栽培性状和分子标记在中国真姬菇遗传多样研究中的应用
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摘要
真姬菇分深色和白色品种，后者是前者的白化变种，称白玉菇。真姬菇口感独特，营养丰富，有良好的药用或保健功效，是颇受青睐且能工厂化大规模生产的新型栽培食用菌品种之一。迄今国内外有关真姬菇品种栽培特性比较和遗传多样性相结合的研究不多。本研究从国内主要的食用菌研究机构、生产企业、部分省级农科院和中国农业微生物菌种保藏中心等收集了32真姬菇菌株，并对其进行工厂化栽培特性比较和遗传多样性结合的研究，获得如下结果：
用核糖体间隔区间序列（ITS）方法鉴定收集菌株，结果显示：一株菌株不是真姬菇，另两株为分子特征一致的同一菌株，其余为具不同分子遗传特征的不同菌株。
在真姬菇生产基地标准工厂化栽培条件下对收集的真姬菇进行工厂化栽培实验，其中3株因故不生长，其中22株在34-50天内菌丝长满栽培瓶，7株需超过51天长满；5株没有收获鲜菇，27株收获鲜菇，其中乳白色及白色的品种10株，褐色、深灰色、浅灰色等深色品种17株。鲜菇菌盖直径多为15-25mm；菌柄长度多为25-50mm；白色菌株鲜菇产量为52.4-188.1g/瓶，平均112.37g/瓶，深色菌株产量为0-227g/瓶，平均93.51g/瓶。真姬菇的栽培性状明显呈现出多样性。用SPSS20.0软件包分析7个栽培表型因素。主成份分析表明影响真姬菇产量的因素有每瓶平均鲜菇重、菌盖直径和菌柄长度等；影响其品质的因素有菌盖直径、菌柄长度等。聚类分析显示鲜重、菌盖直径等性状较差的菌株聚于一簇，性状较好的菌株聚在另一簇。
以18条ISSR引物扩增真姬菇菌株的重复序列，共获199条扩增条带，平均每条引物产生11.10条；特异性条带173条，平均每条引物产生9.61条特异性条带，特异性比例为87.46%。55对SRAP前端和后端引物组合PCR扩增真姬菇内含子与外显子间序列，产生533条扩增条带，平均每对引物组合产生9.63条；特异性条带453条，平均每对引物组合产生8.24条，多态性比例为84.67%。基于ISSR（SRAP）扩增数据分析显示32株菌可聚成两大簇，一簇包含绝大部份菌种保藏中心的菌株，另一簇是涵盖所有来自于食用菌研究所、生产企业直接用于生产的商业菌株和实验室或菌种保藏中心的菌株；每簇细分若干小分支，表明菌株间存在丰富的遗传多样性；ISSR和SRAP多态性信息含量分别是0.39-0.50和0.37-0.50，平均为0.47和0.48，菌株间存在中等程度遗传多样性。栽培表型性状同ISSR、SRAP的分子标记数据相结合综合分析显示：菌株间存在较为丰富的遗传多样性。
以GenBank中获取真姬菇相关蛋白基因7条序列为靶序列，设计TRAP固定引物14条；初步筛选出6条效果好的固定引物与随机引物（SRAP前端和后端引物）配对复筛，共获28组理想的TRAP引物组合。以ISSR、SRAP与栽培表型结果为参照，筛选20株菌株为TRAP模板进行TRAP-PCR扩增，共扩增条带287条，平均每引物组合产生扩增片段10.27条，其中多态性条带202条，平均每对引物组合产生7.21条，多态性比例为72.12%。基于TRAP数据分析：20株供试菌株聚成两簇，一簇2株菌，另一簇18株菌株，菌株间存在较为丰富的遗传多样性；菌株的色泽、产量及来源与TRAP聚类结果无直接关联。
回收试验菌株共有而阴性对照没有的TRAP扩增条带，克隆至大肠杆菌DH5α，PCR检测与回收片段大小相符的片段测序，测序后用DNAstar软件包序列拼接，共获36条真姬菇序列，与GenBank在线对库BLAST，结果显示6条序列没有相似性序列，5条为真姬菇热激蛋白HSP70部分序列。在Softberry网站在线进行内含子和外显子分析显示：18条序列存在1个或多个可阅读框（ORF），可以翻译成功能未知的蛋白质，18条序列不存在ORF。
以6条无相似性序列为靶序列设计6对真姬菇特异性引物；10种常见食用菌（药用菌）和9株真姬菇为模板，验证6对真姬菇特异性引物，结果显示：所有真姬菇菌株均能扩增出期望片段大小相符的特异性条带、对照菌株不能扩增的特异性引物1对。特异性扩增产物测序并用DNAman软件包分析，获得一条120bp的共有序列，该序列在GenBank对库BLAST中无任何相似性序列，表明该序列为真姬菇特异性标记序列，该对引物为真姬菇特异性标记引物。
栽培表型、ISSR、SRAP及TRAP研究揭示真姬菇菌株间存在丰富的遗传多样性，进一步加强了真姬菇的基础遗传的研究，为培育真姬菇新品种选育打下了基础。实验结果表明ISSR、SRAP和TRAP三种分子分析方法，能从不同角度研究食用菌的遗传多样性，评价其种质资源，可为食用菌遗传育种或菌株改良研究提供重要的遗传背景信息。
Hypsizygus marmoreus can be divided into two type according to the color of fruit-body:the brown and the white. The white H. marmoreus, the mutatied strain of the brown one, isnamed White Jade Mushroom. Recently, H. marmoreus has become one of the most popularedible and medicinal mushrooms in East Asia, for its pleasant flavor, and nutritional benefits.H. marmorues is an edible mushroom of commercial importance with medicinal propertieswhich can be produce in large-scale factory production.32strains of H. marmoreus werecollected from the following institutions:9strains from the Agricultural Culture Collection ofChina (ACCC), Beijing,7strains from Provincial Institutes of Agricultural Science (2fromFujian,2from Hunan,2from Sichuuan,1from Zhejiang);1strain from Huazhongagriculture university;4strains from Institutes of Edible Fungi and Mushroom (2fromGaoyou,1fromTianda,1from Mianyang);1strain from Changbaishan, Jinlin; and5strainsfrom commercial mushroom enterprises of mushroom (three from Shanghai,1fromShandong,1from Guangdong). The cultivation and genetic diversity were studied withcollected strains of H. marmoreus as material of research.
The strains of H. marmoreus were identified for reconfirmation with the internaltranscribed spacer of fungus. The result of identification showed that the strain ofACCC50515was Coprinus comatus, strains of GDGM25484and GDGM26168were thesame strain.
To cultivate each strain, the mycelia from a liquid culture were inoculated onto solidsubstrate (a commercial formulation used at the Starway Bio-Technology Co., LTD facility)in a wide-mouth polypropylene bottle, and grown for approximately80d at20°C. Fruitingwas induced by reducing the temperature to15.6°C in an incubation chamber with1,700—3,000ppm CO2and96%relative humidity. Each of the strains had16replications.
Three strains of H. marmoreus did not survive because of pollution or other reasonsduring mycelial growth period. The remaining strains grew on solid substrate, produced whitemycelia, and fruit-bodies. The time for hyphae to cover the fully substrate (HCFS) was from34to50days in common, HCFS of some strain was longer more than50days, after thedecreasing temperature to induce fruiting,27strains produced fruiting bodies. The H. marmoreus strains could be divided into several types according to the fruiting bodymorphology (color, shape, uniformity). The color of the fruiting bodies varied among thestrains: dark grey, dark stipe, grey brown with water spots, grey, white, or ivory white. Thecommon diameter of pileus ranged from15to25mm, while the common length of stiperanged from25to50mm. The fresh weight of white strains ranged52.4to188.1g per bottle,the mean weight was112.37g per bottle. The fresh weight of dark strains ranged from0to227g per bottle, the average weight was93.51g per bottle. The factors of H. marmoreus'cultivation phenotype were analyzed by statistical package for the social sciences (SPSS). Theresult of principal components analysis (PCA) showed that the yields of H. marmoreus wasaffected by fresh-weight of mushroom per bottle, the diameter of pileus and the height of stipe;the quality was mainly affected by the diameter of pileus and the height of stipe. The result ofcluster analysis showed that the strains with lower fresh-weight, the diameter of pileus and theheight of stipe were clustered into one group, and the strain with the higher fresh-weight, thediameter of pileus and height of stipe were clustered into the other group.
The genomic DNA extracted from H. marmoreus was amplified with18inter-simplesequence repeat (ISSR) primers, which generated199bands. The average number ofamplified bands per primer was11.10. There were173polymorphism bands, with a mean of9.61bands per primer. The mean percentage of polymorphism was87.46. The55primercombinations generated a total of533scorable bands, with an average of9.69bands perprimer combination of sequence-related amplified polymorphism (SRAP). The polymorphicbands were453. The percentage of polymorphic bands ranged between50.0%for Me4-Em2combination and100%for primers of Me1-EM4, Me1-EM2, and so on, with an average of84.67%. The polymorphism information content (PIC) value for ISSRs ranged from0.39to0.50(mean PIC value per ISSR was0.48). The PIC value for SRAPs ranged from0.37to0.50,(average PIC value per primer-combination was0.47). The strains of H. marmoreus had amedium level of polymorphism based on the data of ISSR and SRAP. There were plentifulpolymorphism among the H. marmoreus based on the conbination of cultivation and data ofmolecular makers analysis. The combination of molecular markers and cultivated traits wereone of effective methods in breeding and varietal improvement research for H. marmoreus.
Some primers of target region amplified polymorphism were designed by the software of primer3(on line) based on sequence of H. marmoreus from GenBank. After screening,6fixed primers,20anchor primers, and28primer combinations, which could produce clearbands with good polymorphisms and reproducibility, were selected. The28primercombinations generated287scorable bands, including202polymorphic bands. The totalnumber of bands amplified by a primer-combination ranged from4to17with an average of10.27per primer combination. The proportion of polymorphic bands ranged from33.33%(JN00L1-ME11) to100%(JN00R1-ME6) with a mean of72.12%. The20strains of H.marmoreus were clustered into2groups, which one had2strain based on the data of TRAP.The cluster result of TRAP revealed that the cluster of strains were no association with thecolor, yield and stored type of strains.
Recycling the bands that were produced in all strains of H. marmoreus and not incontrols, then they were cloned into Ecoli DH5α by vector pMD1-T. The clone productionswere sequenced by Beijing Genomics Institute (BGI) after PCR amplification checked usinguniversal primers (GV-M,5'-GAG CGG ATA ACA ATT TCA CAC AGG-3′; andM13-47,5′-CGC CAG GGT TTT CCC AGT CAC GAC-3′). There were36sequences of H.marmoreus after assembling sequences with the software of DNAstar package. There were6specific sequences which had no significant similarity sequences found in GenBank data, and5sequences that were the part of heat shock protein70(HSP70) of H. marmoreus by BLASTwith GenBank data online. Online analysis in Softberry site showed that18sequences hadone or more open reading frames (ORF). Six pairs of specific primer were designed withsoftware of primer6.0based on specific sequences which were no significant similaritysequences with GenBank data. The result of a serial check experiments show that one pairspecific primers of H. marmoreus was found. A specific sequence of H. marmoreus with120bp was found.
There were plentiful genetic diversity among the strains of H. marmoreus based on thestudy results of cultivated phenotype, ISSR, SRAP and TRAP. The results of this study mightstrengthen genetic research foundation and the cultivation of new vaarieties of H. marmoreus.The study revealed the molecular markers of ISSR, SRAP and TRAP were useful tools for evaluating genetic diversity and germplasm resource from different aspects, selectingpotential strains and for predicting hybrid performance in the outbreeding of mushrooms.
用核糖体间隔区间序列（ITS）方法鉴定收集菌株，结果显示：一株菌株不是真姬菇，另两株为分子特征一致的同一菌株，其余为具不同分子遗传特征的不同菌株。
在真姬菇生产基地标准工厂化栽培条件下对收集的真姬菇进行工厂化栽培实验，其中3株因故不生长，其中22株在34-50天内菌丝长满栽培瓶，7株需超过51天长满；5株没有收获鲜菇，27株收获鲜菇，其中乳白色及白色的品种10株，褐色、深灰色、浅灰色等深色品种17株。鲜菇菌盖直径多为15-25mm；菌柄长度多为25-50mm；白色菌株鲜菇产量为52.4-188.1g/瓶，平均112.37g/瓶，深色菌株产量为0-227g/瓶，平均93.51g/瓶。真姬菇的栽培性状明显呈现出多样性。用SPSS20.0软件包分析7个栽培表型因素。主成份分析表明影响真姬菇产量的因素有每瓶平均鲜菇重、菌盖直径和菌柄长度等；影响其品质的因素有菌盖直径、菌柄长度等。聚类分析显示鲜重、菌盖直径等性状较差的菌株聚于一簇，性状较好的菌株聚在另一簇。
以18条ISSR引物扩增真姬菇菌株的重复序列，共获199条扩增条带，平均每条引物产生11.10条；特异性条带173条，平均每条引物产生9.61条特异性条带，特异性比例为87.46%。55对SRAP前端和后端引物组合PCR扩增真姬菇内含子与外显子间序列，产生533条扩增条带，平均每对引物组合产生9.63条；特异性条带453条，平均每对引物组合产生8.24条，多态性比例为84.67%。基于ISSR（SRAP）扩增数据分析显示32株菌可聚成两大簇，一簇包含绝大部份菌种保藏中心的菌株，另一簇是涵盖所有来自于食用菌研究所、生产企业直接用于生产的商业菌株和实验室或菌种保藏中心的菌株；每簇细分若干小分支，表明菌株间存在丰富的遗传多样性；ISSR和SRAP多态性信息含量分别是0.39-0.50和0.37-0.50，平均为0.47和0.48，菌株间存在中等程度遗传多样性。栽培表型性状同ISSR、SRAP的分子标记数据相结合综合分析显示：菌株间存在较为丰富的遗传多样性。
以GenBank中获取真姬菇相关蛋白基因7条序列为靶序列，设计TRAP固定引物14条；初步筛选出6条效果好的固定引物与随机引物（SRAP前端和后端引物）配对复筛，共获28组理想的TRAP引物组合。以ISSR、SRAP与栽培表型结果为参照，筛选20株菌株为TRAP模板进行TRAP-PCR扩增，共扩增条带287条，平均每引物组合产生扩增片段10.27条，其中多态性条带202条，平均每对引物组合产生7.21条，多态性比例为72.12%。基于TRAP数据分析：20株供试菌株聚成两簇，一簇2株菌，另一簇18株菌株，菌株间存在较为丰富的遗传多样性；菌株的色泽、产量及来源与TRAP聚类结果无直接关联。
回收试验菌株共有而阴性对照没有的TRAP扩增条带，克隆至大肠杆菌DH5α，PCR检测与回收片段大小相符的片段测序，测序后用DNAstar软件包序列拼接，共获36条真姬菇序列，与GenBank在线对库BLAST，结果显示6条序列没有相似性序列，5条为真姬菇热激蛋白HSP70部分序列。在Softberry网站在线进行内含子和外显子分析显示：18条序列存在1个或多个可阅读框（ORF），可以翻译成功能未知的蛋白质，18条序列不存在ORF。
以6条无相似性序列为靶序列设计6对真姬菇特异性引物；10种常见食用菌（药用菌）和9株真姬菇为模板，验证6对真姬菇特异性引物，结果显示：所有真姬菇菌株均能扩增出期望片段大小相符的特异性条带、对照菌株不能扩增的特异性引物1对。特异性扩增产物测序并用DNAman软件包分析，获得一条120bp的共有序列，该序列在GenBank对库BLAST中无任何相似性序列，表明该序列为真姬菇特异性标记序列，该对引物为真姬菇特异性标记引物。
栽培表型、ISSR、SRAP及TRAP研究揭示真姬菇菌株间存在丰富的遗传多样性，进一步加强了真姬菇的基础遗传的研究，为培育真姬菇新品种选育打下了基础。实验结果表明ISSR、SRAP和TRAP三种分子分析方法，能从不同角度研究食用菌的遗传多样性，评价其种质资源，可为食用菌遗传育种或菌株改良研究提供重要的遗传背景信息。
Hypsizygus marmoreus can be divided into two type according to the color of fruit-body:the brown and the white. The white H. marmoreus, the mutatied strain of the brown one, isnamed White Jade Mushroom. Recently, H. marmoreus has become one of the most popularedible and medicinal mushrooms in East Asia, for its pleasant flavor, and nutritional benefits.H. marmorues is an edible mushroom of commercial importance with medicinal propertieswhich can be produce in large-scale factory production.32strains of H. marmoreus werecollected from the following institutions:9strains from the Agricultural Culture Collection ofChina (ACCC), Beijing,7strains from Provincial Institutes of Agricultural Science (2fromFujian,2from Hunan,2from Sichuuan,1from Zhejiang);1strain from Huazhongagriculture university;4strains from Institutes of Edible Fungi and Mushroom (2fromGaoyou,1fromTianda,1from Mianyang);1strain from Changbaishan, Jinlin; and5strainsfrom commercial mushroom enterprises of mushroom (three from Shanghai,1fromShandong,1from Guangdong). The cultivation and genetic diversity were studied withcollected strains of H. marmoreus as material of research.
The strains of H. marmoreus were identified for reconfirmation with the internaltranscribed spacer of fungus. The result of identification showed that the strain ofACCC50515was Coprinus comatus, strains of GDGM25484and GDGM26168were thesame strain.
To cultivate each strain, the mycelia from a liquid culture were inoculated onto solidsubstrate (a commercial formulation used at the Starway Bio-Technology Co., LTD facility)in a wide-mouth polypropylene bottle, and grown for approximately80d at20°C. Fruitingwas induced by reducing the temperature to15.6°C in an incubation chamber with1,700—3,000ppm CO2and96%relative humidity. Each of the strains had16replications.
Three strains of H. marmoreus did not survive because of pollution or other reasonsduring mycelial growth period. The remaining strains grew on solid substrate, produced whitemycelia, and fruit-bodies. The time for hyphae to cover the fully substrate (HCFS) was from34to50days in common, HCFS of some strain was longer more than50days, after thedecreasing temperature to induce fruiting,27strains produced fruiting bodies. The H. marmoreus strains could be divided into several types according to the fruiting bodymorphology (color, shape, uniformity). The color of the fruiting bodies varied among thestrains: dark grey, dark stipe, grey brown with water spots, grey, white, or ivory white. Thecommon diameter of pileus ranged from15to25mm, while the common length of stiperanged from25to50mm. The fresh weight of white strains ranged52.4to188.1g per bottle,the mean weight was112.37g per bottle. The fresh weight of dark strains ranged from0to227g per bottle, the average weight was93.51g per bottle. The factors of H. marmoreus'cultivation phenotype were analyzed by statistical package for the social sciences (SPSS). Theresult of principal components analysis (PCA) showed that the yields of H. marmoreus wasaffected by fresh-weight of mushroom per bottle, the diameter of pileus and the height of stipe;the quality was mainly affected by the diameter of pileus and the height of stipe. The result ofcluster analysis showed that the strains with lower fresh-weight, the diameter of pileus and theheight of stipe were clustered into one group, and the strain with the higher fresh-weight, thediameter of pileus and height of stipe were clustered into the other group.
The genomic DNA extracted from H. marmoreus was amplified with18inter-simplesequence repeat (ISSR) primers, which generated199bands. The average number ofamplified bands per primer was11.10. There were173polymorphism bands, with a mean of9.61bands per primer. The mean percentage of polymorphism was87.46. The55primercombinations generated a total of533scorable bands, with an average of9.69bands perprimer combination of sequence-related amplified polymorphism (SRAP). The polymorphicbands were453. The percentage of polymorphic bands ranged between50.0%for Me4-Em2combination and100%for primers of Me1-EM4, Me1-EM2, and so on, with an average of84.67%. The polymorphism information content (PIC) value for ISSRs ranged from0.39to0.50(mean PIC value per ISSR was0.48). The PIC value for SRAPs ranged from0.37to0.50,(average PIC value per primer-combination was0.47). The strains of H. marmoreus had amedium level of polymorphism based on the data of ISSR and SRAP. There were plentifulpolymorphism among the H. marmoreus based on the conbination of cultivation and data ofmolecular makers analysis. The combination of molecular markers and cultivated traits wereone of effective methods in breeding and varietal improvement research for H. marmoreus.
Some primers of target region amplified polymorphism were designed by the software of primer3(on line) based on sequence of H. marmoreus from GenBank. After screening,6fixed primers,20anchor primers, and28primer combinations, which could produce clearbands with good polymorphisms and reproducibility, were selected. The28primercombinations generated287scorable bands, including202polymorphic bands. The totalnumber of bands amplified by a primer-combination ranged from4to17with an average of10.27per primer combination. The proportion of polymorphic bands ranged from33.33%(JN00L1-ME11) to100%(JN00R1-ME6) with a mean of72.12%. The20strains of H.marmoreus were clustered into2groups, which one had2strain based on the data of TRAP.The cluster result of TRAP revealed that the cluster of strains were no association with thecolor, yield and stored type of strains.
Recycling the bands that were produced in all strains of H. marmoreus and not incontrols, then they were cloned into Ecoli DH5α by vector pMD1-T. The clone productionswere sequenced by Beijing Genomics Institute (BGI) after PCR amplification checked usinguniversal primers (GV-M,5'-GAG CGG ATA ACA ATT TCA CAC AGG-3′; andM13-47,5′-CGC CAG GGT TTT CCC AGT CAC GAC-3′). There were36sequences of H.marmoreus after assembling sequences with the software of DNAstar package. There were6specific sequences which had no significant similarity sequences found in GenBank data, and5sequences that were the part of heat shock protein70(HSP70) of H. marmoreus by BLASTwith GenBank data online. Online analysis in Softberry site showed that18sequences hadone or more open reading frames (ORF). Six pairs of specific primer were designed withsoftware of primer6.0based on specific sequences which were no significant similaritysequences with GenBank data. The result of a serial check experiments show that one pairspecific primers of H. marmoreus was found. A specific sequence of H. marmoreus with120bp was found.
There were plentiful genetic diversity among the strains of H. marmoreus based on thestudy results of cultivated phenotype, ISSR, SRAP and TRAP. The results of this study mightstrengthen genetic research foundation and the cultivation of new vaarieties of H. marmoreus.The study revealed the molecular markers of ISSR, SRAP and TRAP were useful tools for evaluating genetic diversity and germplasm resource from different aspects, selectingpotential strains and for predicting hybrid performance in the outbreeding of mushrooms.
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