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Article(id=1259888461201400350, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, articleNumber=null, orderNo=null, doi=10.13343/j.cnki.wsxb.20250837, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1762444800000, receivedDateStr=2025-11-07, revisedDate=null, revisedDateStr=null, acceptedDate=1768060800000, acceptedDateStr=2026-01-11, onlineDate=1778310416745, onlineDateStr=2026-05-09, pubDate=1777824000000, pubDateStr=2026-05-04, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1778310416745, onlineIssueDateStr=2026-05-09, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1778310416745, creator=13701087609, updateTime=1778310416745, updator=13701087609, issue=Issue{id=1259888457367806489, tenantId=1146029695717560320, journalId=1192105938417971205, year='2026', volume='66', issue='5', pageStart='2031', pageEnd='2556', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=0, articleOrder=1, issueType=-1, specialIssue=null, createTime=1778310415832, creator=13701087609, updateTime=1778320153326, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1259929299465921482, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1259929299465921483, tenantId=1146029695717560320, journalId=1192105938417971205, issueId=1259888457367806489, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=2393, endPage=2403, ext={EN=ArticleExt(id=1259888462438720039, articleId=1259888461201400350, tenantId=1146029695717560320, journalId=1192105938417971205, language=EN, title=Role of the β-1,3-glucan-binding protein gene in Apis cerana cerana against Ascosphaera apis infection, columnId=1192149543992045670, journalTitle=Acta Microbiologica Sinica, columnName=Research Article, runingTitle=null, highlight=null, articleAbstract=

Objective To analyze the expression profile of the β-glucan-binding protein (Acβ-GBP) gene of Apis cerana cerana in response to Ascosphaera apis infection and to investigate the impacts of Acβ-GBP knockdown on the larval mortality and the incidence of chalkbrood disease following A. apis infection. These findings will provide a foundation for further functional research. Methods The sequence and structural characteristics of Acβ-GBP were analyzed via bioinformatics approaches. RT-qPCR was employed to investigate the expression profiles of Acβ-GBP in the larval midgut following A. apis infection. Furthermore, RNA interference (RNAi) was utilized to explore the impacts of Acβ-GBP on the larval mortality and the incidence of chalkbrood disease. Results The CDS length of Acβ-GBP was 1 440 bp, encoding a protein with a molecular weight of 54.68 kDa and a grand average of hydropathicity value of -0.22, which contained a typical transmembrane domain and signal peptide. Phylogenetic analysis revealed that β-GBP of A. c. cerana, Apis florea and Apis dorsata clustered into a single major clade. After A. apis infection, the expression level of Acβ-GBP in the midgut of A. c. cerana worker larvae was downregulated at 1-3 days post-infection (dpi) (P<0.05). Following RNA interference (RNAi)-mediated silencing of Acβ-GBP, its expression level was lower than that in the ds-egfp group at 2 and 3 dpi (P<0.01). The cumulative larval mortality and the incidence of chalkbrood disease both increased over the infection time, and the overall mortality was higher than that of the control group (P<0.000 1). Conclusion Acβ-GBP was capable of responding to A. apis infection, and knockdown of Acβ-GBP expression significantly impaired the resistance of honeybee larvae to A. apis. Collectively, β-GBP acts as an important immune recognition protein in A. c. cerana, and plays an important role in defending against fungal invasion.

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E-mail: CHEN Dafu, ;
FU Zhongmin,
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These authors contributed equally to this work.

, authorsList=Fangji WANG, Xinrui CHEN, Yaqin GAO, Yuwei ZHANG, Genchao GAN, Shuai ZHOU, Rui GUO, Jianfeng QIU, Zhongmin FU, Dafu CHEN), CN=ArticleExt(id=1259888470298845810, articleId=1259888461201400350, tenantId=1146029695717560320, journalId=1192105938417971205, language=CN, title=中华蜜蜂 β-GBP 基因在抵抗蜜蜂球囊菌侵染中的作用, columnId=1192149544164012138, journalTitle=微生物学报, columnName=研究报告, runingTitle=null, highlight=null, articleAbstract=

目的 解析中华蜜蜂(Apis cerana cerana)的β-1,3-葡聚糖结合蛋白(Acβ-GBP)在响应蜜蜂球囊菌(Ascosphaera apis)侵染时的表达谱，探究干扰Acβ-GBP对蜜蜂球囊菌侵染的幼虫死亡率和白垩病发病率的影响，为进一步的功能研究奠定基础。 方法 基于生物信息学方法分析Acβ-GBP的序列和结构特征；采用实时荧光定量逆转录PCR (real-time RT-PCR, RT-qPCR)技术调查幼虫肠道中Acβ-GBP在球囊菌侵染后的表达特征；通过RNA干扰技术探究Acβ-GBP对幼虫死亡率及白垩病发病率的影响。 结果 中华蜜蜂Acβ-GBP的CDS长度为1 440 bp，编码蛋白的分子质量约为54.68 kDa，平均亲水系数为-0.22，存在典型的跨膜结构域和信号肽。进化分析表明，中华蜜蜂与小蜜蜂(Apis florea)、大蜜蜂(Apis dorsata)的β-GBP共同聚为一大支。蜜蜂球囊菌侵染后，中华蜜蜂工蜂幼虫肠道中Acβ-GBP的表达量在1-3 dpi均显著下调(P<0.05)；干扰Acβ-GBP后，其表达量在2 dpi和3 dpi极显著低于ds-egfp组(P<0.01)。幼虫累计死亡率和白垩病发病率均随侵染时间增加而升高，且整体死亡率极显著高于对照组(P<0.000 1)。 结论 Acβ-GBP能够响应蜜蜂球囊菌的侵染，干扰Acβ-GBP表达显著降低蜜蜂幼虫对蜜蜂球囊菌的抵抗性。β-GBP是中华蜜蜂的重要免疫识别蛋白，在抵御真菌入侵过程中发挥重要作用。

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作者贡献声明

王芳吉：样品制备、生物信息学分析、RNA干扰、表达量测定等实验操作过程、数据分析、执行背景调研、撰写文章；陈心蕊：数据分析、方法论、验证、撰写文章；高雅琴：数据收集与监管，执行调研；张雨薇：协助RNA干扰实验，及工蜂幼虫的死亡率和白垩病发病率统计；干根超：协助完成各实验操作过程；周帅：协助完成各实验操作过程；郭睿：提出概念，获取基金，提供主要试剂与仪器，审阅；邱剑丰：数据收集与监管，数据分析，项目管理，统筹全文思路及审阅；付中民：提出概念，获取基金，提供主要试剂与仪器，审阅；陈大福：提出概念，获取基金，提供主要试剂与仪器，审阅。

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A: Phosphorylation site; B: Hydrophilic property; C: Transmembrane domain; D: Signal peptide; E: Secondary structure; F: Tertiary structure., figureFileSmall=75yUkgd6TBDH7NULbdv6NQ==, figureFileBig=7nDkXKODIRZEP0cIjcbkdA==, tableContent=null), ArticleFig(id=1259928478699405671, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=CN, label=图2, caption=Acβ-GBP蛋白的理化性质和分子特征, figureFileSmall=75yUkgd6TBDH7NULbdv6NQ==, figureFileBig=7nDkXKODIRZEP0cIjcbkdA==, tableContent=null), ArticleFig(id=1259928481195016561, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=EN, label=Figure 3, caption=Motifs (A) and domains (B) of β-GBP proteins in Apis cerana cerana and other nine species., figureFileSmall=ACc+kZjqfhm5udMzjrZS1A==, figureFileBig=oKRCh+mT4PW/eQzEoztHiA==, tableContent=null), ArticleFig(id=1259928482939847029, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=CN, label=图3, caption=中华蜜蜂和其他9个物种β-GBP蛋白含有的保守基序(A)和结构域(B), figureFileSmall=ACc+kZjqfhm5udMzjrZS1A==, figureFileBig=oKRCh+mT4PW/eQzEoztHiA==, tableContent=null), ArticleFig(id=1259928484542071169, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=EN, label=Figure 4, caption=Phylogenetic tree of Apis cerana cerana and other species based on β-GBP proteins by neighbor-joining method. The numbers in parentheses in the figure are the accession numbers of the species in GenBank; The numbers on the branches are the bootstrap values., figureFileSmall=c6EeN5ybPkKecKLsG7C8Gw==, figureFileBig=5tJnVC+Obmq853JfSYSYIg==, tableContent=null), ArticleFig(id=1259928485456429451, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=CN, label=图4, caption=邻接法构建基于β-GBP蛋白的中华蜜蜂与其他物种的系统发育树, figureFileSmall=c6EeN5ybPkKecKLsG7C8Gw==, figureFileBig=5tJnVC+Obmq853JfSYSYIg==, tableContent=null), ArticleFig(id=1259928487469695383, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=EN, label=Figure 5, caption=Relative expression levels of Acβ-GBP in the guts of Apis cerana cerana worker larvae inoculated with Ascosphaera apis. *: P<0.05; ****: P<0.000 1., figureFileSmall=TEnZeg8jgXMYu0WQT64eFg==, figureFileBig=/30WG3NOJrIvjaPykWsrbA==, tableContent=null), ArticleFig(id=1259928488304361887, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=CN, label=图5, caption=蜜蜂球囊菌接种后中华蜜蜂工蜂幼虫肠道中 Acβ-GBP 的相对表达量, figureFileSmall=TEnZeg8jgXMYu0WQT64eFg==, figureFileBig=/30WG3NOJrIvjaPykWsrbA==, tableContent=null), ArticleFig(id=1259928488828649893, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=EN, label=Figure 6, caption=The effect of interfering with Acβ-GBP on the resistance of worker larvae to Ascosphaera apis infection. A: Detection of dsRNA from in vitro transcription by agarose gel electrophoresis; B: Determination of relative expression level of Acβ-GBP in the midguts of Apis cerana cerana worker larvae inoculated with Ascosphaera apis after feeding dsRNA; C, D: Cumulative mortality rate and Chalkbrood incidence rate of Apis cerana cerana worker larvae inoculated with Ascosphaera apis after silencing Acβ-GBP. *: P<0.05; **: P<0.01; ***: P<0.001; ****: P<0.000 1., figureFileSmall=X6GII5BX0Qho6nHct3BKqA==, figureFileBig=Z3fOt7QT0UDqatg+idV3vA==, tableContent=null), ArticleFig(id=1259928489998860722, tenantId=1146029695717560320, journalId=1192105938417971205, articleId=1259888461201400350, language=CN, label=图6, caption=干扰 Acβ-GBP 对工蜂幼虫抵抗蜜蜂球囊菌侵染的影响, figureFileSmall=X6GII5BX0Qho6nHct3BKqA==, figureFileBig=Z3fOt7QT0UDqatg+idV3vA==, tableContent=null)], attaches=null, journal=Journal(id=1192105720683257860, delFlag=0, nameCn=微生物学报, nameEn=Acta Microbiologica Sinica, nameHistory1=null, nameHistory2=null, 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中华蜜蜂 β-GBP 基因在抵抗蜜蜂球囊菌侵染中的作用
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王芳吉 1 , 陈心蕊 1 , 高雅琴 1 , 张雨薇 1 , 干根超 1 , 周帅 1 , 郭睿 1, 2, 3 , 邱剑丰 1, 2, 3 , 付中民 1, 2, 3 , 陈大福 1, 2, 3
微生物学报 | 研究报告 2026,66(5): 2393-2403
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微生物学报 | 研究报告 2026, 66(5): 2393-2403
中华蜜蜂 β-GBP 基因在抵抗蜜蜂球囊菌侵染中的作用
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王芳吉1, 陈心蕊1, 高雅琴1, 张雨薇1, 干根超1, 周帅1, 郭睿1, 2, 3, 邱剑丰1, 2, 3, 付中民1, 2, 3 , 陈大福1, 2, 3
作者信息
  • 1.福建农林大学 蜂学与生物医药学院，福建 福州
  • 2.天然生物毒素国家地方联合工程实验室，福建 福州
  • 3.福建农林大学 蜂疗研究所，福建 福州
Role of the β-1,3-glucan-binding protein gene in Apis cerana cerana against Ascosphaera apis infection
Fangji WANG1, Xinrui CHEN1, Yaqin GAO1, Yuwei ZHANG1, Genchao GAN1, Shuai ZHOU1, Rui GUO1, 2, 3, Jianfeng QIU1, 2, 3, Zhongmin FU1, 2, 3 , Dafu CHEN1, 2, 3
Affiliations
  • 1.College of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
  • 2.National & Local United Engineering Laboratory of Natural Biotoxin, Fuzhou, Fujian, China
  • 3.Apitherapy Research Institute of Fujian Agriculture and Forestry University, Fuzhou, Fujian, China
出版时间: 2026-05-04 doi: 10.13343/j.cnki.wsxb.20250837
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目的 解析中华蜜蜂(Apis cerana cerana)的β-1,3-葡聚糖结合蛋白(Acβ-GBP)在响应蜜蜂球囊菌(Ascosphaera apis)侵染时的表达谱，探究干扰Acβ-GBP对蜜蜂球囊菌侵染的幼虫死亡率和白垩病发病率的影响，为进一步的功能研究奠定基础。 方法 基于生物信息学方法分析Acβ-GBP的序列和结构特征；采用实时荧光定量逆转录PCR (real-time RT-PCR, RT-qPCR)技术调查幼虫肠道中Acβ-GBP在球囊菌侵染后的表达特征；通过RNA干扰技术探究Acβ-GBP对幼虫死亡率及白垩病发病率的影响。 结果 中华蜜蜂Acβ-GBP的CDS长度为1 440 bp，编码蛋白的分子质量约为54.68 kDa，平均亲水系数为-0.22，存在典型的跨膜结构域和信号肽。进化分析表明，中华蜜蜂与小蜜蜂(Apis florea)、大蜜蜂(Apis dorsata)的β-GBP共同聚为一大支。蜜蜂球囊菌侵染后，中华蜜蜂工蜂幼虫肠道中Acβ-GBP的表达量在1-3 dpi均显著下调(P<0.05)；干扰Acβ-GBP后，其表达量在2 dpi和3 dpi极显著低于ds-egfp组(P<0.01)。幼虫累计死亡率和白垩病发病率均随侵染时间增加而升高，且整体死亡率极显著高于对照组(P<0.000 1)。 结论 Acβ-GBP能够响应蜜蜂球囊菌的侵染，干扰Acβ-GBP表达显著降低蜜蜂幼虫对蜜蜂球囊菌的抵抗性。β-GBP是中华蜜蜂的重要免疫识别蛋白，在抵御真菌入侵过程中发挥重要作用。

中华蜜蜂  /  β-1,3-葡聚糖结合蛋白  /  蜜蜂球囊菌  /  免疫响应  /  RNA干扰

Objective To analyze the expression profile of the β-glucan-binding protein (Acβ-GBP) gene of Apis cerana cerana in response to Ascosphaera apis infection and to investigate the impacts of Acβ-GBP knockdown on the larval mortality and the incidence of chalkbrood disease following A. apis infection. These findings will provide a foundation for further functional research. Methods The sequence and structural characteristics of Acβ-GBP were analyzed via bioinformatics approaches. RT-qPCR was employed to investigate the expression profiles of Acβ-GBP in the larval midgut following A. apis infection. Furthermore, RNA interference (RNAi) was utilized to explore the impacts of Acβ-GBP on the larval mortality and the incidence of chalkbrood disease. Results The CDS length of Acβ-GBP was 1 440 bp, encoding a protein with a molecular weight of 54.68 kDa and a grand average of hydropathicity value of -0.22, which contained a typical transmembrane domain and signal peptide. Phylogenetic analysis revealed that β-GBP of A. c. cerana, Apis florea and Apis dorsata clustered into a single major clade. After A. apis infection, the expression level of Acβ-GBP in the midgut of A. c. cerana worker larvae was downregulated at 1-3 days post-infection (dpi) (P<0.05). Following RNA interference (RNAi)-mediated silencing of Acβ-GBP, its expression level was lower than that in the ds-egfp group at 2 and 3 dpi (P<0.01). The cumulative larval mortality and the incidence of chalkbrood disease both increased over the infection time, and the overall mortality was higher than that of the control group (P<0.000 1). Conclusion Acβ-GBP was capable of responding to A. apis infection, and knockdown of Acβ-GBP expression significantly impaired the resistance of honeybee larvae to A. apis. Collectively, β-GBP acts as an important immune recognition protein in A. c. cerana, and plays an important role in defending against fungal invasion.

Apis cerana cerana  /  β-1,3-glucan-binding protein  /  Ascosphaera apis  /  immune response  /  RNA interference
王芳吉, 陈心蕊, 高雅琴, 张雨薇, 干根超, 周帅, 郭睿, 邱剑丰, 付中民, 陈大福. 中华蜜蜂 β-GBP 基因在抵抗蜜蜂球囊菌侵染中的作用. 微生物学报, 2026 , 66 (5) : 2393 -2403 . DOI: 10.13343/j.cnki.wsxb.20250837
Fangji WANG, Xinrui CHEN, Yaqin GAO, Yuwei ZHANG, Genchao GAN, Shuai ZHOU, Rui GUO, Jianfeng QIU, Zhongmin FU, Dafu CHEN. Role of the β-1,3-glucan-binding protein gene in Apis cerana cerana against Ascosphaera apis infection[J]. Acta Microbiologica Sinica, 2026 , 66 (5) : 2393 -2403 . DOI: 10.13343/j.cnki.wsxb.20250837
正文
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β-1,3-葡聚糖结合蛋白(beta-1,3-glucan-binding protein, β-GBP)属于GNBP/β-葡聚糖识别蛋白家族，是识别蛋白中的重要一员。β-GBP是真菌表面β-1,3-葡聚糖的重要识别受体，在昆虫天然免疫中起着重要的作用[1]。黑腹果蝇(Drosophila melanogaster)体内革兰氏阴性结合蛋白(βGRP/GNBP3)识别β-1,3-葡聚糖，激活下游蛋白酶级联反应，最终激活Toll样受体(Toll-like receptors, TLRs)信号通路，合成抗菌肽，抵御真菌感染[2]。类似地，在家蚕(Bombyx mori)[3]、印度明对虾(Fenneropenaeus indicus)[4]和东北大黑鳃金龟(Holotrichia diomphalia)[5]中也发现β-GBP能结合β-1,3-葡聚糖，通过触发酚氧化酶(phenoloxidase, PO)级联反应来抵抗细菌和真菌感染。β-GBP激活的酚氧化酶级联反应是无脊椎动物抗真菌或细菌的关键先天免疫机制。在蜜蜂方面，对西方蜜蜂(Apis mellifera)幼虫注射幼虫芽孢杆菌(Paenibacillus larvae)会诱导β-GBP、PO和丝氨酸蛋白酶等免疫基因表达，以抵抗美洲幼虫腐臭病[6]。
蜜蜂对全球农业生产与经济发展具有不可替代的重要作用，它们不仅是蜂蜜等蜂产品的核心生产者，更承担着农业及园艺作物异花授粉的关键功能。蜜蜂的健康状况直接关系到生态平衡与粮食安全，因此保障蜜蜂群体健康至关重要。然而，蜜蜂的生存正面临多重威胁，其中由蜜蜂球囊菌(Ascosphaera apis)侵染引发的白垩病是危害蜂群存活的重要病害之一[7]。冯睿蓉[8]发现，蜜蜂等昆虫主要通过氧化反应对外源有害物质进行解毒，蜜蜂球囊菌侵染会诱导幼虫体内解毒相关基因上调，增强氧化反应强度，进而影响其氧化应激能力；而在成年工蜂中该真菌侵染可激活免疫缺陷(immune deficiency, IMD)和Toll等免疫相关通路，促使抗菌肽等关键免疫效应分子高表达以抵御病原胁迫[9]。尽管β-GBP作为昆虫先天免疫中的重要模式识别蛋白，其抗真菌功能已在多种无脊椎动物中得到证实，但在蜜蜂中β-GBP的免疫功能尚未被研究。
中华蜜蜂(Apis cerana cerana)的β-GBP (Acβ-GBP)在抵御蜜蜂球囊菌侵染中的具体作用尚不明确。基于此，本研究克隆了中华蜜蜂β-GBP (Acβ-GBP)基因的编码序列(coding sequence, CDS)，预测了其编码蛋白的理化性质与分子特征，分析其与其他物种β-GBP的结构域差异及亲缘关系；进一步解析了Acβ-GBP在蜜蜂球囊菌侵染后的表达模式，并通过RNA干扰技术探究了该基因对幼虫白垩病发病率及死亡率的影响，以期为深入阐明中华蜜蜂抗白垩病的分子机制提供科学依据。
1 材料与方法
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1.1 材料
蜜蜂球囊菌由福建农林大学蜂学与生物医药学院蜜蜂保护实验室保存，该菌在中国普通微生物菌种保藏管理中心(CGMCC)的保藏号为No. 40895。中华蜜蜂工蜂幼虫取自福建农林大学蜂学与生物医药学院饲养的蜂群。
1.2 蜜蜂球囊菌接种及蜜蜂幼虫肠道样品制备
参照Chen等[10]已建立的技术流程，选取2日龄中蜂幼虫置于48孔板(每孔含50 µL的人工饲料)，饲料配比：蜂王浆63% (王浆酸含量≥1.4)，无菌水30%，蜂蜜6% (土蜂蜜，执行标准：GB 14963)，酵母提取物(上海吉至生化科技有限公司) 1%，在(35±0.5) ℃、相对湿度90%条件下饲养；对照组3日龄幼虫饲喂不含蜜蜂球囊菌孢子的饲料，处理组饲喂终浓度1×106个/mL蜜蜂球囊菌孢子的饲料(0 days post inoculation, 0 dpi)，每24 h更换饲料并饲养至6日龄。剖取4-6日龄(1-3 dpi)两组幼虫肠道组织，经液氮速冻后于-80 ℃保存，以3头幼虫肠道为1个生物学重复，共设3个生物学重复。
本研究选用的1×106个/mL蜜蜂球囊菌孢子接种浓度，参考Chen等[10]已建立的标准化侵染体系，并经预实验验证：该浓度可使中华蜜蜂工蜂幼虫呈现稳定且可重复的白垩病发病特征，发病强度与自然蜂群一致，同时避免因浓度过高导致幼虫快速死亡或浓度过低导致发病不规律，确保基因干扰效应能够被有效检测。
1.3 PCR扩增和Sanger测序
根据NCBI GenBank数据库收录的Acβ-GBP (GenBank登录号为XM_017049917.3)的核苷酸序列，对CDS进行分段克隆，设计并合成3对特异性扩增引物[原始数据存储在ScienceDB(www.scidb.cn)微生物学报社区，DOI为10.57760/sciencedb.j00231.00046]。利用SteadyPure快速RNA提取试剂盒(湖南艾科瑞生物工程有限公司)提取幼虫肠道样品的总RNA，并反转录获得cDNA。PCR反应体系(20 µL)：PCR Mix 10 µL，cDNA模板1 µL，上、下游引物(2.5 pmol/µL)各1 µL，DEPC水7 µL。PCR反应程序：95 ℃ 3 min；95 ℃ 30 s，55 ℃ 30 s，72 ℃ 30 s，共34个循环；72 ℃ 1 min。
1.4 生物信息学及系统进化分析
Acβ-GBP的核苷酸序列通过ORF工具获得氨基酸序列。利用ProParam、TMHMM、ProtScale、NetPhos 3.1 Server和SignalP 6.0 Server在线网站预测Acβ-GBP蛋白的理化性质、跨膜结构域、亲水性、磷酸化位点和信号肽。二级结构、三级结构和亚细胞定位的预测利用SOPMA[11]、SWISS-MODEL[12]和PSORT Ⅱ[13]网站进行。
同源性分析所用序列均下载自NCBI GenBank数据库，包括A. c. cerana XP_016905406.1、小蜜蜂(Apis florea)XP_003690362.2、大蜜蜂(Apis dorsata)XP_006607921.1、熊蜂(Bombus affinis)XP_050587351.1、欧洲熊蜂(Bombus terrestris)XP_012167632.1、果壁蜂(Osmia lignaria)XP_034187872.1、毕氏卵角蚁(Ooceraea biroi)XP_011342604.2、狐条蜂(Anthophora quadrimaculata)CAK9811243.1、黑大蜜蜂(Apis laboriosa)XP_043789953.1、黄脚胡蜂(Eufriesea mexicana)XP_017759246.1的β-GBP氨基酸序列。利用MEGA 11.0[14]软件中的ClustalW工具对上述10个物种的β-GBP进行多重比对，再通过bootstrap邻接(neighbor-joining)法构建系统发育树，设置1 000次重复。采用Blast的CD-search工具和MEME[15]网站分别鉴定上述各物种β-GBP的保守基序和结构域。通过TBtools软件[16]将鉴定到的保守基序和结构域进行可视化。以上软件均采用默认参数。
1.5 实时荧光定量逆转录PCR
根据Acβ-GBP的核苷酸序列，利用Primer Premier 6软件[17]设计Acβ-GBP的实时荧光定量逆转录PCR (real-time RT-PCR, RT-qPCR)引物(DOI为10.57760/sciencedb.j00231.00046)。以AcActin (GenBank登录号为XM_017059068.2)作为内参基因。反应在ABI Quant Studio 3荧光定量PCR系统(Applied Biosystems公司)中进行。RT-qPCR反应体系和程序参照郭意龙等[18]的方法。RT-qPCR进行3次技术重复和3次生物学重复。
1.6 RNA干扰
根据Acβ-GBP CDS的核苷酸序列，设计特异性干扰靶点和引物(DOI为10.57760/sciencedb.j00231.00046)。引物PCR扩增并连接pClone007质粒，将测序正确的菌液转入新鲜LB菌液中扩大培养，利用去内毒素质粒提取试剂盒提取重组质粒。按照T7 RNAi Transcription Kit (南京诺唯赞生物科技股份有限公司)试剂盒说明书，在干扰片段特异性引物的5′端增加T7启动子序列(5′-TAATACGACTCACTATAGGG-3′)，以重组质粒为模板进行PCR扩增。通过1.5%的琼脂糖凝胶电泳检测扩增产物后回收目的片段。利用T7 RNAi Transcription Kit (南京诺唯赞生物科技股份有限公司)的步骤进行dsRNA的体外转录合成(ds-Acβ-GBP)。以绿色荧光蛋白基因egfp的干扰片段作为阴性对照(ds-egfp)。dsRNA的浓度和纯度由超微量测定仪检测。
参照郭意龙等[19]的方法进行dsRNA的饲喂。蜜蜂球囊菌侵染的3日龄(0 dpi)幼虫，吸取1 000 ng的ds-Acβ-GBP滴加至50 µL饲料中混匀作为实验组，命名为A. apis+ds-Acβ-GBP。同样地，饲喂1 000 ng的ds-egfp幼虫作为对照组，命名为A. apis+ds-egfp。每隔24 h饲喂含有相同量的dsRNA的人工饲料，直至3 dpi。解剖A. apis+ds-Acβ-GBP和A. apis+ds-egfp组的1-3 dpi肠道样本。3头幼虫的肠道样品作为1个生物学重复，共设3个生物学重复。
1.7 累计死亡率和白垩病发病率统计
幼虫在蜜蜂球囊菌接种和dsRNA干扰后，持续饲喂至7 dpi，更换饲料前统计各组幼虫死亡数量和发病数量，最终计算1-7 dpi的幼虫累计死亡率和白垩病发病率，如公式(1)、(2)所示。
死亡率=(每组每个生物学重复死亡幼虫数量/每组每个生物学重复总幼虫数量)×100%
发病率=(每组每个生物学重复发病幼虫数量/每组每个生物学重复总幼虫数量)×100%
本研究对照组和处理组各设置3个生物学重复，每个生物学重复16头幼虫。
1.8 数据统计
基因的相对表达量利用2-ΔΔCt法[20]进行计算。RT-qPCR的数据分析及图片绘制采用GraphPad Prism (v9.1.0)软件进行，其中数据以平均值±标准差(mean±SD)表示，分析方法为t检验(ns: P>0.05; *: P<0.05; **: P<0.01; ***: P<0.001; ****: P<0.000 1)。幼虫累计死亡率和白垩病发病率的数据结果采用GraphPad Prism 8软件绘制图片，利用mean±SD表达数据，利用双因素方差分析(two-way ANOVA)分析数据显著性。
2 结果与分析
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2.1 Acβ-GBPCDS的分子克隆
凝胶电泳结果显示，分段扩增出3条Acβ-GBP的CDS片段，克隆的Acβ-GBP-1、Acβ-GBP-2、Acβ-GBP-3的长度分别为564、520、567 bp (图1)。Sanger测序的比对结果显示，3条片段序列与NCBI预测的Acβ-GBP序列相同(DOI为10.57760/sciencedb.j00231.00046)。结果表明，Acβ-GBP基因在中蜂工蜂幼虫肠道中表达，且其CDS区被成功克隆。
2.2 Acβ-GBP蛋白的理化性质和分子特征
Acβ-GBP的CDS包含1 440个核苷酸，可编码479个氨基酸。Acβ-GBP分子量约为54.68 kDa，分子式为C2 487H3 831N647O713S15，脂溶系数为97.22，等电点为6.54。Acβ-GBP含有20种氨基酸，其中含量最高的是异亮氨酸(53个)，含量最低的是蛋氨酸(7个)。在Acβ-GBP中丝氨酸、苏氨酸和酪氨酸的磷酸化位点数量分别为18、10、12个(图2A)。Acβ-GBP的平均亲水系数为-0.22，疏水氨基酸数量少于亲水氨基酸(图2B)。Acβ-GBP蛋白具有典型的跨膜结构域和信号肽(图2C、2D)。Acβ-GBP中包含22个(4.59%) α-螺旋，135条(28.18%)延长链，322个(67.22%)无规则卷曲(图2E)。三级结构分析结果显示Acβ-GBP与其模板A0A7M6UV61.1.A之间的同源性为91.18% (图2F)。亚细胞定位预测结果显示，Acβ-GBP可同时定位于内质网、细胞质、高尔基体、分泌系统囊泡、细胞外(包括细胞壁)和线粒体，占比分别为22.20%、22.20%、22.20%、11.10%、11.10%和11.10%。
2.3 Acβ-GBP蛋白的保守基序、结构域和系统进化分析
如图3A所示，Acβ-GBP蛋白存在5个保守基序。在大蜜蜂、黑大蜜蜂、小蜜蜂、黄脚胡蜂、熊蜂、欧洲熊蜂、狐条蜂、果壁蜂和毕氏卵角蚁的β-GBP同样存在上述5个保守基序(图3A)。Acβ-GBP中含有GH16_beta_GRP和CBM39结构域；在小蜜蜂、欧洲熊蜂、黑大蜜蜂、熊蜂和大蜜蜂的β-GBP中也存在上述2个结构域。狐条蜂、黄脚胡蜂、果壁蜂和毕氏卵角蚁的β-GBP含有LamG superfamily和CBM39结构域。
系统进化分析表明中华蜜蜂的β-GBP单独聚为一小支，与大蜜蜂、黑大蜜蜂、和小蜜蜂的β-GBP共同聚为一大支；根据氨基酸序列比对，中华蜜蜂与小蜜蜂的β-GBP氨基酸序列相似性为88.09%，中华蜜蜂与大蜜蜂为90.02%，中华蜜蜂与黑大蜜蜂为89.17%。熊蜂和欧洲熊蜂聚为一支。黄脚胡蜂、果壁蜂和狐条蜂的β-GBP聚为一支(图4)。
2.4 干扰 Acβ-GBP 影响中蜂工蜂幼虫的死亡率和白垩病发病率
RT-qPCR结果显示，蜜蜂球囊菌侵染后Acβ-GBP的表达量显著下调(P<0.05) (图5)。
进一步调查了干扰Acβ-GBP后，幼虫对蜜蜂球囊菌侵染的抵抗性。琼脂糖凝胶电泳检测结果表明成功合成Acβ-GBP的干扰序列ds-Acβ-GBP (248 bp)和阴性对照序列ds-egfp (255 bp) (图6A)。蜜蜂球囊菌侵染后饲喂ds-Acβ-GBP和ds-egfp，干扰Acβ-GBP的肠道中Acβ-GBP的表达量在1 dpi显著低于ds-egfp组(P<0.05)，在2 dpi和3 dpi极显著低于ds-egfp组(P<0.01) (图6B)。蜜蜂球囊菌侵染后，干扰Acβ-GBP的幼虫累计死亡率均随侵染时间而增加，并且整体死亡率极显著高于对照组(P<0.000 1) (图6C)。进一步统计蜜蜂球囊菌接种后，干扰Acβ-GBP死亡幼虫的白垩病发病率。结果显示干扰Acβ-GBP和对照组的幼虫白垩病发病率均随侵染时间而增加。干扰Acβ-GBP的白垩病发病率极显著高于对照组(P<0.000 1) (图6D)。
3 讨论与结论
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昆虫几乎存在于所有栖息地和生态系统中，其快速的繁殖速度、强大的适应能力以及面对病原体威胁时高效的免疫应答起到了至关重要的作用[21]。昆虫的β-GBP的功能是作为模式识别蛋白，能够识别病原体细胞壁表面的β-1,3-葡聚糖，并与之结合，进而激活宿主的Toll信号通路和PO级联反应[4]，这是无脊椎动物抵御病原体入侵的重要免疫防御屏障[22]。β-GBP的免疫功能在无脊椎动物中已被广泛研究，研究对象包括家蚕、小菜蛾(Plutella xylostella)、中华绒螯蟹(Eriocheir sinensis)、拟穴青蟹(Scylla paramamosain)和克氏原螯虾(Procambarus clarkii)等[23-26]。然而，中华蜜蜂的β-GBP在抵抗病原体侵染时的作用尚不清楚。本研究克隆了中华蜜蜂β-GBP的CDS区，解析了蜜蜂球囊菌侵染后β-GBP的表达模式和作用，为后续的功能研究奠定了基础。
Acβ-GBP蛋白具有亲水性、跨膜结构域及信号肽，符合模式识别受体横跨细胞膜、识别病原体的结构特征[27]。Acβ-GBP与其他9个物种的β-GBP均含有5个保守基序和CBM39结构域(图3)，其中CBM39结构域被证实参与病原体识别[28]；而Acβ-GBP特有的GH16_beta_GRP结构域，推测可通过结合并降解β-1,3-葡聚糖，激活PO系统[1]。中华蜜蜂与小蜜蜂和大蜜蜂的β-GBP聚为一支，氨基酸序列相似性高达88.00 %以上，表明该基因在蜜蜂类群中具有高度保守性，暗示其功能的进化稳定性(图4)。
蜜蜂球囊菌的孢子侵入幼虫肠道后在厌氧条件下受CO2诱导而活化萌发，至预蛹期中肠和后肠隔膜解除，孢子随食物残渣涌入后肠，接触氧气后孢子剧烈萌发；菌丝大量生长，肉眼可见白色、黑色或灰色的白垩虫尸[29]。为解析Acβ-GBP对幼虫抵抗蜜蜂球囊菌侵染的作用，本研究初步解析了蜜蜂球囊菌侵染后β-GBP的表达模式和作用。小菜蛾在响应金黄色葡萄球菌(Staphylococcus aureus)侵染时其体内的β-GBP基因mRNA水平显著上调，进一步增强β-GBP对血淋巴酚氧化酶原(pro-phenoloxidase, PPO)的激活，从而杀灭入侵微生物[23]。不同的是，本研究发现蜜蜂球囊菌侵染后幼虫肠道中Acβ-GBP基因的表达量在1-3 dpi均显著下调(P<0.05) (图5)。该结果与其他物种β-GBP的表达模式存在差异，可能是Acβ-GBP对蜜蜂球囊菌的响应存在滞后性。在蜜蜂球囊菌侵染后利用饲喂法成功干扰中蜂幼虫Acβ-GBP的表达(图6A、6B)。干扰Acβ-GBP后，幼虫的死亡率和白垩病发病率均显著高于对照组(P<0.05) (图6C、6D)，可能是由于干扰Acβ-GBP的表达，导致幼虫对蜜蜂球囊菌细胞壁表面的β-1,3-葡聚糖的识别减弱，酚氧化酶级联反应未被充分激活。这一现象与其他研究结论一致。在家蚕和多种对虾中通过抗体阻断或RNAi技术干扰β-GBP的功能会显著抑制酚氧化酶系统的激活，并降低宿主对真菌病原体的抵抗能力[30-31]。同样地，在赤拟谷盗(Tribolium castaneum)等昆虫模型中的研究也证实，β-GBP是启动抗真菌免疫的关键模式识别受体，其功能缺失会导致严重的免疫缺陷[32]。这些来自不同物种的证据共同表明，β-GBP在无脊椎动物的先天免疫防御中扮演着一个古老而保守的核心角色。本研究表明干扰Acβ-GBP会导致中蜂工蜂幼虫在响应蜜蜂球囊菌侵染时的生存能力降低，并提高白垩病发病率。
基金
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  • 国家自然科学基金(32372943)
  • 国家现代农业蜂产业技术体系专项资金(CARS-44-KXJ7)
  • 福建省自然科学基金(2025J01616)
  • 福建省自然科学基金(2023J01447)
  • 福建农林大学科技创新专项基金(KFb22060XA)
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2026年第66卷第5期
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doi: 10.13343/j.cnki.wsxb.20250837
  • 接收时间：2025-11-07
  • 首发时间：2026-05-09
  • 出版时间：2026-05-04
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  • 收稿日期：2025-11-07
  • 录用日期：2026-01-11
基金
The National Natural Science Foundation of China(32372943)
国家自然科学基金(32372943)
The China National Bee Industry Technology System(CARS-44-KXJ7)
国家现代农业蜂产业技术体系专项资金(CARS-44-KXJ7)
The Natural Science Foundation of Fujian Province(2025J01616)
福建省自然科学基金(2025J01616)
The Natural Science Foundation of Fujian Province(2023J01447)
福建省自然科学基金(2023J01447)
The Fujian Agriculture and Forestry University Science and Technology Innovation Special Fund(KFb22060XA)
福建农林大学科技创新专项基金(KFb22060XA)
作者信息
    1.福建农林大学 蜂学与生物医药学院，福建 福州
    2.天然生物毒素国家地方联合工程实验室，福建 福州
    3.福建农林大学 蜂疗研究所，福建 福州
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https://castjournals.cast.org.cn/joweb/wswxb/CN/10.13343/j.cnki.wsxb.20250837
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
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
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
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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