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Article(id=1256548246189629815, tenantId=1146029695717560320, journalId=1255847803461844995, issueId=1256548241764639069, articleNumber=null, orderNo=null, doi=10.13346/j.mycosystema.250251, pmid=null, cstr=32115.14.j.mycosystema.250251, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1755878400000, receivedDateStr=2025-08-23, revisedDate=null, revisedDateStr=null, acceptedDate=1758124800000, acceptedDateStr=2025-09-18, onlineDate=1777514047428, onlineDateStr=2026-04-30, pubDate=1776787200000, pubDateStr=2026-04-22, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1777514047428, onlineIssueDateStr=2026-04-30, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1777514047428, creator=13701087609, updateTime=1777514047428, updator=13701087609, issue=Issue{id=1256548241764639069, tenantId=1146029695717560320, journalId=1255847803461844995, year='2026', volume='45', issue='4', pageStart='250187', pageEnd='250358', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1777514046373, creator=13701087609, updateTime=1777516895320, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1256560191206711468, tenantId=1146029695717560320, journalId=1255847803461844995, issueId=1256548241764639069, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1256560191206711469, tenantId=1146029695717560320, journalId=1255847803461844995, issueId=1256548241764639069, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=250251, endPage=, ext={EN=ArticleExt(id=1256548247053656443, articleId=1256548246189629815, tenantId=1146029695717560320, journalId=1255847803461844995, language=EN, title=Adenylosuccinate synthase negatively controls Metarhizium robertsii pathogenicity, columnId=1256263562373226548, journalTitle=Mycosystema, columnName=Research paper, runingTitle=null, highlight=null, articleAbstract=

Adenylosuccinate synthetase (ADSS) plays an important role in cellular energy metabolism and signal transduction. However, ADSS had not been reported in entomopathogenic fungi. In this study, function of ADSS family protein MrADSS-1 to the growth, stress resistance and pathogenicity in the entomopathogenic fungus Metarhizium robertsii was characterized by investigating the protein subcellular localization and gene disruption, complementation and over-expression. Results showed that MrADSS-1 is exclusively localized within the vacuole. Disruption of the MrADSS-1 resulted in marked reduction of radial growth of the fungus on maltose medium and a significant decrease in UV-B tolerance, but unexpectedly enhanced thermotolerance. Bioassays revealed that loss of MrADSS-1 led to a pronounced increase in appressorium formation and penetration efficiency through cicada wings, resulting in elevated pathogenicity toward Galleria mellonella larvae. Conversely, over-expression of MrADSS-1 attenuated fungal virulence. These findings demonstrated that MrADSS-1 functions as a repressor of both thermotolerance and virulence in M. robertsii.

, correspAuthors=Yulong WANG, authorNote=null, correspAuthorsNote=
*
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ORCID: WANG Yulong (0000-0003-1619-2265)

, authorsList=Lechen WANG, Shiyue GUO, Yutong ZHAO, Yuanyuan DONG, Wenjing WU, Yan REN, Fuming GUO, Yulong WANG), CN=ArticleExt(id=1256548251726111180, articleId=1256548246189629815, tenantId=1146029695717560320, journalId=1255847803461844995, language=CN, title=腺苷酸基琥珀酸合成酶负介导罗伯茨绿僵菌致病力, columnId=1256263563312771301, journalTitle=菌物学报, columnName=研究论文, runingTitle=null, highlight=null, articleAbstract=

腺苷酸基琥珀酸合成酶(adenylosuccinate synthetase, ADSS)在细胞能量代谢与信号传导等过程中具有重要作用，但目前在昆虫病原真菌中的研究未见报道。本研究以罗伯茨绿僵菌Metarhizium robertsii中ADSS家族成员MrADSS-1为研究对象，利用亚细胞定位分析、基因敲除、回补和过表达等方法，系统探究了其在绿僵菌生长、抗逆和致病过程中的作用。结果表明，MrADSS-1分布在罗伯茨绿僵菌细胞的液泡中。敲除MrADSS-1导致菌株在麦芽糖培养基中生长速率显著下降、抗紫外能力减弱，但耐热能力增强。致病力测定结果表明，MrADSS-1敲除显著提高了绿僵菌附着胞形成率和蝉翅穿透能力，增强了对大蜡螟的毒力，而过表达MrADSS-1菌株则致病力下降。本研究结果表明，MrADSS-1负介导罗伯茨绿僵菌的耐热能力和致病力。

, correspAuthors=王玉龙, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=I5dlX2w8pDT2uSTfkw9fZQ==, magXml=nuIyLtM/R5+Ec7MgUmh3RA==, pdfUrl=null, pdf=c+74UK5LsmN37mDeMkyOUw==, pdfFileSize=928226, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=e07HflnerljxyLBTrCMsDg==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=LjrJLd4OT1VpsDG39gjeTw==, mapNumber=null, authorCompany=null, fund=null, authors=

作者贡献

王乐陈：基因敲除、过表达和回补菌株的构建与验证；郭世悦：生物学性状检测与分析；赵雨桐：功能基因的亚细胞定位分析；董媛媛和吴文婧：突变菌株的致病力分析；任言：菌株的保存、试虫的饲养；郭复明：实验思路指导、论文审阅与修订；王玉龙：试验整体设计、研究监管与指导、论文审阅与修订。

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figs=[ArticleFig(id=1256548279307854528, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Fig. 1, caption=Subcellular localization of MrADSS-1. Bars=10 μm., figureFileSmall=E2rKHXqTzy36jMo5weYtow==, figureFileBig=e07HflnerljxyLBTrCMsDg==, tableContent=null), ArticleFig(id=1256548280532591300, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=图1, caption=MrADSS-1的亚细胞定位 标尺=10 μm, figureFileSmall=E2rKHXqTzy36jMo5weYtow==, figureFileBig=e07HflnerljxyLBTrCMsDg==, tableContent=null), ArticleFig(id=1256548281254011596, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Fig. 2, caption=The effect of MrADSS-1 knockout on the asexual growth of Metarhizium robertsii. A, B: Colony morphology and diameter of the mutant strains on PDA, SDAY, and 1/4 SDAY media. C: Conidiation of the mutant strains on PDA medium. D, E: Colony morphology and diameter of the mutant strains on CZA and modified CZA media. Data are mean±SE. Bars=1 cm. *P<0.05., figureFileSmall=eUpNxV/Nw3dKRrnGRiMtgg==, figureFileBig=E15T6vDyK+gGovupIk1zUA==, tableContent=null), ArticleFig(id=1256548281421783759, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=图2, caption=敲除MrADSS-1对罗伯茨绿僵菌生长的影响 A, B：突变株在PDA、SDAY、1/4 SDAY培养基上生长的菌落形态(A)和生长直径(B)；C：突变株在PDA培养基上的产孢量；D, E：突变株在CZA及改良型CZA培养基上生长的菌落形态和生长直径；图中数据为平均数±标准误；标尺=1 cm；*P<0.05, figureFileSmall=eUpNxV/Nw3dKRrnGRiMtgg==, figureFileBig=E15T6vDyK+gGovupIk1zUA==, tableContent=null), ArticleFig(id=1256548281782493907, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Fig. 3, caption=The effect of MrADSS-1 knockout on the stress resistance of Metarhizium robertsii. A, B: Colony morphology and diameter of the mutant strains on PDA medium supplemented with NaCl (0.5 mol/L), H₂O₂ (10 mmol/L), or congo red (2 mg/mL). C: Relative germination rate of mutant spores after heat shock. D: Relative germination rate of mutant spores after UV irradiation. Data are mean±SE. Scale bars=1 cm. *P<0.05, **P<0.01, ***P<0.001., figureFileSmall=zQnr7mgQi8Shdwqxkz3cGA==, figureFileBig=5DU8mVYts3YLZnvAPd8eUw==, tableContent=null), ArticleFig(id=1256548281895740121, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=图3, caption=敲除MrADSS-1对罗伯茨绿僵菌抗胁迫能力的影响 A, B：突变株在添加NaCl (0.5 mol/L)、H2O2 (10 mmol/L)和congo red (2 mg/mL)的PDA培养基上生长的菌落形态；C：热激后突变株的孢子相对萌发率；D：紫外辐射后突变菌的孢子相对萌发率；图中数据为平均数±标准误；标尺=1 cm；*P<0.05，**P<0.01，***P<0.001, figureFileSmall=zQnr7mgQi8Shdwqxkz3cGA==, figureFileBig=5DU8mVYts3YLZnvAPd8eUw==, tableContent=null), ArticleFig(id=1256548282210312923, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Fig. 4, caption=The effect of MrADSS-1 deletion on the penetration and appressorium formation of Metarhizium robertsii. A: Colony morphology of the mutant strains after penetrating cicada wings. B: Colony diameters of the mutant strains after penetrating cicada wings. C: Appressorium formation rates. Data are mean±SE. Scale bars=1 cm. **P<0.01, ***P<0.001., figureFileSmall=yllurmir/VCwxnsgV7b4Rw==, figureFileBig=nQLUoQy35phSE00+lIOLbw==, tableContent=null), ArticleFig(id=1256548282310976224, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=图4, caption=敲除MrADSS-1对罗伯茨绿僵菌穿透及附着孢形成的影响 A：突变株穿透蝉翅后的菌落形态；B：突变株穿透蝉翅后的菌落生长直径；C：附着胞形成率；图中数据为平均数±标准误；标尺=1 cm；**P<0.01，***P<0.001, figureFileSmall=yllurmir/VCwxnsgV7b4Rw==, figureFileBig=nQLUoQy35phSE00+lIOLbw==, tableContent=null), ArticleFig(id=1256548282625549027, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Fig. 5, caption=The effect of MrADSS-1 deletion and over-expression on the pathogenicity of Metarhizium robertsii. A, B: The effect of MrADSS-1 knockout on the pathogenicity of M. robertsii toward Galleria mellonella larvae injected and soaked by the pathogen. C: Quantitative PCR analysis of MrADSS-1OE-1 and MrADSS-1OE-2. D, E: The effect of MrADSS-1 overexpression on the pathogenicity of M. robertsii toward Galleria mellonella larvae injected and soaked by the pathogen. Data are mean±SE. **P<0.01, ***P<0.001., figureFileSmall=gT7ODeEQf4eEpY8fo/cVYg==, figureFileBig=ZvyZM5iYipNusZZ3qnVXnw==, tableContent=null), ArticleFig(id=1256548282784932582, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=图5, caption=敲除及过表达MrADSS-1对罗伯茨绿僵菌致病力的影响 A, B：敲除MrADSS-1对罗伯茨绿僵菌体内注射(A)和体表浸渍(B)致病力影响；C：MrADSS-1OE-1和MrADSS-1OE-2的荧光定量PCR分析；D, E：过表达MrADSS-1对罗伯茨绿僵菌体内注射(D)和体表浸渍(E)致病力影响；图中数据为平均数±标准误；**P<0.01，***P<0.001, figureFileSmall=gT7ODeEQf4eEpY8fo/cVYg==, figureFileBig=ZvyZM5iYipNusZZ3qnVXnw==, tableContent=null), ArticleFig(id=1256548282982064873, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=EN, label=Table 1, caption=

Primers used in this study

, figureFileSmall=null, figureFileBig=null, tableContent=
引物
Primer		 序列
Sequence (5′→3′)
基因敲除载体构建引物
Primers required for
gene-knockout vector
construction		 ΔMrADSS-1-up-F TTTCCTCGTGTATCCCCGGGGGAGTTTGCTCGTGCGTCTTG
ΔMrADSS-1-up-R CTTTTTTCCCACCGCCGAGCTGCAGCCCGGGGGATCCGTC
ΔMrADSS-1-down-F ATCTGATGAACTAGTTCTAGAGCATTGGCCTCTATTCTTTT
ΔMrADSS-1-down-R TGCCTCGACAGGTGGTGCAGGCCGGCCTTGCTCGCCGAGT
基因回补载体构建引物
Primers for complementation
vector construction		 cpΔMrADSS-1-p-F CAAGCTTCGCACTAGTTCTAGAGAACACTATGCGGTGAAGG
cpΔMrADSS-1-p-R CGAGATCGGGGCGTTCATTCGGGAGACGAAATAAACTA
荧光标记载体构建引物
Primers for constructing
fluorescence-labeled vectors		 MrADSS-1-Gfp-F ACTTTGAAGACTGTGGTCTTATGATGGTGAGCAAGGGCGAG
MrADSS-1-Gfp-R CATCTACTCTGCAGGAATTCTTACTTGTACAGCTCGTCCATGC
基因过表达载体构建引物
Primers required for construction
of gene over-expression vector		 MrADSS-1OE-F CAAGAACCTTTAATCGAATTCATGAACGCCCCGATCTCG
MrADSS-1OE-R TGTAGTCCATAAGACCACAGTCTTCAAAGTCGC
突变株验证引物
Primers required for validation
of mutants		 Bar-F GCACCATCGTCAACCACTAC
Bar-R CAAGCTGCTCTAGCATTCG
MrADSS-1-F CAGTCGTCGCAGCCTGTCCCCATG
MrADSS-1-R GGTTGACATCCCGAAGAAAAGTCTCG
Ben-F CGTTACCTCACCTGCTCTG
Ben-R CCTCACTAAAGGGAACAAAA
), ArticleFig(id=1256548283158225648, tenantId=1146029695717560320, journalId=1255847803461844995, articleId=1256548246189629815, language=CN, label=表1, caption=

研究中采用的引物

, figureFileSmall=null, figureFileBig=null, tableContent=
引物
Primer		 序列
Sequence (5′→3′)
基因敲除载体构建引物
Primers required for
gene-knockout vector
construction		 ΔMrADSS-1-up-F TTTCCTCGTGTATCCCCGGGGGAGTTTGCTCGTGCGTCTTG
ΔMrADSS-1-up-R CTTTTTTCCCACCGCCGAGCTGCAGCCCGGGGGATCCGTC
ΔMrADSS-1-down-F ATCTGATGAACTAGTTCTAGAGCATTGGCCTCTATTCTTTT
ΔMrADSS-1-down-R TGCCTCGACAGGTGGTGCAGGCCGGCCTTGCTCGCCGAGT
基因回补载体构建引物
Primers for complementation
vector construction		 cpΔMrADSS-1-p-F CAAGCTTCGCACTAGTTCTAGAGAACACTATGCGGTGAAGG
cpΔMrADSS-1-p-R CGAGATCGGGGCGTTCATTCGGGAGACGAAATAAACTA
荧光标记载体构建引物
Primers for constructing
fluorescence-labeled vectors		 MrADSS-1-Gfp-F ACTTTGAAGACTGTGGTCTTATGATGGTGAGCAAGGGCGAG
MrADSS-1-Gfp-R CATCTACTCTGCAGGAATTCTTACTTGTACAGCTCGTCCATGC
基因过表达载体构建引物
Primers required for construction
of gene over-expression vector		 MrADSS-1OE-F CAAGAACCTTTAATCGAATTCATGAACGCCCCGATCTCG
MrADSS-1OE-R TGTAGTCCATAAGACCACAGTCTTCAAAGTCGC
突变株验证引物
Primers required for validation
of mutants		 Bar-F GCACCATCGTCAACCACTAC
Bar-R CAAGCTGCTCTAGCATTCG
MrADSS-1-F CAGTCGTCGCAGCCTGTCCCCATG
MrADSS-1-R GGTTGACATCCCGAAGAAAAGTCTCG
Ben-F CGTTACCTCACCTGCTCTG
Ben-R CCTCACTAAAGGGAACAAAA
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腺苷酸基琥珀酸合成酶负介导罗伯茨绿僵菌致病力
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王乐陈 1 , 郭世悦 1 , 赵雨桐 1 , 董媛媛 1 , 吴文婧 1 , 任言 1 , 郭复明 2 , 王玉龙 1, *
菌物学报 | 研究论文 2026,45(4): 250251
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菌物学报 | 研究论文 2026, 45(4): 250251
腺苷酸基琥珀酸合成酶负介导罗伯茨绿僵菌致病力
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王乐陈1, 郭世悦1, 赵雨桐1, 董媛媛1, 吴文婧1, 任言1, 郭复明2, 王玉龙1, *
作者信息
  • 1 安徽农业大学林学与园林学院 重大林业有害生物绿色防控安徽省重点实验室， 安徽 合肥 230036
  • 2 涡阳县林业发展中心， 安徽 亳州 233600
Adenylosuccinate synthase negatively controls Metarhizium robertsii pathogenicity
Lechen WANG1, Shiyue GUO1, Yutong ZHAO1, Yuanyuan DONG1, Wenjing WU1, Yan REN1, Fuming GUO2, Yulong WANG1, *
Affiliations
  • 1 Anhui Province Key Laboratory of Green Control for Major Forestry Pests, School of Forestry and Landscape Architecture, Anhui Agricultural University, Hefei 230036, Anhui, China
  • 2 Forestry Development Center of Woyang County, Bozhou 233600, Anhui, China
出版时间: 2026-04-22 doi: 10.13346/j.mycosystema.250251
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腺苷酸基琥珀酸合成酶(adenylosuccinate synthetase, ADSS)在细胞能量代谢与信号传导等过程中具有重要作用，但目前在昆虫病原真菌中的研究未见报道。本研究以罗伯茨绿僵菌Metarhizium robertsii中ADSS家族成员MrADSS-1为研究对象，利用亚细胞定位分析、基因敲除、回补和过表达等方法，系统探究了其在绿僵菌生长、抗逆和致病过程中的作用。结果表明，MrADSS-1分布在罗伯茨绿僵菌细胞的液泡中。敲除MrADSS-1导致菌株在麦芽糖培养基中生长速率显著下降、抗紫外能力减弱，但耐热能力增强。致病力测定结果表明，MrADSS-1敲除显著提高了绿僵菌附着胞形成率和蝉翅穿透能力，增强了对大蜡螟的毒力，而过表达MrADSS-1菌株则致病力下降。本研究结果表明，MrADSS-1负介导罗伯茨绿僵菌的耐热能力和致病力。

腺苷酸基琥珀合成酶  /  罗伯茨绿僵菌  /  亚细胞定位  /  逆境胁迫  /  致病力

Adenylosuccinate synthetase (ADSS) plays an important role in cellular energy metabolism and signal transduction. However, ADSS had not been reported in entomopathogenic fungi. In this study, function of ADSS family protein MrADSS-1 to the growth, stress resistance and pathogenicity in the entomopathogenic fungus Metarhizium robertsii was characterized by investigating the protein subcellular localization and gene disruption, complementation and over-expression. Results showed that MrADSS-1 is exclusively localized within the vacuole. Disruption of the MrADSS-1 resulted in marked reduction of radial growth of the fungus on maltose medium and a significant decrease in UV-B tolerance, but unexpectedly enhanced thermotolerance. Bioassays revealed that loss of MrADSS-1 led to a pronounced increase in appressorium formation and penetration efficiency through cicada wings, resulting in elevated pathogenicity toward Galleria mellonella larvae. Conversely, over-expression of MrADSS-1 attenuated fungal virulence. These findings demonstrated that MrADSS-1 functions as a repressor of both thermotolerance and virulence in M. robertsii.

adenylosuccinate synthase  /  Metarhizium robertsii  /  subcellular localization  /  abiotic stress  /  pathogenicity
王乐陈, 郭世悦, 赵雨桐, 董媛媛, 吴文婧, 任言, 郭复明, 王玉龙. 腺苷酸基琥珀酸合成酶负介导罗伯茨绿僵菌致病力. 菌物学报, 2026 , 45 (4) : 250251 - . DOI: 10.13346/j.mycosystema.250251
Lechen WANG, Shiyue GUO, Yutong ZHAO, Yuanyuan DONG, Wenjing WU, Yan REN, Fuming GUO, Yulong WANG. Adenylosuccinate synthase negatively controls Metarhizium robertsii pathogenicity[J]. Mycosystema, 2026 , 45 (4) : 250251 - . DOI: 10.13346/j.mycosystema.250251
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昆虫病原真菌已经被开发为真菌杀虫剂广泛应用于农林害虫的生物防治(Wang & Wang 2017；Maina et al. 2018)。其中绿僵菌杀虫剂作为主要的一类，可侵染鞘翅目、鳞翅目、直翅目、半翅目、双翅目、膜翅目等30余科200多种昆虫，在国内外被广泛应用(Son et al. 2008；Vorontsova et al. 2018；农向群等2022)。绿僵菌的侵染可分为5个阶段：分生孢子识别并附着寄主体壁、孢子萌发并形成附着胞、穿透体壁进入昆虫血腔、定殖血腔内并杀死昆虫和穿出昆虫体壁生长并产生分生孢子(Gao et al. 2011；Wang & Wang 2017)。复杂的侵染过程有效避免了害虫抗药性的产生，但是同样也导致绿僵菌杀虫剂存在杀虫周期长、效率较低以及防治效果不稳定等问题，严重限制了其大规模应用(王玉龙等 2022)。深入探究绿僵菌与昆虫的互作机制，鉴定新的毒力因子有助于提升绿僵菌的应用效果。
5ʹ-磷酸腺苷(adenosine 5ʹ-monophosphate, AMP)在能量代谢、信号分子传导和核酸合成等生命过程中发挥重要作用(Sharma et al. 2023)。腺苷酸琥珀酸合成酶(adenylosuccinate synthetase, ADSS)广泛存在于细菌、真菌、植物和动物等真核生物中，参与催化AMP合成途径中的首个不可逆步骤，以肌苷-5ʹ-单磷酸(IMP)为底物，合成腺苷酸琥珀酸(Iancu et al. 2002；Zhu et al. 2023；Kano et al. 2024)。哺乳动物腺苷酸琥珀酸合成酶在骨骼肌中高度表达，并且与常染色体隐性遗传的远端肌病有关(Sun et al. 2005；Park et al. 2017)。在人体中，编码肌肉特异性腺苷酸琥珀酸合成酶样1的ADSSL1基因突变后导致一种极罕见的肌病，表现出下肢远端无力(Baskar et al. 2024)。在玉米Zea mays中，ADSS的缺失导致AMP含量显著下降，引起碳水化合物和氨基酸代谢的紊乱，最终导致胚乳发育受损，种子淀粉和蛋白质含量降低(Zhu et al. 2023)。幽门螺杆菌Helicobacter pylori ADSS缺陷株仅在添加腺嘌呤或腺苷的培养基中才能生长，在常规营养培养基中生长严重受限(Liechti & Goldberg 2012；Wojtys et al. 2024)。
ADSS在真菌生长、代谢和致病过程中发挥重要作用。在酿酒酵母Saccharomyces cerevisiae (Desm.) Meyen中，ADSS催化肌苷酸与天冬氨酸转化为腺苷酸琥珀酸。ADSS突变体表现生长缓慢、孢子萌发率低、肌苷和次黄嘌呤大量积累、细胞分裂停滞和DNA复制效率变低等症状，表明ADSS在酵母代谢与基因组稳定性调控中发挥多重作用(Tarakhovskaya et al. 2025)。稻瘟病菌Magnaporthe oryzae中ADSS在分生孢子产生和致病性等方面发挥重要作用，缺失突变体表现为腺嘌呤营养缺陷型，并且完全丧失产孢能力和致病力(Zhang et al. 2022)。在新生隐球菌Cryptoccus neoformans中，ADSS敲除后导致腺嘌呤营养缺陷型和毒力完全丧失(Blundell et al. 2016)。然而，ADSS在昆虫病原真菌的生长和致病等过程中作用尚不清楚。
为明确ADSS昆虫病原真菌与生长发育及致病中的关系，本文研究了罗伯茨绿僵菌Metarhizium robertsii J.F. Bisch. et al. MrADSS-1 (adenylosuccinate synthetase 1, ADSS-1)的亚细胞定位，并通过构建基因敲除和过表达菌株分析MrADSS-1在罗伯茨绿僵菌的生长、抗逆境胁迫及致病等过程中的作用，以期为基于基因编辑提高绿僵菌杀虫能力提供参考。
1 材料与方法
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1.1 材料
1.1.1 供试菌株和虫源
罗伯茨绿僵菌ARSEF23，保存于安徽省重大林业有害生物绿色防控重点实验室菌种库。大肠杆菌TOP10和根癌农杆菌AGL-1均购自唯地生物公司。大蜡螟5龄幼虫购自瑞清钓饵有限公司。
1.1.2 培养基
PDA (potato dextrose agar)培养基：葡萄糖20 g、马铃薯200 g、琼脂20 g、蒸馏水1 000 mL；SDAY (Sabouraud dextrose agar with yeast extract)培养基：葡萄糖40 g、蛋白胨10 g、酵母浸粉10 g、琼脂粉15 g、蒸馏水1 000 mL；1/4 SDAY培养基：葡萄糖10 g、蛋白胨2.5 g、酵母浸粉2.5 g、琼脂粉15 g、蒸馏水1 000 mL；CZA (Czapek yeast autolysate agar)培养基：磷酸氢二钾1.0 g、硝酸钠3.0 g、氯化钾0.5 g、硫酸镁0.5 g、硫酸亚铁0.01 g、蔗糖30.0 g、琼脂粉15 g、蒸馏水1 000 mL；MM液体培养基：硝酸钠6 g、氯化钾0.5 g、硫酸镁0.5 g、磷酸氢二钾0.25 g、丙三醇10 mL、蒸馏水1 000 mL。
1.1.3 试剂
胶回收纯化试剂盒、质粒提取试剂盒购自OMEGA公司；TRIzol试剂、Abclonal重组酶、Taq DNA聚合酶、10× PCR Buffer、dNTPs、DNA Marker和限制性核酸内切酶均购自大连宝生物公司(大连)。
1.2 突变菌株构建
利用农杆菌介导的遗传转化方法进行目的基因敲除、回补、过表达等菌株的构建(Wang et al. 2021)。
MrADSS-1敲除菌株构建：PCR扩增MrADSS-1基因上游(895 bp)和下游(916 bp)的同源臂(表1)。利用一步克隆法，将上、下游片段分别连接到草铵膦抗性的双元载体pDHt-SK-bar上，获得敲除质粒pDHt-SK-bar-MrADSS-1。将构建好的敲除质粒转化进入根癌农杆菌AGL-1中，通过农杆菌介导的遗传转化方法将敲除质粒转化进入绿僵菌中获得敲除菌株。
MrADSS-1回补菌株构建：PCR扩增获得包括MrADSS-1基因上游(1 408 bp)，全长编码序列(231 bp)的片段，连接到苯菌膦抗性的双元载体pDHt-SK-ben以获得回补质粒Com-pben- MrADSS-1 (表1)。将构建好的质粒转入根癌农杆菌AGL-1，基于上述同源转化方法将回补质粒转化进入基因敲除突变体获得回补菌株。
MrADSS-1过表达菌株构建：PCR扩增获得MrADSS-1全长编码序列(231 bp)，连接到含构巢曲霉Aspergillus nidulans甘油醛-3-磷酸脱氢酶启动子的双元载体pDHt-gpdA-bar上，获得过表达质粒pDHt-gpdA-bar-MrADSS-1 (表1)。将构建好的质粒通过根癌农杆菌AGL-1介导的转化方法转入绿僵菌野生菌株获得过表达菌株。
MrADSS-1荧光标记菌株构建：PCR扩增获得MrADSS-1全长编码序列(231 bp)的片段，连接到含绿色荧光蛋白(GFP)的双元载体pDHt-GFP-ben上，获得荧光标记质粒pDHt-GFP-ben- MrADSS-1 (表1)。将构建好的质粒通过根癌农杆菌AGL-1介导的转化方法转入基因敲除突变体获得荧光标记菌株。
提取转化菌株的DNA和RNA，利用PCR或者反转录PCR进行验证。
1.3 亚细胞定位
将MrADSS-1荧光标记菌株培养于PDA培养基，收集4 d的孢子、菌丝。使用液泡染色剂7-氨基-4-氯甲基香豆素对孢子和菌丝进行染色，终浓度为10 μmol/L。
1.4 生物学性状测定
罗伯茨绿僵菌孢悬液制备：将PDA培养基上培养14 d的罗伯茨绿僵菌分生孢子收集至1 mL 0.05% Tween-80水中，涡旋振荡2-5 min，使孢子完全分散。利用脱脂棉过滤除去菌丝，获得分生孢子悬浮液，利用血球计数板计数孢子浓度。
营养生长测定：吸取1 μL浓度为1 × 107 conidia/mL的孢子悬浮液分别点接至PDA、SDAY、1/4 SDAY培养基中央，25 ℃恒温培养箱内培养14 d，使用十字交叉法测量菌落直径。
产孢量测定：吸取30 μL浓度为5 × 106 conidia/mL的孢子悬浮液均匀涂布于60 mm的PDA培养基上，25 ℃恒温培养箱，刮取培养7 d和14 d平板上的所有孢子于30 mL的0.05% Tween-80中，涡旋15 min后，显微镜下使用血球计数板计数孢子浓度。
不同碳、氮源培养基上生长测定：吸取1 μL浓度为1 × 107 conidia/mL的孢悬液点接至CZA及改良型CZA培养基中央，25 ℃恒温培养箱内培养14 d，使用十字交叉法测量菌落直径。
化学试剂耐受力测定：吸取1 μL浓度为1×107 conidia/mL的孢悬液点接至添加化学试剂的PDA培养基(2 mg/mL congo red或10 mmol/L H2O2或0.5 mol/L NaCl)中央，25 ℃恒温培养箱内培养14 d，使用十字交叉法测量菌落直径。
相对生长抑制率=(WT菌株在PDA培养基上生长直径-敲除菌株在添加化学试剂的PDA培养基上生长直径)/WT菌株在PDA培养基上生长直径×100%。
热耐受力的测定：将浓度为5 × 106 conidia/mL的孢子悬浮液于42 ℃水浴1 h，对照为室温放置1 h的孢子悬浮液，吸取10 μL的孢子悬浮液点接至PDA培养基上，25 ℃恒温培养16 h和24 h，显微镜下观察萌发情况并计数。相对萌发率=(处理组萌发率/对照组萌发率)×100%。
紫外耐受力的测定：吸取10 μL浓度为5 × 106 conidia/mL的孢子悬浮液点接至PDA培养基上，吹干后放置于紫外交联仪中90 J/cm2照射10 s，25 ℃恒温培养16 h和24 h，显微镜下观察培养后菌株的孢子萌发情况并计数。相对萌发率=(处理组萌发率/对照组萌发率)×100%。
蝉翅穿透能力测定：吸取1 μL浓度为1 × 107 conidia/mL的孢子悬浮液点接至贴有蝉翅的PDA培养基上，25 ℃培养3 d后揭去蝉翅，再生长7 d后用十字交叉法测量直径。
附着胞形成能力测定：用MM液体培养基重悬配制成浓度为1×106 conidia/mL的孢子悬浮液，吸取1 mL到35 mm的疏水皿中，25 ℃恒温培养箱内培养24 h，显微镜下观察并计算附着胞形成率。
以上试验均设置3次生物学重复。
1.5 昆虫生物测定
体内注射法：取10 μL孢子悬浮液(1 × 105 conidia/mL)注射进大蜡螟第二腹足中，注射无菌水作为对照。将注射后的幼虫放置于铺好无菌滤纸的90 mm玻璃皿内，25 ℃恒温培养箱内培养，每隔12 h统计大蜡螟死亡数据，直至所有试虫死亡。体壁侵染法：将大蜡螟置于30 mL孢子悬浮液(1 × 107 conidia/mL)的离心管中，浸渍60 s后取出，放于90 mm玻璃皿内，加入棉球保湿，25 ℃恒温培养箱内培养，每隔12 h统计大蜡螟死亡数据，直至所有试虫死亡。每个处理30只幼虫，试验重复3次。
1.6 MrADSS-1基因过表达菌株荧光定量PCR检测
野生型菌株和MrADSS-1基因过表达菌株在PDA培养基上培养14 d，收集真菌。采用TRIzol试剂提取总RNA，利用浓度1%凝胶电泳检测RNA的完整性，使用分光光度计及生物分析仪系统检测RNA的纯度及浓度。荧光定量PCR反应体系：12.5 μL 2 × SYBR® Ex Premix TaqTM Ⅱ、正反向引物各1 μL、DNA模板2 μL、双蒸水8.5 μL。扩增程序：95 ℃预变性10 s；95 ℃变性5 s，60 ℃退火30 s，循环40次；95 ℃变性15 s，60 ℃退火1 min、95 ℃变性15 s。以甘油酸-3-磷酸脱氢酶(glyceraldehyde-3-phosphate dehydrogenase, GPDH)为内参基因，采用2-ΔΔCt 法分析不同基因的相对表达量。每组试验重复3次。
1.7 数据分析
使用GraphPad Prism 8.3软件对数据进行统计分析，并生成图表；使用SPSS 26.0软件对数据进行统计学显著性分析，具体方法为：首先进行单因素方差分析(one-way ANOVA)，当ANOVA结果存在显著差异时，进一步采用Tukey’s honestly significant difference (HSD)检验进行组间多重比较。
2 结果与分析
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2.1 MrADSS-1的亚细胞定位
7-氨基-4-氯甲基香豆素染色剂与液泡内的硫醇反应，呈现蓝色，实现对液泡的特异性染色。亚细胞定位显示，绿色荧光蛋白标记MrADSS-1蛋白的荧光信号与液泡特异性染料CMAC信号重叠(图1)。
2.2 MrADSS-1的敲除影响罗伯茨绿僵菌的营养生长
分别在PDA、SDAY、1/4 SDAY这3种培养基上进行营养生长测定，敲除菌株ΔMrADSS-1的菌落形态和生长直径与野生型菌株WT和回补菌株cpΔMrADSS-1无显著性差异(图2A，2B)。测定PDA培养基上生长14 d的菌株孢子数量，ΔMrADSS-1与WT和cpΔMrADSS-1的产孢量无显著性差异(P>0.05，图2C)。
为明确MrADSS-1敲除对罗伯茨绿僵菌在不同碳、氮源培养基生长性状的影响，在CZA和替换碳、氮源的不同改良型CZA培养基上测定不同菌株菌落生长直径。当培养基中的碳源为麦芽糖时，与WT [(3.59±0.04) cm]和cpΔMrADSS-1 [(3.55±0.12) cm]相比，ΔMrADSS-1 [(3.41±0.04) cm]的菌落生长直径显著减少(P<0.05)，而在CZA和其他改良型CZA培养基上，ΔMrADSS-1与WT和cpΔMrADSS-1生长的菌落形态和生长直径无显著性差异(P>0.05) (图2D，2E)。由此表明，MrADSS-1基因缺失影响罗伯茨绿僵菌利用麦芽糖的能力。
2.3 敲除MrADSS-1影响罗伯茨绿僵菌对热和紫外的耐受力
为明确MrADSS-1的敲除对罗伯茨绿僵菌胁迫环境耐受能力的影响，在PDA培养基中分别添加NaCl (高渗胁迫)、H2O2 (氧化胁迫)和congo red (细胞壁胁迫)，检测不同菌株的菌落生长特征。与WT和cpΔMrADSS-1相比，ΔMrADSS-1的生长直径无显著性差异(P>0.05，图3A，3B)；在热激胁迫实验中，在热处理后16 h或者24 h，ΔMrADSS-1分生孢子相对萌发率都显著高于WT和cpΔMrADSS-1 (P<0.01，图3C)；而在紫外辐射胁迫后16 h或者24 h时，ΔMrADSS-1孢子相对萌发率都显著低于WT和cpΔMrADSS-1 (P<0.05，图3D)，尤其在24 h时，MrADSS-1的敲除使得紫外辐射胁迫后罗伯茨绿僵菌孢子相对萌发率下降29.8%。
2.4 敲除MrADSS-1后显著提高罗伯茨绿僵菌的穿透能力
蝉翅穿透实验证明，WT、ΔMrADSS-1和cpΔMrADSS-1菌株均能成功穿过蝉翅，并在去除蝉翅后的PDA培养基上形成了菌落(图4A)，且ΔMrADSS-1 [(3.70±0.05) cm]在PDA培养基上生长的菌落直径显著大于WT [(3.59±0.04) cm]和cpΔMrADSS-1 [(3.54±0.07) cm] (P<0.01，图4B)。在疏水皿诱导24 h观察附着胞形成情况，结果显示，WT、ΔMrADSS-1和cpΔMrADSS-1附着胞形成率分别为(66.40±1.85)%、(78.05±0.92)%和(65.07±2.77)%。与WT相比，ΔMrADSS-1的附着胞形成率提高11.64% (图4C)。以上结果表明，MrADSS-1敲除提高罗伯茨绿僵菌的蝉翅穿透和附着胞形成的能力。
2.5 MrADSS-1负介导罗伯茨绿僵菌的毒力
昆虫生物测定结果表明，敲除MrADSS-1引起菌株毒力显著提高。体内注射生物测定显示，WT、ΔMrADSS-1和cpΔMrADSS-1侵染大蜡螟的半致死时间(LT50)分别为(3.26±0.05)、(3.42±0.06)和(3.41±0.04) d，三者之间无显著性差异，表明敲除MrADSS-1对罗伯茨绿僵菌的大蜡螟血腔侵染能力影响不显著(图5A)。而体表浸渍生物测定显示，与WT相比[(5.28±0.06) d]，感染ΔMrADSS-1 [(4.83±0.18) d]菌株的大蜡螟的LT50显著降低约0.5 d，表明敲除MrADSS-1显著提高罗伯茨绿僵菌体表侵染的能力(P<0.01，图5B)。
为进一步明确MrADSS-1对罗伯茨绿僵菌致病力的负调控作用，构建了MrADSS-1过表达菌株(MrADSS-1OE-1和MrADSS-1OE-2)，并对其致病力进行了测定。荧光定量PCR检测证实，相较于野生型，MrADSS-1OE-1和MrADSS-1OE-2中MrADSS-1表达量提高2.9-3.1倍(图5C)。生物测定显示，无论体内注射还是体表浸渍，过表达MrADSS-1显著降低罗伯茨绿僵菌的致病力(图5D，5E)。其中，与WT相比，体内注射MrADSS-1OE-1和MrADSS-1OE-2侵染的大蜡螟LT50分别延长0.4 d和0.51 d (图5D)，体表浸渍MrADSS-1OE-1和MrADSS-1OE-2侵染的大蜡螟LT50分别延长1.23 d和1.26 d (图5E)。结果表明，MrADSS-1参与罗伯茨绿僵菌的毒力调控。
3 讨论
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AMP广泛存在于真核与原核生物中，对于维持生命体的细胞活动和生长代谢发挥重要作用(Honzatko & Fromm 1999)。作为AMP合成的限速酶，ADSS通过调控AMP/ADP/ATP的代谢平衡，在细胞能量稳态维持中发挥核心作用(Zhu et al. 2023)。ADSS在动物、植物和微生物等不同物种中的功能具有一定的保守性(Zhu et al. 2023)。本研究通过对昆虫病原真菌模式生物—罗伯茨绿僵菌中ADSS进行研究，表明ADSS在绿僵菌的抗紫外、抗热激和致病等过程中发挥重要作用。
尽管ADSS广泛存在，但是在不同物种中的结构存在显著差异，可分为不同家族类群，且不同类群间功能同样存在差异(Mišković et al. 2024)。研究表明，ADSS的开关环区域从开放构象转变为闭合构象有助于GTP在活性位点的紧密堆积，促使ADSS更好发挥AMP合成代谢功能(Iancu et al. 2002)。与大肠杆菌Escherichia coli和拟南芥Arabidopsis thaliana等物种ADSS结构相比，杜氏利什曼原虫Leishmania donovani ADSS的开关环功能区域具有更多的氨基酸位点变异性，致使ADSS与ADP结合后，其开关环构象仍然部分开放，表明其在腺嘌呤的紧密堆积方面存在不足(Mochi et al. 2024)。因此，杜氏利什曼原虫ADSS在功能上表现出差异性，负责嘌呤补救途径中的腺苷琥珀酸合成，在寄生虫的生长、代谢和感染能力方面起关键作用(Boitz et al. 2013)。而在玉米中，ADSS分布于细胞质体中，对种子发育和养分积累至关重要，其缺失会导致AMP含量降低，碳水化合物和氨基酸代谢紊乱(Zhu et al. 2023)。在酿酒酵母中，ADSS突变体表现出生长缓慢、孢子萌发不良、肌苷和次黄嘌呤大量积累(Tarakhovskaya et al. 2025)。在本研究中，敲除MrADSS-1后对于罗伯茨绿僵菌的营养生长、产孢并没有显著影响，但是致病能力发生显著变化。进一步对不同物种ADSS的亚细胞定位分析发现，玉米中的ADSS分布于细胞质体中；在盘基网柄菌Dictyostelium discoideum中，ADSS定位于细胞质中(Wiesmuller et al. 1991)；细脚拟青霉Paecilomyces tenuipes中ADSS分布于细胞质中，在腺苷产生过程中可能发挥重要作用(杜林娜等2018)；而本研究中，MrADSS-1荧光信号与液泡特异性染料CMAC信号重叠，表明不同物种间ADSS的结构、亚细胞定位和功能等方面具有显著差异。
在稻瘟病菌中，ADSS参与腺苷酸从头合成途径，ADSS的缺失导致稻瘟病菌无法产生分生孢子、对刚果红和氧化剂等化合物的敏感性增加、子囊壳形成数量减少、致病性显著降低(Zhang et al. 2022)。在新生隐球菌中，降低ADSS的表达导致真菌表现出腺嘌呤营养缺陷，且致病能力完全丧失(Blundell et al. 2016)。本研究中，敲除MrADSS-的罗伯茨绿僵菌产孢能力、对刚果红和氧化剂等化合物的敏感性等性状与亲本菌株无明显差异，但穿透昆虫体壁能力和致病力显著升高，表明侵染寄主的差异致使ADSS在不同病原真菌中的功能发生改变，以更好适应进化的需要。
研究表明，罗伯茨绿僵菌存在单胺氧化酶(MAO)，能够催化色胺分解为无毒代谢产物，致使色胺在宿主体内的积累速率下降，从而降低色胺对蝗虫的毒性。敲除MAO后绿僵菌的致病能力显著提高(Tong et al. 2020)。ADSS参与生物AMP的合成，而AMP在病原真菌的致病过程中发挥重要作用(Sun et al. 2024)。本研究中，敲除MrADSS-1后罗伯茨绿僵菌致病力显著升高，过表达MrADSS-1能够显著降低致病力，明确了MrADSS-1负介导绿僵菌的致病力。但是，MrADSS-1如何介导AMP的合成参与绿僵菌致病的作用机制，尚需要进一步的研究。
基因编辑技术已广泛应用于农业、医学、生产及科学研究等领域，其在“精准度和高效性”等方面的优势为提高昆虫病原真菌致病能力开辟了新路径(霍贯中等2025)。当前，基于CRISPR/Cas9等基因编辑技术可实现对绿僵菌和白僵菌等昆虫病原真菌的基因靶向改造，提升真菌的耐高温、耐紫外辐射、黏附和致病等能力(Mascarin et al. 2024)。本研究中，敲除MrADSS-1后罗伯茨绿僵菌致病力显著升高，证实MrADSS-1负调控绿僵菌致病力，为将来基于基因编辑技术改造绿僵菌致病能力提供了靶标基因。
基金
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  • 合肥市自然科学基金(202312)
  • 安徽省大学生创新创业训练计划(S202410364133)
  • 安徽省大学生创新创业训练计划(X202410364462)
  • 安徽省大学生创新创业训练计划(X202410364493)
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doi: 10.13346/j.mycosystema.250251
  • 接收时间：2025-08-23
  • 首发时间：2026-04-30
  • 出版时间：2026-04-22
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  • 收稿日期：2025-08-23
  • 录用日期：2025-09-18
基金
Hefei Municipal Natural Science Foundation(202312)
合肥市自然科学基金(202312)
Anhui College Student Innovation and Entrepreneurship Training Program(S202410364133)
安徽省大学生创新创业训练计划(S202410364133)
Anhui College Student Innovation and Entrepreneurship Training Program(X202410364462)
安徽省大学生创新创业训练计划(X202410364462)
Anhui College Student Innovation and Entrepreneurship Training Program(X202410364493)
安徽省大学生创新创业训练计划(X202410364493)
作者信息
    1 安徽农业大学林学与园林学院 重大林业有害生物绿色防控安徽省重点实验室， 安徽 合肥 230036
    2 涡阳县林业发展中心， 安徽 亳州 233600

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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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