Yuanzheng Yue, Wuwei Zhu, Jiahui Wang, Tengteng Wang, Lisha Shi, Hannah Rae Thomas, Huirong Hu, Lianggui Wang
{"title":"Integration of DNA Methylation, MicroRNAome, Degradome and Transcriptome Provides Insights into Petunia Anther Development.","authors":"Yuanzheng Yue, Wuwei Zhu, Jiahui Wang, Tengteng Wang, Lisha Shi, Hannah Rae Thomas, Huirong Hu, Lianggui Wang","doi":"10.1093/pcp/pcae126","DOIUrl":"10.1093/pcp/pcae126","url":null,"abstract":"<p><p>Petunia hybrida is an annual herb flower that is prevalently cultivated both in public landscaping and home gardening. Anthers are vital reproductive organs for plants, but the molecular mechanism controlling petunia anther development remains elusive. In this work, we combined DNA methylation, microRNAome, degradome and transcriptome data to generate a comprehensive resource focused on exploring the complex molecular mechanism of petunia anther development. This study shows that DNA methylation could have an important impact in repressing the anther-expressed genes in the late stages of anther maturation. A total of 8,096 anther-preferential genes and 149 microRNAs (miRNAs) were identified that highly expressed in the five typical petunia anther developmental stages. Gene Ontology enrichment analysis of differentially expressed genes as well as miRNAs target genes revealed that metabolic, cellular and single-organism processes were significantly activated during the anther maturation processes. Moreover, a co-expression regulatory network for five typical anther development stages was constructed based on transcriptomic data, in which two hub transcription factors, PhERF48 and PhMS1, were demonstrated to be important regulatory genes for male fertility. Furthermore, two DNA demethylase proteins (PhDME and PhDML3) and three methyl-CpG-binding-domain proteins (PhMBD2, PhMBD3 and PhMBD4) were identified as potential critical DNA methylation regulators in petunia anther development. Our results provide new knowledge regarding the regulatory mechanism of petunia anther development, which will support the breeding of novel sterile petunia lines in the future.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"36-49"},"PeriodicalIF":3.9,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142823758","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":"Discovery of 4-(2-phenylethynyl) benzoic acid as a potential potent chemical pruner.","authors":"Pingping Fang, Xiaofang Li, Mingxuan Li, Zhen Shi, Yusu Cheng, Jiazhong Shen, Chuanqing Zhang, Ting Sun, Kang Ning, Xinyang Wu, Dong Fang, Pei Xu","doi":"10.1093/pcp/pcae142","DOIUrl":"10.1093/pcp/pcae142","url":null,"abstract":"<p><p>Rocketing labor cost is a major challenge threatening agricultural sustainability and food security worldwide. The replacement of manual pruning of horticultural plants with chemical pruning has long been a goal for saving cost and reducing virus spreading. Here, guided by the structure-function relationship of allelochemical benzoic acid derivatives, we have identified 4-(2-phenylethynyl)-benzoicacid (PEBA) as a highly bioactive compound. PEBA arrested tomato seed germination at a concentration as low as 0.5 μM, and effectively suppressed lateral branching at 10-100 μM. In field conditions, a foliar spraying of 25 μM PEBA altered tomato plant architecture by repressing emergence and elongation of lateral buds, without significantly affecting plant growth and final fruit yield. Moreover, PEBA could also inhibit seed germination in cereals, albeit at a lower efficacy. The application of 500 μM and 750 μM PEBA profoundly curbed preharvest sprouting in wheat and rice. Acute toxicity analysis using silkworm and Trichogramma chilonis revealed that PEBA posed a low risk of toxicity. The persistence analysis further indicated that residue levels of PEBA in various plant organs were very low following applications. The inhibitory effect of PEBA on tomato seed germination was associated with the suppression of GA1 accumulation and reactive oxygen species generation, while its effect on lateral bud outgrowth were related to perturbations in the plant hormones and the modulation of genes involved in secondary metabolism and those encoding ABC transporters. Collectively, our findings demonstrate the potential of PEBA as a potent plant growth regulator with significant value for chemical pruning.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"75-88"},"PeriodicalIF":3.9,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142829760","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":"Catalytic mechanism underlying the regiospecificity of coumarin-substrate transmembrane prenyltransferases in Apiaceae.","authors":"Junwen Han, Ryosuke Munakata, Hironobu Takahashi, Takao Koeduka, Mayumi Kubota, Eiko Moriyoshi, Alain Hehn, Akifumi Sugiyama, Kazufumi Yazaki","doi":"10.1093/pcp/pcae134","DOIUrl":"10.1093/pcp/pcae134","url":null,"abstract":"<p><p>Plant membrane-bound prenyltransferases (PTs) catalyze the transfer of prenyl groups to acceptor substrates, phenols, using prenyl diphosphates as the donor substrate. The presence of prenyl residues in the reaction products, prenylated phenols, is key to the expression of a variety of physiological activities. Plant PTs generally exhibit high specificities for both substrate recognition and prenylation sites, while the molecular mechanism involved in these enzymatic properties is largely unknown. In this study, we performed a systematic biochemical analysis to elucidate the catalytic mechanism responsible for the reaction specificity of plant PTs. Using two representative PTs, PsPT1 and PsPT2, from parsnip (Pastinaca sativa, Apiaceae), which differ only in the regiospecificity of the prenylation site, we performed domain swapping and site-directed mutagenesis of these PTs, followed by detailed enzymatic analysis combined with 3D modeling. As a result, we discovered the domains that control prenylation site specificity and further defined key amino acid residues responsible for the catalytic mechanism. In addition, we showed that the control mechanism of prenylation specificity revealed here is also highly conserved among coumarin-substrate PTs. These data suggest that the regulatory domain revealed here is commonly involved in prenylation regiospecificity in Apiaceae PTs.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"1-14"},"PeriodicalIF":3.9,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11775389/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142688657","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}
Jihwan Park, Shota Yamamoto, Ayako Tsushima, Koh Aoki
{"title":"Host responses to haustorium invasion of the stem parasitic plant, Cuscuta campestris, differ from responses to wounding.","authors":"Jihwan Park, Shota Yamamoto, Ayako Tsushima, Koh Aoki","doi":"10.1093/pcp/pcae130","DOIUrl":"10.1093/pcp/pcae130","url":null,"abstract":"<p><p>The parasitic mechanism employed by the stem parasitic plant, Cuscuta campestris, involves degradation of the host epidermis and intrusion of the cortical tissue of the host stem by a specialized organ called the haustorium. In host plants, the mechanical stimuli associated with this degradation and intrusion of host tissues is considered to be comparable to wounding. However, it has not yet been clarified whether parasitic invasion and wounding induce equivalent responses in host plants. In this study, we demonstrated that parasitic intrusion-induced responses that were comparable to wounding in the host plant, Arabidopsis thaliana, including upregulation of Arabidopsis NAC DOMAIN-CONTAINING PROTEIN 71 (ANAC071), which is a key transcription factor associated with wound repair, cell division, and vascular development. Despite these similarities, we found that the mechanism regulating the induction of cell division- and vascular development-related genes at the host-parasite interface differed from that associated with wound repair. Specifically, ANAC071 was not required for the induction of cell division-related genes, as their upregulation was observed in anac071/096/011 triple mutants as well as in wild-type host plants. We also found that neither auxin nor ethylene plays a significant role in inducing the expression of vascular development-related genes. Thus, the findings show that the mechanisms responsible for upregulating cell division- and vascular development-related genes differ between parasitic and wound repair responses.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":"50-59"},"PeriodicalIF":3.9,"publicationDate":"2025-01-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142807886","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}
Loreen Linnenbrügger, Lennart Nico Doering, Louisa-Marlen Tägtmeyer, Kerstin Fischer, Antje von Schaewen
{"title":"Evidence for Peroxisomal Redundancy among the Glucose-6-phosphate Dehydrogenase Isoforms of Arabidopsis thaliana.","authors":"Loreen Linnenbrügger, Lennart Nico Doering, Louisa-Marlen Tägtmeyer, Kerstin Fischer, Antje von Schaewen","doi":"10.1093/pcp/pcaf012","DOIUrl":"https://doi.org/10.1093/pcp/pcaf012","url":null,"abstract":"<p><p>The oxidative pentose phosphate pathway (OPPP) plays an important role for the generation of reducing power in all eukaryotes. In plant cells the OPPP operates in several cellular compartments, but as full cycle only in the plastid stroma where it is essential. As suggested by our recent results, OPPP reactions are also mandatory inside peroxisomes, at least during fertilisation. For the first enzyme of the OPPP, glucose-6-phosphate dehydrogenase (G6PD), so far only one Arabidopsis isoform (G6PD1) was shown to be directed to peroxisomes under specific circumstances. Since g6pd1 knock-out plants are viable, we aimed at elucidating potential redundancy regarding peroxisomal targeting among the other G6PD isoforms. Localisation studies of so far cytosolic annotated G6PD5 and G6PD6 (both ending -PTL>) using different reporter fusions of full-length versus the last 50 amino acids revealed that GFP-C-short versions are efficiently imported into peroxisomes. Modification of the final tripeptide to a canonical peroxisomal targeting signal type 1 (PTS1) also resulted in peroxisomal localisation of the full-length versions, and revealed that G6PD5/6 import may occur as homo- or heterodimer. Interestingly, the new non-canonical PTS1 motif is highly conserved among the cytosolic G6PD isoforms of the Angiosperms, whereas members of the Poaceae (rice, maize) possess two variants, one ending with an additional amino acid (-PTLA>), and the other extended by a stronger PTS1 motif. From both evolutionary and physiological perspectives, we postulate that import as homo- and heterodimer restricted the acquisition of more efficient peroxisomal targeting motifs to leave some G6PDH activity to the cytosol.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143010303","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":"Auxin fluctuation and PIN polarization in moss leaf cell reprogramming.","authors":"Han Tang, Li-Hang Chen, Jiří Friml","doi":"10.1093/pcp/pcaf008","DOIUrl":"https://doi.org/10.1093/pcp/pcaf008","url":null,"abstract":"<p><p>Auxin and its PIN-FORMED (PIN) exporters are essential for tissue repair and regeneration in flowering plants. To gain insight into the evolution of this mechanism, we investigated their roles in leaves excised from Physcomitrium patens, a bryophyte known for its remarkable cell reprogramming capacity. We used various approaches to manipulate auxin levels, including exogenous application, pharmacological manipulations, and auxin biosynthesis mutants. We observed no significant effect on the rate of cell reprogramming. Rather, our analysis of auxin dynamics revealed a decrease in auxin levels upon excision, which was followed by a local increase before the reprogramming process began. Mutant analysis revealed that PpPINs are required for effective cell reprogramming, and endogenously expressed PpPINA-GFP accumulates polarly at sites that will develop into future filamentous stem cells. In addition, hyperpolarized PpPINA variants carrying mutated phosphorylation sites showed a marked delay in reprogramming, whereas endogenous or non-polar versions do not have this effect. These results underscore that both, the levels and the polarity of PpPINA are important for efficient cell reprogramming. Overall, these findings highlight the pivotal role of PIN polarity in plant regeneration. Furthermore, they suggest that understanding polarity mechanisms could have broader implications for improving regenerative processes across various plant species.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143010287","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}
Mie N Honjo, Naoko Emura, Mari Kamitani, Hiroshi Kudoh
{"title":"Cold suppresses virus accumulation and alters the host transcriptomic response in the turnip mosaic virus ̶ Arabidopsis halleri system.","authors":"Mie N Honjo, Naoko Emura, Mari Kamitani, Hiroshi Kudoh","doi":"10.1093/pcp/pcaf010","DOIUrl":"https://doi.org/10.1093/pcp/pcaf010","url":null,"abstract":"<p><p>Since plant viruses cause lifelong infections, virus-plant interactions are exposed to large temperature fluctuations in evergreen perennials. In such circumstances, virus-plant interactions are expected to change significantly between the warm and cold seasons. However, few studies have investigated the effects of cold temperatures on virus-plant interactions. Here, we show that in a persistent infection system of the turnip mosaic virus (TuMV) -Arabidopsis halleri, cold temperatures lead to slow viral replication/spreading within the host, slow attenuation of host symptoms, and slow cold-specific transcriptomic responses. Many differentially expressed genes (DEGs) were detected between virus-inoculated and mock-inoculated plants under warm and cold conditions; however, the sets of DEGs and response timings were temperature-dependent. Under cold temperatures, the expression of photosynthesis-related genes decreased in the early stages of infection. However, it recovered to the same level as that in uninfected plants in the later stages. In contrast, the transcriptomic changes under warm conditions suggest that viral infections cause auxin-signaling disruption. These responses coincided with the inhibition of host growth. We identified 6 cold- and 38 warm-specific DEGs, that changed their expression in response to TuMV infection under more than half of the conditions for either cold or warm temperatures. Further validation of the putative relationships between transcriptomic and phenotypic responses of the host is required. Our findings on temperature-dependent host responses at both symptomatic and transcriptomic levels help us understand how warm and cold temperatures affect virus-plant interactions in seasonal environments.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143010290","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}
Flavia Pavan, Eléanore Lacoste, Vincent Castric, Sylvain Legrand
{"title":"Scenarios for the emergence of new miRNA genes in the plant Arabidopsis halleri.","authors":"Flavia Pavan, Eléanore Lacoste, Vincent Castric, Sylvain Legrand","doi":"10.1093/pcp/pcaf004","DOIUrl":"https://doi.org/10.1093/pcp/pcaf004","url":null,"abstract":"<p><p>MicroRNAs (miRNAs) are central players of the regulation of gene expression in Eukaryotes. The repertoires of miRNA genes vary drastically even among closely related species, indicating that they are evolutionarily labile. However, the processes by which they originate over the course of evolution and the nature of their progenitors across the genome remain poorly understood. Here we analyzed miRNA genes in Arabidopsis halleri, a plant species where we recently documented a large number of species-specific miRNA genes, likely to represent recent events of emergence. Analysis of sequence homology across the genome indicates that a diversity of sources contributes to the emergence of new miRNA genes, including inverted duplications from protein-coding genes, rearrangements of transposable element sequences and duplications of preexisting miRNA genes. Our observations indicate that the origin from protein-coding genes was less common than was previously considered. In contrast, we estimate that almost half of the new miRNA genes likely emerged from transposable elements. Miniature inverted transposable elements (MITE) seem to be particularly important contributors to new miRNA genes, with the Harbinger and Mariner transposable element superfamilies representing disproportionate sources for their emergence. We further analyzed the recent expansion of a miRNA family derived from MuDR elements, and the duplication of miRNA genes formed by two hAT transposons. Overall, our results illustrate the rapid pace at which new regulatory elements can arise from the modification of preexisting sequences in a genome, and highlight the central role of certain categories of transposable elements in this process.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143010309","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}
Fanmiao Wang, Keitaro Tanoi, Takaki Yamauchi, Ken Naito
{"title":"Multi-layered Apoplastic Barrier Underlying the Ability Of Na+ Exclusion In Vigna Marina.","authors":"Fanmiao Wang, Keitaro Tanoi, Takaki Yamauchi, Ken Naito","doi":"10.1093/pcp/pcaf005","DOIUrl":"https://doi.org/10.1093/pcp/pcaf005","url":null,"abstract":"<p><p>Soil salinization and ground water depletion are increasingly constraining crop production. Identifying useful mechanisms of salt tolerance is an important step towards development of salt-tolerant crops. Of particular interest are mechanisms that are present in wild crop relatives, as they may have greater stress tolerance than crop species. The coastal species Vigna marina is one of the promising plant resources for salt tolerance. V. luteola is another wild species with diverse habitats including seaside and riverbank, hereafter, V. luteola-beach and V. luteola-river, respectively. By comparative transcriptome and histological analyses, this study elucidated one important aspect of how V. marina achieves an extraordinary ability to suppress Na+ uptake. Under salt stress, V. marina specifically upregulated genes involved in Casparian strip formation and developed a multi-layered lignified apoplastic barrier around endodermis, whereas V. luteola-beach formed typical, band-like Casparian strips, and V. luteola-river formed only spot-like Casparian strips. As such, the ability of developing apoplastic barrier strongly correlated with those of suppressing Na+ uptake. The disruption of lignified barrier led to a dramatic increase of Na+ allocation to the shoot in V. marina, which was manifested in leaf etiolation and burning. Interestingly, despite the presence of reinforced apoplastic barrier, V. marina maintained transport of essential ions including K+, Mg2+, and Ca2+. This study shows the multi-layered Casparian strip-like structure plays important role in salt tolerance.</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142953958","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":"Excitation Spillover from PSII to PSI in Leaves at 77K.","authors":"Ichiro Terashima, Riichi Oguchi, Kimie Atsuzawa, Yasuko Kaneko, Masaru Kono","doi":"10.1093/pcp/pcaf002","DOIUrl":"10.1093/pcp/pcaf002","url":null,"abstract":"<p><p>Heterogeneous distribution of PSI and PSII in thick grana in shade chloroplasts is argued to hinder spillover of chlorophyll excitations from PSII to PSI. To examine this dogma, we measured fluorescence induction at 77K at 690 nm (PSII) and 760 nm (mostly PSI) in the leaf discs of Spinacia oleracea, Cucumis sativus and shade tolerant Alocasia odora, grown at high and low light, and quantified their spillover capacities. PSI fluorescence (FI) consists of the intrinsic PSI fluorescence (FIα) and fluorescence caused by excitations spilt over from PSII (FIβ). When FI and FII parameters between State 1 and State 2, induced by weak far-red and blue light, were compared, PSII maximum fluorescence (FIIm) and FIβ were greater, and FIα was smaller in State 1 and thereby the spillover ratio, FIβ/(FIα+FIβ), was greater in State 1. When non-photochemical quenching (NPQ) was induced, the spillover ratio decreased. Since analyses of Fv/Fm spectra tentatively suggested that about 15% of Fm at 760 nm was from PSII, all data were corrected accordingly. Even after the correction, the spillover ratio in FIm in State 1 ranged from 16 to 28%. The spillover ratios did not greatly differ between the species or growth light levels. Although extensive grana in low light grown plants would suggest that PSII and PSI are too separated for spillover, the ratios of non-appressed thylakoid membranes/total thylakoid membranes in A. odora chloroplasts were little affected by growth light and more than 40%. Abundant non-appressed thylakoids and margins of appressed-thylakoids would enable efficient spillover. (250 words).</p>","PeriodicalId":20575,"journal":{"name":"Plant and Cell Physiology","volume":" ","pages":""},"PeriodicalIF":3.9,"publicationDate":"2025-01-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143754241","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}