張代玉,駱 凱,吳 凡,王彥榮,張吉宇(草地農(nóng)業(yè)生態(tài)系統(tǒng)國家重點(diǎn)實(shí)驗(yàn)室 蘭州大學(xué)草地農(nóng)業(yè)科技學(xué)院,甘肅 蘭州 730020)
被子植物閉花授粉的研究進(jìn)展
張代玉,駱 凱,吳 凡,王彥榮,張吉宇
(草地農(nóng)業(yè)生態(tài)系統(tǒng)國家重點(diǎn)實(shí)驗(yàn)室 蘭州大學(xué)草地農(nóng)業(yè)科技學(xué)院,甘肅 蘭州 730020)
閉花授粉(cleistogamy,CL)是一種完全自交的繁殖系統(tǒng),屬于最典型的自花授粉,近年來已經(jīng)受到人們?cè)絹碓蕉嗟年P(guān)注。本文概述了閉花授粉的類型、花器官變異、在被子植物中的分布、系統(tǒng)進(jìn)化和相關(guān)調(diào)控基因。閉花授粉分為兼性閉花授粉、完全閉花授粉和誘變閉花授粉3種類型,其中兼性閉花授粉所占的比例最大,約占總數(shù)的77.3%?;谶@些分類,目前閉花授粉現(xiàn)象存在于53個(gè)科236個(gè)屬705種被子植物中。與開花授粉(chasmogamy,CH)相比,CL花器官的數(shù)目相對(duì)減少,漿片退化。控制CL的基因有單基因、雙基因和3對(duì)基因。無芒隱子草(Cleistogenessongorica)為典型的兼性閉花授粉植物,其CH和CL花存在明顯的形態(tài)差異,種子具有異型性。通過對(duì)禾本科內(nèi)植物進(jìn)行系統(tǒng)進(jìn)化分析發(fā)現(xiàn),隱子草屬(Cleistogenes)和雙稃草屬(Diplachne)的親緣關(guān)系最近,同屬于三齒稃亞族(Tridentinae)。這些信息為理解閉花授粉和其基因的生態(tài)學(xué)意義提供了寶貴的參考價(jià)值。
閉花授粉;開花授粉;系統(tǒng)進(jìn)化;閉花授粉相關(guān)基因;被子植物
閉花授粉(cleistogamy,CL)由開花授粉(chasmogamy,CH)進(jìn)化而來[1],是花器官發(fā)育的一種變態(tài)。目前,在高粱(Sorghumbicolor)[2]、大麥(Hordeumvulgare)[3]、水稻(Oryzasativa)[4]等多種作物中均發(fā)現(xiàn)有CL現(xiàn)象。Darwin[5]對(duì)鳳仙花屬(Impatiens)、酢漿草屬(Oxalis)及堇菜屬(Viola)3個(gè)屬的CL進(jìn)行了描述,并認(rèn)為CL是自然選擇的結(jié)果。此后,CL的遺傳基礎(chǔ)、生理機(jī)制和進(jìn)化對(duì)群體遺傳結(jié)構(gòu)的影響逐漸受到了植物學(xué)家和形態(tài)學(xué)家的關(guān)注[6-8]。目前CL的研究已經(jīng)在50科228屬693種中進(jìn)行了報(bào)道[9];尤其1970年以來,JSTOR全文庫(http://www.jstor.org,Journal Storage)上發(fā)表的有關(guān)CL的文章數(shù)目明顯增加(圖1)。另外,CL能使植物避免受到外來花粉干擾而保持純種,因此在不影響其農(nóng)藝性狀的前提下,培育具有閉花授粉特性的轉(zhuǎn)基因新品種是抑制基因漂流、減少環(huán)境風(fēng)險(xiǎn)的一種理想策略[10]。鑒于閉花授粉機(jī)制逐漸受到廣泛關(guān)注,為使人們進(jìn)一步了解被子植物閉花授粉目前的研究現(xiàn)狀、今后的發(fā)展趨勢(shì)和應(yīng)用前景,在前人對(duì)被子植物閉花授粉研究的基礎(chǔ)上,搜集整理了此領(lǐng)域的最新成果,并結(jié)合閉花授粉在轉(zhuǎn)基因作物上的重要性,簡要總結(jié)了閉花授粉的分類、分布、系統(tǒng)進(jìn)化及相關(guān)基因的研究進(jìn)展。
圖1 1910-2015年引用“閉花授粉”或“閉花授粉的”文章數(shù)目Fig. 1 Number of papers published from 1910-2015 that cite either “cleistogamy” or “cleistogamous”
閉花授粉是指在花朵未開放時(shí)成熟花粉粒在花粉囊內(nèi)萌發(fā),花粉管穿出花粉囊,伸向柱頭,進(jìn)入子房,把精子送入胚囊并完成授粉的過程。早在1906年,Hackel[11]對(duì)特有閉花授粉、兩性閉花授粉和無性器官閉花授粉3種閉花授粉方式進(jìn)行了區(qū)分。1981年,Lord[12]將Hackel對(duì)閉花授粉的分類方式歸納為“真”閉花授粉,并對(duì)所有閉花授粉方式進(jìn)行了分類:1)花前閉花授粉,主要指花授粉發(fā)生在開花之前,這在栽培豆科、禾本科植物和其它農(nóng)作物中普遍存在;2)假閉花授粉,開花期間花瓣不開放而完成的授粉;3)完全閉花授粉,僅產(chǎn)生CL花的授粉方式;4)“真”閉花授粉,CH花雄蕊和花冠減小形成CL花,這是由于同一品種或單株CH和CL花的不同起源所形成。由于Lord所觀察的植物生長于非自然條件下,Darwin對(duì)這一分類方式提出了質(zhì)疑。直到2007年,Culley和Klooster[9]根據(jù)CL發(fā)育過程又將閉花授粉分為3種類型:兼性閉花授粉(dimorphic cleistogamy,DC)、完全閉花授粉(complete cleistogamy,CC)和誘變閉花授粉(induced cleistogamy,IC),這種分類方式已經(jīng)被廣泛認(rèn)可并使用。
1.1 兼性閉花授粉
兼性閉花授粉類型和Lord[12]對(duì)閉花授粉分類中的“真”閉花授粉一致,CH和CL花的形態(tài)學(xué)差異源自它們不同的發(fā)育途徑。與CH花相比,CL花的花冠和雄蕊長度較短或雄蕊數(shù)目較少。該類型的CH和CL兩種花可在同一植株的不同位置同時(shí)存在,或者按照一定的時(shí)間順序相繼產(chǎn)生。CH和CL花的出現(xiàn)順序取決于植物物種,草本植物毛竹(Violapubescens)的CH花僅在早春產(chǎn)生,CL花在其幾周之后出現(xiàn)[8];而其它植物種的CL花早于CH出現(xiàn)。CH花的出現(xiàn)是由早春特定的光周期和溫度引起,例如二型花屬植物Dichantheliumclandestinum是春季產(chǎn)生CL花,而在晚夏產(chǎn)生CH花[13]。筆者試驗(yàn)過程中在無芒隱子草(Cleistogenessongorica)中也發(fā)現(xiàn),葉鞘內(nèi)CL花早于CH花產(chǎn)生。
1.2 完全閉花授粉
完全閉花授粉的植株僅產(chǎn)生CL花,該授粉類型存在于多個(gè)植物物種。例如,日本科學(xué)家新發(fā)現(xiàn)的植物黑島天麻(Gastrodiakuroshimensis)只產(chǎn)生CL花[14];夏威夷地方性物種Schiedeatrinervis的花在授粉過程中一直處于閉合狀態(tài)[15]。然而大部分CL植株的確定只是基于一部分單株在非自然條件下(例如溫室)的觀察。因此,確定一個(gè)植物種是否為完全閉花授粉,調(diào)查的對(duì)象必須包括自然環(huán)境中多個(gè)單株以確保無CH花的產(chǎn)生。
1.3 誘變閉花授粉
誘變閉花授粉是指CH花因環(huán)境阻礙未能開放,進(jìn)而轉(zhuǎn)變?yōu)镃L花,這和Lord分類中的假閉花授粉相同。與兼性閉花授粉相比,該類型的CH和CL花并無形態(tài)學(xué)差異,而且CH花轉(zhuǎn)變?yōu)镃L花的速度較快。在此分類中,干旱和溫度是促進(jìn)CL花產(chǎn)生的主要因素。例如,一些東北極羊茅屬(Festuca)的物種只有在低溫和相對(duì)濕度較高的條件下才能由CH花轉(zhuǎn)變CL花[16]。夏威夷馬齒莧屬(Portulaca)植物在光照和溫度都降低的條件下,導(dǎo)致花未能張開,進(jìn)而產(chǎn)生CL花[17]。也有研究表明,水稻經(jīng)30 ℃高溫連續(xù)處理4周后,其授粉類型可由CH轉(zhuǎn)變?yōu)镃L[18]。
閉花授粉廣泛存在于被子植物中,據(jù)不完全統(tǒng)計(jì),在被子植物的53科236屬705種中均發(fā)現(xiàn)閉花授粉(表1)。統(tǒng)計(jì)結(jié)果還發(fā)現(xiàn),有關(guān)閉花授粉的報(bào)道多集中在單子葉植物的禾本科(Poaceae)(326種)、蘭科(Orchidaceae)(25種)和雙子葉植物的堇菜科(Violaceae)(83種)、豆科(Fabaceae)(62種)及爵床科(Acanthaceae)(19種)中,這和Darwin的歸類稍有差異,Darwin指出閉花授粉普遍存在于豆科、爵床科和金虎尾科(Malpighiaceae)中[5]。在屬的水平上,有關(guān)閉花授粉的報(bào)道主要出現(xiàn)在針茅屬(Stipa)(41種)、堇菜屬(Viola)(80種)、二型花屬(Dichanthelium)(19種)、扁芒草屬(Danthonia)(17種)、裂稃草屬(Schizachyrium)(17種)、喇叭茉莉?qū)?Acleisanthes)(16種)、鼠茅屬(Vulpia)(15種)、凌風(fēng)草屬(Briza)(14種)、車前屬(Plantago)(13種)以及胡枝子屬(Lespedeza)(13種)這10個(gè)屬中。在所有的閉花授粉類型中,兼性閉花授粉所占的比例最大,約占總數(shù)的77.3%,這與Plitmann[53]得出的結(jié)論相似;完全閉花授粉(72種,10.4%)和誘變閉花授粉(81種,8.8%)分散于多個(gè)科和屬種;僅有24種閉花授粉植物因缺少相關(guān)信息而尚未鑒定出閉花授粉類型。
CH和CL花數(shù)在不同植物單株、群體內(nèi)和群體間所占的比例不同。一些植物單株上的CH/CL比值與植株的個(gè)體發(fā)育以及環(huán)境因素密切相關(guān)。Campbell等[19]對(duì)柔枝莠竹(Microstegiumvimineum)的CH/CL比值進(jìn)行了統(tǒng)計(jì)分析,在陽光充足、種群競爭壓力小的環(huán)境下,高大植株的CH/CL比值小于矮小植株;相反,光線不足且種群競爭壓力大的森林中矮小植株的CH/CL比值達(dá)到最高。一些植物的CH/CL比值在種群內(nèi)也會(huì)發(fā)生波動(dòng)。Culley[8]在毛竹(Phyllostachysheterocyda)群體內(nèi)發(fā)現(xiàn),所有單株在第1年可同時(shí)產(chǎn)生CH和CL兩種授粉類型,但是第2年CH和CL的分配會(huì)發(fā)生變化。其中74%的單株可同時(shí)產(chǎn)生CH和CL兩種授粉類型,13%和9%的單株分別產(chǎn)生CH和CL花,剩余的4%僅進(jìn)行營養(yǎng)生長。在鳳仙花屬植物Impatienspallida和I.biflora群體內(nèi)對(duì)CL百分率(CL花數(shù)占總花的數(shù)目的比例)的調(diào)查發(fā)現(xiàn),其CL百分率分別為69%~100%和80%~98%[21]。
CL植物的花器官相對(duì)CH植物較小,數(shù)目也相對(duì)較少。CL的形成原因有一部分是由CH轉(zhuǎn)變而來,另一部分是為了適應(yīng)由漿片敗育等原因引起的花閉合現(xiàn)象。
與CH植物的花相比,CL花中雄蕊、花藥和花瓣的數(shù)目較少,漿片通常很小或者完全缺失。雄蕊退化是CL花的主要特征,利用掃描電鏡觀察兩型豆(Amphicarpaeaedgeworthii)花的個(gè)體發(fā)育過程發(fā)現(xiàn),CL花的雄蕊在發(fā)育過程中出現(xiàn)退化現(xiàn)象,僅1/5的花藥可以正常發(fā)育并完成授粉[54];在紫花地丁(Violaphilippica)中發(fā)現(xiàn),經(jīng)14 h光照誘變產(chǎn)生的CL花的花瓣缺失,并且花藥由原來的5個(gè)減少為2個(gè)[55]。漿片吸水膨脹,將外稃向外推開,同時(shí)將內(nèi)稃向內(nèi)壓擠,從而使外稃和內(nèi)稃的鉤合點(diǎn)松開并最終完成授粉,這是調(diào)控花開閉的關(guān)鍵因素[56]。CL和CH兩種大麥栽培品種的比較研究發(fā)現(xiàn),漿片于白色花藥期開始表現(xiàn)出差異,綠色花藥期差異達(dá)到最大,CL漿片厚度不及CH漿片一半[57];筆者在無芒隱子草花形態(tài)學(xué)的觀察中也發(fā)現(xiàn),CH第1漿片和第2漿片的厚度分別為46.38和60.67 μm,是CL相同部位的1.58和2.25倍,而CL花的花藥長度顯著小于CH(P<0.01)。
種子異型性(seed polymorphism)是指同一植株的不同部位產(chǎn)生不同形態(tài)或行為種子的現(xiàn)象。異型性種子之間往往在大小、產(chǎn)量等生物學(xué)特征以及休眠和萌發(fā)等生態(tài)行為上存在明顯差異。大部分植物的異型性種子具有不同生態(tài)行為,這種特點(diǎn)在被子植物中普遍存在[58]。因此,種子異型性被認(rèn)為是許多植物適應(yīng)多樣環(huán)境的重要策略,在生態(tài)進(jìn)化方面具有重要的研究價(jià)值。
閉花授粉植株的種子具有異型性。如紅毛菜(Triplasispurpure)通過CL產(chǎn)生的種子產(chǎn)量至少占總產(chǎn)量的72%,但CH的圓錐花序的種子產(chǎn)量最多占28%[59];無芒隱子草葉鞘內(nèi)CL小穗的種子產(chǎn)量占總產(chǎn)量的82%[60-61];類似的現(xiàn)象在韓信草(Scutellariaindica)等閉花授粉物種中均有報(bào)道[62]。不同物種的CL和CH種子的休眠和萌發(fā)生態(tài)行為不同。如紅毛菜頂穗CH種子萌發(fā)率明顯高于CL葉鞘內(nèi)種子萌發(fā)率,CL小穗中從下往上不同節(jié)種子僅在萌發(fā)時(shí)間上存在差異,其最終發(fā)芽率不隨節(jié)間的變化而變化[63]。Imanishi等[64]在低溫儲(chǔ)藏處理對(duì)芡實(shí)(Euryaleferox)種子休眠的研究表明,CL種子小,在低溫儲(chǔ)藏90 d即可達(dá)到最大萌發(fā)率;而CH種子較大,需要180 d才能達(dá)到。無芒隱子草不同節(jié)間部位種子均存在休眠;經(jīng)85 ℃處理后CL種子的的萌發(fā)率明顯高于CH種子[65-66]。
閉花授粉在禾本科中的分布最多,該科有88屬326種中皆存在閉花授粉現(xiàn)象,因此從分子水平上研究和分析禾本科閉花授粉植物的系統(tǒng)進(jìn)化,可為閉花授粉系統(tǒng)進(jìn)化提供分子生物學(xué)依據(jù)。選取禾本科88個(gè)屬植物,從美國國立生物技術(shù)信息中心(National Center for Biotechnology Information,NCBI)獲得rbcL和matK兩個(gè)葉綠體基因序列,采用MEGA軟件的ML分析(1 000次重復(fù))進(jìn)行系統(tǒng)進(jìn)化分析(圖2)。其中,鼠尾栗屬(Sporobolus)、Tridens、三毛草屬(Trisetum)、發(fā)草屬(Deschampsia)、Thyridolepis、早熟禾屬(Poa)、凌風(fēng)草屬(Briza)、Brachyachne、單花針茅屬(Nassella)、Piptochaetium、針茅屬(Stipa)11個(gè)屬含有兼性閉花授粉和完全閉花授粉兩種授粉類型(DC和CC)。而穗草屬(Garnotia)、腸須草屬(Enteropogon)、Tetrapogon、尖稃草屬(Acrachne)、Habrochloa等僅產(chǎn)生完全閉花授粉類型(CC)。隱子草屬(Cleistogenes)和雙稃草屬(Diplachne)親緣關(guān)系最近,同屬于三齒稃亞族(Tridentinae)。
CL是植物在長期進(jìn)化過程中有效抵御不良環(huán)境的一種發(fā)育策略。CL可以擴(kuò)大對(duì)干旱、高溫等惡劣環(huán)境的適應(yīng)性。Abdel-Ghani等[67]發(fā)現(xiàn)大麥在處于極度干旱時(shí)仍可繼續(xù)完成授粉;Miranda等[68]的研究也表明,處于不同水分條件下的Ruelliasubsessilis在干旱季節(jié)進(jìn)行CL,而CH發(fā)生在雨季。Koike等[18]對(duì)CL水稻高溫處理4 h后發(fā)現(xiàn),其可育比率高于CH植株,并認(rèn)為CL植株的高可育性是由花穎片氣孔的蒸騰作用而引起的。CL轉(zhuǎn)基因新品種是減少環(huán)境風(fēng)險(xiǎn)的一種理想策略。無芒隱子草已被證實(shí)為一種極抗旱的荒漠旱生植物,可在年降水量為100 mm的地區(qū)生長,通過研究其抗旱生理生態(tài)和機(jī)理,利用克隆的抗旱基因顯著改良了擬南芥(Arabidopsisthaliana)和紫花苜蓿(Medicagosativa)等植物的抗逆性[69-71]。
自1983年出現(xiàn)第1個(gè)轉(zhuǎn)基因植物后,基因轉(zhuǎn)化因其基因資源多樣化、物種間基因流動(dòng)的可能性等優(yōu)點(diǎn)而深受人們關(guān)注,但轉(zhuǎn)基因植物和野生種間的基因漂流可能危及生態(tài)平衡。近年來,閉花授粉被看作是一種阻止基因漂流的理想工具而備受關(guān)注[72]。至今,閉花授粉的遺傳已被證實(shí)受單基因、雙基因和3個(gè)基因控制。
單隱性控制的CL基因遺傳方式已經(jīng)在水稻[4]、木豆(Cajanuscajan)[73]、日本二棱大麥(H.vulgaressp.)[3]、硬粒小麥(Triticumturgidum)[74]中進(jìn)行了報(bào)道。高粱[2]和大豆(Glycinemax)[75]的CL受雙基因控制。受3個(gè)隱性基因控制的CL僅在小麥中進(jìn)行了報(bào)道,該植物的CL基因在綠色花粉、黃色花粉和開花期的基因表達(dá)量達(dá)到最高[76]。大麥閉花授粉的表達(dá)受等位基因cly1和cly2控制,其中隱性基因cly1決定漿片能否吸水膨脹,顯性基因cly2控制開花期能否提前,它們位于染色體2HL的同一位置[77]。
圖2 禾本科閉花授粉植物系統(tǒng)發(fā)育樹Fig. 2 Phylogenetic tree of cleistogamous plants in Gramineae
注:含邊框的表示同時(shí)含有DC和IC兩種閉花授粉類型;黑色表示含DC閉花授粉類型;紅色表示僅包括CC閉花授粉類型;綠色表示尚未確定;圖中僅顯示大于50%的自展支持率。
Note:Orders in boldfaced, italic fonts enclosed within frames contain both DC and IC flowers; black bars indicate the presence of DC flowers; red bars indicate only CC flowers, and green line indicate uncertain flowers; only the nodes receiving bootstrap or jackknife support above 50% are indicated.
目前普遍認(rèn)為雙子葉植物花器官發(fā)育的ABCDE模型也基本適用于單子葉植物。在水稻中,A類基因[78-79]包括RAP1A(rice apetalalgene A)、RAP1B(rice apetalalgene B);B類基因[79-81]包括OsMADS2、OsMADS4和SPW1(superwoman1);C類基因[82-84]包括RAG(rice agamous)和DL(drooping leaf)類;D類基因[83]包括OsMADS13;E類基因[85-86]包括LHS、OsMADS5、OsMADS7和OsMADS8。目前在水稻中已發(fā)現(xiàn)了4種CL突變體類型(表2):d7(cleistoganous dwarf)、ld(t)(lodiculeless spikelet)、spw1-cls(superwoman1-cleistogamy)和cl7(t)[cleistogamy7(t)]。d7突變體漿片發(fā)育正常,內(nèi)、外穎交界處部分融合,致使花藥不外露,位于第7染色體長臂上。ld(t)突變體由于缺少漿片,致使開花期內(nèi)外穎不能被正常推開,ld(t)已定位在第1染色體的末端。spw1-cls突變體是由于SPW1第45位氨基酸發(fā)生錯(cuò)義突變,致使?jié){片發(fā)生變形,形成漿片穎片嵌合體,導(dǎo)致內(nèi)外穎不能打開。cl7(t)突變體花器官發(fā)育正常,內(nèi)外穎并沒有發(fā)生融合現(xiàn)象,由于細(xì)胞數(shù)量減少或者細(xì)胞變小引起株型、穗型、籽粒等性狀的改變,位于第7染色體的RM21964和RM234之間。
表2 水稻不同CL突變體的突變位置和特征Table 2 The position and characteristics of different rice mutants
雖然CL物種的研究在迅速發(fā)展,但由于大自然龐大的植物物種數(shù),許多未知的CL植物有待人們?nèi)グl(fā)掘和鑒定。而JSTOR目前報(bào)道的CL物種數(shù)目僅僅是其中很小的一部分,且其分類群的研究更是少之又少。對(duì)于已知的閉花授粉物種,多數(shù)研究主要集中在重要作物的生物學(xué)特性觀察、花器官形態(tài)學(xué)比較以及對(duì)環(huán)境適應(yīng)性的響應(yīng)等方面,對(duì)其產(chǎn)生和作用的機(jī)理未進(jìn)行深入研究。所以今后的研究可以從表型和現(xiàn)象觀察過度到更加深入的分子和機(jī)理方面,如CL物種的轉(zhuǎn)基因、其形成的機(jī)制以及系統(tǒng)進(jìn)化關(guān)系三方面進(jìn)行研究。
第一,挖掘更多CL特性基因并培育具有CL基因的轉(zhuǎn)基因新品種。CL小麥對(duì)穗部病害赤霉病的抵抗力比CH小麥更高[87],CL小麥完成授粉后,病蟲不易入侵。葡萄(Vitislabruscana)在環(huán)境適宜條件下進(jìn)行CH,但花期長時(shí)間遭遇陰雨或人為因素等則可通過CL完成繁衍后代的目的[88]。這種CL的特性是植物在長期進(jìn)化過程中有效抵御不良環(huán)境的一種發(fā)育策略。另外,由于CL的穎花不張開,花藥不外露,花粉不會(huì)向外傳播,能使植物避免外來花粉干擾而保持純種,因此在不影響其它農(nóng)藝性狀的前提下,培育具有CL特性的轉(zhuǎn)基因新品種是抑制基因漂流、減少環(huán)境風(fēng)險(xiǎn)的一種理想策略。
第二,發(fā)現(xiàn)閉花授粉的生殖和生態(tài)信息。多數(shù)物種的CL表達(dá)受環(huán)境影響,其中大部分物種的生殖和生態(tài)信息尚未報(bào)道。例如,對(duì)單株、群體內(nèi)部以及單株和群體之間花類型的變化進(jìn)行量化。另外,在一些物種中應(yīng)明確指出CL表達(dá)是受環(huán)境的單一影響還是受遺傳和環(huán)境相互作用的影響。
第三,對(duì)閉花授粉花的發(fā)育生物學(xué)進(jìn)行分析。在閉花授粉的3種類型中,分別對(duì)花類型的發(fā)育生物學(xué)進(jìn)行詳細(xì)描述,尤其對(duì)處于不同種群的花。然后通過進(jìn)一步研究環(huán)境對(duì)花基因表達(dá)的影響,可能會(huì)更好地理解影響花由CH轉(zhuǎn)變?yōu)镃L的直接因素和閉花授粉在被子植物中的進(jìn)化。
References:
[1] Kuhn M.Einige Bermerkungen über Vandellia und den Blüten Dimorphismus.Botanische Zeitung,1867,25:65-67.
[2] Merwine N C,Glurey L M,Blackwell K H.Inheritance of papery glume and cleistogamy in sorghum.Crop Science,1981,21(6):953-956.
[3] Kurauchi N,Makino T,Hirose S.Inheritance of cleistogamy-chasmogamy in barley.Barley Genetics Newsletter,1993,23:19.
[4] Nagao S,Takahashi M.Trial construction of twelve linkage groups in Japanese rice.Journal of the Faculty of Agriculture,1963,53(1):72-130.
[5] Darwin C.The Different Forms of Flowers on Plants of the Same Species.Chicago:University of Chicago Press,1877.
[6] McCall C,Mitchell-Olds T,Waller D M.Fitness consequences of outcrossing inImpatienscapensis:Tests of the frequency-dependent and sib-competition models.Evolution,1989,43(5):1075-1084.
[7] Bennington C C,McGraw J B.Natural selection and ecotypic differentiation inImpatienspallida.Ecological Monographs,1995,65(3):303-323.
[8] Culley T M.Reproductive biology and delayed selfing inViolapubescens(Violaceae), an understory herb with chasmogamous and cleistogamous flowers.International Journal of Plasticity,2002,163(1):113-122.
[9] Culley T M,Klooster M R.The cleistogamous breeding system:A review of its frequency,evolution,and ecology in angiosperms.The Botanical Review,2007,73(1):1-30.
[10] Hilu K W,Borsch T,Müller K,Soltis D E,Soltis P S,Savolainen T,Chase M W,Powell M P,Alice L E,Evans R,Sauquet H,Neinhuis C,Slotta T A B,Rohwer J G,Campbell C S,Chatrou L W.Angiosperm phylogeny based onmatKsequence information.American Journal of Botany,2003,90(12):1758-1776.
[11] Hackel E.über Kleistogamie bei den Gr?sern.Plant Systematics and Evolution,1906,56(5):180-186.
[12] Lord E M.Cleistogamy:A tool for the study of floral morphogenesis,function and evolution.Botanical Review,1981,47(4):421-449.
[13] Bell T J,Quinn J A.Relative importance of chasmogamously and cleistogamously derived seeds ofDichantheliumclandestinum(L.) Gould.Botanical Gazette,1985,46(2):252-258.
[14] Suetsugu S.Gastrodia kuroshimensis(Orchidaceae:Epidendroideae:Gastrodieae),a new mycoheterotrophic and complete cleistogamous plant from Japan.Phytotaxa,2016,278(3):265-272.
[15] Wagner W L,Weller S G,Sakai A.Monograph of schiedea(caryophyllaceae-alsinoideae).Systematic Botany Monographs,2005,72:1-169.
[16] Connor H E.Breeding systems in New Zealand grasses.New Zealand Journal of Botany,1998,36:471-476.
[17] Columbus T J.Morphology and leaf blade anatomy suggest a close relationship betweenBoutelouaaristidoidesandB. (Chondrosium)eriopoda(Gramineae:Chloroideae).Systematic Botany,1998,23(4):467-478.
[18] Koike S,Yamaguchi T,Ohmori S,Hayashi T,Yatou O,Yoshida H.Cleistogamy decreases the effect of high temperature stress at flowering in rice.Plant Production Science,2015,18(2):111-117.
[19] Campbell C S,Quinn J A,Cheplick G P,Timothy J B.Cleistogamy in grasses.Annual Review of Ecology and Systematics,1983,14:411-441.
[20] Cheplick G P.Plasticity of chasmogamous and cleistogamous reproductive allocation in grasses.Journal of Systematic and Evolutionary Botany,2005,23(1):286-294.
[21] Uphof J C T.Cleistogamic flowers.Botanical Review,1938,4(1):21-49.
[22] Cheplick G P.Biomass partitioning and reproductive allocation in the invasive, cleistogamous grassMicrostegiumvimineum:Influence of the light environment.Journal of the Torrey Botanical Society,2009,132:214-224.
[23] Maheshwari J K.Cleistogamy in angiosperms.Maheshwari P,Johri B,Vasil I.Proceedings of the Summer School of Botany.New Delhi:Ministry of Scientific Research and Cultural Affairs,1962:145-155.
[24] Suetsugu K.Gastrodiaflexistyloides(Orchidaceae),a new mycoheterotrophic plant with complete cleistogamy from Japan.Phytotaxa,2014,175(5):270-274.
[25] Hardy C R,Faden R B.Plowmanianthus,a new genus of Commelinaceae with five new species from tropical America.Systematic Botany,2004,29(2):316-333.
[26] Gilmartin A J,Brown G K.Cleistogamy inTillandsiacapillaries(Bromeliaceae).Biotropica,1985,17(3):256-259.
[27] Jacquemart A L,Desloover J R.The part taken by cleistogamy inNartheciumossifragumreproductive strategy.Flora,1992,187(1):67-72.
[28] Corff J L.Effects of light and nutrient availability on chasmogamy and cleistogamy in an understory tropical herb,Calatheamicans(Marantaceae).American Journal of Botany,1993,80(12):1392-1399.
[29] Kerner von M A.The Natural History of Plants:Their Forms,Growth,Reproduction,and Distribution.Olive F W(translation).London:Blackie & Son,1902.
[30] Culley T M.Inbreeding depression and floral type differences inViolacanadensis(Violaceae),a perennial herb with chasmogamous and cleistogamous flowers.Canadian Journal of Botany,2000,78(11):1420-1429.
[31] Marcussen T.A new violet species(Violaceae) from the south-west Alps.Botanical Journal of the Linnean Society,2003,142(1):119-123.
[32] Oakley C G.Inbreeding depression and mating system evolution in the perennial herbViolaseptemlobaand the evolutionary maintenance of cleistogamy.Master thesis.Tallahassee:Florida State University,2004.
[33] Forrest J,Thomson J D.Pollen limitation and cleistogamy in subalpineViolapraemorsa.Botany,2008,86(5):511-519.
[34] Havran J C.Violakauaensisvar.hosakae(Violaceae),a new variety of endemic Hawaiian violet.Phytokeys,2014,39(39):35-48.
[35] Kaul V,Koul A K, Sharma M C.The underground flower.Current Science,2000,78(1):39-44.
[36] Moyle L C,Olson M S,Tiffin P.Patterns of reproductive isolation in three angiosperm genera.Evolution,2004,58(6):1195-1208.
[37] Speroni G.On the causes of the differential seed production in the anficarpic speciesTrifoliumpolymorphum(Leguminosae).Boletin de la Sociedad Argentina de Botanica,2010,45(1):57-72.
[38] Levin R A.Taxonomic status ofAcleisanthes,Selinocarpus,andAmmocodon(Nyctaginaceae).Novon,2002,12(1):58-63.
[39] Primack R B.Evolutionary aspects of wind pollination in the genusPlantago(Plantaginaceae).New Phytologist,1978,81(2):449-458.
[40] Calvino A,Galetto L.Cleistogamy in the rare high Andean perennial herbCryptanthacapituliflora(Boraginaceae).Plant Systematics and Evolution,2003,237(1-2):41-50.
[41] Muhiddinov T I.Genetic specifics of the breeding of cotton varieties with cleistogamous flowers.Russian Journal of Genetics,2010,46(6):689-698.
[42] Kim I,Carr G D.Reproductive biology and uniform culture ofPortulacain Hawaii.Pacific Science,1990,44:123-129.
[43] van der Kloet S P.Biosystematic studies ofVacciniumsectionMacropelma(Ericaceae) in Hawaii.Pacific Science,1993,47(1):76-85.
[44] Keighery G J.Breeding systems of the Western Australian flora.West Australian Naturalist,1988,17(5):121-125.
[45] Pfeifer H W.Revision of the north and central American hexandrous species ofAristolochia(Aristolochiaceae).Annals of the Missouri Botanical Garden,1966,53:116-196.
[46] Liu B L,Yang X.Characterization, efficient transformation and regeneration ofChiritapumila(Gesneriaceae), a potential evo-devo model plant.Plant cell,Tissue and Organ Culture,2014,118(2):357-371.
[47] Kadono Y,Schneider E L.The life history of theEuryaleferoxSalisb. in southwestern Japan with special reference to reproductive ecology.Plant Species Biology,1987,2(1-2):109-115.
[48] Khosla C,Shivanna K R,Mohan Ram H Y.Cleistogamy inGriffithellahookeriana(Podostemaceae).South African Journal of Botany,2001,67(2):320-324.
[49] Sehgal A,Sethi M,Ram H Y.Development of the floral shoot and pre-anthesis cleistogamy inHydrobryopsissessilis(Podostemaceae).Botanical Journal of the Linnean Society,2009,159(2):222-236.
[50] Kulkarni R N,Baskaran K.From herkogamy to cleistogamy-development of cleistogamy in Periwinkle.Journal of Heredity,2013,104(1):140-148.
[51] Ginwal H S.Inbreeding depression inEucalyptustereticornisSm. due to cleistogamous flowering.New Forests,2010,40(2):205-212.
[52] Martín R P.Seed formation and pollination system inCuscutaobtusiflora:First record of preanthesis cleistogamy in parasitic plants and some functional inferences.Flora,2009,204(3):228-237.
[53] Plitmann U.Distribution of dimorphic flowers as related to other elements of the reproductive strategy.Plant Species Biology,1995,10(1):53-60.
[54] Zhang Y,Yang J,Rao G Y.Comparative Study on the aerial and subterranean flower development inAmphicarpaeaedgeworthiiBenth.(Leguminosae:Papilionoideae), an amphicarpic species.International Journal of Plant Sciences,2006,167(5):943-949.
[55] Li Q X,Huo Q D,Wang J,Zhao J,Sun K,He C.Expression of B-class MADS-box genes in response to variations in photoperiod is associated with chasmogamous and cleistogamous flower development inViolaphilippica.BMC Plant Biology,2016,16:151.
[56] Heslop-Harrison Y,Heslop-Harrison J S.Lodicule function and filament rxtension in the grasses:Potassium ion movement and tissue specialization.Annals of Botany,1996,77:573-582.
[57] Nair S K,Wang N,Turuspekov Y,Pourkheirandish M,Sinsuwongwat S,Chen G X,Sameri M,Tagiri A,Honda I,Watanabe Y,Kanamori H,Wicker T,Stein N,Nagamura Y,Matsumoto T,Komatsuda T.Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage.PNAS,2010,107:490-495.
[58] Venable D L.The evolutionary ecology of seed heteromorphism.The American Naturalist,1985,126(5):577-595.
[59] Cheplick G P.Cleistogamy and seed heteromorphism inTriplasispurpurea(Poaceae).Bulletin of the Torrey Botanical Club,1996,123(1):25-33.
[60] 邰建輝,王彥榮,陳谷.無芒隱子草種子萌發(fā)、出苗和幼苗生長對(duì)土壤水分的響應(yīng).草業(yè)學(xué)報(bào),2008,17(3):105-110. Tai J H,Wang Y R,Chen G.Responses of seed germination,seedling emergence and seedling growth inCleistogenessongoricato soil water content.Acta Pratacultura Sinica,2008,17(3):105-110.(in Chinese)
[61] 賈存志.不同施氮和收獲方式對(duì)無芒隱子草種子產(chǎn)量和質(zhì)量的影響.蘭州:蘭州大學(xué)碩士學(xué)位論文,2015:9-11. Jia C Z.Effects of nitrogen application and harvest methods on seed yield and quality ofCleistengenessongorica.Master thesis,Lanzhou:Lanzhou University,2015.(in Chinese)
[62] Sun M.Cleistogamy inScutellariaindica(Labiatae):Effective mating system and population genetic structure.Molecular Ecology,1999,8(8):1285-1295.
[63] Cheplick G P,Sung L Y.Effects of maternal nutrient environment and maturation position on seed heteromorphism, germination, and seedling Growth inTriplasispurpurea(Poaceae).International Journal Plant Science,1998,159(2):338-350.
[64] Imanishi A,Imanishi J.Seed dormancy and germination traits of an endangered aquatic plant species,EuryaleferoxSalisb.(Nymphaeaceae).Aquatic Botany,2014,119:80-83.
[65] 魏學(xué),王彥榮,胡小文,武艷培.無芒隱子草不同節(jié)間部位的種子休眠對(duì)高溫處理的響應(yīng).草業(yè)學(xué)報(bào),2009,18(6):169-173. Wei X,Wang Y R,Hu X W,Wu Y P.Response to high temperature ofCleistogenessongoricaseed dormancy from different positions.Acta Prataculturae Sinice,2009,18(6):169-173.(in Chinese)
[66] 魚小軍,王彥榮,曾彥軍,蘇德.溫度和水分對(duì)無芒隱子草和條葉車前種子萌發(fā)的影響.生態(tài)學(xué)報(bào),2004,24(5):883-887. Yu X J,Wang Y R,Zeng Y J,Su D.Effects oftem perature and osm otic potentialon seed germ ination ofCleistogenessongoricaandPlantagolessingii.Acta Ecologica Sinice,2004,24(5):883-887.(in Chinese)
[67] Abdel-Ghani A H,Parzies H K,Omary A,Geiger H.Estimating the outcrossing rate of barley landraces and wildbarley populations collected from ecologically different regions of Jordan.Theoretical and Applied Genetics,2004,109(3):588.
[68] Miranda A S,Vieira M F.Ruelliasubsessilis(Nees) Lindau(Acanthaceae):A species with a sexual reproductive system that responds to different water availability levels.Flora,2014,209:711-717.
[69] Zhang J Y,Kong L F,Liu Z P,Jahufer Z,Duan Z.Stress-induced expression inArabidopsiswith a DehydrinLEAprotein fromCleistogenessongorica,a xerophytic desert grass.Plant Omics Journal,2015,8(6):485-492.
[70] Duan Z,Zhang D Y,Zhang J Q,Di H Y,Wu F,Hu X W,Meng X C,Luo K,Zhang J Y,WangY R.Co-transforming bar andCsALDHgenes enhanced resistance to herbicide and drought and salt stress in transgenic alfalfa (MedicagosativaL.).Frontiers in Plant Science,2015,6:1115.
[71] Zhang J Y,Duan Z,Zhang D Y,Zhang J Q,Di H Y,Wu F,Wang Y R.Co-transforming Bar andCsLEAenhanced tolerance to drought and salt stress in transgenic alfalfa(MedicagosativaL.).Biochemical and Biophysical Research Communications,2016,472(1):75-82.
[72] Daniell H.Molecular strategies for gene containment in transgenic crops.Nature Biotechnology,2002(20):581-586.
[73] Saxena K B,Singh L,Ariyanayagam R P.Role of partial cleistogamy in maintaining genetic purity of pigeonpea.Euphytica,1993,66(3):225-229.
[74] Chhabra A K,Sethi S K.Inheritance of cleistogamic flowering in durum wheat(Triticumdurum).Euphytica,1991,55(2):147-150.
[75] Takahashi R,Kurosaki H,Yumoto S.Genetic linkage analysis of cleistogamy in soybean.Journal Heredity,2001,92(1):89-92.
[76] Ning S Z,Wang N,Sakuma S,Pourkheirandish M,Wu J Z,Matsumoto T,Koba T,Komatsuda T.Structure, transcription and post-transcriptional regulation of the bread wheat orthologs of the barley cleistogamy geneCly1.Theoretical and Applied Genetics,2013,126(5):1273-1283.
[77] Turuspekov Y,Mano Y,Honda I,Kawada N,Watanabe Y,Komatsuda T.Identification and mapping of cleistogamygenes in barley.Theoretical and Applied Genetics,2004,109(3):480.
[78] Kyozuka J,Kobayashi T,Morita M,Shimamoto K.Spatially and temporally regulated expression of rice MADS box genes with similarity toArabidopsisclass A, B and C genes.Plant and Cell Physiology,2000,41(6):710-718.
[79] 葛磊,譚克輝,種康,許智宏.水稻花發(fā)育基因調(diào)控的研究進(jìn)展.科學(xué)通報(bào),2001,46(9):705-712.
[80] Nagasawa N,Miyoshi M,Sano Y,Satoh H,Hirano H,Sakai H,Nagato Y.SUPERWOMAN1 andDROOPINGLEAFgenes control floral organ identity in rice.Development,2003,130(4):705-718.
[81] Yoshida H,Itoh J I,Ohmori S,Miyoshi K,Horigome A,Uchida E,Kimizu M,Matsumura Y,Kusaba M,Satoh H.Superwoman1-cleistogamy,a hopeful allele for gene containment in GM rice.Plant Biotechnology Journal,2007,5(6):835-846.
[82] Mizukami Y,Huang H,Tudor M,Hu Y,Ma H.Functional domains of the floral regulatorAGAMOUS:Characterization of the DNA binding domain and analysis of dominant negative mutations.The Plant Cell,1996,8(5):831-845.
[83] Lopez-Dee Z P,Wittich P,Enrico P M,Rigola D,Del B I,Gorla M S,Kater M M,Colombo L.OsMADS13,a novel rice MADS-box gene expressed during ovule development.Developmental Genetics,1999,25(3):237-244.
[84] Yamaguchi T,Lee D Y,Miyao A,Hirochika H,An G,Hirano H Y.Functional diversification of the two C-class MADS box genesOSMADS3 andOSMADS58 inOryzasativa.The Plant Cell,2006,18(1):15-28.
[85] Jeon J S,Jang S,Lee S,Nam J,Kim C,Lee S H,Chung Y Y,Kim S R,Lee Y H,Cho Y G.Leafy hull sterile1 is a homeotic mutation in a rice MADS box gene affecting rice flower development.The Plant Cell,2000,12(6):871-884.
[86] Cui R,Han J,Zhao S,Su K,Wu F,Du X,Xu Q,Chong K,Thei?en G,Meng Z.Functional conservation and diversification of class E floral homeotic genes in rice(Oryzasativa).The Plant Journal,2010,61(5):767-781.
[87] Gilsinger J,Kong L,Shen X.DNA markers associated with lowFusariumhead blight incidence and narrow flower opening in wheat.Theoretical and Applied Genetics,2005,110(7):1218-1225.
[88] 白惠磊,張素麗,梁慶沙,胡建芳.巨峰葡萄閉花受精機(jī)理的研究.中國農(nóng)業(yè)大學(xué)學(xué)報(bào),2007,12(2):27-33. Bai H L,Zhang S L,Liang Q S,Hu J F.Mechanism of cleistogamy in ‘Kyoho’ grape(Vitislabruscana).Journal of China Agricultural University,2007,12(2):27-33.(in Chinese)
(責(zé)任編輯 王芳)
Advances in cleistogamy of angiosperms
Zhang Dai-yu, Luo Kai, Wu Fan, Wang Yan-rong, Zhang Ji-yu
(State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China)
Cleistogamy (CL), a breeding system in which permanently closed and self-pollinated flowers are produced, has
increasing attention in recent years. The present study summarised the different types of cleistogamy, the variation of floral organs, their distribution in angiosperms, phylogenetic evolution, and related regulatory genes. There are three types of cleistogamy: dimorphic, complete, and induced cleistogamy. Among them, the occurrence of dimorphic cleistogamy is 77.3%. Cleistogamy is present in 705 angiosperm species, distributed across 236 genera and 53 families. Compared with chasmogamy (CH), the number of floral organs in cleistogamous flowers is reduced and the lodicules are degraded. Genetic control of cleistogamy involves one to three genes.Cleistogenessongoricais a representative plant with dimorphic cleistogamy. The morphology of CH and CL flowers revealed a significant difference, and the seeds are heteromorphic. The phylogenetic tree of the genera in Poaceae indicated that the relationship betweenCleistogenesandDiplachne, belonging to Tridentinae, is closer than originally presumed. Such information will provide valuable background for understanding the ecological significance and role of genes in cleistogamy.
cleistogamy; chasmogamy; phylogenetic evolution; cleistogamy related genes; angiosperms
Zhang Ji-yu E-mail:zhangjy@lzu.edu.cn
2017-01-07 接受日期:2017-03-24
科技部“973”課題(2014CB138704);國家自然科學(xué)基金(31572453、31101759);蘭州大學(xué)中央高?;究蒲匈M(fèi)自由探索項(xiàng)目(lzujbky-2016-10)
張代玉(1989-),女,甘肅靖遠(yuǎn)人,在讀碩士生,研究方向?yàn)樽魑镌耘嗯c耕作學(xué)。E-mail:zhangdy2014@lzu.edu.cn
張吉宇(1977-),男,甘肅民樂人,副教授,博導(dǎo),博士,研究方向?yàn)椴蓊愖魑镉N與生物技術(shù)。E-mail:zhangjy@lzu.edu.cn
10.11829/j.issn.1001-0629.2017-0028
Q944.42
A
1001-0629(2017)06-1215-13
張代玉,駱凱,吳凡,王彥榮,張吉宇.被子植物閉花授粉的研究進(jìn)展.草業(yè)科學(xué),2017,34(6):1215-1227.
Zhang D Y,Luo K,Wu F,Wang Y R,Zhang J Y.Advances in cleistogamy of angiosperms.Pratacultural Science,2017,34(6):1215-1227.