中國傘形科柴胡屬果實結構的系統(tǒng)學價值

常修奇，劉玫，程薪宇，王宇婷，魏雪瑩，王雪微

(哈爾濱師范大學生命科學與技術學院，黑龍江省普通高等學校植物生物學重點實驗室，黑龍江 哈爾濱 150025)

中國傘形科柴胡屬果實結構的系統(tǒng)學價值

常修奇，劉玫*，程薪宇，王宇婷，魏雪瑩，王雪微

(哈爾濱師范大學生命科學與技術學院，黑龍江省普通高等學校植物生物學重點實驗室，黑龍江 哈爾濱 150025)

摘要：本文首次深入研究了中國柴胡屬29種，5變種及2變形果實的三維結構。結構顯示果實結構變化較大，分果表面平滑, 橫切面近圓形，脊略微突出。中果皮有兩種分泌結構，伴生油管及非伴生油管(油管)。前者僅存在于少數物種，且直徑小，后者包括不分支及分支油管。不分支油管存在于多數物種的溝(1~5)和結合面(2~7)，油管通常與分果近等長，但亦存在短油管。少數物種的油管呈分支狀，在中果皮不規(guī)則分布。種皮由1或2層薄壁細胞構成。胚乳在結合面平直或微凹。中果皮無結晶。心皮柄多為2個，在結合面彼此相對。柴胡屬果實的多數特征存在于芹亞科其他類群，但分支狀油管及2層細胞的種皮僅見于牽環(huán)花亞科，變豆菜亞科及芹亞科的基礎類群。柴胡屬果實的解剖結構支持分子系統(tǒng)學將柴胡屬位于芹亞科其他類群的基礎位置。

關鍵詞：柴胡屬；果實解剖；油管；傘形科；系統(tǒng)學

The phylogenetic significance of fruit structures inBupleurumof the family Apiaceae

CHANG Xiu-Qi, LIU Mei*, CHENG Xin-Yu, WANG Yu-Ting, WEI Xue-Ying, WANG Xue-Wei

CollegeofLifeScienceandTechnology,HarbinNormalUniversity,KeyLaboratoryofPlantBiology,CollegeofHeilongjiangProvince,Harbin150025,China

Abstract:The three-dimensional structure of fruits of 29 species, 5 varieties and 2 forms in the genus Bupleurum, from China were studied in depth and are reported for the first time in this paper. The fruit structures were found to vary greatly. The mericarp surfaces are smooth, approximately circular in transverse section, and ribs are slightly prominent. Two types of secretory structures, rib ducts and vittae, occur in the mesocarps. The former which are small in diameter are found in a few taxa and the latter include unbranched and branched vittae. The vittae occur in the furrow (1-5) and commissure (2-7) in most taxa, and they are similar to mericarps in length, usually unbranched, and sometimes short. The vittae are branched in a few taxa and dispersed in the mesocarps. The testa is composed of one or two layers of parenchyma cells. The endosperm is flat or slightly concave on the commissural side. Crystals are not present in the mesocarp. There are usually two carpophores, which are arranged on opposite sides of the commissural plane. Most features of the genus are present in other groups of the Apioideae, but branching vittae and testa with two layers of cells are only found in the Azorelloideae, Saniculoideae, and some groups of the Apioideae. The anatomical structures of Bupleurum fruits support its continued classification in the Apioideae, as shown by molecular studies.

Key words:Bupleurum; fruit anatomy; vitta; Apiaceae; systematics

柴胡屬(Bupleurum)是傘形科(Apiaceae)芹亞科(Apioideae)的大屬之一，全世界約180種，主要分布于歐洲，亞洲，非洲及北美[1-3]。中國有42種，其中22種為特有種[4]。植物主要為多年生(稀為一年生)草本，少為木本，單葉[3-5]。芹亞科植物通常為復葉，具單葉的物種主要存在于天胡荽亞科(Drude’s Hydrocotyloideae)和變豆菜亞科(Saniculoideae)[1]，前者已被分子系統(tǒng)學證明不是個自然類群, 其中大部分屬被分別移入兩個新的亞科，參棕亞科(Makinlayoideae)及牽環(huán)花亞科(Azorelloideae)[6]。花粉研究[7-9]表明柴胡屬的花粉同參棕亞科，牽環(huán)花亞科及變豆菜亞科類似，近菱形，近圓形及橢圓形，為原始類型。染色體數亦同這幾個亞科相似，通常為n=4, 6, 7 或 8, 很少為芹亞科多數物種具有的染色體數n=11[10-12]。

分子系統(tǒng)學研究[13-27]顯示芹亞科不是個自然的類群，傳統(tǒng)位于這一亞科的非洲特有屬Polemanniopsis及Steganotaenia應靠近變豆菜亞科，其他一些屬Anginon，Heteromorpha，Dracosciadium，Polemannia，Glia這5個屬組成一個新的族Heteromorpheae[24]，Annesorhiza及Chamarea應位于芹亞科的基礎位置[24]。盡管分子系統(tǒng)研究證明柴胡屬是單系類群，比這些非洲特有屬進化，但仍位于芹亞科的基礎位置[6,28-31]。

柴胡屬的果實具有游離的心皮柄，5個絲狀的脊，每個溝里通常具1~3個油管，通常無伴生油管[1,3]。Snogerup 和Snogerup[32]指出柴胡屬果實解剖結構的變化大于傘形科任何一個類群。Liu[33]及王長寶等[34]揭示了柴胡屬果實油管數量變化較大。然而迄今為止缺少這一屬果實結構的詳細報道。傘形科果實結構常被視為其亞科、族及屬的重要分類特征[1,35-36]，近年來隨著果實研究的深入，進一步揭示了果實微形態(tài)(如油管、維管束、結合面及心皮柄等)對傘形科系統(tǒng)分類的重要性，為分子系統(tǒng)學的研究提供了重要的形態(tài)學支持[33-40]。本文的目的是深入研究中國柴胡屬果實的三維結構,比較不同物種果實結構的異同，并將所研究的結構與已研究的傘形科的其他類群相比較，為分子系統(tǒng)學確立的柴胡屬的系統(tǒng)位置提供形態(tài)學依據，并為進一步深入研究世界柴胡屬及傘形科系統(tǒng)學奠定了形態(tài)學基礎。

1材料與方法

1.1　材料

選取中國柴胡屬29種、5變種及2變型作為研究對象，物種名稱及憑證標本信息見表1。果實材料分別取自于中國科學院華南植物園標本館(IBSC-South China Botanical Garden Herbarium)，中國科學院沈陽應用生態(tài)研究所標本館(IFP-Herbarium, Institute of Appling Ecology, CAS)，中國科學院昆明植物研究所標本館(KUN-Herbarium, Kunming Institute of Botany, CAS)，中國科學院植物研究所標本館(PE-Herbarium, Institute of Botany, CAS)，四川大學標本館(SZ-Herbarium, Sichuan University)，中國科學院新疆生態(tài)與地理研究所標本館(XJBI-Herbarium, Xinjiang Institute of Ecology and Geography，CAS)。

1.2　方法

觀察果實外形，油管及心皮柄的結構：用具數碼相機(Olympus DP 70)的解剖鏡(Olympus SP-350)觀察柴胡屬果實外形及心皮柄的結構并照相。將干的果實放入熱水(約90℃)中浸泡，待材料完全吸水膨脹并沉入水底(約2 h)時，取出果實，撕取果皮，將其放在載玻片上并加1~2滴50%甘油水溶液，用具數碼相機(Olympus DP 26)的顯微鏡(Olympus BX 51)觀察油管結構并照相。

GMA(glycolmethacrylate：乙二醇甲基丙烯酸酯)切片：每個物種取2~3個果實，根據Feder和O’Brien[41]的方法，果實經吸水膨脹后，放入FAA(formalin-acetic acid-alcohol: 福爾馬林-冰醋酸-酒精)固定，時間不少于24 h。材料經50%乙醇(4~6 h)，100%乙醇(4~6 h)，異丙醇(6 h)和正丁醇(6 h)脫水, 每步各重復1次。接著材料進入GMA滲透，共3次，第1和2次各1 d，第3次不少于5 d。之后將材料及GMA裝入無色膠囊，置于60℃溫箱聚合(24 h)。用Leica Ultracut R 切片機切片，厚度約2~3 μm。同樣根據Feder和O’Brien[41]的方法，將切片用甲苯胺藍染色，中性樹膠封片。用具數碼相機(Olympus DP 26)的顯微鏡(Olympus BX 51)觀察果實結構并照相。

2結果與分析

本文詳細地描述了中國柴胡屬果實的形態(tài)結構，其主要特征見表2。圖1A~L展示了分果的果皮，伴生油管及非伴生油管，維管束，種皮及心皮柄等特征，圖2A~JJ展示了不同物種果實結構的變化。

分果形狀：研究的柴胡分果(mericarp)的橫切面均為近圓形(圖1I, J，2A~JJ)，具5個脊，1個中脊(median rib)，2個側脊(lateral rib)及2個邊脊(marginal rib)(圖1I, 2A)。多數物種的脊略微突起，如線葉柴胡，金黃柴胡及錐葉柴胡(圖2A~C)，少數物種，即北柴胡，秦嶺柴胡，有柄柴胡，紅柴胡及小柴胡的脊具較明顯突起，大于果皮厚度的2倍(圖2E, U, BB, DD, GG)。

表1　用于研究果實結構的中國柴胡屬物種的憑證標本信息及其采集地

表2　中國柴胡屬果實的重要分類特征Table 2 Summary of taxonomically important characters of the fruits in various taxa of Bupleurum in China

續(xù)表2　Continued

分果表面，表皮，中果皮及內果皮：分果表面平滑，具角質層(cuticle)，多數物種的角質層較薄，橫切面不明顯(圖1G)，但少數物種，如金黃柴胡，紫花鴨趾柴胡及細柄柴胡的角質層較厚，約等于表皮細胞的厚度(圖1F)。表皮(epidermis)為1層扁平狀細胞，多數物種其細胞的外壁是平的(圖1F, H)，細柄柴胡、纖細柴胡及小柴胡的外壁向外突起，呈弧形(圖1I)。中果皮(mesocarp)通常由5~8層近圓形薄壁細胞構成(如圖1F, H)。內果皮(endocarp)為1層長方形薄壁細胞，其細胞的長軸與果實的表面平行(圖1F, H)。

圖1　柴胡屬果實或果實橫切面Fig.1　Fruits or their transverse sections of Bupleurum　示分果表面，表皮，中果皮，內果皮，分泌油管，種皮，結合面及心皮柄。(A,F)金黃柴胡。(B)細柄柴胡。(C)錐葉柴胡。(D)大苞柴胡。(E)紅柴胡。(G)北柴胡。(H)紫花大葉柴胡。(I)小柴胡。(J)北京柴胡。(K)有柄柴胡。(L)細柄柴胡。縮寫：bv=分支油管；c=心皮柄；co=結合面；cu=角質層；cv=結合面油管；e=內果皮；en=胚乳；ep=表皮；lr=側脊；m=中果皮；mar=邊脊；mer=中脊；rd=伴生(或脊中)油管；sv=短油管；vb=維管束；vv=溝中油管; t=種皮。下同。標尺：A~C=1 mm; D, E=0.1 mm; F~H, K, L=0.05 mm; I, J=0.3 mm。Showing mericarp surface, epidermis, mesocarp, endocarp, secretary oil ducts, testa, commissural side, and carpophores. (A, F) B. aureum. (B) B. gracilipes. (C) B. bicaule. (D) B. euphorbioides. (E) B. scorzonerifolium. (G) B. chinense. (H) B. longiradiatum var. porphyranthum. (I) B. tenue. (J) B. chinense f. pekinense. (K) B. petiolulatum. (L) B. gracilipes. Abbreviations: bv=branching vitta; c=carpophore; co=commissure; cu=cuticle；cv=commissural vitta; e=endocarp; en=endosperm; ep=epidermis; lr=lateral rib; m=mesocarp; mar=marginal rib; mer=median rib; rd=rib duct; sv=short vitta; vb=vascular bundle; vv=vallecular vitta; t=testa. The same below. Scale bar=1 mm in A-C; 0.1 mm in D, E; 0.05 mm in F-H, K, L; 0.3 mm in I, J.

維管束：每個分果具5個維管束(vascular bundle)，分別存在于中脊，側脊及邊脊(圖1I，2A)。多數物種維管束的直徑小于果皮厚度，如錐葉柴胡，川滇柴胡及簇生柴胡(圖2C, D, I)。少數物種，包括線葉柴胡、北柴胡、紅柴胡及小柴胡的維管束大，直徑等于或大于果皮的厚度(圖2A, E, DD, GG)。

圖2　柴胡屬果實橫切面Fig.2　Transverse sections of fruits of Bupleurum 　示分果形狀，維管束，分泌油管，胚乳，結合面及心皮柄的變化。(A)線葉柴胡。(B)金黃柴胡。(C)錐葉柴胡。(D)川滇柴胡。(E)北柴胡。(F)百花山柴胡。(G)北京柴胡。(H)紫花鴨趾柴胡。(I)簇生柴胡。(J)葡枝柴胡。(K)密花柴胡。(L)太白柴胡。(M)大苞柴胡。(N)新疆柴胡。(O)細柄柴胡。(P)纖細柴胡。(Q)長白柴胡。(R)阿爾泰柴胡。(S)抱莖柴胡。(T)空心柴胡。(U)秦嶺柴胡。(V)大葉柴胡。(W)短傘大葉柴胡。(X)紫花大葉柴胡。(Y)馬爾康柴胡。(Z)竹葉柴胡。(AA)馬尾柴胡。(BB)有柄柴胡。(CC)麗江柴胡。(DD)紅柴胡。(EE)興安柴胡。(FF)黑柴胡。(GG)小柴胡。(HH)三輻柴胡。(II)銀州柴胡。(JJ)云南柴胡。標尺=0.3 mm。Showing variation in mericarp shape, vascular bundles, secretary oil ducts, endosperm shape, commissural width and carpophores. (A) B. angustissimum. (B) B. aureum. (C) B. bicaule. (D) B. candollei. (E) B. chinense. (F) B. chinense f. octoradiatum. (G) B. chinense f. pekinense. (H) B. commelynoideum. (I) B. condensatum. (J) B. dalhousianum. (K) B. densiflorum. (L) B. dielsianum. (M) B. euphorbioides. (N) B. exaltatum. (O) B. gracilipes. (P) B. gracillimum. (Q) B. komarovianum. (R) B. krylovianum. (S) B. longicaule var. amplexicaule. (T) B. longicaule var. franchetii. (U) B. longicaule var. giraldii. (V) B. longiradiatum. (W) B. longiradiatum var. breviradiatum. (X) B. longiradiatum var. porphyranthum. (Y) B. malconense. (Z) B. marginatum. (AA) B. microcephalum. (BB) B. petiolulatum. (CC) B. rockii. (DD) B. scorzonerifolium. (EE) B. sibiricum. (FF) B. smithii. (GG) B. tenue. (HH) B. triradiatum. (II) B. yinchowense. (JJ) B. yunnanense. Scale bar=0.3 mm.

伴生油管：伴生油管(rib duct)為與維管束相伴的油管，存在于分果的脊內維管束的外側，所研究的物種通常無伴生油管，如金黃柴胡，葡枝柴胡及密花柴胡(圖2B, J, K)。少數物種，錐葉柴胡，北柴胡, 大苞柴胡及長白柴胡有直徑小的伴生油管(圖1D)，他們可存在分果的5個脊(圖2B, M)，或僅1或2個脊(圖2E, Q)。

非伴生油管(簡稱油管)：非伴生油管(vitta)存在于中果皮，不與維管束相伴。研究的柴胡均具油管，油管不分支(圖1D)或分支(圖1E)。多數物種的油管不分支(unbranching vittae)，他們規(guī)則地分布在溝里，即兩個脊之間(vallecular vitta)和結合面(commissural vitta)(圖1C, I, 2C)。油管數目在不同物種有變化，簇生柴胡，密花柴胡，新疆柴胡，阿爾泰柴胡，小柴胡的油管為每個溝里1個，結合面2個，每個分果共有6個油管(圖2I, K, N, R, GG)。多數物種分果的油管數量多于6，如錐葉柴胡，川滇柴胡及太白柴胡，溝里油管2~3個，結合面油管2~4個，每個分果具12~14個油管(圖2C, D, L)。大苞柴胡及細柄柴胡溝里的油管4~5個，結合面油管4~6個，每個分果具22~24個油管(圖2M, O)。油管通常與分果的長度近似(圖1C)，但短油管存在于紫花鴨趾柴胡，大苞柴胡及大葉柴胡(圖1D)。分支油管(branching vitta)不規(guī)則地分布在中果皮(圖1E)，果實橫切面油管的位置不定(圖1J)，這些分支油管存在于線葉柴胡、北柴胡、百花山柴胡、北京柴胡、長白柴胡及紅柴胡(圖2A, E~G, Q, DD)。

種皮：幾乎所有物種的種皮由1層薄壁細胞構成，細胞較大，長方形(圖1F, G)，但紫花大葉柴胡的種皮可見2層細胞(圖1H)。

胚乳：胚乳(endosperm)在結合面通常平直，如葡枝柴胡，密花柴胡及太白柴胡(圖2J-L)，但少數物種的胚乳微凹，如川滇柴胡，麗江柴胡及云南柴胡(圖2D, CC, JJ) 。

結合面，心皮柄及結晶：結合面(commissure)為2分果的結合處，所有物種具有較窄的結合面，其寬度為果寬的10%~20%。心皮柄(carpophore)通常較細(直徑小于0.1 mm)，在結合面2個彼此相對，各支持1個分果(圖1A, K)，如馬爾康柴胡及竹葉柴胡(圖2Y, Z)。但纖細柴胡及細柄柴胡的心皮柄較粗(直徑大于 0.2 mm)(圖2O, P)。細柄柴胡的心皮柄僅在頂端裂開(圖1B)，因而果實中部橫切面顯示為單心皮柄(圖1L)。所有物種缺少結晶(crystal)。

3討論

分果形狀：與柴胡類似，芹亞科及變豆菜亞科許多類群(如Alepidea及Hacquetia)分果的橫切面近圓形[37]。然而參棕亞科的果實明顯兩側壓扁，牽環(huán)花亞科除了幾個屬(如Bowlesia及Oschatzia)的果實略微背腹壓扁外，其他的果實明顯兩側壓扁[42]。

表皮細胞外壁：芹亞科多數物種表皮細胞外壁平直，但突起的外壁普遍存在于變豆菜亞科(如Actinolema macrolema，Astrantia maxima，Eryngium armatum，Hacquetia epipactis及Sanicula lamelligera)，Heteromorpheae(Anginon，Glia及Heteromorpha)及幾個其他芹亞科類群(如Eremodaucus lehmannii，Spermolepis patens)[33]。果實表皮細胞外具厚角質層的幾種柴胡均生長在較干旱的地方，可見角質層的厚度與物種生長的環(huán)境有關。

內果皮：內果皮在芹亞科多為1層薄壁細胞構成[1]，然而這一亞科的基礎類群，如非洲的Heteromorpheae(Anginon swellendamense，Glia prolifera)及Lichtensteinia lacera的內果皮輕微木化。這種輕微木化的內果皮還存在變豆菜亞科及相關類群(如Eryngium planum，Sanicula lamelligera，Arctopus echinatus，Polemanniopsis marlothii及Steganotaenia araliacea)[33,37,43]。參棕亞科和牽環(huán)花亞科的內果皮由多層木化細胞構成[1,33]。

伴生油管及非伴生油管：分泌油管在Baumann[44]，Tikhomitov[45]及Eyde和Tseng[46]的系統(tǒng)學研究起著重要的作用。芹亞科許多類群無明顯的伴生油管，然而伴生油管普遍存在于芹亞科基礎類群(Heteromorpheae，Annesorhiza及Chamarea)，變豆菜亞科，參棕亞科及牽環(huán)花亞科，其中變豆菜亞科及相關類群(如Sanicula，Alepidea，Polemanniopsis，Steganotaenia，Marlothiella及Lichtensteinia)的伴生油管明顯較大[30,33,37-38,43,47-48]。芹亞科許多類群(如Angelica及Peucedanum)不分支油管在溝里可多于1個，結合面多于2個，然而Heteromorpheae，Annesorhiza及Chamarea的油管數通常溝里只有1個，結合面2個[33,47-49]。分支油管存在于牽環(huán)花亞科(Dickinsia，Hermas，Klotzschia)，變豆菜亞科及相關類群(Alepidea，Sanicula，Eryngium及Steganotaenia)[37-38,48]，靠近Heteromorpheae的馬達加斯加特有物種Pseudocarpum laxiflorum，然而在芹亞科若果實中油管分支，總是與不分支油管同時存在(如Ferula)。

結晶：草酸鈣單晶或晶簇出現在五加科(Araliaceae)的一些薄壁組織[50],單晶存在于參棕亞科和牽環(huán)花亞科緊挨內果皮的中果皮[1,30,37-38,43,51]，但不存在于變豆菜亞科及芹亞科。Burtt[52]指出芹亞科如果有結晶，只發(fā)生在結合面。然而我們觀察到芹亞科所有基礎類群(Heteromorpheae，Annesorhiza，Chamarea，Lichtenisteinia及Marlothiella)均具有晶簇。此外晶簇還普遍存在在變豆菜亞科及相關類群(Steganotaenia及Polemanniopsis)及牽環(huán)花亞科(如Huanaca andina及Bolax caespitosus)的中果皮，但芹亞科其他類群多無結晶[35,38,47]。

種皮：種皮被認為是有價值的分類特征[53-55]。多數芹亞科的種皮由1層細胞構成，但我們觀察到多于1層細胞的種皮存在于變豆菜亞科(如Alepidea natalensis及Eryngium hookeri)，非洲的Heteromorpheae(如Anginon pumilum)，Annesorhiza(如Annesorhiza wilmsii)，Chamarea(如Chamarea capensis),及Itasina(Itasina filifolia)。Magee等[30]的研究顯示Itasina與Annesorhiza的親緣關系較近。此外多于1層細胞的種皮還存在于Bupleirumbaldense(產于不列顛群島)，B.distichophyllum(產于印度)及B.rigidum(產于阿爾及利亞)(未發(fā)表)。王艷杰和申家恒[56]指出北柴胡具一層珠被，然而這個屬的其他物種的珠被結構尚不知曉。

心皮柄：心皮柄來源于腹束，連同周圍的非維管組織一起支持著心皮[57]。芹亞科多數物種具2個心皮柄，類似于細柄柴胡(圖1B)的一個頂端分裂的心皮柄在芹亞科見于Eremodaucus及Scandix(未發(fā)表)，但廣泛存在于牽環(huán)花亞科(如Bolax，Dickinsia，Hermas及Huanaca)及變豆菜亞科(Alepidea及Arctopus)[40]。

葉及導管分子：單葉是參棕亞科，牽環(huán)花亞科，變豆菜亞科及柴胡屬的主要特征[1,40]，但亦存在于Heteromorpheae(Anginon及Heteromorpha)[58]。同傘形科木本類群一樣柴胡屬的導管分子通常短，具單穿孔板[59-62]，此外柴胡屬及非洲的Heteromorpha，Anginon，Glia及Polemannia的導管具螺紋增厚[60,62]。Stepanova和Oskolski[5]指出導管壁螺紋增厚應視為芹亞科的原始類型。

柴胡屬果實的多數特征同樣存在于芹亞科的其他類群(如橫切面近圓形，中果皮有伴生油管及規(guī)則分布的非伴生油管。中果皮無結晶。心皮柄2個)，然而有些特征(如油管呈分支狀，種皮由2層細胞構成)僅見于芹亞科的基礎類群及傘形科的其他亞科，因而果實結構的研究為分子系統(tǒng)學將柴胡屬放在靠近芹亞科的基礎類群，即這一亞科其他類群的基礎位置提供了形態(tài)學依據，進而為進一步研究芹亞科系統(tǒng)學提供了果實形態(tài)學基礎。

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http://cyxb.lzu.edu.cn

常修奇，劉玫，程薪宇，王宇婷，魏雪瑩，王雪微. 中國傘形科柴胡屬果實結構的系統(tǒng)學價值.草業(yè)學報, 2015, 24(10): 108-119.

CHANG Xiu-Qi, LIU Mei, CHENG Xin-Yu, WANG Yu-Ting, WEI Xue-Ying, WANG Xue-Wei. The phylogenetic significance of fruit structures inBupleurumof the family Apiaceae. Acta Prataculturae Sinica, 2015, 24(10): 108-119.

通訊作者*Corresponding author.E-mail: m.r.liu@126.com

作者簡介：常修奇(1991-)，男，黑龍江雙鴨山人，在讀碩士。E-mail: goalhia420@163.com

基金項目：國家自然科學基金(31270235和31070169)資助。

收稿日期：2015-01-29；改回日期：2015-04-30

DOI：10.11686/cyxb2015067