轉(zhuǎn)座子在植物XY性染色體起源與演化過程中的作用

李書粉，李莎，鄧傳良，盧龍斗，高武軍

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轉(zhuǎn)座子在植物XY性染色體起源與演化過程中的作用

李書粉，李莎，鄧傳良，盧龍斗，高武軍

河南師范大學(xué)生命科學(xué)學(xué)院，新鄉(xiāng) 453007

XY性染色體決定系統(tǒng)是決定植物性別的主要方式，但是對于其起源與演化機制卻知之甚少。目前認(rèn)為，攜帶控制雌蕊或雄蕊發(fā)育基因的一對常染色體由于某種未知原因的突變形成早期的neo-Y或neo-X性染色體，隨著演化的進(jìn)行，早期XY性染色體之間的重組逐漸受到抑制，非重組區(qū)域擴(kuò)展最終形成異型的性染色體。研究發(fā)現(xiàn)，重復(fù)序列的累積以及DNA甲基化等因素都可能參與了XY性染色體的異染色質(zhì)化、重組抑制及Y染色體體積增大過程。轉(zhuǎn)座子作為一種基因組中含量最高的重復(fù)序列在性染色體演化中扮演了重要的角色，包括性染色體演化的起始激發(fā)，以及導(dǎo)致性染色體局部表觀遺傳修飾使其發(fā)生異染色質(zhì)化擴(kuò)展和重組抑制。文章綜述了轉(zhuǎn)座子在植物性染色體上的累積及其與性染色體異染色質(zhì)化之間的關(guān)系，并簡要分析了轉(zhuǎn)座子在性染色體演化過程中的作用。

表觀遺傳修飾；異染色質(zhì)化；重組抑制；轉(zhuǎn)座子；XY性染色體

植物性別及性染色體起源和演化是植物學(xué)研究的熱點之一。在顯花植物中，包括6個雙子葉和5個單子葉亞綱在內(nèi)的75%的科都存在雌雄單性或者雌雄異株種，大約38%(167個)的科和7.1%(959個)的屬中有6%(14 620種)是雌雄異株植物[1]。在開花植物中，幾乎所有的雌雄異株植物都屬于雄性具有XY和雌性具有XX性染色體的性別決定系統(tǒng)[2]。相對于哺乳動物性染色體而言，植物XY性染色體起源較晚。最早的哺乳動物Y染色體的進(jìn)化已經(jīng)超過250~300百萬年[3,4]。而最早的植物Y染色體可能比動物的要年輕至少10倍，如白麥瓶草()[5~7]和酸模()[8]的Y染色體起源估計[9]距今僅約3000萬年。而番木瓜()[10]和[11,12]的Y染色體距今還不足7百萬年。因此，植物XY性染色體系統(tǒng)為性別及性染色體早期的起源進(jìn)化提供了有利的研究材料，且其研究結(jié)果可為人類性別演化機制的研究提供一定的參考。

目前的理論認(rèn)為，雌雄異株植物是從不同科中的雌雄同株祖先獨立進(jìn)化而來[13,14]。在雌雄同株植物中擁有完全一樣的一套產(chǎn)生雌蕊和雄蕊的基因。在這些種中，控制雌蕊和雄蕊發(fā)育的基因或多或少地分布在所有常染色體上[15~17]，控制雄蕊發(fā)育的基因偶然發(fā)生失去功能的隱性突變產(chǎn)生雌性個體，而這些基因發(fā)生獲得功能的顯性突變則產(chǎn)生雄性個體[4,18~27]?？刂菩詣e的突變基因所在的染色體就成為原始的性染色體neo-X和neo-Y，而突變位點即為早期的性別決定區(qū)。隨著時間的推移，neo-X和neo-Y染色體由于某種未知的原因，其性別決定區(qū)的重組逐漸被完全抑制[28,29]。這種重組抑制作用的出現(xiàn)加速了性染色體的演化過程，導(dǎo)致異型XY性染色體的出現(xiàn)，且大多數(shù)植物的Y染色體往往大于X染色體。但是，是什么原因激發(fā)了性染色體的重組抑制？Y染色體的體積又是如何增大的？目前還知之甚少。越來越多的證據(jù)發(fā)現(xiàn)在性染色體上分布有大量的轉(zhuǎn)座子[10,30~34]，這些轉(zhuǎn)座子和性別決定區(qū)的異染色質(zhì)化可能參與了早期性染色體的演化過程。在番木瓜中，X和Y染色體均存在高密度的轉(zhuǎn)座子，且Y染色體上轉(zhuǎn)座子密度遠(yuǎn)高于X染色體，導(dǎo)致了Y染色體在體積上大于X染色體[10,34]。其次，轉(zhuǎn)座子可能還引起了番木瓜[10,34]、白麥瓶草[35~37]和人[38]的Y染色體比X染色體產(chǎn)生更大程度上的重排[4]。顯然，轉(zhuǎn)座子可能通過多種途徑參與了XY染色體的演化過程。但是，轉(zhuǎn)座子如何參與XY染色體的演化？轉(zhuǎn)座子和XY性染色體的異染色質(zhì)化及重組抑制之間有什么樣的關(guān)系？轉(zhuǎn)座子在激發(fā)了性別決定區(qū)的重組抑制中可能的作用是什么？本文就這幾個方面的問題進(jìn)行了綜述。

1 性染色體重組抑制的產(chǎn)生是XY性染色體演化的關(guān)鍵

在三刺魚()中，位于性別決定位點兩側(cè)的兩個微衛(wèi)星標(biāo)記Stn186和Stn191在Y染色體上的遺傳距離是6.4 cM，而在X染色體上卻有25.7 cM，顯然這兩個標(biāo)記在Y染色體上的重組率降低了約４倍。因此，相對于X染色體，Y染色體上的這兩個標(biāo)記之間的重組受到了抑制[28]。同樣，在植物XY性染色體間也存在普遍類似的重組抑制現(xiàn)象[39]，這種現(xiàn)象的產(chǎn)生主要是由于倒位和異染色質(zhì)化引起的。倒位造成的染色體重排使倒位區(qū)域的重組被完全抑制[40]。在人類Y染色體上發(fā)現(xiàn)了4個倒位區(qū)域，這些倒位導(dǎo)致了人類Y染色體的退化與重組抑制[41]。在番木瓜中，Y染色體上兩個大的倒位造成了Y染色體的非重組區(qū)排列不同于X染色體，也是XY重組抑制產(chǎn)生的主要原因[10]，這充分說明倒位能夠使得性染色體發(fā)生重組抑制。但是，一些研究發(fā)現(xiàn)并非所有的XY性別特異區(qū)的重組抑制區(qū)都是由倒位引起的[30,42,43]，性染色體的異染色質(zhì)化也能使性染色體的重組受到抑制，這一現(xiàn)象最早是在對動物的性染色體上轉(zhuǎn)座子及其衍生的重復(fù)序列的研究中發(fā)現(xiàn)的[29,44~46]。在赒魚()中，性染色體X/Y二價體末端部分聯(lián)會缺失[47]，這是因為在該區(qū)域缺乏配對區(qū)域引起的，但是進(jìn)一步的細(xì)胞學(xué)分析發(fā)現(xiàn)該區(qū)域染色體并未出現(xiàn)類似倒位的染色體重排現(xiàn)象[48]，那么引起其性染色體配對缺失的原因可能是異染色質(zhì)的過度累積，進(jìn)而導(dǎo)致了重組的降低。Steinemann等[49]也認(rèn)為(一種果蠅)的Y染色體大量的反轉(zhuǎn)座子的插入可能使該染色體的常染色質(zhì)向異染色質(zhì)轉(zhuǎn)變。在雌雄異株植物酸模的Y染色體上發(fā)生的大規(guī)模異染色質(zhì)化和功能喪失的現(xiàn)象[50~55]，形成了其兩條Y染色體均為組成型異染色質(zhì)[56]。因此，Y染色體在演化過程中可能由于某種未知的原因而逐步異染色質(zhì)化，進(jìn)而抑制了和X染色體的重組。

2 XY性染色體上轉(zhuǎn)座子的分布特征與作用

轉(zhuǎn)座子是廣泛存在于真核生物基因組中的可移動的DNA分子，通過其轉(zhuǎn)座行為可以引起基因突變[57]、染色體重排[58]、異常重組和基因組重建[59,60]。因此轉(zhuǎn)座子也被認(rèn)為是引起基因組不穩(wěn)定的重要因素之一[61,62]。為了阻止轉(zhuǎn)座子活動對基因組的傷害，基因組自身相應(yīng)產(chǎn)生了對抗轉(zhuǎn)座子活動的防御機制，其中異染色質(zhì)化可能是主要的防御機制之一。因此，在植物Y染色體進(jìn)化過程中轉(zhuǎn)座子的大量累積可能是其進(jìn)化的第一步，正是由于轉(zhuǎn)座子的累積激發(fā)了基因組通過異染色質(zhì)化來消除轉(zhuǎn)座子的危害[49]。而早期性染色體的這種異染色質(zhì)化既可以抑制重組的發(fā)生[63]，又可能會進(jìn)一步吸引更多的轉(zhuǎn)座子插入[64]來促使異染色質(zhì)化向兩側(cè)區(qū)域擴(kuò)展。一些研究也為這一假設(shè)提供了初步的證據(jù)。Bachtrog等[65]研究表明，在的Y染色體上轉(zhuǎn)座子的插入數(shù)量是X染色體的20倍，Steinemann等[66]認(rèn)為的Y染色體從常染色質(zhì)到異染色質(zhì)的轉(zhuǎn)變很可能就是由于大量的反轉(zhuǎn)座子的插入引起的，并且他們認(rèn)為反轉(zhuǎn)座子是的Y染色體異染色質(zhì)化理想的驅(qū)動力。最近，Zhou等[67]對雄性果蠅基因組文庫的雙端測序讀序的關(guān)系進(jìn)行了分析，檢測了Y染色體上基因附近及其上下游的重復(fù)序列密度，并與X染色體進(jìn)行對比。他們將基因組讀序錨定在X/Y特征性SNP上，與果蠅的重復(fù)序列數(shù)據(jù)庫中的序列進(jìn)行比對分析。結(jié)果發(fā)現(xiàn)Y染色體重復(fù)序列密度高的區(qū)域內(nèi)的基因具有更高的H3K9me2(異染色質(zhì)的特征性的修飾形式)結(jié)合水平。該研究證實了Y染色體異染色質(zhì)形成確實是由轉(zhuǎn)座子激發(fā)，并導(dǎo)致插入位點臨近的基因發(fā)生沉默[67,68]。在植物中，番木瓜[10,34]和白麥瓶草[35~37]Y染色體較大程度的重排是通過Y染色體的不同位置上的重復(fù)序列之間出現(xiàn)的異位配對和交換引起的[4]，因此，這種轉(zhuǎn)座子在性染色體上的存在也能引起XY染色體形態(tài)產(chǎn)生異型的改變。轉(zhuǎn)座子的插入可能也是早期調(diào)控雌蕊或雄蕊發(fā)育基因突變的原因，當(dāng)轉(zhuǎn)座子插入到這些基因中或者基因附近就能引起基因功能的缺失或基因表達(dá)水平的降低[69]。

目前，在一些雌雄異株植物性染色體的異染色質(zhì)區(qū)域也發(fā)現(xiàn)了轉(zhuǎn)座子的存在。在大麻()Y染色體長臂上發(fā)現(xiàn)了非LTR 反轉(zhuǎn)座子的累積[70]；番木瓜的Y染色體雄性特異區(qū)域也發(fā)現(xiàn)大量的反轉(zhuǎn)座子[71]。通過對番木瓜雄性特異的BAC克隆測序表明，性染色體上出現(xiàn)高密度的反轉(zhuǎn)座子[30]，說明反轉(zhuǎn)座子或者其衍生的衛(wèi)星重復(fù)序列是形成異染色質(zhì)的主要原因之一[72]。更進(jìn)一步的研究發(fā)現(xiàn)，轉(zhuǎn)座子及其他重復(fù)序列占番木瓜Yh(番木瓜Y染色體的一種，控制雌雄同株性別)染色體特異區(qū)域(Hermaphrodite-specific region on the Y chromosome, HSY)的79.3%，占相對應(yīng)的X染色體的67.2%，都遠(yuǎn)高于整個基因組轉(zhuǎn)座子及其他重復(fù)序列的比例(51%)[10,73]，支持了轉(zhuǎn)座子在性染色體進(jìn)化的初期大量累積導(dǎo)致性別決定區(qū)域擴(kuò)展的這一假設(shè)[62]。另外，在具有異型性染色體的雌雄異株植物中，Y染色體通常比X染色體大，這種特性可能正是由于在Y染色體上累積了大量的轉(zhuǎn)座子及其他類型的重復(fù)序列所造成的[74]。番木瓜Yh染色體特異區(qū)的轉(zhuǎn)座子主要為和反轉(zhuǎn)座子，X染色體和HSY上的反轉(zhuǎn)座子是常染色體上的兩倍[10]。番木瓜Yh染色體特異區(qū)的轉(zhuǎn)座子主要為和反轉(zhuǎn)座子，X染色體和HSY上的反轉(zhuǎn)座子是常染色體上的兩倍[10]。最近研究者也相繼從瀉根()[33]、新月魚()[32]、酸模[31]和虎脂鯉的()[75]性染色體上發(fā)現(xiàn)了轉(zhuǎn)座子存在的證據(jù)。最近，Akagi等[76]在君遷子(，一種具有XY性染色體的木本植物)的Y染色體上發(fā)現(xiàn)了一個雄性特異的基因，該基因編碼一個21 bp的小RNA，并以RNAi的方式調(diào)控雌雄性別的形成，而值得注意的是在這一性別決定基因的周圍150 kb范圍內(nèi)也存在高度重復(fù)序列。本實驗室通過對石刁柏()基因組進(jìn)行測序和分析也發(fā)現(xiàn)了在其雌雄性別間存在大量的拷貝數(shù)具有明顯差異的轉(zhuǎn)座子[77]，這些轉(zhuǎn)座子可能位于其性染色體上。盡管以上報道表明了植物XY性染色體上存在大量的轉(zhuǎn)座子序列，且可能和XY染色體的異染色質(zhì)化、重組抑制具有密切的關(guān)系，但是轉(zhuǎn)座子是通過什么方式激發(fā)性染色體的異染色質(zhì)化和引起重組抑制的機制仍不清楚。

3 轉(zhuǎn)座子可能通過表觀遺傳修飾的方式參與XY染色體的演化

轉(zhuǎn)座子激發(fā)植物性染色體異染色質(zhì)化可能是通過引起其鄰近區(qū)域染色質(zhì)表觀遺傳修飾模式變化來實現(xiàn)的。表觀遺傳修飾，如DNA和組蛋白甲基化的作用之一是保護(hù)生物體自身遺傳物質(zhì)不被外來遺傳物質(zhì)所侵染，維持基因組的完整性[78~80]。最近越來越多的證據(jù)發(fā)現(xiàn)表觀遺傳機制參與了動植物性別的表達(dá)調(diào)控[81~84]。Kuroki等[82]的研究發(fā)現(xiàn)，當(dāng)缺乏去甲基化酶Jmjd1a時，小鼠性別會發(fā)生反轉(zhuǎn)。這種性別的反轉(zhuǎn)是通過去甲基化酶調(diào)控了Y染色體上基因區(qū)域組蛋白H3K9me2的甲基化來決定的。生物體基因組中一些轉(zhuǎn)座子及其衍生的重復(fù)序列往往更容易作為這種表觀遺傳修飾的靶標(biāo)[69, 85]。那么，在轉(zhuǎn)座子自身被表觀遺傳修飾的同時其側(cè)翼一定范圍內(nèi)的染色質(zhì)也可能被修飾，而且這種修飾可能和距離轉(zhuǎn)座子的遠(yuǎn)近有關(guān)。Takata等[86]采用高通量測序技術(shù)分析了水稻中的12種轉(zhuǎn)座子，結(jié)果發(fā)現(xiàn)反轉(zhuǎn)座子側(cè)翼序列都是高度甲基化的，且這種甲基化程度與轉(zhuǎn)座子距離的遠(yuǎn)近有關(guān)。植物S1反轉(zhuǎn)座子主要整合到低甲基化的DNA區(qū)域，并且作為甲基化酶的靶標(biāo)激發(fā)側(cè)翼基因組序列甲基化，從而產(chǎn)生遠(yuǎn)端表觀遺傳修飾[87]。擬南芥中異染色質(zhì)的形成也和特異的DNA甲基化轉(zhuǎn)移酶、H3K9組蛋白甲基化酶和組蛋白去乙?；?H4K16)有關(guān)[88]；而且通過去甲基化試劑處理后可以引起擬南芥和真菌中轉(zhuǎn)座子的激活和遷移[89]。因此，我們推測早期植物的性染色體的起源也可能先是由于某些反轉(zhuǎn)座子的插入而導(dǎo)致基因組通過表觀遺傳修飾來抑制轉(zhuǎn)座子的活性，并由此激發(fā)了早期性染色體以此轉(zhuǎn)座子為核心向兩側(cè)通過表觀遺傳修飾的方式異染色質(zhì)化，從而導(dǎo)致性染色體重組抑制的發(fā)生。Martin 等[81]的研究為這一推測提供了實驗證據(jù)，他們發(fā)現(xiàn)一個轉(zhuǎn)座子插入到轉(zhuǎn)錄因子CmWIP1中，并且引起該轉(zhuǎn)座子側(cè)翼的轉(zhuǎn)錄因子DNA序列甲基化，使得甜瓜產(chǎn)生單性的雄花。盡管這一報道沒有證明轉(zhuǎn)座子插入能夠引起其鄰近染色質(zhì)較大范圍的表觀遺傳修飾，但是這一結(jié)果也將轉(zhuǎn)座子、表觀遺傳修飾和植物性別聯(lián)系起來，為我們的推測提供了一定的理論依據(jù)。

4 結(jié)論與展望

除了倒位和異染色質(zhì)化能夠引起XY性染色體間的重組抑制外，也存在其他引起重組抑制的方式。如早期的性別決定基因突變位置可能恰好是在不容易發(fā)生重組的染色體區(qū)域，如著絲粒及其周圍區(qū)域。研究發(fā)現(xiàn)在一些植物染色體上存在大的交換被限制的著絲粒區(qū)，這些區(qū)域也包含了較多的功能基因[90]。最近也發(fā)現(xiàn)了番木瓜的性別決定區(qū)可能是在著絲粒周圍的低重組區(qū)域[10]，而美洲山楊()的性別決定區(qū)也被定位在性染色體著絲粒區(qū)域[91]。另外，雖然易位在某些情況下也可以產(chǎn)生染色體重排而抑制交換的發(fā)生，如在雄性果蠅中，性染色體與常染色體之間的易位可以形成一個新的非重組原始Y染色體[45,92]。但是，目前除了這一特例外在其他能夠發(fā)生交換的兩性物種中，盡管在接近斷裂點附近的交換可能被降低，但是這樣的重排一般不會產(chǎn)生一個非重組區(qū)[93,94]。由此可見，性染色體XY間的重組抑制雖然主要是由早期突變基因所在區(qū)域的異染色質(zhì)化和倒位引起的，但是由于雌雄異株植物性染色體具有獨立起源的特征，因此也不能排除其他未知的細(xì)胞學(xué)行為引起了XY染色體間的重組抑制。

轉(zhuǎn)座子積累與性染色體異染色質(zhì)化及重組抑制之間存在密切的關(guān)系，對于轉(zhuǎn)座子激發(fā)性染色體的異染色質(zhì)化和引起重組抑制的機制還需要綜合生物信息學(xué)、分子生物學(xué)和細(xì)胞生物學(xué)的技術(shù)進(jìn)行更為深入的研究。轉(zhuǎn)座子插入激發(fā)Y染色體的表觀遺傳修飾的變化，進(jìn)而引起Y染色體異染色質(zhì)化和重組抑制，如果這樣的假設(shè)成立需要更為可靠的細(xì)胞及分子生物學(xué)證據(jù)。首先需要通過高通量的測序數(shù)據(jù)來比較雌雄異株植物及其近緣雌雄同株種基因組中轉(zhuǎn)座子分布特征及差異，并且結(jié)合遺傳連鎖圖進(jìn)行XY染色體上轉(zhuǎn)座子或基因進(jìn)行定位。其次，利用高分辨率的Fiber-FISH和染色體及組蛋白甲基化檢測技術(shù)比較分析XY染色體上轉(zhuǎn)座子及其側(cè)翼區(qū)域DNA甲基化及組蛋白修飾的特征。綜合分析這些研究結(jié)果有助于闡明轉(zhuǎn)座子是否是通過表觀遺傳修飾的方式激發(fā)了植物XY性染色體的異染色質(zhì)化和重組抑制這一基本問題。

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老徐笑：五年前，第一回見到你就感覺你特別，坐在輪椅上，比誰都愛說愛笑；我跟老伴說，也沒見女孩的媽媽跟來陪讀，可憐見的，問你，你說學(xué)校已經(jīng)挺照顧你，把你安排在一樓的宿舍，還敲掉一小段臺階，修了個可供輪椅出入的坡道?！皨寢屄?，有媽媽的事，是我不要她陪的。要不然我再大一點，也不會洗床單，不會曬被子?！?/p>

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(責(zé)任編委: 劉寶)

Role of transposons in origin and evolution of plant XY sex chromosomes

Shufen Li, Sha Li, Chuanliang Deng, Longdou Lu, Wujun Gao

TheXY sex-determination system is crucial for plant reproduction. However, little is known about the mechanism of the origin and evolution of the XY sex chromosomes. It has been believed that a pair of autosomes is evolved to produce young sex chromosomes (neo-X chromosome and neo-Y chromosome) by loss of function or gain of function mutation, which influences the development of pistil or stamen. With the aggravation of the recombination suppression between neo-X and neo-Y and consequent expanding of the non-recombination region, the proto-sex chromosomes were finally developed to heteromorphic sex chromosomes. Accumulation of repetitive sequences and DNA methylation were probably involved in this process. Transposons, as the most abundant repetitive sequences in the genome, might be the initial motivation factors for the evolution of sex chromosome. Moreover, transposons may also increase heterochromatin expansion and recombination suppression of sex chromosome by local epigenetics modification. In this review, we summarize the function of transposon accumulation and the relationship between transposon and heterochromatization in the evolution of plant sex chromosome.

epigenetic modification; heterochromatization; recombination suppression; transposon; XY sex chromosome

2014-09-13;

2014-11-20

國家自然科學(xué)基金項目(編號：31300202和31470334)和河南省高校青年骨干教師項目(編號：2013GGJS-060)資助

李書粉，博士，副教授，碩士生導(dǎo)師，研究方向：植物遺傳學(xué)。E-mail: lishufen83@163.com

高武軍，博士，副教授，碩士生導(dǎo)師，研究方向：植物遺傳學(xué)。E-mail: gaowujun1@163.com

10.16288/j.yczz.14-305

網(wǎng)絡(luò)出版時間: 2014-12-8 11:46:04

URL: http://www.cnki.net/kcms/detail/11.1913.R.20141208.1146.001.html