mechanisms during the germination of aged oat seeds, providing a theoretical foundation for the safe preservation of oat germplasm and the development of aging-tolerant varieties.
{"title":"Lipid remodeling and response mechanisms during the germination of aged oat seeds.","authors":"Kun Yi, Luyan Gao, Yue Xu, Jiajia Yang, Peisheng Mao, Liru Dou, Manli Li","doi":"10.1186/s12870-025-06191-9","DOIUrl":"10.1186/s12870-025-06191-9","url":null,"abstract":"<p><strong>Background: </strong>The high fat content in oat seeds makes them susceptible to aging during storage, leading to reduced seed vigor, delayed germination, and even seed death. Much evidence suggests that lipid remodeling is closely associated with successful seed germination. However, the dynamic behavior and response mechanisms of lipids during the germination of aged oat seeds remain unclear. In this study, 'Monida' (aging-tolerant) and 'Haywire' (aging-sensitive), were used to investigate the lipid profiles in the embryo and endosperm and the dynamic transcriptomic differences in the embryo during the germination.</p><p><strong>Results: </strong>The results demonstrate that phospholipid alterations during the germination of aged seeds are more significant compared to unaged seeds, indicating that aging affects lipid remodeling during germination, particularly in the 'Haywire'. Further analysis revealed that the most critical lipid response events occurred at the end of germination stage II (32 h) in embryo, primarily regulated through the PLC-DGK pathway to modulate phospholipid and glycerolipid molecules. Specifically, transcripts of PLC, DGK, and DGAT were upregulated, promoting the generation of diacylglycerol (DG) from various phospholipids, which further increased the monogalactosyldiacylglycerol/digalactosyldiacylglycerol (MGDG/DGDG) ratio, thereby influencing membrane repair. Additionally, at 6 h of germination in aged seeds, PC(3:0/0:0) levels significantly decreased. Compared to 'Monida,' the aging-sensitive 'Haywire' seeds exhibited substantial production of PE(19:0/0:0) and PC(15:0/0:0) at 32 h of germination, which may be key factors contributing to the seed's sensitivity to aging and the significant reduction in germination percentage after aging. Therefore, PC(3:0/0:0), PE(19:0/0:0), and PC(15:0/0:0) could serve as important lipid metabolic markers in future studies on the mechanisms of oat seed vigor.</p><p><strong>Conclusions: </strong>The findings of this study provide insights into the specificity of lipid remodeling and its response mechanisms during the germination of aged oat seeds, providing a theoretical foundation for the safe preservation of oat germplasm and the development of aging-tolerant varieties.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"186"},"PeriodicalIF":4.3,"publicationDate":"2025-02-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11823238/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143413455","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}
Background: The genus Pseudoroegneria (Nevski) Á.Löve contributes the St genome for more than 60% of perennial Triticeae species. However, the strong dominant character of the St genome makes it challenging to distinguish each species and/or even genus based on single or combined morphological traits. Moreover, the phylogeny and taxonomy of the St-genome containing polyploid genera remain controversial.
Results: In this study, we used nuclear and chloroplast DNA-based phylogenetic analyses to reveal the systematic relationships between the St-genome containing polyploid species. The maximum likelihood (ML) tree based on nuclear ribosomal internal transcribed spacer region (nrITS) and three single-copy nuclear genes data (Acc1 + Pgk1 + DMC1) showed that polyploid species with the St genome were separated into seven genera with StStHH, StStYY, StStYYHH, StStYYPP, StStYYWW, StStPP, and StStEE genome constitutions, moreover, the polyploid species in Caucasus, America, and Australia have independent polyploidization events. The ML tree for the chloroplast DNA fragments (matK + rbcL + trnL-trnF) displayed that the P genome served as a maternal donor of Kengyilia melanthera and K. dingqinensis from the Hengduan Mountains region, while the St or StY genome served as the maternal donor of other St-genome containing species. Herein, we reported the genomic constitution of Kengyilia tibetica, K. changduensis, and K. dingqinensis with the StStYYPP genome for the first time.
Conclusions: The St-genome-containing polyploid species should be treated as distinct genera according to different genome constitutions, and those species experienced independent allo-polyploidization events in different distribution regions and had two relatively independent maternal origins from the P or St/StY genomes. Besides, the Xp genome might have contributed to the unknown Y genome formation.
{"title":"Phylogeny and taxonomy of the polyploid species that contain St genome (Triticeae; Poaceae) based on four nuclear DNA and three chloroplast genes.","authors":"Xiaoyang Pan, Tingting Zheng, Yuxin Zhao, Junhao Bao, Xing Fan, Lina Sha, Yinghui Li, Wei Zhu, Lili Xu, Yi Wang, Yiran Cheng, Haiqin Zhang, Houyang Kang, Yonghong Zhou, Dandan Wu","doi":"10.1186/s12870-025-06179-5","DOIUrl":"10.1186/s12870-025-06179-5","url":null,"abstract":"<p><strong>Background: </strong>The genus Pseudoroegneria (Nevski) Á.Löve contributes the St genome for more than 60% of perennial Triticeae species. However, the strong dominant character of the St genome makes it challenging to distinguish each species and/or even genus based on single or combined morphological traits. Moreover, the phylogeny and taxonomy of the St-genome containing polyploid genera remain controversial.</p><p><strong>Results: </strong>In this study, we used nuclear and chloroplast DNA-based phylogenetic analyses to reveal the systematic relationships between the St-genome containing polyploid species. The maximum likelihood (ML) tree based on nuclear ribosomal internal transcribed spacer region (nrITS) and three single-copy nuclear genes data (Acc1 + Pgk1 + DMC1) showed that polyploid species with the St genome were separated into seven genera with StStHH, StStYY, StStYYHH, StStYYPP, StStYYWW, StStPP, and StStEE genome constitutions, moreover, the polyploid species in Caucasus, America, and Australia have independent polyploidization events. The ML tree for the chloroplast DNA fragments (matK + rbcL + trnL-trnF) displayed that the P genome served as a maternal donor of Kengyilia melanthera and K. dingqinensis from the Hengduan Mountains region, while the St or StY genome served as the maternal donor of other St-genome containing species. Herein, we reported the genomic constitution of Kengyilia tibetica, K. changduensis, and K. dingqinensis with the StStYYPP genome for the first time.</p><p><strong>Conclusions: </strong>The St-genome-containing polyploid species should be treated as distinct genera according to different genome constitutions, and those species experienced independent allo-polyploidization events in different distribution regions and had two relatively independent maternal origins from the P or St/StY genomes. Besides, the Xp genome might have contributed to the unknown Y genome formation.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"183"},"PeriodicalIF":4.3,"publicationDate":"2025-02-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11817382/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143398277","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}
Pub Date : 2025-02-12DOI: 10.1186/s12870-025-06200-x
Yi Dai, Yilei Wu, Dake Zhao, Yupeng Cun
Background: Aconitum is an important medicinal genus widely used in traditional Chinese medicine, which produces types of diterpenoid alkaloids (DA) among different species. We performed whole genome resequencing (WGS) research in Aconitum spp., and wish to find diterpenoid alkaloids related genetic variations.
Results: In this study, we re-sequenced 150 Aconitum vilmorinianum (A. vilmorinianum) including 102 from the cultivation garden and 48 from the wild, as well as nine wild samples of Aconitum weixiense. The intra-population differentiation of A. vilmorinianum was detected by evolutionary tree and population structure inference. We identify 47 DA biosynthesis genes that might be highly associated with the specialization of DA based on whole-genome resequencing. Of 616 significant SNPs and 105 significant InDels among these genes could be developed as polymorphic molecular markers capable of effectively recognizing A. vilmorinianum from A. weixiense. Furthermore, the significant SNPs and InDels were almost homozygous alternates in A. weixiense, whereas they tended to be homozygous references in the A. vilmorinianum.
Conclusions: Our results discussed the difference in genetic background in A. vilmorinianum compared to A. weixiense and these high-quality DA biosynthesis-associated polymorphic locus provided useful genetic information for discrimination of A. vilmorinianum and could serve as a vehicle to study the mechanism of DA differentiation in Aconitum.
{"title":"Whole-genome sequencing revealed genetic basis of diterpenoid alkaloid difference in Aconitum vilmorinianum.","authors":"Yi Dai, Yilei Wu, Dake Zhao, Yupeng Cun","doi":"10.1186/s12870-025-06200-x","DOIUrl":"10.1186/s12870-025-06200-x","url":null,"abstract":"<p><strong>Background: </strong>Aconitum is an important medicinal genus widely used in traditional Chinese medicine, which produces types of diterpenoid alkaloids (DA) among different species. We performed whole genome resequencing (WGS) research in Aconitum spp., and wish to find diterpenoid alkaloids related genetic variations.</p><p><strong>Results: </strong>In this study, we re-sequenced 150 Aconitum vilmorinianum (A. vilmorinianum) including 102 from the cultivation garden and 48 from the wild, as well as nine wild samples of Aconitum weixiense. The intra-population differentiation of A. vilmorinianum was detected by evolutionary tree and population structure inference. We identify 47 DA biosynthesis genes that might be highly associated with the specialization of DA based on whole-genome resequencing. Of 616 significant SNPs and 105 significant InDels among these genes could be developed as polymorphic molecular markers capable of effectively recognizing A. vilmorinianum from A. weixiense. Furthermore, the significant SNPs and InDels were almost homozygous alternates in A. weixiense, whereas they tended to be homozygous references in the A. vilmorinianum.</p><p><strong>Conclusions: </strong>Our results discussed the difference in genetic background in A. vilmorinianum compared to A. weixiense and these high-quality DA biosynthesis-associated polymorphic locus provided useful genetic information for discrimination of A. vilmorinianum and could serve as a vehicle to study the mechanism of DA differentiation in Aconitum.</p>","PeriodicalId":9198,"journal":{"name":"BMC Plant Biology","volume":"25 1","pages":"184"},"PeriodicalIF":4.3,"publicationDate":"2025-02-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11817038/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143397829","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}