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Article(id=1218551235125362913, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1218551215219196089, articleNumber=null, orderNo=null, doi=10.16438/j.0513-4870.2018-0408, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1525276800000, receivedDateStr=2018-05-03, revisedDate=1527696000000, revisedDateStr=2018-05-31, acceptedDate=null, acceptedDateStr=null, onlineDate=1768454854041, onlineDateStr=2026-01-15, pubDate=1534003200000, pubDateStr=2018-08-12, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1768454854041, onlineIssueDateStr=2026-01-15, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1768454854041, creator=13701087609, updateTime=1768454854041, updator=13701087609, issue=Issue{id=1218551215219196089, tenantId=1146029695717560320, journalId=1189982191388893191, year='2018', volume='53', issue='8', pageStart='1195', pageEnd='1386', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1768454849295, creator=13701087609, updateTime=1768457095505, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1218560636561313952, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1218551215219196089, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1218560636561313953, tenantId=1146029695717560320, journalId=1189982191388893191, issueId=1218551215219196089, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1215, endPage=1224, ext={EN=ArticleExt(id=1218551236203299156, articleId=1218551235125362913, tenantId=1146029695717560320, journalId=1189982191388893191, language=EN, title=Multivariate data analysis of volatile metabolites in rhizomes and radixes of four medicinal plants from Curcuma L., columnId=1218263312677130587, journalTitle=Acta Pharmaceutica Sinica, columnName=SPECIAL REPORTS, runingTitle=null, highlight=null, articleAbstract=

The commonly used traditional Chinese medicines Curcumae Rhizome (Ezhu) and Curcumae Radix (Yujin), are representatives of multi-plant sources. The relationship among the original source plant species is intricate. In this study, by using multivariate data analysis, volatile metabolites in rhizomes and radixes of source plants of Curcumae Longae rhizome (Jianghuang), Yujin and Ezhu in traditional Chinese medicine were compared and analyzed. The source plants included Curcuma longa, Curcuma kwangsuensis, Curcuma wenyujing and Curcuma phaeocaulis. The results indicated that:① volatile metabolites were similar in quality but variation in quantity for rhizomes and radixes origin from the same plant species; ② volatile metabolites of C. longa rhizomes showed bigger difference compared with others; ③ although common volatile metabolites were observed in rhizome of C. kwangsuensis, C. wenyujing and C. phaeocaulis, the difference among them were significant; and ④ significant differences were observed for the four kinds of radixes. Results in this study revealed the differences of the four source plants species, and similar metabolites in source plants of Curcumae Rhizome (Ezhu) and Curcumae Radix (Yujin) from the level of volatile metabolites. These results provided a reference for the clinical use of the three kinds of traditional Chinese medicine.

, correspAuthors=Juan GUO, Lu-qi HUANG, authorNote=null, correspAuthorsNote=null, copyrightStatement=Copyright ©2018 Acta Pharmaceutica Sinica. All rights reserved., copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=Jing-ru SUN, Jun-ling BU, Huan ZHAO, Ya-ping MAO, Wen ZENG, Juan GUO, Lu-qi HUANG), CN=ArticleExt(id=1218551238401114691, articleId=1218551235125362913, tenantId=1146029695717560320, journalId=1189982191388893191, language=CN, title=四种姜黄属药用植物根茎和块根挥发性代谢物的多元数据比较分析, columnId=1218263312865874270, journalTitle=药学学报, columnName=专题报道, runingTitle=null, highlight=null, articleAbstract=

常用传统中药莪术和郁金是中药中多基源现象的典型代表，其基源植物关系错综复杂。本研究以中药姜黄、郁金、莪术的基源植物姜黄（Curcuma longa）、广西莪术（Curcuma kwangsuensis）、温郁金（Curcuma wenyujing）和蓬莪术（Curcuma phaeocaulis）为研究材料，通过多元数据分析方法对比4种药用植物根茎和块根的挥发性代谢物。结果表明，来源于同一物种的根茎和块根的挥发性代谢物种类相似但含量存在差异；植物姜黄根茎（药材姜黄的基源）与其他3种植物根茎的挥发性代谢物差异大；除植物姜黄根茎外的其他3种植物根茎（药材莪术的基源）含有多种共有成分，但3种根茎挥发性代谢物差异均达到了显著水平；4种植物块根（药材郁金的基源）含有多种共有单萜类化合物，但总体挥发性代谢物差异也达到了显著水平。本研究从挥发性代谢物角度揭示了中药姜黄、郁金、莪术基源植物的共有代谢物及代谢差异，能够为这3种中药的临床用药提供参考，具有重要理论意义。

, correspAuthors=郭娟, 黄璐琦, authorNote=null, correspAuthorsNote=
* 郭娟, Tel:86-10-64087469, E-mail:;
黄璐琦, E-mail:
, copyrightStatement=版权所有©《药学学报》编辑部2018, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=HSVcFOWtkwocfZ13GVlDNA==, magXml=lQyN1UUwLfda0N8ZgXknDw==, pdfUrl=null, pdf=D8MSlSX2biNsdAMajm6R/A==, pdfFileSize=670472, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=5cde7XUeu1lSOHNafBtdlw==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=4RBFbTSBlV9VGO3y3r9yaw==, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=孙敬茹, 卜俊玲, 赵欢, 毛亚平, 曾雯, 郭娟, 黄璐琦)}, authors=[Author(id=1218970824208470743, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, orderNo=0, firstName=null, middleName=null, lastName=null, nameCn=null, orcid=null, stid=null, country=null, authorPic=null, dead=0, email=null, emailSecond=null, emailThird=null, correspondingAuthor=0, authorType=1, ext={EN=AuthorExt(id=1218970824372048619, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, authorId=1218970824208470743, language=EN, stringName=Jing-ru SUN, firstName=Jing-ru, middleName=null, lastName=SUN, prefix=null, suffix=null, authorComment=null, nameInitials=null, affiliation=null, department=null, xref=1, 2, address=1. State Key Laboratory Breeding Base of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
2. Center for Post-doctoral Research, China Academy of Chinese Medical Sciences, Beijing 100700, China, bio=null, bioImg=null, bioContent=null, aboutCorrespAuthor=null), CN=AuthorExt(id=1218970824577569527, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, authorId=1218970824208470743, language=CN, stringName=孙敬茹, firstName=敬茹, middleName=null, lastName=孙, prefix=null, suffix=null, authorComment=null, nameInitials=null, affiliation=null, department=null, xref=1, 2, address=1.中国中医科学院中药资源中心, 道地药材国家重点实验室培育基地, 北京 100700
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Score and loading plot of principal component analysis obtained from all rhizomes and radixes. A: Score plot; B: Loading plot. Yellow diamond: Rhizomes of C. longa; Yellow open diamond: Radixes of C. longa; Red dot: Rhizomes of C. wenyujing; Red circle: Radixes of C. wenyujing; Black square: Rhizomes of C. kwangsuensis; Black open square: Radixes of C. kwangsuensis; Green triangle: Rhizomes of C. phaeocaulis; Green open triangle: Radixes of C. phaeocaulis

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Comparison of rhizomes and radixes origin from the same plant species. A: Representative total ion chromatograms of rhizomes and radixes from C. longa; B: Representative total ion chromatograms of rhizomes and radixes from C. kwangsuensis; C: Representative total ion chromatograms of rhizomes and radixes from C. wenyujing; D: Representative total ion chromatograms of rhizomes and radixes from C. phaeocaulis; E: OPLS-DA score plot of rhizomes and radixes of C. longa; F: OPLS-DA loading plot of rhizomes and radixes of C. longa; G: OPLS-DA score plot of rhizomes and radixes of C. kwangsuensis; H: OPLS-DA loading plot of rhizomes and radixes of C. kwangsuensis; I: OPLS-DA score plot of rhizomes and radixes of C. wenyujing; J: OPLS-DA loading plot of rhizomes and radixes of C. wenyujing; K: OPLS-DA score plot of rhizomes and radixes of C. phaeocaulis; L: OPLS-DA loading plot of rhizomes and radixes of C. phaeocaulis. In A, B, C and D the above total ion chromatograms are for rhizomes and the below total ion chromatograms are for radixes

, figureFileSmall=SbQKjjumjXxdFTVeyerFbA==, figureFileBig=psMGV7kclfWXBsPMpD1jbg==, tableContent=null), ArticleFig(id=1218970831456227521, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=EN, label=null, caption=null, figureFileSmall=dnCBjrFfnVNMxjEpzaZBfQ==, figureFileBig=llENmQXJ32D3K152iJSPww==, tableContent=null), ArticleFig(id=1218970831569473739, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=CN, label=Figure 3, caption=

Score, VIP loading plot and heatmap of rhizomes from C. longa and other three kinds of rhizomes. A: PLS-DA score plot; B: PLS-DA loading plot; C: Heatmap. In figure A, yellow diamond: Rhizomes of C. longa; black inverted triangle: Other three kinds of rhizomes; in figure C, J: C. longa, G: C. kwangsuensis, P: C. phaeocaulis, W: C. wenyujing

, figureFileSmall=dnCBjrFfnVNMxjEpzaZBfQ==, figureFileBig=llENmQXJ32D3K152iJSPww==, tableContent=null), ArticleFig(id=1218970831678525653, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=EN, label=null, caption=null, figureFileSmall=8mgSglxuP7CWVP8H8OTDRw==, figureFileBig=x1PC+skjfHlGKo/pM3PuSQ==, tableContent=null), ArticleFig(id=1218970831766606051, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=CN, label=Figure 4, caption=

Score and loading plots of PLS-DA model and OPLS-DA model. A: Score plot of PLS-DA model for rhizomes of C. kwangsuensis, C. wenyujing and C. phaeocaulis; B: Loading plot of PLS-DA model for rhizomes of C. kwangsuensis, C. wenyujing and C. phaeocaulis; C: Score plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. phaeocaulis; D: Loading plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. phaeocaulis; E: Score plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. wenyujing; F: Loading plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. wenyujing; G: Score plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. wenyujing; H: Loading plot of OPLS-DA model for rhizomes of C. kwangsuensis and C. wenyujing

, figureFileSmall=8mgSglxuP7CWVP8H8OTDRw==, figureFileBig=x1PC+skjfHlGKo/pM3PuSQ==, tableContent=null), ArticleFig(id=1218970831921795310, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=EN, label=null, caption=null, figureFileSmall=PfEvR5of96GhkN4EvoXxxQ==, figureFileBig=SeLeWMhtTtCpGNs2C1glwQ==, tableContent=null), ArticleFig(id=1218970832068595967, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=CN, label=Figure 5, caption= Peak areas of monoterpenes in the four kinds of radixes. Peak areas of monoterpenes in radixes of <i>C.</i> <i>kwangsuensis</i>, <i>C.</i> <i>wenyujing</i> and <i>C.</i> <i>phaeocaulis</i> were compared with those in <i>C.</i> <i>longa</i> radixes and significant symbol "*" were labeled for <i>P</i> < 0.05, ** for <i>P</i> < 0.01 , figureFileSmall=PfEvR5of96GhkN4EvoXxxQ==, figureFileBig=SeLeWMhtTtCpGNs2C1glwQ==, tableContent=null), ArticleFig(id=1218970832311865617, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=EN, label=null, caption=null, figureFileSmall=9rghL0J2NsT77vONxy1TuQ==, figureFileBig=ae5BezjGNwBEqNxnUeesrw==, tableContent=null), ArticleFig(id=1218970832475443487, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=CN, label=Figure 6, caption= Peak areas of sesquiterpenes in the four kinds of radixes. Peak areas of sesquiterpenes in radixes of <i>C.</i> <i>kwangsuensis</i>, <i>C.</i> <i>wenyujing</i> and <i>C.</i> <i>phaeocaulis</i> were compared with those in <i>C.</i> <i>longa</i> radixes and significant symbol "*" were labeled for <i>P</i> < 0.05, ** for <i>P</i> < 0.01 , figureFileSmall=9rghL0J2NsT77vONxy1TuQ==, figureFileBig=ae5BezjGNwBEqNxnUeesrw==, tableContent=null), ArticleFig(id=1218970832597078312, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=EN, label=null, caption=null, figureFileSmall=null, figureFileBig=null, tableContent=
tR/min Compounds Formula
Alkanes and alcohols
6.25 2-Heptanol C7H16O
9.53 Undecane C11H24
13.49 Dodecane C12H26
16.6 Tridecane C13H28
Aromatic compounds
15.59 1, 3-Ditertiarybutylbenzene C14H22
Monoterpenes
6.7 Cyclene C10H16
6.82 3-Thujene C10H16
6.95 1R-α-Pinene C10H16
7.27 Camphene C10H16
7.8 β-Thujene C10H16
7.86 (-)-β-Pinene C10H16
8.16 β-Pinene C10H16
8.44 α-Phellandrene C10H16
8.57 3-Carene C10H16
8.7 α-Terpinene C10H16
8.87 o-Cymene C10H14
8.95 Limonene C10H16
8.99 Cineole C10H18O
9.34 β-cis-Ocimene C10H16
9.58 γ-Terpinene C10H16
10.22 Terpinolene C10H16
10.47 Linalool C10H18O
11.68 (+)-Camphor C10H16O
12.1 Isoborneol C10H18O
12.38 endo-Borneol C10H18O
12.74 (-)-Terpinen-4-ol C10H18O
13.01 p-Cymen-8-ol C10H14O
13.21 α-Terpinol C10H18O
Sesquiterpenes
18.95 δ-Elemene C15H24
20.88 β-Elemene like C15H24
21.17 β-Elemene C15H24
21.72 (-)-Zingiberene like C15H24
22.23 Caryophyllene C15H24
22.85 γ-Elemene C15H24
22.91 trans-α-Bergamotene C15H24
23.44 α-Gurjunene C15H24
23.62 Humulene C15H24
23.77 cis-β-Farnesene C15H24
24.74 Germacrene D C15H24
24.8 Ar-Curcumene C15H22
24.94 β-Selinene/β-Eudesmene C15H24
25.35 (-)-Zingiberene C15H24
25.39 Curzerene C15H20O
25.69 Germacrene A C15H24
25.85 β-Bisabolene C15H24
26.12 2, 4-Di-tert-butylphenol C14H22O
26.35 δ-Elemene C15H24
26.44 β-Sesquiphellandrene C15H24
26.61 3, 7(11)-Selinadiene C15H24
27.59 7-epi-cis-sesquisabinene hydrate C15H26O
27.69 γ-Elemene C15H24
28 (±)-trans-Nerolidol C15H26O
28.88 Viridiflorol C15H26O
28.99 cis-Sesquisabinene hydrate 1 C15H26O
29.19 β-Eudesmol C15H26O
29.53 β-Elemenone C15H22O
29.89 cis-Sesquisabinene hydrate 2 C15H26O
32.47 α-Eudesmol C15H26O
30.54 cis-Sesquisabinene hydrate 3 C15H26O
30.56 γ-Eudesmol C15H26O
31.23 β-Eudesmol like C15H26O
31.8 Ar-tumerone C15H20O
32 Tumerone C15H22O
32.8 Curzerene C15H20O
32.92 Germacrone C15H22O
33.15 Curlone C15H22O
33.74 Curdione C15H24O2
34.93 Curdione like C15H24O2
35.22 Ledene oxide-(Ⅱ) C15H24O
36.34 Velleral C15H20O2
), ArticleFig(id=1218970832878096705, tenantId=1146029695717560320, journalId=1189982191388893191, articleId=1218551235125362913, language=CN, label=Table 1, caption=

Identified volatile metabolites in C. longa, C. kwangsuensis, C. wenyujing and C. phaeocaulis

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tR/min Compounds Formula
Alkanes and alcohols
6.25 2-Heptanol C7H16O
9.53 Undecane C11H24
13.49 Dodecane C12H26
16.6 Tridecane C13H28
Aromatic compounds
15.59 1, 3-Ditertiarybutylbenzene C14H22
Monoterpenes
6.7 Cyclene C10H16
6.82 3-Thujene C10H16
6.95 1R-α-Pinene C10H16
7.27 Camphene C10H16
7.8 β-Thujene C10H16
7.86 (-)-β-Pinene C10H16
8.16 β-Pinene C10H16
8.44 α-Phellandrene C10H16
8.57 3-Carene C10H16
8.7 α-Terpinene C10H16
8.87 o-Cymene C10H14
8.95 Limonene C10H16
8.99 Cineole C10H18O
9.34 β-cis-Ocimene C10H16
9.58 γ-Terpinene C10H16
10.22 Terpinolene C10H16
10.47 Linalool C10H18O
11.68 (+)-Camphor C10H16O
12.1 Isoborneol C10H18O
12.38 endo-Borneol C10H18O
12.74 (-)-Terpinen-4-ol C10H18O
13.01 p-Cymen-8-ol C10H14O
13.21 α-Terpinol C10H18O
Sesquiterpenes
18.95 δ-Elemene C15H24
20.88 β-Elemene like C15H24
21.17 β-Elemene C15H24
21.72 (-)-Zingiberene like C15H24
22.23 Caryophyllene C15H24
22.85 γ-Elemene C15H24
22.91 trans-α-Bergamotene C15H24
23.44 α-Gurjunene C15H24
23.62 Humulene C15H24
23.77 cis-β-Farnesene C15H24
24.74 Germacrene D C15H24
24.8 Ar-Curcumene C15H22
24.94 β-Selinene/β-Eudesmene C15H24
25.35 (-)-Zingiberene C15H24
25.39 Curzerene C15H20O
25.69 Germacrene A C15H24
25.85 β-Bisabolene C15H24
26.12 2, 4-Di-tert-butylphenol C14H22O
26.35 δ-Elemene C15H24
26.44 β-Sesquiphellandrene C15H24
26.61 3, 7(11)-Selinadiene C15H24
27.59 7-epi-cis-sesquisabinene hydrate C15H26O
27.69 γ-Elemene C15H24
28 (±)-trans-Nerolidol C15H26O
28.88 Viridiflorol C15H26O
28.99 cis-Sesquisabinene hydrate 1 C15H26O
29.19 β-Eudesmol C15H26O
29.53 β-Elemenone C15H22O
29.89 cis-Sesquisabinene hydrate 2 C15H26O
32.47 α-Eudesmol C15H26O
30.54 cis-Sesquisabinene hydrate 3 C15H26O
30.56 γ-Eudesmol C15H26O
31.23 β-Eudesmol like C15H26O
31.8 Ar-tumerone C15H20O
32 Tumerone C15H22O
32.8 Curzerene C15H20O
32.92 Germacrone C15H22O
33.15 Curlone C15H22O
33.74 Curdione C15H24O2
34.93 Curdione like C15H24O2
35.22 Ledene oxide-(Ⅱ) C15H24O
36.34 Velleral C15H20O2
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四种姜黄属药用植物根茎和块根挥发性代谢物的多元数据比较分析
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孙敬茹 1, 2 , 卜俊玲 1 , 赵欢 1 , 毛亚平 1 , 曾雯 1 , 郭娟 1, * , 黄璐琦 1, *
药学学报 | 专题报道 2018,53(8): 1215-1224
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药学学报 | 专题报道 2018, 53(8): 1215-1224
四种姜黄属药用植物根茎和块根挥发性代谢物的多元数据比较分析
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孙敬茹1, 2, 卜俊玲1, 赵欢1, 毛亚平1, 曾雯1, 郭娟1, * , 黄璐琦1, *
作者信息
  • 1.中国中医科学院中药资源中心, 道地药材国家重点实验室培育基地, 北京 100700
  • 2.中国中医科学院博士后研究中心, 北京 100700

通讯作者:

* 郭娟, Tel:86-10-64087469, E-mail:;
黄璐琦, E-mail:
Multivariate data analysis of volatile metabolites in rhizomes and radixes of four medicinal plants from Curcuma L.
Jing-ru SUN1, 2, Jun-ling BU1, Huan ZHAO1, Ya-ping MAO1, Wen ZENG1, Juan GUO1, * , Lu-qi HUANG1, *
Affiliations
  • 1. State Key Laboratory Breeding Base of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China
  • 2. Center for Post-doctoral Research, China Academy of Chinese Medical Sciences, Beijing 100700, China
出版时间: 2018-08-12 doi: 10.16438/j.0513-4870.2018-0408
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摘要
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常用传统中药莪术和郁金是中药中多基源现象的典型代表，其基源植物关系错综复杂。本研究以中药姜黄、郁金、莪术的基源植物姜黄（Curcuma longa）、广西莪术（Curcuma kwangsuensis）、温郁金（Curcuma wenyujing）和蓬莪术（Curcuma phaeocaulis）为研究材料，通过多元数据分析方法对比4种药用植物根茎和块根的挥发性代谢物。结果表明，来源于同一物种的根茎和块根的挥发性代谢物种类相似但含量存在差异；植物姜黄根茎（药材姜黄的基源）与其他3种植物根茎的挥发性代谢物差异大；除植物姜黄根茎外的其他3种植物根茎（药材莪术的基源）含有多种共有成分，但3种根茎挥发性代谢物差异均达到了显著水平；4种植物块根（药材郁金的基源）含有多种共有单萜类化合物，但总体挥发性代谢物差异也达到了显著水平。本研究从挥发性代谢物角度揭示了中药姜黄、郁金、莪术基源植物的共有代谢物及代谢差异，能够为这3种中药的临床用药提供参考，具有重要理论意义。

姜黄属药用植物  /  挥发性代谢物  /  多元数据分析  /  根茎  /  块根

The commonly used traditional Chinese medicines Curcumae Rhizome (Ezhu) and Curcumae Radix (Yujin), are representatives of multi-plant sources. The relationship among the original source plant species is intricate. In this study, by using multivariate data analysis, volatile metabolites in rhizomes and radixes of source plants of Curcumae Longae rhizome (Jianghuang), Yujin and Ezhu in traditional Chinese medicine were compared and analyzed. The source plants included Curcuma longa, Curcuma kwangsuensis, Curcuma wenyujing and Curcuma phaeocaulis. The results indicated that:① volatile metabolites were similar in quality but variation in quantity for rhizomes and radixes origin from the same plant species; ② volatile metabolites of C. longa rhizomes showed bigger difference compared with others; ③ although common volatile metabolites were observed in rhizome of C. kwangsuensis, C. wenyujing and C. phaeocaulis, the difference among them were significant; and ④ significant differences were observed for the four kinds of radixes. Results in this study revealed the differences of the four source plants species, and similar metabolites in source plants of Curcumae Rhizome (Ezhu) and Curcumae Radix (Yujin) from the level of volatile metabolites. These results provided a reference for the clinical use of the three kinds of traditional Chinese medicine.

medicinal plants from Curcuma  /  volatile metabolites  /  multivariate data analysis  /  rhizome  /  radixes
孙敬茹, 卜俊玲, 赵欢, 毛亚平, 曾雯, 郭娟, 黄璐琦. 四种姜黄属药用植物根茎和块根挥发性代谢物的多元数据比较分析. 药学学报, 2018 , 53 (8) : 1215 -1224 . DOI: 10.16438/j.0513-4870.2018-0408
Jing-ru SUN, Jun-ling BU, Huan ZHAO, Ya-ping MAO, Wen ZENG, Juan GUO, Lu-qi HUANG. Multivariate data analysis of volatile metabolites in rhizomes and radixes of four medicinal plants from Curcuma L.[J]. Acta Pharmaceutica Sinica, 2018 , 53 (8) : 1215 -1224 . DOI: 10.16438/j.0513-4870.2018-0408
正文
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常用传统中药郁金、莪术均为中药中一药多基源的典型代表, 中药姜黄、郁金、莪术均来源于姜科姜黄属药用植物, 基源植物种类交叉, 关系错综复杂, 并随时代不同存在基源变迁。依据谢宗万[1]对这3种中药进行的本草考证, 《唐本草》表明药材姜黄来源于多个品种并与莪术混称, 据《唐本草》、《本草图经》、《本草衍义》、《本草纲目》等记载, 明代以前郁金的基源是植物姜黄的根茎, 而清末明初的《增订伪药条辨》对郁金的描述则表明郁金的基源转换为姜黄属植物的块根。2015年版《中华人民共和国药典》 (简称《中国药典》)收载药材姜黄基源1种, 为姜科植物姜黄(Curcuma longa L.)的干燥根茎; 莪术基源3种, 为姜科植物蓬莪术(Curcuma phaeocaulis Val.)、广西莪术(Curcuma kwangsuensis S. G. Lee et C. F. Liang)或温郁金(Curcuma wenyujing Y. H. Chen et C. Ling)的干燥根茎; 郁金基源4种, 为这4种姜科植物的干燥块根[2]。因而, 中药姜黄、郁金、莪术在我国药用历史上不仅基源部位发生了变化, 基源植物种类也存在差异, 目前临床用药过程中, 药材郁金和莪术往往不根据基源植物做区分, 对4种药用植物入药部位物质基础的研究能够为其临床用药提供研究基础。
姜黄素类化合物和挥发油类化合物是中药姜黄、郁金和莪术的药效活性成分, 但中药莪术和郁金中姜黄素类化合物含量很低[3]。挥发油类化合物为抗肿瘤、消炎、抗病毒的重要药效成分, 如中药姜黄倍半萜β-倍半水芹烯对白血病、多发性骨髓瘤和结肠直肠癌细胞具有与姜黄素相似水平的抗增殖能力[4], 中药莪术和郁金中β-榄香烯、δ-榄香烯、呋喃二烯、呋喃二烯酮、莪术醇、吉马酮、莪术酮、莪术二酮都具有较好的抗癌药效活性[5]。早期的研究表明, 姜黄属药用植物根茎挥发油代谢物中存在多种共有代谢物, 但主要组分存在差异[6]。中药姜黄、郁金、莪术基源植物根茎和块根挥发性代谢物的系统性比较和多元数据分析能够为3种中药基源的识别和临床用药提供帮助。
鉴于中药长期以来对药材道地性的认可, 为了分析药材姜黄、郁金、莪术3种中药差异的物质基础, 本研究以采自各自道地产区的4种基源植物为实验材料。通过气相色谱和质谱联用仪器(GC-MS), 对比分析了4种药用植物根茎和块根的挥发性代谢物。通过分析这4种姜黄属植物根茎和块根间药效活性物质种类和含量的差异将为探究其不同部位存在药效差别的现象提供基础, 也为药材郁金和莪术的一药多基源现象提供科学依据。
材料与方法
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仪器与试剂  Thermo fisher Trace 1310气相色谱仪与Thermo Scientific TSQ8000质谱仪(Thermo Scientific, Germany)串联仪器。Xcalibur 3.2软件; Metalign软件, 甲基叔丁基醚为色谱纯(Aladdin)。
植物材料  2015年12月从4种姜黄属药用植物的道地产区采集4种姜黄属植物的根茎和块根, 姜黄(Curcuma longa L.)根茎和块根采自四川乐山犍为, 广西莪术(Curcuma kwangsuensis S. G. Lee et C. F. Liang)根茎和块根采自广西南宁药用植物园, 温郁金(Curcuma wenyujing Y. H. Chen et C. Ling)根茎和块根采自浙江温州瑞安, 蓬莪术(Curcuma phaeocaulis Val.)根茎和块根采自四川双流。样品采集由全国第四次中药资源普查工作人员协助, 采集后孙敬茹根据《中国药典》和《中国植物志》对4种药用植物的描述, 进行了严格鉴定。完整健康根茎连同块根被采集后, 用自来水清洗, 吸水纸吸干后切为小块, 迅速丢入液氮淬灭, 样品经液氮预冻后快速用球磨机磨粉, 然后进行挥发性代谢物提取。
样品提取  称取1 g样品粉末, 加入甲基叔丁基醚2 mL, 涡旋2 min后, 200 r·min-1摇动过夜提取, 然后12 000 ×g离心20 min, 吸取上清, 经0.2 μm聚四氟乙烯(PTFE)滤膜过滤后进行挥发性代谢物测定。
GC-MS检测  样品检测均在Thermo三重四级杆气质联用仪上进行, 气相为Trace1310, 质谱为MS TSQ8000。测定用Thermo TG-5 MS毛细管柱(30 m × 0.25 mm × 0.25 μm), 进样口温度250 ℃, 氦气流速1 mL·min-1, 程序升温的起始温度为70 ℃, 保持3 min, 然后8 ℃·min-1升温到230 ℃, 20 ℃·min-1升温到 300 ℃, 保持2 min。扫描质量(m/z) 50~600。电子轰击离子源(EI), 电子电离能量70 eV。
数据处理  代谢物通过质谱图与NIST质谱库比对和相关参考文献来鉴定, 与NIST谱库比对进行化合物鉴定中, 只有色谱峰强度 > 1×105, 质谱图与NIST质谱库质谱图正向比对大于800的峰才确定为鉴定物质。GC-MS扫描数-峰高数据通过metalign软件进行提取, 提取的有效数据(Rt = 5~42 min)用于多元数据分析。自动质谱解卷积和识别系统(Automated Mass Spectral Deconvolution & Identification System, AMDIS)软件用于自动去卷积后分析色谱峰的纯度和保留时间-特征离子列表的获取, 代谢组学离子数据提取算法软件(Metabolomics Ion-based Data Extraction Algorithm, MET-IDEA)按照AMDIS软件获得的保留时间-特征离子提取峰面积。
本研究所用主成分分析(PCA)、偏最小二乘判别分析(PLS-DA)、正交偏最小二乘判别分析(OPLS-DA)均通过SIMCA-P (Umetrics, 11.5)进行, PCA、OPLS-DA建模前, 数据进行pareto预处理, PLS-DA建模前数据进行UV预处理。峰面积的方差分析(ANOVA)和组间比较通过SPSS (IBM, 13.0)软件进行, 箱线图用sigmaplot绘制。
结果
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1 挥发性代谢物鉴定
通过将质谱图与NIST库及参考文献[7-10]比对, 本研究从4种姜黄属药用植物根茎和块根中共鉴定出80种次生代谢物(表 1), 包括烷烃、醇、单萜和倍半萜类化合物, 其中单萜和倍半萜类化合物为主要成分。
植物广西莪术、温郁金和蓬莪术根茎样品含有多种共有单萜和倍半萜类代谢物, 但含量存在差异, 这些共有的代谢物包括2-庚醇(2-heptanol)、1R-α-蒎烯(1R-α-pinene)、莰烯(camphene)、β-侧柏烯(β- thujene)、(-)-β-蒎烯[(-)-β-pinene]、β-蒎烯(β-pinene)、正癸烷(decane)、柠檬烯(limonene)、桉叶油醇(cineole)、β-顺-罗勒烯(β-cis-ocimene)、十一烷(undecane)、芳樟醇(linalool)、(+)-樟脑[(+)-camphor]、异龙脑(isoborneol)、内型冰片(endo-borneol)、(-)-4-萜烯醇[(-)-terpinen-4-ol]、α-松油醇(α-terpineol)、1, 3-二叔丁基苯(1, 3-ditertiarybutylbenzene)、δ-榄香烯(δ-elemene)、β-榄香烯(β-elemene)、石竹烯(caryo-phyllene)、γ-榄香烯(γ-elemene)、蛇麻烯(humulene)、吉马烯D (germacrene D)、莪术烯(curzerene)、吉马烯A (germacrene A)、3, 7(11)-芹子二烯[3, 7(11)-selina-diene]、绿花白千层醇(viridiflorol)、吉马酮(ger-macrone)。4种块根中也含有一些共有的挥发性代谢物, 这些代谢物包括1R-α-蒎烯(1R-α-pinene)、莰烯(camphene)、(-)-β-蒎烯[(-)-β-pinene]、柠檬烯(limonene)、桉叶油醇(cineole)、γ-松油烯(γ-terpinene)、十一烷(undecane)和十二烷(dodecane)。
2 4种植物根茎和块根挥发性代谢物比较分析
为了获取4种植物根茎和块根代谢物的关系, 首先对样品进行了无监督的主成分分析(PCA), PCA得分图表明(图 1A)样品大致沿两个方向分布, 植物姜黄根茎和块根沿一个方向分布, 植物广西莪术、温郁金和蓬莪术根茎样品沿另一方向分布, 而植物广西莪术、温郁金和蓬莪术的块根样品分布在两个方向的交叉部位。PCA载荷图(图 1B)中代谢成分也按照相似的两个方向分布。因而, 植物姜黄根茎和块根成分与其他3种植物根茎和块根代谢物差异较大, 而植物温郁金、广西莪术和蓬莪术根茎存在较多相似的代谢物。
3 相同植物来源根茎和块根挥发性代谢物比较分析
4种姜黄属药用植物的根茎和块根入药后名称和药效不同, 本研究首先分析了相同植物来源的根茎和块根挥发性代谢物的差异。相同植物来源根茎和块根的挥发性代谢物指纹总离子流图比较(图 2A~D)表明, 同种植物根茎和块根的挥发性成分相似, 但含量存在差异, 根茎的挥发性代谢物含量总体都较高, 而块根挥发性代谢物总体含量低, 只有少数几种挥发性化合物在块根中含量高于根茎。4组根茎和相应块根的PLS-DA模型200次排列交叉验证表明, 这4种药用植物的根茎和块根的挥发性代谢物之间都存在显著性差异, 得分图和载荷图为图 2E~L, OPLS-DA模型的第一主成分VIP值(VIP > 1)用于分析差异化合物。
植物姜黄块根与根茎相比, 1R-α-蒎烯、崁烯、β-蒎烯、桉树脑、石竹烯和几种未鉴定结构的萜类化合物含量较高, 而其他代谢物含量较低。植物广西莪术块根癸烷、十一烷、十二烷、十三烷、1, 3-二叔丁基苯、2, 4-二叔丁基苯酚、乙酸冰片酯、保留时间为25.38和40.61 min的两种未鉴定结构倍半萜、及保留时间为5.48和15.97 min两种烷烃含量较高, 而其他代谢物均含量较低。植物温郁金块根与根茎相比, 癸烷、十一烷、十二烷、1, 3-二叔丁基苯、2, 4-二叔丁基苯酚和保留时间为5.48、16.62、21.51 min的3种烷烃含量较高, 其他代谢物含量低。植物蓬莪术块根与根茎相比只有γ-松油烯含量较高。
4 植物姜黄根茎与其他3种根茎挥发性代谢物比较分析
基于所有样品的PCA得分图分组关系(图 1A), 以姜黄的根茎为一组样品, 其他3种药用植物根茎为一组样品, 进行PLS-DA分析, 200次排列交叉验证表明, 姜黄根茎与其他3种植物的根茎样品的挥发性成分存在显著性差异。PLS-DA模型的前两个主成分解释了4种植物根茎挥发性代谢物方差和的43.7%, 而预测了样品分组信息差异的94.2% (图 3A), 模型质量较好, 具备较好的预测能力。
VIP和相关系数的载荷图(图 3B)分析表明, 植物广西莪术、温郁金、蓬莪术的根茎中含有较高的单萜、倍半萜、烷烃及一些苯丙素类化合物, 包括2-庚醇、3-崖柏烯、1R-α-蒎烯、崁烯、β-侧柏烯、(-)-β-蒎烯、β-蒎烯、正癸烷、β-cis-罗勒烯、芳樟醇、(+)-樟脑、异龙脑、endo-龙脑、4-萜烯醇、α-萜品醇、1, 3-叔丁基苯、乙酸龙脑酯、δ-榄香烯、β-榄香烯类似物、β-榄香烯、γ-榄香烯、γ-榄香烯类似物、香树烯、蛇麻烯、吉马烯D、α-瑟琳烯、β-瑟琳烯、2-异丙基-4a、8-二甲基-1, 2, 3, 4a, 5, 6, 7-八氢萘、莪术烯、吉马烯A、α-古芸烯类似物、2, 4-二叔丁基苯酚、β-榄香酮、α-桉叶油醇、β-桉叶油醇、γ-桉叶油醇、β-桉叶油醇类似物、莪术烯类似物、吉马酮、莪术二酮、莪术二酮类似物、喇叭烯氧化物(Ⅱ)、绒白乳菇醛和一些未鉴定的化合物。而植物姜黄根茎中另外的多种倍半萜和单萜含量较高, 这些化合物为α-水芹烯、α-萜烯、o-环烯、柠檬烯、桉树脑、β-cis-罗勒烯、γ-萜烯、对-聚伞花素醇-8、姜烯类似物、反式-α-香柠檬烯、α-古芸烯、顺-β-法尼烯、芳姜黄烯、姜烯、β-甜没药烯、β-倍半水芹烯、3, 7(11)-芹子二烯、7-表-顺式-倍半香桧烯水合物、橙花叔醇、芳姜黄酮、姜黄新酮、3种倍半萜香桧烯水合物和一些没有鉴定结构的化合物。
分层聚类分析热图(图 3C)表明, 植物姜黄根茎样品挥发性成分与其他3种根茎样品间存在明显差异, 而其他三种根茎样品间挥发性代谢物也存在差异。
5 莪术基源植物根茎挥发性代谢物比较分析
植物广西莪术、温郁金和蓬莪术根茎挥发性成分间的分析表明, 3种根茎间的差异都达到了显著性水平。3组根茎样品的PLS-DA模型得分图(图 4A)表明, 植物蓬莪术根茎样品的组内差异较小且与植物广西莪术及温郁金根茎的差异较大, 而后两种植物根茎的挥发性代谢物差异较小。进一步分析这个模型的载荷图(图 4B)可见, 相对于蓬莪术, 广西莪术和温郁金根茎中的多种化合物含量都较高。
3种植物根茎两两比较的OPLS-DA模型用于分析3种根茎间差异代谢物。两两比较的得分图中, 来源于不同物种的根茎存在分组趋势(图 4C、E、G)。植物蓬莪术根茎与广西莪术根茎样品比较的载荷图(图 4D)表明, 与植物蓬莪术根茎相比, 植物广西莪术根茎中桉树脑、绒白乳菇醛、莪术二酮和一种与莪术二酮碎裂模式一致的倍半萜含量较高, 而植物蓬莪术根茎中两种未鉴定结构的氧化倍半萜类化合物含量较高, 这两种化合物的保留时间分别为29.54和36.00 min。而与植物温郁金根茎相比, 植物蓬莪术含量高的化合物依旧是保留时间为29.54和36.00 min的两个倍半萜, 而植物温郁金根茎含有较多的桉树脑、(+)-樟脑、莪术烯、莪术烯类似物、莪术二酮、莪术二酮类似物和一种氧化倍半萜(保留时间为38.09 min) (图 4F)。而与植物广西莪术相比, 植物温郁金根茎中莪术烯、莪术烯类似物、吉马烯A、γ-榄香烯类似物、吉马酮和一种结构未鉴定的氧化倍半萜(保留时间为38.09 min)含量较高, 而绒白乳菇醛和一种结构未知保留时间为39.21 min的氧化倍半萜含量较低(图 4H)。
6 4种郁金的代谢差异
4种植物块根样品挥发性代谢物的PLS-DA模型分析表明, 4种块根挥发性代谢物之间存在显著性差异。载荷图分析表明, 对4种块根差异贡献大的代谢物包括单萜类化合物、倍半萜类化合物、烷烃和苯丙素类化合物。
为了进一步了解植物姜黄块根与其他3种块根的单萜和倍半萜含量差异, 对已鉴定单萜和倍半萜类化合物中总离子流图峰纯度 > 50%的化合物进行了相对含量分析。单萜相对含量分析表明, 植物姜黄块根中特异性含有芳樟醇(linalool)、α-水芹烯(α- phellandrene)和α-松油烯(α-terpinene), 累积了较多的β-蒎烯(β-pinene)和邻伞花烃(o-cymene), 而其他3种块根中单萜含量存在差异, 两种块根中崁烯(camphene)和樟脑[(+)-camphor]含量显著性比植物姜黄块根高(图 5)。倍半萜的分析表明, 姜黄块根特异性含有石竹烯(caryophyllene)、芳姜黄烯(ar- curcumene)、姜烯(zingiberene)、β-倍半萜水芹烯(β-sesquiphellandrene)、芳姜黄酮(ar-tumerone)、α-姜黄酮(α-tumerone)和β-姜黄酮(β-tumerone), 而吉马酮(germacrone)、莪术二酮(curdione)、绒白乳菇醛(velleral)虽然特异性地存在于广西莪术、温郁金和蓬莪术的块根中, 这些化合物含量在3种块根间存在差异(图 6)。此外, β-榄香烯、δ-榄香烯、蛇麻烯、吉马烯D、吉马烯A、3, 7(11)-芹子二烯也特异性存在于广西莪术、温郁金和蓬莪术中, 但由于含量低, 峰纯度较低, 没有进行这些化合物相对含量的比较。
讨论
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本研究的研究对象虽然不是中药材, 但其基源植物采收期入药部位的代谢差异在一定程度上也能够为中药的临床应用提供理论依据。本研究结果中, 植物姜黄块根与植物广西莪术、温郁金和和蓬莪术块根挥发性成分差异大的结果与药材黄丝郁金与桂郁金、温郁金、绿丝郁金挥发油成分差异大的结果一致(黄丝郁金、桂郁金、温郁金和绿丝郁金的基源分别为植物姜黄、广西莪术、温郁金和蓬莪术的块根)[10, 11]。植物姜黄块根不含有吉马酮而其他3种药用植物块根中有较高含量吉马酮, 这与黄丝郁金挥发油不含吉马酮而其他3种郁金吉马酮含量较高相符[10]。植物姜黄根茎与其他3种植物根茎的显著性差异可能是药材姜黄和莪术差异的基础, 植物广西莪术、温郁金、蓬莪术根茎含有的多种共有挥发性代谢物则可能是其作为中药莪术的物质基础, 而植物姜黄、广西莪术、温郁金、蓬莪术根茎与相应块根挥发性代谢物种类相似而含量存在差异可能是其入药后药效不同的原因。
4种药用植物根茎和块根间药效活性物质种类和含量的差异可能是其药效差异的原因。目前的研究表明, 姜黄素可能是药材姜黄、莪术、郁金寒热药性差异的物质基础[3], 挥发性代谢物对这3种中药药性差异的影响还不清楚。目前的研究表明, 姜黄属药用植物精油中的部分单萜和倍半萜能够抗癌、消炎、抗病毒, 这些药效活性代谢物包括植物姜黄根茎和块根中特异性含有的芳姜黄烯[4]、姜烯[12]、β-倍半水芹烯[4]、芳姜黄酮[13], 也包括植物蓬莪术、广西莪术和温郁金根茎中共有部分单萜和δ-榄香烯、β-榄香烯、γ-榄香烯、莪术烯、β-桉叶油醇、吉马酮、莪术二酮[5]等。随着这些药效活性物质药效机制的逐步解析, 这些代谢物可能成为药材姜黄、郁金、莪术抗癌、消炎、抗病毒药理差异的物质基础。
4种姜黄属药用植物挥发性代谢物主要为单萜和倍半萜。植物通过MEP途径合成萜类共同底物二甲基丙烯基焦磷酸(DMAPP)和异戊二烯基焦磷酸(IPP), 之后二者缩合产生的牻牛儿基焦磷酸(GPP)在单萜合酶的作用下形成多种单萜的骨架, 细胞色素P450酶等催化修饰后形成具有生物活性的单萜类代谢物。倍半萜类代谢物通过MVA途径合成萜类底物DMAPP和IPP, 二者缩合产生法尼基焦磷酸(FPP), FPP经倍半萜合酶催化形成倍半萜的多种骨架, 经细胞色素P450酶等催化修饰形成具有生物活性的倍半萜类代谢物。相同植物来源根茎和块根萜类挥发性代谢物种类相似, 含量有明显差异, 推测其单萜合酶、倍半萜合酶及下游细胞色素P450酶等可能相同, 但表达水平不同, 而不同来源的根茎和块根挥发性代谢物种类差异显著, 推测其单萜合酶、倍半萜合酶及下游细胞色素P450酶等存在较大差异。本实验数据, 为寻找新的萜类合酶及下游细胞色素P450酶等提供支持。
中药长期以来注重道地性, 道地性是中药材的“品质标杆”, 道地性包含了诸多环境因素的影响[14]。外在环境因素是植物次生代谢物累积差异的重要影响因素[15, 16], 中药长期以来的道地性则将中药基源植物生长过程中的光照、温度、水分、空气、土壤、取食昆虫、共生菌等影响因素进行了综合, 是保证中药品质的重要因素。如连续两年对温州7个温郁金道地产区温郁金药材挥发油、吉马酮和莪术醇的监测表明, 各批次温郁金药材均符合中国药典2010年版标准要求[17]。本研究中4种药用植物均采自各自的道地产区, 挥发性代谢物的差异包含了物种本身的差异也包含了环境因素引起的差异, 材料具备典型性。
基金
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  • 国家自然科学基金资助项目(81603244)
  • 中国博士后科学基金资助项目(2015M571252)
  • 中央本级重大增减支项目“名贵中药资源可持续利用能力建设”项目(2060302)
文献
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参考文献 引证文献
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2018年第53卷第8期
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doi: 10.16438/j.0513-4870.2018-0408
  • 接收时间：2018-05-03
  • 首发时间：2026-01-15
  • 出版时间：2018-08-12
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  • 收稿日期：2018-05-03
  • 修回日期：2018-05-31
基金
国家自然科学基金资助项目(81603244)
中国博士后科学基金资助项目(2015M571252)
中央本级重大增减支项目“名贵中药资源可持续利用能力建设”项目(2060302)
作者信息
    1.中国中医科学院中药资源中心, 道地药材国家重点实验室培育基地, 北京 100700
    2.中国中医科学院博士后研究中心, 北京 100700

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* 郭娟, Tel:86-10-64087469, E-mail:;
黄璐琦, E-mail:
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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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