{"title":"Sperm, eggs, pollen, and gelato, oh my!","authors":"Emma Whittington, Murielle Ålund","doi":"10.1002/mrd.23722","DOIUrl":"10.1002/mrd.23722","url":null,"abstract":"<p>On September 4, 2023, the sky cleared over Nynäshamn, Sweden, and researchers from across the globe gathered for the 16th Biology of Spermatozoa (BoS) meeting. What followed was a week fuelled by tasty food (find out below about the gelato!) and beautiful weather discussing sperm, eggs, reproductive fluids, fertility, and all things reproductive evolution. Held biennially from its inception in the early 1990s, BoS relocated from the Sheffield, UK area to Stockholm, Sweden in 2019 (Rowe & Rosengrave, <span>2020</span>) and is now organised by Rhonda Snook and John Fitzpatrick. The winning formula for this meeting is simple: gather scientists passionate about reproduction in one conference centre for a few days, where they will live and eat together surrounded by beautiful nature, favouring fruitful exchanges and collaborations.</p><p>BoS16 felt particularly special as regular participants finally reunited after a 4-year pandemic-induced hiatus. On top of this, BoS16 welcomed many new attendees from across the globe (over 20% of delegates and 11 of the 22 contributed talks), providing the opportunity to discover new cutting-edge research and expand the community and collaboration. The topics were varied and covered a broad range of methods and study systems, highlighting the breadth of the field of evolutionary reproductive biology. Researchers used extensive field sampling, meta-analyses, mathematical modelling, experimental evolution, proteomics, lipidomics, single-cell transcriptomics, gene editing and more across the animal and plant kingdoms to tackle exciting topics such as the huge variation in gamete morphology and reproductive tactics, the genetic basis of reproductive barriers, the influence of the female reproductive tract and external environment on fertilisation outcome, and nongenetic transgenerational inheritance.</p><p>The 2023 meeting was also a time to remember the late Professor Matthew (Matt) J.G. Gage (1967–2022), who was “the life and soul of Biology of Sperm meetings,” as highlighted by Dave Hosken in his dedicated talk. Matt's contributions to the field of evolutionary biology and to promoting and supporting young researchers have been excellently summarized elsewhere (Chapman & Stockley, <span>2022</span>; Hosken et al., <span>2022</span>; Vasudeva et al., <span>2022</span>). In memoriam, BoS16 introduced the Matt Gage Award for the best poster presented by an early career researcher. As decided by a panel of judges (Nina Wedell, Leigh Simmons, and Dave Hosken), the inaugural winners of this award were Lennart Winkler (TU Dresden) and Erin Macartney (Stockholm University) with their posters titled “Population density affects sexual selection in an insect model” and “Ejaculate traits and paternity share under sperm competition: a meta-analysis across species and fertilisation modes,” respectively. Winkler manipulated population density in red flour beetles (<i>Tribolium castaneum</i>) and showed that differences i","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 8","pages":""},"PeriodicalIF":2.7,"publicationDate":"2023-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mrd.23722","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138488026","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nathalie Oulhen, Shumpei Morita, Cosmo Pieplow, Thomas M. Onorato, Stephany Foster, Gary Wessel
{"title":"Conservation and contrast in cell states of echinoderm ovaries","authors":"Nathalie Oulhen, Shumpei Morita, Cosmo Pieplow, Thomas M. Onorato, Stephany Foster, Gary Wessel","doi":"10.1002/mrd.23721","DOIUrl":"10.1002/mrd.23721","url":null,"abstract":"<p>Echinoderms produce functional gametes throughout their lifespan, in some cases exceeding 200 years. The histology and ultrastructure of echinoderm ovaries has been described but how these ovaries function and maintain the production of high-quality gametes remains a mystery. Here, we present the first single cell RNA sequencing data sets of mature ovaries from two sea urchin species (<i>Strongylocentrotus purpuratus [Sp]</i> and <i>Lytechinus variegatus [Lv]</i>), and one sea star species (<i>Patiria miniata [Pm]</i>). We find 14 cell states in the Sp ovary, 16 cell states in the Lv ovary and 13 cell states in the ovary of the sea star. This resource is essential to understand the structure and functional biology of the ovary in echinoderms, and better informs decisions in the utilization of in situ RNA hybridization probes selective for various cell types. We link key genes with cell clusters in validation of this approach. This resource also aids in the identification of the stem cells for prolonged and continuous gamete production, is a foundation for testing changes in the annual reproductive cycle, and is essential for understanding the evolution of reproduction of this important phylum.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 8","pages":""},"PeriodicalIF":2.7,"publicationDate":"2023-12-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138488024","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Yu-Qing Su, Yan Lin, Shu-Jing Huang, Yan-Ting Lin, Jing Ran, Fang-Fang Yan, Xian-Lan Liu, Long-Cheng Hong, Mei Huang, Huan-Zhong Su, Xiao-Dong Zhang, Jian-Hong You, Yi-Ming Su
{"title":"Pyroptosis is involved in maternal nicotine exposure-induced metabolic associated fatty liver disease progression in offspring mice","authors":"Yu-Qing Su, Yan Lin, Shu-Jing Huang, Yan-Ting Lin, Jing Ran, Fang-Fang Yan, Xian-Lan Liu, Long-Cheng Hong, Mei Huang, Huan-Zhong Su, Xiao-Dong Zhang, Jian-Hong You, Yi-Ming Su","doi":"10.1002/mrd.23719","DOIUrl":"10.1002/mrd.23719","url":null,"abstract":"<p>We have investigated whether inflammasomes and pyroptosis are activated in maternal nicotine exposure (MNE) offspring mice and whether they are involved in MNE-promoted metabolic associated fatty liver disease (MAFLD) in adult offspring. We injected pregnant mice subcutaneously with saline vehicle or nicotine twice a day on gestational days 11–21. Offspring mice from both groups were fed with a normal diet (ND) or a high-fat diet (HFD) for 6 months at postnatal day 21 to develop the MAFLD model. Serum biochemical indices were analyzed, and liver histology was performed. The expression levels of inflammasome and pyroptosis proteins were detected by western blot. We found MNE significantly aggravated the injury of MAFLD in adult offspring mice. MNE activated inflammasomes and pyroptosis in both infant and adult offspring mice. HFD treatment activated inflammasomes but not pyroptosis at 3 months, while it showed no effect at 6 months. However, pyroptosis was more severe in MNE-HFD mice than in MNE-ND mice at 6 months. Taken together, our data suggest MNE promotes MAFLD progression in adult offspring mice. MNE also induces NLRP3 and NLRP6 inflammasome activation and pyroptosis in both infant and adult offspring mice, which may be involved in MNE-promoted progression of MAFLD.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 8","pages":""},"PeriodicalIF":2.7,"publicationDate":"2023-11-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138452022","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Epigenetic aging of mammalian gametes","authors":"Michael Klutstein, Nitzan Gonen","doi":"10.1002/mrd.23717","DOIUrl":"10.1002/mrd.23717","url":null,"abstract":"<p>The process of aging refers to physiological changes that occur to an organism as time progresses and involves changes to DNA, proteins, metabolism, cells, and organs. Like the rest of the cells in the body, gametes age, and it is well established that there is a decline in reproductive capabilities in females and males with aging. One of the major pathways known to be involved in aging is epigenetic changes. The epigenome is the multitude of chemical modifications performed on DNA and chromatin that affect the ability of chromatin to be transcribed. In this review, we explore the effects of aging on female and male gametes with a focus on the epigenetic changes that occur in gametes throughout aging. Quality decline in oocytes occurs at a relatively early age. Epigenetic changes constitute an important part of oocyte aging. DNA methylation is reduced with age, along with reduced expression of DNA methyltransferases (DNMTs). Histone deacetylases (HDAC) expression is also reduced, and a loss of heterochromatin marks occurs with age. As a consequence of heterochromatin loss, retrotransposon expression is elevated, and aged oocytes suffer from DNA damage. In sperm, aging affects sperm number, motility and fecundity, and epigenetic changes may constitute a part of this process. 5 methyl-cytosine (5mC) methylation is elevated in sperm from aged men, but methylation on Long interspersed nuclear elements (LINE) elements is reduced. Di and trimethylation of histone 3 lysine 9 (H3K9me2/3) is reduced in sperm from aged men and trimethylation of histone 3 lysine 27 (H3K27me3) is elevated. The protamine makeup of sperm from aged men is also changed, with reduced protamine expression and a misbalanced ratio between protamine proteins protamine P1 and protamine P2. The study of epigenetic reproductive aging is recently gaining interest. The current status of the field suggests that many aspects of gamete epigenetic aging are still open for investigation. The clinical applications of these investigations have far-reaching consequences for fertility and sociological human behavior.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"90 12","pages":"785-803"},"PeriodicalIF":2.5,"publicationDate":"2023-11-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mrd.23717","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138299623","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Shaomei Mo, Keming Deng, Congcong Cao, Yaoting Gui, Qian Ma
{"title":"FAM71D is dispensable for spermatogenesis and male fertility in mice","authors":"Shaomei Mo, Keming Deng, Congcong Cao, Yaoting Gui, Qian Ma","doi":"10.1002/mrd.23716","DOIUrl":"10.1002/mrd.23716","url":null,"abstract":"<p>In mammals, the generation of sperm cells capable of fertilization is a highly complex process including spermatogenesis in the testis and maturation in the epididymis. In our previous study, we have demonstrated that FAM71D (Family with sequence similarity 71, member D), which could interact with calmodulin, was highly expressed in human and mouse testis. To investigate the physiological role of FAM71D in spermatogenesis, we next generate <i>Fam71d</i> loss-of-function mouse model using CRISPR/Cas9 technology. We performed immunofluorescence and RT-qPCR to examine the protein and mRNA expression in testicular cells. We found that FAM71D was predominantly localized in the round and elongated spermatids. And FAM71D KO mice displayed normal development of germ cell and fertility. Furthermore, testicular histology and sperm concentration showed no significant difference between WT and KO mice. These data demonstrate that FAM71D is dispensable for mouse spermatogenesis and male fertility.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"90 12","pages":"804-809"},"PeriodicalIF":2.5,"publicationDate":"2023-11-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138295491","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lan Yuan, Yulin Li, Xueping Li, Zhu Mao, Yi Liu, Chengzhi Feng, Rongxing Jiang
{"title":"The molecular mechanism of naringin improving endometrial receptivity of OHSS rats","authors":"Lan Yuan, Yulin Li, Xueping Li, Zhu Mao, Yi Liu, Chengzhi Feng, Rongxing Jiang","doi":"10.1002/mrd.23715","DOIUrl":"10.1002/mrd.23715","url":null,"abstract":"<p>Controlling ovarian hyperstimulation syndrome (OHSS) in the controlled ovarian hyperstimulation treatment is necessary to increase the implantation success rate. This study aimed to explore the effect of naringin on the endometrial receptivity of OHSS rats. Female rats were randomly assigned to six groups: Blank, model, low-dose naringin (100 mg/kg/day), medium-dose naringin (200 mg/kg/day), high-dose naringin (400 mg/kg/day), and positive (0.18 mg/kg/day estradiol valerate) groups. Except for the blank group, rats established the OHSS model on Day 7, and their treatments were from Day 0 to 14, separately. Hematoxylin and eosin, immunohistochemical, and scanning electron microscopy were performed to detect the naringin effects on the endometrial receptivity of the OHSS model. Next, circRNAs transcriptome analysis was performed to screen circRNAs. Western blot analysis and real-time quantitative PCR were used to verify it. Our study showed that naringin treatments increased embryo number, endometrial thickness, pinopodes number, and Ki67 expression in the OHSS rats. Moreover, the result of circRNAs transcriptome sequencing showed that naringin significantly inhibited the rnocirc_008140 expression in the OHSS rats and significantly inhibited the changes of 28 gene ontology terms and three Kyoto Encyclopedia of Genes and Genomes pathways which were induced by OHSS. Abcc4 and Rps6ka5 genes were the enriched genes of those pathways. Finally, 24 miRNA target genes of rnocirc_008140 were predicted. Our study showed that naringin significantly improved the endometrial receptivity of OHSS rats to increase the embryo implantation success by reducing rnocirc_008140-adsorbed miRNAs to regulate Abcc4 and Rps6ka5 expression.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 8","pages":""},"PeriodicalIF":2.7,"publicationDate":"2023-11-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"107591772","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Long-term storage does not affect the DNA methylation profiles of vitrified-warmed human embryos","authors":"Ling Zhu, Liwei Sun, Weiwei Liu, Wei Han, Guoning Huang, Jingyu Li","doi":"10.1002/mrd.23713","DOIUrl":"10.1002/mrd.23713","url":null,"abstract":"<p>With the widespread application of embryo cryopreservation in assisted reproductive techniques, it is necessary to assess the safety of long-term cryopreservation of human embryos and it is unclear whether storage time has an impact on the DNA methylation profiles of human embryos. Nine women who received IVF treatment were recruited for this study. The retrieved eight-cell human embryos were classified into three groups including fresh embryos, cryopreserved embryos stored for 3 years, and cryopreserved embryos stored for 8 years. Single-cell whole-genome bisulfite sequencing (scWGBS) was conducted. The genome-wide methylation pattern of the fresh and two cryopreserved groups were similar. In addition, the methylation level in different genomic regions showed comparable patterns and no significant differences were observed in the methylation level of imprinted genes among the three groups. A total of 587 differentially methylated regions (DMRs) in the 3-year group and 540 DMRs in the 8-year group were identified comparing to fresh group. However, they were not enriched in promoters and had a similar genome-wide distributions, suggesting that these DMRs may not contribute to the changes in corresponding gene expressions. Our study illustrated that long-term cryopreservation will not affect the DNA methylation profiles of human eight-cell embryos at single-cell level.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 8","pages":""},"PeriodicalIF":2.7,"publicationDate":"2023-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"50162257","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Seiki Haraguchi, Thanh Q. Dang-Nguyen, Kazuhiro Kikuchi, Tamás Somfai
{"title":"Electroporation-mediated genome editing in vitrified/warmed porcine zygotes obtained in vitro","authors":"Seiki Haraguchi, Thanh Q. Dang-Nguyen, Kazuhiro Kikuchi, Tamás Somfai","doi":"10.1002/mrd.23712","DOIUrl":"10.1002/mrd.23712","url":null,"abstract":"<p>Clustered regularly interspaced short palindromic repeats (CRISPR)-associated 9 (Cas9) system is the most efficient and widely used technology for genome editing in all sorts of organisms, including livestock animals. Here, we examined the feasibility of CRISPR/Cas9-derived genome editing (GE) in vitrified porcine zygotes, where the flexible planning of experiments in time and space is expected. <i>OCT4</i> and <i>CD46</i> genes were targeted, and the Cas9/sgRNA ribonucleoprotein complexes (RNP) were electroporated into zygotes at 2 h after warming. Vitrification or GE alone did not significantly reduce the developmental rates to the blastocyst stage. However, vitrification followed by GE significantly reduced blastocyst development. Sequencing analysis of the resultant blastocysts revealed efficient GE for both <i>OCT4</i> (nonvitrified: 91.0%, vitrified: 95.1%) and <i>CD46</i> (nonvitrified: 94.5%, vitrified: 93.2%), with no significant difference among them. Immunocytochemical analysis showed that GE-blastocysts lacked detectable proteins. They were smaller in size, and the cell numbers were significantly reduced compared with the control (<i>p</i> < 0.01). Finally, we demonstrated that double GE efficiently occurs (100%) when the <i>OCT4</i>-RNP and <i>CD46</i>-RNP are simultaneously introduced into zygotes after vitrification/warming. This is the first demonstration that vitrified porcine zygotes can be used in GE as efficiently as nonvitrified ones.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 1","pages":""},"PeriodicalIF":2.5,"publicationDate":"2023-10-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"50162256","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Long-term culture induces Bax-dependent apoptosis in rat preimplantation embryos","authors":"Kazuomi Nakamura, Misako Seno, Yuki Yoshimura, Osamu Suzuki","doi":"10.1002/mrd.23711","DOIUrl":"10.1002/mrd.23711","url":null,"abstract":"<p>Although rat preimplantation embryos are necessary for producing genetically modified rats, their in vitro culture remains a challenge. Rat zygotes can develop from the one-cell stage to the blastocyst stage in vitro; however, long-term culture reduces their developmental competence via an unknown mechanism. In this study, we examined how in vitro conditions affect rat preimplantation embryos, which may explain this reduced competence. Comprehensive gene expression analysis showed that genes related to apoptosis and energy metabolism were differentially expressed in rat embryos cultured long-term in vitro compared with those developed in vivo. Furthermore, we found that the expression of <i>Bak1</i> and <i>Bax</i>, which are responsible for mitochondrial outer membrane permeabilization, were more upregulated in embryos cultured in vitro than those developed in vivo. Similarly, apoptosis-dependent DNA fragmentation was also exacerbated in in vitro culture conditions. Finally, gene disruption using CRISPR/Cas9 showed that <i>Bax</i>, but not <i>Bak1</i>, was responsible for these effects. These findings suggest that long-term in vitro culture induces <i>Bax</i>-dependent apoptosis through the mitochondrial pathway and may provide clues to improve the long-term culture of rat preimplantation embryos for genetic engineering research.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"91 1","pages":""},"PeriodicalIF":2.5,"publicationDate":"2023-10-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41205517","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The cell volume-regulatory glycine transporter GLYT1 is activated following metallopeptidase-mediated detachment of the oocyte from the zona pellucida","authors":"Chyna S. Ortman, Jay M. Baltz","doi":"10.1002/mrd.23708","DOIUrl":"10.1002/mrd.23708","url":null,"abstract":"<p>Independent cell volume regulation is first acquired by the oocyte in two steps that occur during meiotic maturation: (1) activation of the glycine transporter GLYT1 (<i>Slc6a9</i>) that mediates the intracellular accumulation of glycine to provide osmotic support in the mature egg and early preimplantation embryo, and (2) release of the oocyte from the strong attachment to its rigid extracellular matrix shell, the zona pellucida (ZP). It was recently shown that oocyte-ZP detachment requires metallopeptidase activity that is proposed to cleave transmembrane ZP proteins connecting the oocyte to the ZP. It is unknown, however, how GLYT1 is activated. We hypothesized that oocyte-ZP detachment precedes and may be required for GLYT1 activation. In identically treated pools of oocytes, oocyte-ZP detachment occurred ~20 min before GLYT1 activation. In individual oocytes, GLYT1 activity was detected only in those that were mostly or fully detached. Blocking detachment using previously validated small molecule metallopeptidase inhibitors partly suppressed GLYT1 activation. However, removal of the ZP did not accelerate GLYT1 activation. This indicates that oocyte-ZP detachment or cleavage of transmembrane ZP proteins may be required for GLYT1 to become fully activated, or alternatively that metallopeptidase activity independently affects both detachment and GLYT1 activation.</p>","PeriodicalId":18856,"journal":{"name":"Molecular Reproduction and Development","volume":"90 12","pages":"824-834"},"PeriodicalIF":2.5,"publicationDate":"2023-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/mrd.23708","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41151660","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}