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Article(id=1297571037961539796, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1297570992835023717, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20260118, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1770393600000, receivedDateStr=2026-02-07, revisedDate=null, revisedDateStr=null, acceptedDate=1775491200000, acceptedDateStr=2026-04-07, onlineDate=1787294643153, onlineDateStr=2026-08-21, pubDate=1785772800000, pubDateStr=2026-08-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1787294643153, onlineIssueDateStr=2026-08-21, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1787294643153, creator=13701087609, updateTime=1787294643153, updator=13701087609, issue=Issue{id=1297570992835023717, tenantId=1146029695717560320, journalId=1192105938417971205, year='2026', volume='66', issue='8', pageStart='3681', pageEnd='4288', issueExtLink='null', onlineDate='null', pubDate='1785772800000', pubDateStr='2026-08-04', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1787294632395, creator='13701087609', updateTime=1787294931551, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1297572247670124783, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1297570992835023717, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1297572247670124784, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1297570992835023717, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=3981, endPage=3993, ext={EN=ArticleExt(id=1297571038368387285, articleId=1297571037961539796, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Protein disulfide isomerase A4 regulates autophagy to promote replication of bovine viral diarrhea virus, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

[Objective] To investigate the specific role and molecular mechanism of the host protein protein disulfide isomerase A4 (PDIA4) during bovine viral diarrhea virus (BVDV) infection, thus providing a theoretical basis for elucidating the role of this protein in viral replication and developing novel prevention and control strategies. [Methods] Western blotting and qPCR were employed to analyze PDIA4 expression in Madin-Darby bovine kidney (MDBK) cells following BVDV infection. The expression levels of autophagy-related proteins microtubule-associated protein 1 light chain 3 (LC3) and sequestosome 1 (p62) were measured by Western blotting and laser confocal microscopy. MDBK cell lines with pdia4 knockdown and overexpression were constructed. The effects of pdia4 on LC3 and p62 expression were examined, and the autophagic flux was evaluated by a tandem GFP-mRFP-LC3 reporter system. Cells were subjected to starvation or treated with bafilomycin A1 (BafA1), followed by BVDV infection. Viral replication was assessed by measuring BVDV mRNA levels through qPCR and double-stranded RNA (dsRNA) levels through immunofluorescence staining. [Results] BVDV infection significantly upregulated the endogenous expression of PDIA4. The LC3 level increased progressively with infection time, whereas the p62 level showed an initial increase followed by a decrease. The cell lines with pdia4 knockdown and overexpression were successfully established. pdia4 knockdown significantly increased both LC3 and p62 levels, whereas pdia4 overexpression increased the LC3 level and decreased the p62 level. Under starvation or BafA1 treatment, pdia4 knockdown inhibited BVDV replication, whereas pdia4 overexpression promoted BVDV replication. [Conclusion] BVDV infection upregulates host PDIA4 expression. PDIA4 promotes BVDV replication by activating the autophagic flux through regulation of LC3 and p62. These findings provide new insights into the pathogenic mechanism of BVDV and offer a theoretical basis for developing targeted antiviral strategies.

, authors=Zichen QUAN1, 2, Qianshuo LIU1, 2, Tingting YU1, 2, Junzhen CHEN3, Rulong CHEN4, Zheng JIN5, Huijun SHI1, 2, Qiang FU1, 2, authorsList=Zichen QUAN, Qianshuo LIU, Tingting YU, Junzhen CHEN, Rulong CHEN, Zheng JIN, Huijun SHI, Qiang FU, authorCompany=null, correspAuthors=Huijun SHI, Qiang FU, authorNote=null, correspAuthorsNote=
E-mail: SHI Huijun, ;
FU Qiang,
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【目的】 为研究宿主蛋白二硫键异构酶A成员4 (protein disulfide isomerase A4, PDIA4)在牛病毒性腹泻病毒(bovine viral diarrhea virus, BVDV)感染中的具体作用及分子机制，阐明PDIA4在BVDV复制中的致病机制并为制定新型防控策略提供理论依据。 【方法】 Western blotting和qPCR检测BVDV感染MDBK细胞后PDIA4的表达变化；使用Western blotting和激光共聚焦显微镜检测BVDV感染后自噬相关蛋白LC3和p62的表达水平变化。分别构建pdia4敲低/过表达MDBK细胞系，使用Western blotting检测pdia4敲低/过表达对LC3和p62蛋白表达的影响，并用激光共聚焦显微镜观察GFP-mRFP-LC3荧光情况。对pdia4敲低/过表达细胞系分别进行饥饿和巴佛洛霉素A1 (bafilomycin A1, BafA1)处理，感染BVDV后用qPCR检测BVDV mRNA水平，免疫荧光染色技术检测BVDV dsRNA水平。 【结果】 BVDV感染显著上调内源性PDIA4表达；LC3水平随BVDV感染时间延长逐渐升高，p62先升后降；成功构建pdia4敲低和过表达细胞系；pdia4敲低细胞中LC3和p62均显著升高，过表达细胞中LC3升高且p62降低；在饥饿或BafA1处理下，pdia4敲低抑制BVDV复制，相反pdia4过表达促进BVDV复制。 【结论】 本研究表明BVDV感染上调宿主PDIA4表达，PDIA4通过调控LC3和p62激活自噬流，正向促进BVDV复制，为解析BVDV致病机制及开发靶向防控策略提供理论支撑。

, authors=权子晨1, 2, 刘千硕1, 2, 于婷婷1, 2, 陈俊贞3, 陈如龙4, 靳征5, 史慧君1, 2, 付强1, 2, authorsList=权子晨, 刘千硕, 于婷婷, 陈俊贞, 陈如龙, 靳征, 史慧君, 付强, authorCompany=null, correspAuthors=史慧君, 付强, authorNote=

作者贡献声明

权子晨：实验操作、论文撰写；刘千硕：协助实验操作；于婷婷、陈俊贞：数据处理；陈如龙：提供技术支持；靳征：参与论文讨论；史慧君：研究构思和设计；付强：论文修改。

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A: qPCR analysis of pdia4 mRNA levels after BVDV infection; B: Western blotting analysis of PDIA4 protein expression; C: Quantitative analysis of PDIA4 protein levels normalized to GAPDH. Data are presented as mean±SD from three independent experiments. **: P<0.01., figureFileSmall=BewjYsfbNYLs7W2WJXXaDg==, figureFileBig=hGMCamPqfoeIxN5NVBh5Hw==, tableContent=null), ArticleFig(id=1297571045309960484, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=图1, caption=BVDV感染后MDBK细胞中PDIA4的表达, figureFileSmall=BewjYsfbNYLs7W2WJXXaDg==, figureFileBig=hGMCamPqfoeIxN5NVBh5Hw==, tableContent=null), ArticleFig(id=1297571045507092773, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Figure 2, caption=Autophagy levels in MDBK cells following BVDV infection. A: Western blotting analysis of LC3 and p62 protein expression; B: Quantitative analysis of LC3-Ⅱ/LC3-I ratio; C: Quantitative analysis of p62 protein levels normalized to GAPDH; D: Confocal microscopy analysis of autophagic flux using GFP-mRFP-LC3 reporter. Data are presented as mean±SD from three independent experiments. **: P<0.01., figureFileSmall=8ConiwmC8ug3XJLKXuzbqg==, figureFileBig=4EmO0blLUcfAetLmlIxbTw==, tableContent=null), ArticleFig(id=1297571045590978854, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=图2, caption=BVDV感染后MDBK细胞自噬水平变化, figureFileSmall=8ConiwmC8ug3XJLKXuzbqg==, figureFileBig=4EmO0blLUcfAetLmlIxbTw==, tableContent=null), ArticleFig(id=1297571045653893415, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Figure 3, caption=Validation of pdia4 knockdown and overexpression cell lines. A: qPCR analysis of pdia4 mRNA levels in knockdown cells; B: qPCR analysis of pdia4 mRNA levels in overexpression cells; C: Western blotting analysis of PDIA4 protein expression; D: Quantitative analysis of PDIA4 protein levels after knockdown; E: Quantitative analysis of PDIA4 protein levels after overexpression. Data are presented as mean±SD from three independent experiments. **: P<0.01., figureFileSmall=Sqcs1UXib4zcIYOGEjCRgQ==, figureFileBig=c3qtwnLdZ7nCpOZfg+TQTA==, tableContent=null), ArticleFig(id=1297571045750362408, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=图3, caption=pdia4 敲低及过表达细胞系的鉴定, figureFileSmall=Sqcs1UXib4zcIYOGEjCRgQ==, figureFileBig=c3qtwnLdZ7nCpOZfg+TQTA==, tableContent=null), ArticleFig(id=1297571045834248489, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Figure 4, caption=Effects of PDIA4 on autophagic flux. A: Western blotting analysis of LC3 and p62 in pdia4 knockdown cells; B: Quantitative analysis of p62 protein levels; C: Quantitative analysis of LC3-Ⅱ/LC3-I ratio; D: Confocal microscopy analysis of autophagic flux in pdia4 knockdown cells; E: Western blotting analysis of LC3 and p62 in pdia4-overexpressing cells; F: Quantitative analysis of p62 protein levels; G: Quantitative analysis of LC3-Ⅱ/LC3-I ratio; H: Confocal microscopy analysis of autophagic flux in pdia4-overexpressing cells. Data are presented as mean±SD from three independent experiments. **: P<0.01., figureFileSmall=h4swRYLsPXo7LeQx+QVv2A==, figureFileBig=pQGl6ZJXAjnNrkhPi988xw==, tableContent=null), ArticleFig(id=1297571045901357354, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=图4, caption=PDIA4对自噬流的调控作用, figureFileSmall=h4swRYLsPXo7LeQx+QVv2A==, figureFileBig=pQGl6ZJXAjnNrkhPi988xw==, tableContent=null), ArticleFig(id=1297571045985243435, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Figure 5, caption=PDIA4 regulates BVDV replication through autophagy. A: qPCR analysis of BVDV mRNA levels in pdia4 knockdown cells under autophagy modulation; B: qPCR analysis of BVDV mRNA levels in pdia4-overexpressing cells; C: Immunofluorescence detection of dsRNA in pdia4 knockdown cells; D: Immunofluorescence detection of dsRNA in pdia4-overexpressing cells. Data are presented as mean±SD from three independent experiments. **: P<0.01; *: P<0.05., figureFileSmall=8cJK+I1faz9J7jSRNUiTJA==, figureFileBig=/61NeMq2sTRZTjdE+N9uIw==, tableContent=null), ArticleFig(id=1297571046060740908, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=图5, caption=PDIA4通过自噬调控BVDV复制, figureFileSmall=8cJK+I1faz9J7jSRNUiTJA==, figureFileBig=/61NeMq2sTRZTjdE+N9uIw==, tableContent=null), ArticleFig(id=1297571046169792813, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Table 1, caption=

qPCR primer sequences for PDIA4 and GAPDH

, figureFileSmall=null, figureFileBig=null, tableContent=
Primer namesPrimer sequences (5′→3′)Product size/bp
pdia4-qPCR-FTCCAGGACCCAGGAAGAAATTG140
pdia4-qPCR-RTCTACCAGGATGATGTCGGC
gapdh-qPCR-FAAGGTCGGAGTGAACGGATT178
gapdh-qPCR-RCGTTCTCTGCCTTGACTGTG
), ArticleFig(id=1297571046379508014, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=表1, caption=

pdia4 和 GAPDH 的qPCR引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Primer namesPrimer sequences (5′→3′)Product size/bp
pdia4-qPCR-FTCCAGGACCCAGGAAGAAATTG140
pdia4-qPCR-RTCTACCAGGATGATGTCGGC
gapdh-qPCR-FAAGGTCGGAGTGAACGGATT178
gapdh-qPCR-RCGTTCTCTGCCTTGACTGTG
), ArticleFig(id=1297571046538891567, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=EN, label=Table 2, caption=

sgRNA sequences

, figureFileSmall=null, figureFileBig=null, tableContent=
Primer namesPrimer sequences (5′→3′)
pdia4 sgRNA1ForwardGATCCTGAAGAAGGGCCAGG
ReverseCTAGGACTTCTTCCCGGTCC
pdia4 sgRNA2ForwardAGTCACACTTGTGCTGACCA
ReverseTCAGTGTGAACACGACTGGT
pdia4 sgRNA3ForwardAGGGTCGTTCTCCTTCAAGG
ReverseTCCCAGCAAGAGGAAGTTCC
ScrambleForwardCACCGCACTACCAGAGCTAACTCA
ReverseAAACTGAGTTAGCTCTGGTAGTGC
), ArticleFig(id=1297571046622777648, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1297571037961539796, language=CN, label=表2, caption=

sgRNA序列

, figureFileSmall=null, figureFileBig=null, tableContent=
Primer namesPrimer sequences (5′→3′)
pdia4 sgRNA1ForwardGATCCTGAAGAAGGGCCAGG
ReverseCTAGGACTTCTTCCCGGTCC
pdia4 sgRNA2ForwardAGTCACACTTGTGCTGACCA
ReverseTCAGTGTGAACACGACTGGT
pdia4 sgRNA3ForwardAGGGTCGTTCTCCTTCAAGG
ReverseTCCCAGCAAGAGGAAGTTCC
ScrambleForwardCACCGCACTACCAGAGCTAACTCA
ReverseAAACTGAGTTAGCTCTGGTAGTGC
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蛋白二硫键异构酶A成员4调控细胞自噬促进牛病毒性腹泻病毒的复制
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权子晨 1, 2 , 刘千硕 1, 2 , 于婷婷 1, 2 , 陈俊贞 3 , 陈如龙 4 , 靳征 5 , 史慧君 1, 2 , 付强 1, 2
微生物学报 | 研究报告 2026,66(8): 3981-3993
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微生物学报 |研究报告 2026 , 66 (8) : 3981 -3993
蛋白二硫键异构酶A成员4调控细胞自噬促进牛病毒性腹泻病毒的复制
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权子晨1, 2, 刘千硕1, 2, 于婷婷1, 2, 陈俊贞3, 陈如龙4, 靳征5, 史慧君1, 2 , 付强1, 2
作者信息
  • 1.新疆农业大学 动物医学学院，新疆 乌鲁木齐
  • 2.新疆动物临床医学研究重点实验室，新疆 乌鲁木齐
  • 3.新疆农业职业技术大学，新疆 昌吉
  • 4.新疆天莱农牧集团股份有限公司，新疆 博乐
  • 5.巴州若羌县畜牧兽医站，新疆 巴州
通讯作者:
史慧君, 付强
作者简介:

作者贡献声明

权子晨：实验操作、论文撰写；刘千硕：协助实验操作；于婷婷、陈俊贞：数据处理；陈如龙：提供技术支持；靳征：参与论文讨论；史慧君：研究构思和设计；付强：论文修改。

Protein disulfide isomerase A4 regulates autophagy to promote replication of bovine viral diarrhea virus
Zichen QUAN1, 2, Qianshuo LIU1, 2, Tingting YU1, 2, Junzhen CHEN3, Rulong CHEN4, Zheng JIN5, Huijun SHI1, 2 , Qiang FU1, 2
Affiliations
  • 1.College of Veterinary Medicine, Xinjiang Agricultural University, Urumqi, Xinjiang, China
  • 2.Xinjiang Regional Key Laboratory of Clinical Veterinary Medicine Research, Urumqi, Xinjiang, China
  • 3.Xinjiang Agricultural Vocational and Technical University, Changji, Xinjiang, China
  • 4.Xinjiang Tianlai Agriculture and Animal Husbandry Group Co., Ltd., Bole, Xinjiang, China
  • 5.Ruoqiang County Station of Animal Husbandry and Veterinary Medicine, Bayingolin, Xinjiang, China
    • Corresponding Author:
    E-mail: SHI Huijun, ;
    FU Qiang,
出版时间: 2026-08-04 doi: 10.13343/j.cnki.wsxb.20260118
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【目的】 为研究宿主蛋白二硫键异构酶A成员4 (protein disulfide isomerase A4, PDIA4)在牛病毒性腹泻病毒(bovine viral diarrhea virus, BVDV)感染中的具体作用及分子机制，阐明PDIA4在BVDV复制中的致病机制并为制定新型防控策略提供理论依据。 【方法】 Western blotting和qPCR检测BVDV感染MDBK细胞后PDIA4的表达变化；使用Western blotting和激光共聚焦显微镜检测BVDV感染后自噬相关蛋白LC3和p62的表达水平变化。分别构建pdia4敲低/过表达MDBK细胞系，使用Western blotting检测pdia4敲低/过表达对LC3和p62蛋白表达的影响，并用激光共聚焦显微镜观察GFP-mRFP-LC3荧光情况。对pdia4敲低/过表达细胞系分别进行饥饿和巴佛洛霉素A1 (bafilomycin A1, BafA1)处理，感染BVDV后用qPCR检测BVDV mRNA水平，免疫荧光染色技术检测BVDV dsRNA水平。 【结果】 BVDV感染显著上调内源性PDIA4表达；LC3水平随BVDV感染时间延长逐渐升高，p62先升后降；成功构建pdia4敲低和过表达细胞系；pdia4敲低细胞中LC3和p62均显著升高，过表达细胞中LC3升高且p62降低；在饥饿或BafA1处理下，pdia4敲低抑制BVDV复制，相反pdia4过表达促进BVDV复制。 【结论】 本研究表明BVDV感染上调宿主PDIA4表达，PDIA4通过调控LC3和p62激活自噬流，正向促进BVDV复制，为解析BVDV致病机制及开发靶向防控策略提供理论支撑。

牛病毒性腹泻病毒  /  PDIA4  /  细胞自噬

[Objective] To investigate the specific role and molecular mechanism of the host protein protein disulfide isomerase A4 (PDIA4) during bovine viral diarrhea virus (BVDV) infection, thus providing a theoretical basis for elucidating the role of this protein in viral replication and developing novel prevention and control strategies. [Methods] Western blotting and qPCR were employed to analyze PDIA4 expression in Madin-Darby bovine kidney (MDBK) cells following BVDV infection. The expression levels of autophagy-related proteins microtubule-associated protein 1 light chain 3 (LC3) and sequestosome 1 (p62) were measured by Western blotting and laser confocal microscopy. MDBK cell lines with pdia4 knockdown and overexpression were constructed. The effects of pdia4 on LC3 and p62 expression were examined, and the autophagic flux was evaluated by a tandem GFP-mRFP-LC3 reporter system. Cells were subjected to starvation or treated with bafilomycin A1 (BafA1), followed by BVDV infection. Viral replication was assessed by measuring BVDV mRNA levels through qPCR and double-stranded RNA (dsRNA) levels through immunofluorescence staining. [Results] BVDV infection significantly upregulated the endogenous expression of PDIA4. The LC3 level increased progressively with infection time, whereas the p62 level showed an initial increase followed by a decrease. The cell lines with pdia4 knockdown and overexpression were successfully established. pdia4 knockdown significantly increased both LC3 and p62 levels, whereas pdia4 overexpression increased the LC3 level and decreased the p62 level. Under starvation or BafA1 treatment, pdia4 knockdown inhibited BVDV replication, whereas pdia4 overexpression promoted BVDV replication. [Conclusion] BVDV infection upregulates host PDIA4 expression. PDIA4 promotes BVDV replication by activating the autophagic flux through regulation of LC3 and p62. These findings provide new insights into the pathogenic mechanism of BVDV and offer a theoretical basis for developing targeted antiviral strategies.

bovine viral diarrhea virus (BVDV)  /  protein disulfide isomerase A4 (PDIA4)  /  autophagy
权子晨, 刘千硕, 于婷婷, 陈俊贞, 陈如龙, 靳征, 史慧君, 付强. 蛋白二硫键异构酶A成员4调控细胞自噬促进牛病毒性腹泻病毒的复制. 微生物学报, 2026 , 66 (8) : 3981 -3993 . DOI: 10.13343/j.cnki.wsxb.20260118
Zichen QUAN, Qianshuo LIU, Tingting YU, Junzhen CHEN, Rulong CHEN, Zheng JIN, Huijun SHI, Qiang FU. Protein disulfide isomerase A4 regulates autophagy to promote replication of bovine viral diarrhea virus[J]. Acta Microbiologica Sinica, 2026 , 66 (8) : 3981 -3993 . DOI: 10.13343/j.cnki.wsxb.20260118
正文
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牛病毒性腹泻(bovine viral diarrhea, BVD)是由牛病毒性腹泻病毒(bovine viral diarrhea virus, BVDV)感染引发的一种高度接触性传染病，其流行范围广、传播速度快，对养牛业危害严重[1]。BVDV的危害兼具直接经济损失与间接防控成本：既导致动物死亡、生产性能下滑，又产生疫病防控相关的额外投入，已然成为全球范围内危害最严重的牛传染病之一[2]。同时，持续性感染(persistently infected, PI)牛的管理、疫苗接种、诊断检测及治疗费用将进一步增加养殖场运营成本，单头感染牛年均直接经济损失达42.1 EUR[3]。目前，针对BVDV的防控主要依赖疫苗接种，但由于病毒基因型多样、易发生变异，现有防控措施仍存在局限性，因此深入探究BVDV的复制机制及宿主细胞的抗病毒调控网络具有重要意义。
蛋白二硫键异构酶A成员4 (protein disulfide isomerase A4, PDIA4)属于蛋白二硫键异构酶(protein disulfide isomerase, PDI)家族，是一类定位于内质网的催化酶。其核心功能为介导蛋白质二硫键的形成、断裂与重排，通过调控这一过程参与蛋白质的氧化折叠，确保蛋白质获得正确的空间构象。已有研究表明，PDIA4在病毒的复制过程中发挥调控作用[4]。PDI家族通过自噬/自噬溶酶体途径抑制了埃博拉病毒结构蛋白的表达[5]；pdi1、pdia3、pdia4敲低能够降低A型和B型流感病毒在细胞中的复制[6]；PDIA1、PDIA3、PDIA4和PDIA6增加戊型肝炎病毒ORF3蛋白的表达，并且PDIA3和PDIA6与ORF3蛋白相互作用，从而促进戊型肝炎病毒的复制[7]。然而，PDIA4在BVDV复制及相关调控机制中的作用尚未明确。
细胞自噬是真核生物中一种高度保守的细胞降解过程，通过形成自噬体包裹胞内异常蛋白、受损细胞器等物质，并与溶酶体融合完成降解，在维持细胞稳态、抵御病原体感染等过程中发挥双重作用。研究证实，自噬与BVDV的感染过程密切相关，能够显著影响病毒的复制与增殖[8]。近年来研究发现，BVDV感染与宿主细胞自噬之间存在复杂而精细的相互作用，病毒通过多种机制劫持自噬通路以促进自身复制与免疫逃逸，BVDV的非结构蛋白NS4B抑制mTOR磷酸化，降低p62蛋白水平并增加LC3-Ⅱ转化，直接诱导自噬流[9]；同时，BVDV还可通过下调宿主miRNA (bta-miR-221)解除对自噬关键基因atg7的抑制，激活ATG7/LC3自噬通路[10]。PDIA4是连接内质网应激和自噬的关键分子，通过IRE1α-XBP1s分支介导的未折叠蛋白反应(unfolded protein response, UPR)通路调控自噬流，PDIA4缺失可特异性激活IRE1α- XBP1s信号，导致细胞增殖受损和G1期阻滞，并伴随自噬通量的改变[11]，同时，PDIA4本身可作为自噬降解的底物，研究发现PDIA4通过激活PERK/ATF4/SLC7A11轴增强肾癌细胞的铁死亡抗性；盐霉素(salinomycin, Sal)通过自噬降解PDIA4，解除该抗性、诱导铁死亡、抑制肿瘤[12]。目前，PDIA4已被发现参与调控多种细胞过程，如免疫应答调控、细胞凋亡和自噬等[13]，但其是否通过影响自噬来调节BVDV复制目前尚不明确。
前期研究已证实pdia4是BVDV感染后差异表达的基因[14]。本研究拟进一步探究BVDV感染后PDIA4的表达特征，通过构建pdia4敲低与过表达细胞系，验证其过表达是否可促进细胞自噬流的发生，初步阐明PDIA4是否通过介导自噬信号通路参与调控BVDV增殖过程，以期为揭示BVDV致病机制、开发靶向抗BVDV防控手段提供理论依据。
1 材料与方法
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1.1 质粒、细胞和病毒
人胚肾细胞HEK-293T及牛肾细胞MDBK，中国科学院典型培养物保藏委员会细胞库、BVDV毒株TC (BVDV 1b亚型，CP型)、大肠杆菌Stbl3细胞均由本实验室保存。pLenti-GFP(17448)、ptfLC3(21074)、pMD2.G(12259)、pSPAX2(12260)、lentiCRISPR v2(53961)购自Addgene公司。
1.2 主要试剂和仪器
Anti-dsRNA mAb J2，SCICONS公司；LC3抗体，Abcam公司；Anti-p62 (SQSTM1) pAb，MBL公司；PDIA4多克隆抗体(14712-1-AP)、GAPDH多克隆抗体(10494-1-AP)、HRP标记山羊抗兔IgG(H+L) (SA00001-2)和CoraLite594标记驴抗小鼠IgG(H+L) (SA00013-7)，Proteintech公司。
实时荧光定量PCR仪，福际生物技术有限公司(成都)；倒置荧光显微镜，Nikon公司；低温高速离心机，ThermoFisher Scientific公司；二氧化碳细胞培养箱，Galaxy公司。
1.3 BVDV感染后PDIA4表达水平检测
1.3.1 qPCR检测 pdia4 表达水平变化
BVDV感染MDBK细胞48 h后收集细胞，采用TRIzol法提取总RNA，反转录合成cDNA。反转录体系(10 μL)：2×RT OR-EasyTM Mix 5.0 μL，总RNA 500.0 ng，RNase-Free ddH2O补足至10.0 μL。反应程序：42 ℃逆转录15 min，85 ℃失活5 min。设计PCR特异性引物(表1)，由擎科生物股份有限公司西安分部合成。以cDNA为模板，采用qPCR试剂盒检测pdia4 mRNA表达水平，内参基因为gapdh。qPCR反应体系(20 μL)：2×Real PCR EasyTM Mix-SYBR 10 μL，50×ROX Reference Dye 0.4 μL，上、下游引物(10 μmol/L)各1 μL，cDNA模板2 μL，DNase-Free ddH2O 5.6 μL。反应条件：95 ℃预变性3 min；95 ℃变性5 s，56 ℃退火30 s，共40个循环；95 ℃变性15 s，56 ℃退火1 min，95 ℃熔解30 s。
1.3.2 Western blotting检测PDIA4表达水平变化
收集BVDV感染48 h的MDBK细胞，加入RIPA裂解液(含终浓度1%的PMSF与磷酸酶抑制剂)提取总蛋白，使用BCA法测定总蛋白浓度。取等量总蛋白进行SDS-PAGE，转印至PVDF膜，5%脱脂奶粉封闭1 h，加入兔源PDIA4 (1:5 000)及兔源GAPDH (1:5 000)一抗，4 ℃孵育过夜。TBST洗涤后，加入HRP标记山羊抗兔IgG(H+L)二抗，室温孵育1 h，经ECL化学发光试剂盒显影，ImageJ软件分析蛋白条带灰度值，采用2-ΔΔCt法计算PDIA4蛋白的相对表达量。
1.4 BVDV感染后细胞自噬水平变化检测
1.4.1 Western blotting检测细胞自噬水平变化
将MDBK细胞接种至6 cm细胞培养皿，感染BVDV (MOI=1)，于感染后12、24、36、48 h收集细胞，提取总蛋白，Western blotting检测自噬标志蛋白LC3和p62的表达水平。
1.4.2 激光共聚焦显微镜观察LC3定位情况
将ptfLC3与慢病毒包装质粒pSPAX2、pMD2.G按照质量比2:2:1混匀，同时加入5倍体积浓度为1 mg/mL的PEI转染试剂，共转染至HEK-293T细胞中，48 h后收集含有慢病毒颗粒的细胞悬液，室温1 500 r/min离心5 min，上清过滤清除细胞碎片，将获得的慢病毒液与相等体积完全培养基混合，加入悬浮MDBK细胞中，并添加终浓度为8 μg/mL的聚凝胺，经嘌呤霉素(终浓度为6 μg/mL)筛选3代次后感染BVDV (MOI=1)，分别在感染后24 h和48 h于荧光显微镜下观察荧光情况。红绿荧光同时存在表明自噬流受阻，当绿色荧光淬灭，仅存在红色荧光时表明自噬流通畅。
1.5 pdia4 敲低/过表达细胞系的构建
1.5.1 pdia4 敲低载体构建
根据GenBank数据库中pdia4基因序列(登录号为415110)，使用Benchling (www.benchling.com)和ChopChop (www.chopchop.cbu.uib.no)网站设计sgRNA，其序列见表2，由北京擎科生物工程股份有限公司合成pdia4 sgRNA和Scramble序列，并克隆至LentiCRISPR v2-puro载体中，构建LentiCRISPR v2-puro-pdia4 sgRNA1/sgRNA2/sgRNA3/Scramble质粒。
1.5.2 pdia4 过表达载体构建
从GenBank数据库获取pdia4基因(登录号为415110) CDS序列，交由北京擎科生物工程股份有限公司合成pdia4基因并克隆至慢病毒质粒pLVML-Myc-MCS-IRES-Puro中，构建pLVML- Myc-pdia4-IRES-Puro质粒。
1.5.3 pdia4 敲低/过表达细胞系的构建
采用无内毒素质粒小提试剂盒提取质粒，分别将LentiCRISPR v2-puro-pdia4 sgRNA1/sgRNA2/sgRNA3、Scramble、pLVML-Myc-pdia4- IRES-Puro(Myc-pdia4)、pLVML-Myc-MCS-IRES-Puro (Myc-MCS)与慢病毒包装质粒pSPAX2、pMD2.G按质量比2:2:1混匀，实验流程同1.4.2节。其中分别使用3个独立sgRNA和混合sgRNA (sgRNA cocktail)感染24 h，得到pdia4 KD、Scramble、Myc-pdia4、Myc-MCS细胞系，通过Western blotting和qPCR对其进行鉴定。
1.6 pdia4 敲低/过表达对细胞自噬的影响
1.6.1 Western blotting检测自噬相关蛋白LC3和p62表达水平变化
将1.5.3节构建的Scramble、pdia4 KD、Myc-MCS、Myc-pdia4四种细胞系分别接种于6 cm培养皿，培养24 h后收集细胞，实验流程同1.3.2节，其中兔源LC3和p62稀释比例分别为1:2 000和1:5 000。ImageJ软件分析条带灰度值，计算LC3-Ⅱ/LC3-I比值及p62蛋白相对表达量。
1.6.2 激光共聚焦显微镜观察LC3定位情况
为探究PDIA4对自噬流的影响，将ptfLC3质粒分别转染至Scramble、pdia4 KD、Myc-MCS及Myc-pdia4组细胞，实验流程同1.4.2节。48 h后，通过共聚焦显微镜观察绿色荧光蛋白(green fluorescent protein, GFP)和单体红色荧光蛋白(monomeric red fluorescent protein, mRFP)的分布及融合情况。
1.7 PDIA4调控自噬影响BVDV复制检测
1.7.1 qPCR检测BVDV 5′ UTR水平
分别经饥饿和0.5 μmol/L BafA1处理pdia4 KD和Myc-pdia4细胞系12 h后，感染BVDV (MOI=1)，BVDV感染24 h后收集细胞，提取总RNA并反转录成cDNA，使用引物F (5′-CC TAGCCATGCCCTTAGTAGGACT-3′)和R (5′-G GAACTCCATGTGCCATGTACA-3′)进行qPCR，检测BVDV 5′ UTR mRNA的表达，按1.3.1节配制qPCR反应体系。反应条件：95 ℃ 3 min；95 ℃ 5 s，60 ℃ 30 s，共40个循环；95 ℃ 15 s，60 ℃ 1 min，95 ℃ 30 s。
1.7.2 免疫荧光染色检测BVDV dsRNA水平
通过间接免疫荧光试验检测BVDV在pdia4 KD和Myc-pdia4细胞中的分布情况，经饥饿和0.5 μmol/L BafA1处理pdia4 KD与Myc-pdia4细胞12 h后，接种BVDV (MOI=1) 2 h，PBS冲洗后改用含2%胎牛血清的DMEM培养基继续培养24 h。用PBS洗涤3次，4%多聚甲醛固定30 min，0.1% Triton X-100透化处理20 min，37 ℃条件下用200 μL预混封闭液(1%山羊血清+3% BSA+1% Triton X-100)，室温孵育1 h。与J2 anti-dsRNA一抗(1:1 200) 4 ℃孵育过夜，接着室温下用山羊抗小鼠IgG594(H+L)抗体(1:200)孵育2 h，细胞核经DAPI染色后，通过激光共聚焦显微镜进行观察。
1.8 统计学方法
所有实验重复3次及以上，采用GraphPad Prism 10.1.2软件进行统计分析，所有数据以mean±SD表示。组间比较采用t检验或单因素方差分析，*：P<0.05表示差异显著；**：P<0.01表示差异极显著。
2 结果与分析
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2.1 BVDV感染对MDBK细胞中PDIA4表达的影响
BVDV感染MDBK细胞48 h后，采用qPCR和Western blotting分别检测pdia4的mRNA和蛋白表达水平。结果显示，与未感染对照组相比，BVDV感染后pdia4 mRNA水平显著上调(P<0.01)，其蛋白表达水平也显著升高(P<0.01) (图1)。
2.2 BVDV感染对MDBK细胞自噬的影响
为分析BVDV感染对细胞自噬的影响，在不同感染时间点(12、24、36、48 h)检测自噬相关蛋白的表达水平。结果显示，随着感染时间延长，LC3-Ⅱ/LC3-I比值逐渐升高(P<0.01)，在36 h左右达到峰值并维持在较高水平；p62蛋白表达水平呈先升高后降低的变化趋势(P<0.01) (图2A-2C)。免疫荧光结果显示，BVDV感染24 h和48 h后，GFP-mRFP-LC3串联细胞中主要呈现红色荧光信号，绿色荧光明显减弱(图2D)。
2.3 稳定敲低/过表达 pdia4 细胞系的建立
为验证pdia4敲低或过表达对BVDV的影响，通过CRISPR/Cas9基因编辑技术构建pdia4敲低或过表达细胞系，并采用qPCR和Western blotting检测敲低或过表达效率。结果显示，与Scramble对照组相比，3个sgRNA或混合sgRNA (sgRNA cocktail)均可有效敲低pdia4 (P<0.01)，其中sgRNA2敲低效率最佳(图3A)。Western blotting结果显示，3个sgRNA或混合sgRNA (sgRNA cocktail)均可使PDIA4蛋白表达水平显著下调(P<0.01) (图3C、3D)。综合qPCR和Western blotting结果，后续实验均采用sgRNA2敲低细胞系完成。同时，过表达pdia4后，其mRNA和蛋白水平均显著上调(P<0.01) (图3B、3E)。上述结果表明pdia4敲低和过表达细胞系构建成功。
2.4 pdia4 敲低/过表达对细胞自噬的调控作用
为探究PDIA4对细胞自噬流的影响，利用Western blotting检测pdia4 KD和Myc-pdia4细胞中自噬相关蛋白LC3和p62的表达水平。与Scramble组相比，pdia4敲低后，LC3-Ⅱ/LC3-I比值显著升高(P<0.01)，p62蛋白表达水平也显著升高(P<0.01) (图4A-4C)。免疫荧光染色结果显示，GFP-mRFP-LC3串联细胞中pdia4 KD组细胞内红绿荧光同时存在(图4D)，表明自噬体形成但未能有效降解，证实敲低pdia4阻断了自噬流。与Myc-MCS组相比，Myc-pdia4组细胞中LC3-Ⅱ/LC3-I比值显著升高(P<0.01)，但p62蛋白表达水平显著降低(P<0.01) (图4E-4G)。免疫荧光染色结果显示，Myc-pdia4组细胞内绿色荧光淬灭(图4H)，表明pdia4过表达可促进自噬流。上述结果说明，pdia4敲低可导致自噬流受阻，过表达pdia4可促进自噬流通畅。
2.5 PDIA4调控细胞自噬影响BVDV复制
为检测PDIA4是否通过自噬调控BVDV复制，经饥饿和0.5 μmol/L BafA1处理pdia4 KD和Myc-pdia4细胞系12 h后感染BVDV，利用qPCR和免疫荧光检测细胞内BVDV 5′ UTR mRNA和dsRNA的积累。结果显示，与Scramble组相比，pdia4 KD组BVDV 5′ UTR mRNA表达水平在相同处理条件下均显著降低(P<0.01) (图5A)，pdia4 KD组BVDV dsRNA荧光强度也显著低于Scramble组(图5C)。与Myc-MCS组相比，Myc-pdia4组BVDV 5′ UTR mRNA表达水平在相同处理条件下均显著升高(P<0.05) (图5B)，Myc-pdia4组BVDV dsRNA荧光强度显著高于Myc-MCS组(图5D)。上述结果表明，PDIA4通过促进细胞自噬进而促进BVDV的复制。
3 讨论
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BVDV属于黄病毒科瘟病毒属，呈球形，直径约40-60 nm，有包膜，其基因组为单股正链RNA。BVDV可引起牛的多种疾病，如呼吸道疾病、消化道疾病、繁殖障碍等，给养牛业带来严重的经济损失[15]。PDIA4是BVDV感染后差异表达的蛋白，也是最大的PDI家族成员之一，由645个氨基酸组成，含有3个经典的CGHC活性位点，主要参与蛋白质折叠和错误折叠蛋白的清除，对维持细胞内蛋白质稳态至关重要[16]。同时，PDIA4还是一种具有细胞内外双向功能的氧化还原酶[17]：在细胞内，它作为内质网定位的蛋白质折叠催化剂，通过氧化还原活性维持蛋白稳态，是正常细胞功能的基础保障；在细胞表面，它可作为跨膜信号枢纽，与细胞外因子相互作用，激活尚未被充分揭示的细胞内通路，如介导中性粒细胞渗透和甲状腺球蛋白成熟[18-19]。本研究发现PDIA4可显著促进BVDV的复制，这与已有报道中PDIA4抑制人类乳头瘤病毒16型(HPV16)[20]和流感病毒复制的结论不同[21]，但与其促进多瘤病毒侵袭的作用方向一致[22]。这种差异凸显了PDIA4功能的复杂性，其效应可能高度依赖于特定病毒与宿主相互作用的背景，提示同一宿主因子在不同感染模型中可能发挥不同的功能。
自噬是一种基本的细胞代谢过程，可清除异常或多余的细胞内容物，并通过溶酶体介导的降解回收代谢底物以维持细胞内稳态[23]。自噬过程的关键标志蛋白包括LC3和p62，LC3蛋白可分为胞质型LC3-Ⅰ和自噬体膜结合型LC3-Ⅱ，LC3-Ⅱ水平与自噬活性正相关。自噬接头蛋白p62作为连接LC3-Ⅱ与泛素化底物的桥梁，其水平与自噬活性负相关，并在自噬溶酶体中被降解[24]。已有研究表明，自噬既可被宿主利用来降解病毒蛋白、抑制猪流行性腹泻病毒复制，又可被病毒利用其N蛋白选择性降解宿主抗病毒蛋白，从而促进自身复制[25]。PDIA4对自噬的调控并非通过随机通路实现，而是靶向自噬核心分子与关键信号节点发挥精准调控作用：其主要通过调控LC3 (atg8)的脂化转化、Beclin-1自噬起始复合物组装、atg7泛素结合系统活性，AKT/mTOR/ULK1信号轴和PERK/ATF4内质网应激通路实现对自噬流的正向驱动；同时，PDIA4还可通过靶向线粒体自噬受体PHB2、解除其对LC3的结合抑制进一步强化自噬进程。本研究通过Western blotting验证了BVDV对自噬的影响。结果显示，BVDV感染早期(12 h) p62蛋白水平升高，而在感染后期(24 h和48 h) p62降解显著，同时LC3-Ⅰ向LC3-Ⅱ转化增加，表明BVDV感染能够激活细胞自噬，与已有研究结论一致[26]。
本研究利用CRISPR/Cas9技术与慢病毒介导成功构建了pdia4基因敲低细胞系与过表达细胞系。结果发现，pdia4 KD可显著上调LC3-Ⅱ和p62的表达，抑制MDBK细胞的自噬水平；而Myc-pdia4在显著上调LC3-Ⅱ的同时使p62显著降解，促进MDBK细胞的自噬水平。免疫荧光染色检测GFP-mRFP-LC3荧光变化显示，pdia4 KD细胞中红绿荧光同时存在，表明自噬流受阻；Myc-pdia4细胞中绿色荧光淬灭，表明自噬流通畅，进一步验证了PDIA4对自噬的正向调控作用。为探究PDIA4影响BVDV复制的途径，在pdia4敲低和过表达细胞中分别经饥饿或BafA1处理以促进或抑制自噬后感染BVDV，利用qPCR检测细胞中BVDV 5′ UTR mRNA水平。结果发现，激活自噬可显著上调BVDV 5′ UTR mRNA水平，但pdia4 KD组的上调幅度显著低于Scramble对照组；抑制自噬则降低BVDV 5′ UTR mRNA水平，且pdia4 KD组的抑制效应更强。反之，Myc-pdia4组在促进或抑制自噬条件下均可显著增强BVDV 5′ UTR mRNA水平的变化，说明PDIA4通过自噬途径调控BVDV的复制。上述结果表明，BVDV感染可上调宿主细胞内PDIA4的表达，而PDIA4能够通过促进自噬流进而促进BVDV的复制。
尽管本研究明确了PDIA4通过自噬正向调控BVDV复制的现象与基本过程，但尚未阐明PDIA4调控自噬的具体分子靶点及互作机制，同时缺乏动物模型的验证，无法完全反映自然感染过程中PDIA4与自噬在BVDV致病中的实际作用。后续研究中可寻找PDIA4在自噬通路中的直接互作蛋白以揭示作用靶点，并在动物感染模型中验证靶向PDIA4或自噬的干预效果，在体内水平验证PDIA4对自噬及病毒复制的调控效应，评估其治疗潜力，以期为抗BVDV研究提供新靶标。
4 结论
收起
本研究明确了BVDV感染可上调宿主细胞内PDIA4的表达，且PDIA4能够通过促进自噬流来促进BVDV的复制。通过实验验证了BVDV感染能够激活细胞自噬，以及PDIA4对自噬的正向调控作用，并证实PDIA4通过自噬途径影响BVDV的复制。该发现从分子层面揭示了BVDV借助宿主PDIA4和自噬通路完成复制的机制，为病毒与宿主相互作用网络提供了新见解。同时，PDIA4作为关键调控节点，可作为抗BVDV感染的潜在宿主靶点，为后续靶向阻断病毒复制通路、研发新型抗病毒药物及开展抗病育种研究提供重要的理论依据，对畜牧业疫病防控具有应用价值。
基金
收起
  • 新疆维吾尔自治区重大科技专项(2023A02007-2)
  • 新疆维吾尔自治区“天山英才”青年科技拔尖人才项目(2022TSYCCX0049)
  • 新疆维吾尔自治区“天山英才”青年科技拔尖人才项目(2024TSYCCX0033)
  • 中央引导地方科技发展资金
  • 新疆维吾尔自治区天山创新团队计划(2025D14006)
  • 新疆维吾尔自治区自然科学基金(2025D01E15)
  • 新疆维吾尔自治区自然科学基金(2025D01A116)
  • 国家自然科学基金(32260881)
文献
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2026年第66卷第8期
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doi: 10.13343/j.cnki.wsxb.20260118
  • 接收时间：2026-02-07
  • 首发时间：2026-08-21
  • 出版时间：2026-08-04
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  • 收稿日期：2026-02-07
  • 录用日期：2026-04-07
基金
Major Science and Technology Special Project of Xinjiang Uygur Autonomous Region(2023A02007-2)
新疆维吾尔自治区重大科技专项(2023A02007-2)
“Tianshan Talents” Young Scientific and Technological Leading Talents Project of Xinjiang Uygur Autonomous Region(2022TSYCCX0049)
新疆维吾尔自治区“天山英才”青年科技拔尖人才项目(2022TSYCCX0049)
“Tianshan Talents” Young Scientific and Technological Leading Talents Project of Xinjiang Uygur Autonomous Region(2024TSYCCX0033)
新疆维吾尔自治区“天山英才”青年科技拔尖人才项目(2024TSYCCX0033)
Central Government Funds for Guiding Local Scientific and Technological Development
中央引导地方科技发展资金
Tianshan Innovation Team Program of Xinjiang Uygur Autonomous Region(2025D14006)
新疆维吾尔自治区天山创新团队计划(2025D14006)
Natural Science Foundation of Xinjiang Uygur Autonomous Region(2025D01E15)
新疆维吾尔自治区自然科学基金(2025D01E15)
Natural Science Foundation of Xinjiang Uygur Autonomous Region(2025D01A116)
新疆维吾尔自治区自然科学基金(2025D01A116)
National Natural Science Foundation of China(32260881)
国家自然科学基金(32260881)
作者信息
    1.新疆农业大学 动物医学学院，新疆 乌鲁木齐
    2.新疆动物临床医学研究重点实验室，新疆 乌鲁木齐
    3.新疆农业职业技术大学，新疆 昌吉
    4.新疆天莱农牧集团股份有限公司，新疆 博乐
    5.巴州若羌县畜牧兽医站，新疆 巴州

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
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红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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