{"title":"Revalidation of the ICE1–CBF Regulatory Model in Arabidopsis Cold Stress Response","authors":"Jihyeon Park, Jae-Hoon Jung","doi":"10.1007/s12374-024-09440-w","DOIUrl":"https://doi.org/10.1007/s12374-024-09440-w","url":null,"abstract":"<p>Plants encountering cold stress undergo physiological adaptations crucial for acquiring freezing tolerance, involving the transcriptional activation of genes encoding C-repeat binding factors (CBFs). Inducer of CBF expression 1 (ICE1) has long been acknowledged as a master regulator in the cold response, positively modulating the expression of cold-inducible <i>CBF</i> genes. However, recent studies that ICE1 is not involved in the regulation of <i>CBF</i> genes have challenged this established notion, prompting a critical reevaluation of the ICE1-CBF regulatory model. To address this controversy, <i>ice1-2</i> mutants were germinated on media containing 1% glucose and grown under short periodic conditions, ensuring comparable growth to wild-type (WT) plants before cold treatment. Surprisingly, our modified growth conditions revealed no discernible differences in the cold induction of <i>CBF</i> genes and their downstream targets between WT plants and <i>ice1-2</i> mutants. Moreover, cold-induced degradation of ICE1, mediated by the E3 ubiquitin ligase high expression of osmotically-responsive genes 1 (HOS1), was notably absent in two different <i>ICE1</i> transgenic plants. Consistent with this, cold-responsive gene expression profiling showed no difference between WT plants and <i>hos1</i> mutants. All our data strongly suggest that the HOS1-ICE1 regulatory module does not play a role in the cold regulation of the <i>CBF</i> signaling pathway in <i>Arabidopsis</i>.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142250113","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}
Giha Song, Sang Ryeol Park, Yujeong Jeong, Jinjeong Lee, Duk-Ju Hwang, Nam-Chon Paek, Seungmin Son
{"title":"OsWRKY9 is Involved in Transcriptional Regulatory Cascade Enhancing Broad-Spectrum Disease Resistance","authors":"Giha Song, Sang Ryeol Park, Yujeong Jeong, Jinjeong Lee, Duk-Ju Hwang, Nam-Chon Paek, Seungmin Son","doi":"10.1007/s12374-024-09439-3","DOIUrl":"https://doi.org/10.1007/s12374-024-09439-3","url":null,"abstract":"<p>Diverse pathogens, including <i>Fusarium fujikuroi</i> and <i>Xanthomonas oryzae</i> pv. <i>oryzae</i> (<i>Xoo</i>), cause significant yield losses in rice (<i>Oryza sativa</i>). The situation is expected to worsen due to rapid climate change. Thus, identifying novel genes conferring innate immunity against these pathogens is crucial for global food security. WRKY transcription factors are involved in various plant processes, including innate immunity. In rice, there are 125 OsWRKYs, with some functions reported. However, the roles of many OsWRKYs in rice immunity remain largely unknown. In this study, we investigate the role of OsWRKY9 in broad-spectrum disease resistance. <i>OsWRKY9</i> transcripts increased in response to <i>F. fujikuroi</i> and <i>Xoo</i>. The promoter of <i>OsWRKY9</i> was indirectly activated by OsWRKY65, which confers broad-spectrum resistance to <i>F. fujikuroi</i> and <i>Xoo</i>. Moreover, <i>OsWRKY9</i>-overexpressing transgenic plants exhibited enhanced resistance to both pathogens in a manner similar to transgenic plants overexpressing <i>OsWRKY65</i>. Additionally, OsWRKY9 modulated the expression of various defense-related genes regulated by OsWRKY65. These results indicate that the OsWRKY65-OsWRKY9 module enhances resistance to bakanae disease and bacterial blight.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142250029","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}
Eun Young Kim, Sang Dae Yun, Myung-Hee Kim, Ji-Hyun Kim, Sung-Aeong Oh, Jung Hyun Lee, Ye-Jin Son, Woo-Jong Hong, Chan Mi Yun, Sunok Moon, Ki-Hong Jung, Yu-Jin Kim, Soon Ki Park
{"title":"Pollen-Expressed Plant U-Box Protein, OsPUB14 Involves in Rice Fertility and Degrades OsMTD2","authors":"Eun Young Kim, Sang Dae Yun, Myung-Hee Kim, Ji-Hyun Kim, Sung-Aeong Oh, Jung Hyun Lee, Ye-Jin Son, Woo-Jong Hong, Chan Mi Yun, Sunok Moon, Ki-Hong Jung, Yu-Jin Kim, Soon Ki Park","doi":"10.1007/s12374-024-09441-9","DOIUrl":"https://doi.org/10.1007/s12374-024-09441-9","url":null,"abstract":"<p>Understanding the intricacies of pollen tube growth in cereal crops, such as rice, is crucial for understanding crossbreeding, seed formation, and crop productivity. In this study, we investigated the molecular mechanisms underlying pollen tube germination and elongation in rice, focusing on the interaction between OsPUB14 and OsMTD2 and its impact on reactive oxygen species (ROS) regulation. Expression studies revealed that <i>OsPUB14</i> was highly expressed in pollen and anther tissues, indicating its involvement in pollen function. We demonstrated that OsPUB14 belonging to group II U-box domain proteins, interacts with the kinase domain of OsMTD2 (a pollen-specific CrRLK1L member) and degrades it. This interaction subsequently reduces OsMTD2-mediated ROS generation. Moreover, the overexpression of <i>OsPUB14</i> resulted in decreased ROS levels and reduced fertility in rice plants, emphasizing its role in reproductive processes. Yeast two-hybrid screening identified OsCRK10P and OsNET2D as potential interactors of OsPUB14, further expanding our understanding of the regulatory networks associated with pollen development. This study provides insight into the intricate interplay between pollen-specific plant U-box domain proteins (PUBs), demonstrating their roles in regulating ROS levels and ultimately influencing plant fertility.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142250028","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":"Effects of CO2 Concentration and Temperature on Growth Characteristics, Physiological Activities, and Antioxidant Activities of Angelica gigas Nakai","authors":"Yeong-Bae Yun, Hyun-Jung Koo, Hae-Yun Kwon, Yeonggeun Song, Kyeong-Cheol Lee, Yurry Um","doi":"10.1007/s12374-024-09437-5","DOIUrl":"https://doi.org/10.1007/s12374-024-09437-5","url":null,"abstract":"<p><i>Angelica gigas</i> Nakai is an important medicinal plant. Several environmental factors such as altitude, physiognomy, and atmospheric temperature can affect the cultivation of <i>A. gigas</i>. Therefore, climate change is likely to influence the growth of <i>A. gigas</i> and the synthesis of its active ingredients. This study aimed to investigate the effects of different carbon dioxide concentrations and temperatures according to Shared Socioeconomic Pathways (SSP) scenarios (SSP1-2.6, SSP2-4.5, SSP3-7.0, SSP5-8.5) on the growth, physiological activities, and antioxidant activities of <i>A. gigas</i>. The photosynthesis rate of <i>A. gigas</i> under SSP1-2.6 and SSP5-8.5 conditions showed a steady reduction. Chlorophyll a, total chlorophyll, and carotenoid content decreased with the prolongation of the growing season under climate change conditions. Chlorophyll a fluorescence showed significantly higher RC/CSo, RC/ABS, PI<sub>abs</sub>, SFI<sub>abs</sub> in higher CO<sub>2</sub> concentration and temperature conditions. Only the total dry weight of <i>A. gigas</i> for each climate change scenario was significantly different, while the other growth characteristics were not significantly different because of high inter-individual variation. The antioxidant activities of <i>A. gigas</i> (DPPH, ABTS, and NO scavenging activities) under each of the different conditions showed no significant differences. The reducing power was significantly increased in SSP5-8.5 compared to SSP1-2.6. The differences in phenolic contents of both aerial parts and root parts were not statistically significant, while the flavonoid content of aerial parts increased depending on the temperature and CO<sub>2</sub> concentration. These results indicated that climate change can affect the growth, physiological activities, and antioxidant activities of <i>A. gigas</i> Nakai. Our findings underline the need to develop strategies to overcome the adverse aspects of climate change.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142250027","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":"Many Flowers but few Fruits: Pollinator and Pollen Limitation in the Early-Spring Flowering Cold Desert Perennial Iris tenuifolia","authors":"Jannathan Mamut, Caiyun Zhang, Dunyan Tan","doi":"10.1007/s12374-024-09436-6","DOIUrl":"https://doi.org/10.1007/s12374-024-09436-6","url":null,"abstract":"<p>Most flowers of plants did not develop into fruits due to limitations of pollen and resources for plant growth, but few studies have investigated effects of the abiotic environment in relation to pollination on seed production. Here we examine the flowering biology, the effect of flower display, resources, pollen availability and weather conditions on reproductive success of <i>Iris tenuifolia</i>. Flowers of <i>I. tenuifolia</i> began to open in late March and mid – April, and it exhibited a concentrated flowering pattern. Four types of bees were effective pollinators of this species. Flowers of <i>I. tenuifolia</i> are self-incompatible and not capable of autonomous selfing, outcross pollination ensures reproductive success in natural population. Plants with high numbers of flowers are attractive to pollinators and received significantly more visits and more pollen than flowers with a low number of flowers, this increases fruit and seed set. Resource addition of water and fertilizer had no significant effect on seed production, but weather conditions affected pollinator activity and influence female reproduction through pollen availability. Our results indicated that the desert environment in early spring can reduce the visitation by pollinators, further reducing the outcrossing success of plants, which leads to low seed set in this self-incompatible species.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141883079","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}
Sivabalan Karthik, Seong Ju Han, Jia Chae, Hye Jeong Kim, Jee Hye Kim, Young-Soo Chung, Jae Bok Heo
{"title":"The Function of Like Heterochromatin Protein 1 (LHP1) as an Epigenetic Regulator of Plant Development","authors":"Sivabalan Karthik, Seong Ju Han, Jia Chae, Hye Jeong Kim, Jee Hye Kim, Young-Soo Chung, Jae Bok Heo","doi":"10.1007/s12374-024-09435-7","DOIUrl":"https://doi.org/10.1007/s12374-024-09435-7","url":null,"abstract":"<p>Plants have the fascinating ability to regulate their genetic expression through epigenetic mechanisms. Polycomb group (PcG) proteins in Polycomb repressive complexes (PRC1 and PRC2) especially regulate cellular and developmental processes in eukaryotes through epigenetic mechanisms. <i>Arabidopsis thaliana</i> has a fascinating name, LIKE HETEROCHROMATIN PROTEIN 1 (LHP1), called TERMINAL FLOWER 2 (TFL2). This protein was initially recognized as the plant equivalent of animal HP1 due to the presence of a chromo domain and a chromo shadow domain. It can bind to the trimethylated lysine 27 of histone H3 (H3K27me3) mark spread throughout the genome and regulate gene expression. This is crucial for the plant PcG system, which PRC2 establishes for epigenetic control. Although LHP1 has been found to perform diverse functions, it is still unclear whether these functions are carried out through similar mechanisms and whether it regulates the same target genes. This highlights the need for further research on LHP1 to better understand its mechanisms and functions. The following review provides detailed information about LHP1, which is closely linked to histone marks and the regulation of gene expression and explores how LHP1 influences flower timing and root development to improve crop traits. Recent progress in tomato and soybean production highlights the crucial role of LHP1 in shaping crop characteristics. The review suggests that LHP1 may control H3K27me3 in different plant species by regulating specific genes through epigenetic mechanisms. In summary, it emphasizes the importance of understanding LHP1’s role in plant development for breeding purposes.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-06-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141503481","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}
Chunshu Lyu, Mengting Mao, Jianyu Huo, Shuning Cui, Lugang Zhang, Shanshan Nie
{"title":"Functional Characterization of Chinese Cabbage BrCML49 Gene in Pollen Germination and Pollen Tube Elongation and the Regulation of Ca2+-Mediated Self-Incompatibility Response","authors":"Chunshu Lyu, Mengting Mao, Jianyu Huo, Shuning Cui, Lugang Zhang, Shanshan Nie","doi":"10.1007/s12374-024-09434-8","DOIUrl":"https://doi.org/10.1007/s12374-024-09434-8","url":null,"abstract":"","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-06-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141347754","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":"Light-Induced Degradation and Nocturnal Retrograde Movement of Nonexpressor of Pathogenesis-Related Genes 1 from the Chloroplasts to the Nucleus","authors":"So Yeon Seo, Yu Mi Kim, Ky Young Park","doi":"10.1007/s12374-024-09432-w","DOIUrl":"https://doi.org/10.1007/s12374-024-09432-w","url":null,"abstract":"<p>This study investigated the complex interplay among circadian rhythms, redox balance, and retrograde signaling in plants, focusing on the role of nonexpressor of pathogenesis-related genes 1 (NPR1). Using transgenic tobacco expressing the NPR1-GFP, we observed circadian oscillations and nuclear accumulation during night and continuous night conditions, suggesting a link between circadian signals and environmental responses of NPR1. We found that NPR1 nuclear localization is influenced by light conditions and the levels of NADPH and NADP<sup>+</sup>, affecting its translocation from the chloroplasts to the nucleus and thereby indicating the circadian gene expression. Our findings on the upregulation of nuclear import components under dark conditions and in NPR1-overexpressing plants shed light on nuclear import processes, indicating the significance of importin proteins in protein translocation. This study enhances our understanding of how plants integrate circadian and redox signals to regulate environmental responses, providing insights into potential strategies for boosting plant resilience via the modulation of the NPR1 pathway.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-05-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141190256","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":"Rice H2-Type RING E3 Ligase Gene, OsSIRH2-3, Positively Regulates Salt Tolerance by Maintaining Na+/K+ Homeostasis","authors":"Min Seok Choi, Ju Hee Kim, Cheol Seong Jang","doi":"10.1007/s12374-024-09433-9","DOIUrl":"https://doi.org/10.1007/s12374-024-09433-9","url":null,"abstract":"<p>High soil salinity possesses a major challenge for plant growth and productivity. Plants have evolved various mechanisms to withstand the adverse effects of salt stress, including E3 ubiquitin ligases that label salt-responsive proteins for degradation. Here, we characterized the mechanisms RING E3 ubiquitin ligase OsSIRH2-3 (Oryza sativa Salt Induced RING H2-type-3 E3 ligase) used to facilitate salt tolerance in rice. <i>OsSIRH2-3</i> expression was upregulated under high NaCl concentrations and upon abscisic acid (ABA) treatment. OsSIRH2-3 was primarily found in the nucleus of rice protoplasts. The OsSIRH2-3 protein contains an H2-type-RING domain that confers E3 ligase activity. <i>OsSIRH2-3</i> overexpression was also found to be associated with enhanced salt tolerance in transgenic plants, decreased Na<sup>+</sup> accumulation in both roots and leaves, decreased Na<sup>+</sup> transport activity in the xylem sap, increased levels of proline and soluble sugars, elevated activity of reactive oxygen species scavenging enzymes, and altered expression of Na<sup>+</sup>/K<sup>+</sup> transporters. Furthermore, <i>OsSIRH2-3</i>-overexpressing plants also exhibited high sensitivity to exogenous ABA treatment. Our findings demonstrate that OsSIRH2-3 enhances salt tolerance by regulating Na<sup>+</sup>/K<sup>+</sup> homeostasis and modulating Na<sup>+</sup>/K<sup>+</sup> transporter expression. This study illuminates the molecular mechanisms involved in RING E3 ubiquitin ligase-mediated salt tolerance in rice and provides a potential strategy for enhancing crop productivity in saline environments.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-05-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141190243","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}
Heewon Moon, Byoung-Ho Hwang, Minkyu Park, Enamul Huq, Dong-Hwan Kim
{"title":"Time Course Transcriptomic Analysis of Cabbage (Brassica oleracea ssp. capitata L.) During Vernalization","authors":"Heewon Moon, Byoung-Ho Hwang, Minkyu Park, Enamul Huq, Dong-Hwan Kim","doi":"10.1007/s12374-024-09430-y","DOIUrl":"https://doi.org/10.1007/s12374-024-09430-y","url":null,"abstract":"<p>Long-term exposure to cold during the winter season, so-called vernalization, triggers the transition from the vegetative to the reproductive stage in many biennial and perennial plants. In the last decades, intensive researches have revealed the molecular mechanisms underlying this phenomenon, particularly using <i>Arabidopsis</i> model plant. Most Brassicaceae family plants, including the <i>Arabidopsis</i>, require vernalization for floral transition. Brassicaceae family plants can be classified into two groups: seed vernalization responsive type and plant vernalization responsive type. Cabbage belongs to plant vernalization responsive type. Molecular details on plant vernalization responsive trait of cabbage on vernalization are still poorly understood. In this study, we conducted a transcriptomic analysis of the cabbage inbred line ‘BN2348’ in response to vernalization. Similar to the case of <i>Arabidopsis</i>, two <i>VIN3</i> homologs (<i>BoVIN3.C3</i> and <i>BoVIN3.C2</i>) were highly induced by the exposure to long-term cold in <i>B. oleracea</i>. Our transcriptome analysis identified that two <i>FT</i> homologs (<i>BoFT.C2</i> and <i>BoFT.C6</i>) and three <i>SOC1</i> homologs (<i>BoSOC1.1.C4</i>, <i>BoSOC1.2.C4</i>, and <i>BoSOC1.C3</i>) were functioning for the regulation of floral transition in <i>B. oleracea</i>. In addition, by phylogenic and syntenic analyses, a total of five <i>FLC</i> homologs, named <i>BoFLC1.a</i>, <i>BoFLC1.b</i>, <i>BoFLC2</i>, <i>BoFLC3</i>, and <i>BoFLC5</i>, were identified in the genome of <i>B. oleracea</i>. Transcriptomic analysis indicated that these genes could be grouped into vernalization-responsive (<i>BoFLC2</i> and <i>BoFLC3</i>) and vernalization-insensitive genes (<i>BoFLC1.a</i>, <i>BoFLC1.b</i>, <i>and BoFLC5</i>). As green plant vernalization type, it might suggest the existence of vernalization-insensitive <i>BoFLC</i> homologs in young seedlings might be the reason why cabbage exhibits longer exposure of cold compared to seed vernalization type plants such as Chinese cabbage and <i>Arabidopsis</i>. These findings improve our understanding of the molecular dynamics underlying floral transition in cabbage plants.</p>","PeriodicalId":16762,"journal":{"name":"Journal of Plant Biology","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-05-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141190101","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}