趙洪，薛勇彪

特邀綜述

顯花植物自交不親和性的分子與演化機(jī)制

趙洪，薛勇彪

中國科學(xué)院遺傳與發(fā)育生物學(xué)研究所，北京 100101

自交不親和性(self-incompatibility, SI)是雌雄同花植物廣泛采取的一種種內(nèi)促進(jìn)異交機(jī)制，通常由一個(gè)多態(tài)且復(fù)等位的位點(diǎn)控制。目前共發(fā)現(xiàn)6種不同分子機(jī)制的SI，包括由花柱因子和花粉因子s控制且常見于車前科、茄科、薔薇科和蕓香科的I類、和控制的十字花科II類、和控制的罌粟科III類、----控制的報(bào)春花科IV類、-控制的時(shí)鐘花科V類及-和-控制的禾本科VI類SI，其中I類SI為異己識(shí)別體系，而II、III和VI類均為自己識(shí)別系統(tǒng)。此外，近年來對其起源和演化機(jī)制研究也取得顯著進(jìn)展。其中，I類SI起源于真雙子葉植物的最近共同祖先，II～V類則為丟失I類后分別進(jìn)化產(chǎn)生的新機(jī)制，而單子葉禾本科特有的VI類SI則可能是在丟失古老I類SI后演化出的新系統(tǒng)。本文主要總結(jié)已報(bào)道SI的分子和演化機(jī)制，以期為顯花植物SI的理論研究和育種應(yīng)用提供參考和幫助。

顯花植物；自交不親和性；起源；演化；自交系；雜交育種

被子植物因具有獨(dú)特的花器官，又稱為顯花植物。迄今為止，已定名的被子植物約有30萬種，是植物界最大的類群，其花器官形態(tài)亦是紛繁多姿?；ㄊ潜蛔又参锓毖苌⒌闹匾鞴?，是傳粉受精的重要載體。與動(dòng)物相似，植物也有性別之分。然而，除了少部分表現(xiàn)為雌雄異株、雌雄異花同株等外，約85%的被子植物表現(xiàn)為雌雄同花，即雌蕊和雄蕊著生在同一朵花中，從而顯著增加了自花授粉及近交衰退的可能性。于是，被子植物在快速崛起建立陸地植物霸主地位的過程中，進(jìn)化出了多種自交限制策略，其中最為常見的便是自交不親和性(self-incompatibility, SI)。超過40%的顯花植物所具有的SI是指正?？捎拇菩弁ㄖ参镒越皇诜酆蟛荒墚a(chǎn)生合子的現(xiàn)象與機(jī)制[1]。作為一種嚴(yán)格的種內(nèi)生殖障礙，SI可有效抑制自交并促進(jìn)異交，對于種群遺傳多樣性的維持和適應(yīng)生存至關(guān)重要。

盡管SI對自交花粉的作用大體表現(xiàn)為限制花粉在柱頭上的萌發(fā)或花粉管在雌蕊中的生長，但實(shí)現(xiàn)這一過程的具體機(jī)制卻不盡相同。在真雙子葉植物中，SI通常由單一多態(tài)且復(fù)等位的位點(diǎn)或基因座控制，而單子葉禾本科SI則由多態(tài)、復(fù)等位且獨(dú)立遺傳的和雙位點(diǎn)控制。在控制SI的基因座中，通常包含兩類基因，分別為決定花柱識(shí)別特異性的花柱或基因和決定花粉識(shí)別特異性的花粉或基因，二者緊密連鎖構(gòu)成的獨(dú)立遺傳單元稱為或單倍體型[2～9]。以位點(diǎn)為例，來自相同單倍體型的花柱和花粉因子的識(shí)別稱為自己識(shí)別，反之為異己識(shí)別，二者可分別導(dǎo)致自交不親和反應(yīng)(self-pollen incompatibility, SPI)與異交親和反應(yīng)(cross-pollen compatibility, CPC)。根據(jù)花的形態(tài)是否存在差異，SI分為同型自交不親和性(homomorphic SI)和異型自交不親和性(heteromorphic SI)。異型SI主要指花柱異長(heterostyly)，包括二型花柱和三型花柱兩種類型，存在于報(bào)春花科、時(shí)鐘花科等28個(gè)科中，主要通過雌雄蕊的形態(tài)差異來抑制自交和促進(jìn)異交(圖1)。與之相比，同型SI分布十分廣泛，該類型又分為配子體自交不親和性(gametophytic SI, GSI)和孢子體自交不親和性(sporophytic SI, SSI)。GSI常見于17～25個(gè)科中，其花粉自交不親和表型由花粉自身的或單倍體型決定；而SSI僅存在于十字花科、菊科、旋花科、樺木科、石竹科等，其花粉自交不親和表型由產(chǎn)生花粉的親本基因型決定[10]。

根據(jù)分子機(jī)制的不同，已發(fā)現(xiàn)的SI主要分為6種類型[11]，包括由花柱和花粉因子(-)和()控制的配子體I類SI，常見于車前科、茄科、薔薇科和蕓香科[12～17]；由()和()/()控制的十字花科的孢子體II類[18,19]；(,)和()控制的罌粟科的配子體III類[20,21]；()、()、()、()和()控制的報(bào)春花科異型花柱IV類[22]；()、和控制的時(shí)鐘花科異型花柱V類[23]；/和/-/控制的禾本科配子體VI類SI[24～29]。本文將主要總結(jié)近年來已報(bào)道SI的分子和演化機(jī)制，以期為顯花植物SI的理論研究和育種應(yīng)用提供參考和幫助。

圖1 顯花植物自交不親和性的遺傳控制與分類

1 真雙子葉植物自交不親和性的分子與演化機(jī)制

1.1 I類自交不親和性的分子機(jī)制

I類位點(diǎn)通常包含1個(gè)花柱特異表達(dá)的-和9～37個(gè)花粉特異表達(dá)的s。作為一類T2核酸酶，花柱因子S-RNase不僅可以降解自己花粉管的核糖體RNA，還可通過形成SRCs (S-RNase condensates)、破壞花粉管細(xì)胞骨架的動(dòng)態(tài)平衡、調(diào)節(jié)花粉管尖端的鈣離子流等抑制自交花粉管生長[30～35]。成熟的S-RNase通常具有一或多個(gè)糖基化修飾[36]。當(dāng)自交和異交授粉后，在花柱道傳輸組織細(xì)胞特異表達(dá)進(jìn)而分泌至細(xì)胞外基質(zhì)(extracellular matrix, ECM)的S-RNase盡管可以同時(shí)轉(zhuǎn)運(yùn)至自己和異己花粉管，但是僅在自交花粉管中發(fā)揮細(xì)胞毒性[13]。S-RNase對自己花粉管的毒性作用通常存在閾值效應(yīng)，當(dāng)其在花粉管中的積累量大于或等于閾值時(shí)才具有拒絕自己花粉的能力[37]。Liu等[38]發(fā)現(xiàn)S-RNase的細(xì)胞毒閾值與其糖鏈數(shù)目成正相關(guān)，但其具體機(jī)制尚無報(bào)道。此外，S-RNase的活性還與自身的氧化還原狀態(tài)有關(guān)，如NaTrxh (thioredoxin type)通過減弱S-RNase中特定半胱氨酸位點(diǎn)間的二硫鍵作用來增強(qiáng)其核酸酶活性，進(jìn)而特異調(diào)控自交不親和反應(yīng)[39]。作為一種F-box蛋白，I類花粉因子SLF的C端通常具有典型的FBA (F-box associated)/FBK (F-box associated kelch repreat)結(jié)構(gòu)域，且可與SSK1 (SLF-interacting skp1-like)和Cullin1結(jié)合形成SCF (SKP1-CUL1-F-box)復(fù)合體發(fā)揮功能[4,40～44]。的遺傳學(xué)驗(yàn)證主要基于競爭性相互作用(competitive interaction)的原理[45,46]，即四倍體植株產(chǎn)生的雜合二倍體花粉可以打破SI的現(xiàn)象。在薔薇科中，蘋果亞科SLF被命名為SFBB (-locus F-box brothers)[47]，而李亞科則包含同源基因()和其特有-基因(-)兩種類型[48]。Zhao等[11]發(fā)現(xiàn)薔薇科的、、轉(zhuǎn)基因與其他物種的一樣均可基于競爭性相互作用打破雜交矮牽牛()的SI，從而證明其功能相似。

I類SI屬于異己識(shí)別系統(tǒng)，盡管SLF可與自己和異己S-RNase互作，但與后者的相互作用更強(qiáng)[40,49,50]。在茄科和車前科中，S-RNase通常含有C1～C5五個(gè)保守區(qū)和Hva與Hvb兩個(gè)高變區(qū)[51]。Li等[52]發(fā)現(xiàn)僅包含高變區(qū)的S-RNase即可與SLF的C端互作。當(dāng)把雜交矮牽牛S3LSLF1和S3SLF1中受到正選擇且存在帶電性差異的293位氨基酸位點(diǎn)相互替換后，其單倍體型特異性也在一定程度上被改變，于是提出了S-RNase與SLF的“靜電勢識(shí)別模型”。其中，異己SLF與S-RNase的互作區(qū)由于帶有相反靜電勢而相互吸引，促使SLF與SSK1和Cullin1結(jié)合形成正常的SCF復(fù)合體，而自己SLF與S-RNase的互作區(qū)由于靜電勢相同而相互排斥，導(dǎo)致SLF無法進(jìn)一步形成SCF復(fù)合體發(fā)揮E3泛素連接酶功能。此外，Kubo等[50]基于膨大矮牽牛()的轉(zhuǎn)基因及互作檢測，提出了“協(xié)同異己識(shí)別模型”，即每個(gè)SLF可以特異識(shí)別一個(gè)或多個(gè)來自其他-單倍體型的S-RNase，而同一位點(diǎn)編碼的所有SLF可協(xié)同識(shí)別除自己S-RNase以外的所有異己S-RNase，由此也可以解釋序列多態(tài)性較低的SLF如何識(shí)別多態(tài)性較高的S-RNase。SLF對S-RNase的異己識(shí)別主要通過解除其細(xì)胞毒性產(chǎn)生異交親和反應(yīng)。關(guān)于異交花粉管中S-RNase的解毒機(jī)制，目前最為認(rèn)可的是“S-RNase降解模型”[40,53,54]。其中，識(shí)別為異己的S-RNase可被SCFSLF復(fù)合體在多個(gè)區(qū)域進(jìn)行K48類型的多聚泛素化修飾，進(jìn)而導(dǎo)向26S蛋白酶體降解以解除其細(xì)胞毒性，而識(shí)別為自己的S-RNase由于不能被有功能的SCFSLF泛素化并導(dǎo)向降解途徑，因而穩(wěn)定存在于自交花粉管并對其造成生長抑制(圖2)。

1.2 II類自交不親和性的分子機(jī)制

II類位點(diǎn)編碼一個(gè)花柱乳突細(xì)胞特異表達(dá)的花柱因子SRK和一個(gè)花藥絨氈層細(xì)胞特異表達(dá)的花粉因子SP11/SCR[18,19]。作為一類受體激酶，SRK包含三個(gè)結(jié)構(gòu)域：細(xì)胞外(-locus)結(jié)構(gòu)域、單次跨膜結(jié)構(gòu)域和絲氨酸/蘇氨酸型蛋白激酶催化結(jié)構(gòu)域，其中胞外結(jié)構(gòu)域又存在四個(gè)高變區(qū)。SP11/SCR的多態(tài)性高于SRK，除N端信號(hào)肽外，一般僅包含8個(gè)保守的半胱氨酸殘基。II類SI屬于自己識(shí)別系統(tǒng)。當(dāng)自交授粉后，分泌至花粉外殼的SCR可與自己eSRK (ectodomain SRK)特異識(shí)別，促使SRK同源二聚化及自磷酸化[55,56]。Ma等[57]通過晶體結(jié)構(gòu)解析，揭示eSRK9可與SCR9以2:2的分子構(gòu)成形成一個(gè)“A”型異源四聚體，且每個(gè)SCR分子可同時(shí)與兩個(gè)eSRK9單體的高變區(qū)互作，而兩個(gè)SCR之間沒有相互作用。Murase等[58]發(fā)現(xiàn)SRK與自己SCR互作所形成復(fù)合體的結(jié)合自由能最穩(wěn)定，并且來自相同或不同亞族的eSRK與SCR的互作模式不同。II類自交不親和反應(yīng)的發(fā)生依賴于一系列磷酸化級(jí)聯(lián)反應(yīng)，被SCR配體結(jié)合并自磷酸化激活的SRK可磷酸化另一個(gè)花柱乳突細(xì)胞膜錨定的絲氨酸/蘇氨酸蛋白激酶MLPK (-locus protein kinase)，二者進(jìn)一步磷酸化激活E3泛素連接酶ARC1 (ARM-repeat containing 1)并促使Exo70A1、GLO1 (glyoxalase 1)、PLD1 (phospholipase D alpha 1)等多個(gè)花粉萌發(fā)促進(jìn)因子被泛素化降解[59～66]。其中，泡外復(fù)合體亞基Exo70A1可以通過介導(dǎo)囊泡轉(zhuǎn)運(yùn)促進(jìn)花粉的吸水萌發(fā)及花粉管的生長[63]，乙二醛酶GLO1可以解除甲基乙二醛MG (methylglyoxal)對Exo70A1等的毒性作用[64,65]，磷脂酶PLD1則通過催化磷脂酸PA (phosphatidic acid)的產(chǎn)生增強(qiáng)乳突細(xì)胞的胞吐作用[66]，但其只在異交花粉管中穩(wěn)定存在。此外，不親和授粉后柱頭乳突細(xì)胞還會(huì)發(fā)生由FERONIA信號(hào)介導(dǎo)的活性氧ROS (reactive oxygen species)升高以及由谷氨酸鹽受體樣通道蛋白GLR (glutamate receptor- like channel)介導(dǎo)的鈣離子內(nèi)流[67,68]，最終導(dǎo)致自交花粉無法萌發(fā)及花粉管生長受阻(圖2)。

圖2 顯花植物自交不親和性的分子機(jī)制

I～VI類SI的分子機(jī)制示意圖。虛線框中分別指示花粉、花粉管、乳突細(xì)胞或花柱中發(fā)生的自交不親和反應(yīng)(self-pollen incompatibility, SPI)和異交親和反應(yīng)(cross-pollen compatibility, CPC)。右側(cè)展示I～VI類S因子。

1.3 III類自交不親和性的分子機(jī)制

III類位點(diǎn)編碼一個(gè)柱頭乳突細(xì)胞表達(dá)的小的分泌型糖蛋白PrsS和一個(gè)花粉細(xì)胞膜定位的跨膜蛋白PrpS[20,21]。III類SI屬于自己識(shí)別系統(tǒng)，其花柱因子PrsS與花粉因子PrpS以配體和受體形式進(jìn)行自己識(shí)別并最終導(dǎo)致花粉或花粉管中的自交不親和反應(yīng)。Ca2+和K+的快速內(nèi)流是對自己識(shí)別響應(yīng)最早的細(xì)胞學(xué)事件[69]，該過程進(jìn)一步導(dǎo)致無機(jī)焦磷酸酶(inorganic pyrophosphotases, sPPases) Pr-26.1a/b和MAPK (mitogen-activated protein kinase)蛋白p56的磷酸化、微絲解聚、活性氧ROS和一氧化氮(nitric oxide, NO)含量升高等[70]。其中，異交花粉管中的無機(jī)焦磷酸酶Pr-26.1a/b可通過水解無機(jī)焦磷酸(inorganic pyrophosphate, PPi)促進(jìn)物質(zhì)合成與細(xì)胞快速生長，而磷酸化導(dǎo)致其在自交花粉管中失活，從而抑制了花粉管尖端的正常生長[71]。MAPK是引發(fā)細(xì)胞程序性死亡(programmed cell death, PCD)的一個(gè)關(guān)鍵信號(hào)，當(dāng)MAPK蛋白p56被磷酸化激活后，可進(jìn)一步增強(qiáng)花粉中caspase-3-like的活性以促進(jìn)DNA的片段化[72]。與之相似，細(xì)胞骨架動(dòng)態(tài)平衡被破壞及ROS和NO含量升高也會(huì)激活自交花粉或花粉管中的caspase-3-like，進(jìn)一步誘發(fā)DNA片段化即不可逆PCD[73,74]，從而抑制自交傳粉(圖2)。

1.4 IV類和V類自交不親和性的分子機(jī)制

IV類和V類SI均為異型花柱SI，通常由一個(gè)半合子超基因位點(diǎn)控制，其中至少包含3個(gè)亞單元：控制花柱長度和雌性不親和性的位點(diǎn)、控制花藥位置的位點(diǎn)以及控制花粉大小和雄性不親和性的位點(diǎn)。以二型花柱為例，當(dāng)基因型為和時(shí)，分別表現(xiàn)為短花柱(S-morph/Thrum)和長花柱(L-morph/Pin)[75]。在報(bào)春花科的IV類位點(diǎn)中，目前共發(fā)現(xiàn)5個(gè)基因：位點(diǎn)基因，位點(diǎn)基因，以及未知功能的、和[22]。其中，細(xì)胞色素家族成員CYP734A50在短花柱中特異表達(dá)，通過降解油菜素甾醇(brassi-nosteroids, BRs)來抑制細(xì)胞擴(kuò)張，進(jìn)而產(chǎn)生短花柱表型[76]。GLO2是一類花藥特異表達(dá)的MADS-box轉(zhuǎn)錄因子，通過控制管狀花冠中花絲著生點(diǎn)處的細(xì)胞擴(kuò)張來控制花藥高度[77]。Huu等[76]發(fā)現(xiàn)BR在長型花柱中十分豐富，而在短型花柱中幾乎檢測不到，提出長型花柱中豐富的BR可分別促進(jìn)和抑制短花柱花和長花柱花的花粉授精，因此短花柱和長花柱花給長花柱授粉后分別表現(xiàn)為親和與不親和；而在短花柱中由于CYP734A50促進(jìn)BR降解，因此短花柱和長花柱花給短花柱授粉后分別表現(xiàn)為不親和與親和。與報(bào)春花科不同，時(shí)鐘花科的V類位點(diǎn)包含3個(gè)基因：在花藥和花絲表達(dá)的及分別只在花藥和花柱表達(dá)的和[23]。其中，具有保守的BAHD酰基轉(zhuǎn)移酶活性域的TsBAHD與CYP734A50功能相似，通過抑制BR來調(diào)控花柱表型及花粉管生長[78](圖2)。此外，在同樣具有異型花柱SI的蕎麥和亞麻的位點(diǎn)中，基因類型也不同，例如亞麻超基因位點(diǎn)包含9個(gè)基因，其中和-在短花柱中特異表達(dá)[79]，但其功能還有待進(jìn)一步研究。

1.5 其他自交不親和性

菊科(Asteraceae)約包含30,000個(gè)種，是被子植物的第一大科，其中至少60%的植物表現(xiàn)為自交不親和。既不同于I類SI植物的濕柱頭，也不同于II類SI植物的干柱頭，菊科植物具有半干花柱[80]。菊科SSI最早報(bào)道于20世紀(jì)50年代，隨后在灰白銀膠菊()、秋英()、向日葵()、除蟲菊()、菊苣()和糙葉千里光()中相繼被發(fā)現(xiàn)，但其分子機(jī)制還不清楚。在菊苣中，Gonthier等[81]將位點(diǎn)定位至一個(gè)1.8 cM的QTL區(qū)域，然而并未報(bào)道其詳細(xì)基因。在全葉松香草()中，Price等[82]將位點(diǎn)定位于6號(hào)連鎖群一個(gè)18.9 cM的QTL區(qū)間內(nèi)，進(jìn)一步通過與向日葵17號(hào)染色體的共線性分析，發(fā)現(xiàn)12個(gè)緊密連鎖的-基因，但并未發(fā)現(xiàn)與其連鎖的-，與Zhao等[11]發(fā)現(xiàn)向日葵中不存在I類位點(diǎn)一致，表明其SI機(jī)制與I類不同。不僅如此，雖然同屬于SSI，研究人員在候選位點(diǎn)與其他菊科物種的共線區(qū)域中也未發(fā)現(xiàn)SRK類似基因[82]。盡管Tabah等[83]在糙葉千里光中克隆到一個(gè)雌蕊表達(dá)的-，但后續(xù)證明其并非雌蕊因子。因此，菊科SI應(yīng)該也不同于十字花科的II類SI機(jī)制。Wollenweber等[84]通過橡膠草()差異表達(dá)基因分析，鑒定到3個(gè)候選基因(、和)。Palumbo等[85]認(rèn)為()是控制菊苣自交不親和的關(guān)鍵候選基因，但其功能仍有待進(jìn)一步證實(shí)。

SI在豆科植物中也十分常見，其中云實(shí)亞科、含羞草亞科和蝶形花亞科中分別約有62.3%、66.7%和22.1%的物種為自交不親和[86]。與I類SI相似，豆科植物通常為濕柱頭且具有GSI，但目前對其SI的詳細(xì)分子機(jī)制知之甚少。由于白三葉()花柱對自交花粉管的抑制作用與I類SI相似，人們普遍認(rèn)為白三葉甚至豆科植物也采取I類SI系統(tǒng)。Casey等[87]雖然定位到了白三葉的單一位點(diǎn)，但并未報(bào)道其中是否包含緊密連鎖的和。Aguiar等[88]雖然在蒺藜苜蓿(L.)和鷹嘴豆()中鑒定到了I類位點(diǎn)的類似結(jié)構(gòu)，但其編碼的T2核酸酶和F-box并不分別在雌雄蕊中特異表達(dá)或高表達(dá)，且鷹嘴豆的候選花柱基因也不符合因子的序列多態(tài)性特征。因此，白三葉及其他豆科植物與I類SI的關(guān)系仍存在疑問。此外，作為被子植物的第三大科，豆科約包含650個(gè)屬，其自交不親和反應(yīng)在屬內(nèi)及屬間均表現(xiàn)出較大差異，可發(fā)生在柱頭、花柱、受精過程、合子后等多個(gè)階段[89]。例如，黃耆屬()、銀合歡屬()、百脈根屬()物種的自交不親和反應(yīng)發(fā)生于柱頭，羊蹄甲屬()、苜蓿屬()、車軸草屬()等物種對自交花粉管的抑制發(fā)生于花柱，而菜豆屬()、金合歡屬()、云實(shí)屬()等物種的花粉管則在到達(dá)胚珠后無法正常授精或授精后發(fā)生合子敗育等，這一現(xiàn)象可能是SI在豆科中經(jīng)歷高度動(dòng)態(tài)起源、丟失和重獲的結(jié)果。

1.6 真雙子葉植物自交不親和性的起源與演化

在已發(fā)現(xiàn)的真雙子葉五類SI系統(tǒng)中，I類SI起源最早且分布最為廣泛，而II～V類則分別為十字花科、罌粟科、報(bào)春花科和時(shí)鐘花科特有的SI系統(tǒng)(圖3)。對于I類SI，Xue等[90]率先提出其單一起源的觀點(diǎn)。I類花柱因子所屬的T2核酸酶共包含3個(gè)分支，分別命名為i、ii和iii類，其中S-RNase單獨(dú)聚為一支且屬于iii類。除了已報(bào)道具有I類SI系統(tǒng)的茄科、車前科、薔薇科和蕓香科外，錦葵科、茜草科、大戟科、葫蘆科、豆科、木犀科、山茶科和鼠李科等的T2核酸酶也可與iii類T2核酸酶/ S-RNase聚為一支，且該分支僅包含真雙子葉植物，因此I類花柱因子S-RNase單一起源于真雙子葉植物的最近共同祖先(most recent common ancestor, MRCA)[11,91,92]。與S-RNase不同，SLF/SFB/SFBB是否單起源一直存在爭議。直到近期，Zhao等[11]通過系統(tǒng)發(fā)育和遺傳學(xué)功能分析，證明與SLF和SFBB聚為一支的SFB同樣能夠解除茄科雜交矮牽牛()中S-RNase的細(xì)胞毒性，證明它們具有保守的I類花粉因子功能。此外，基部真雙子葉植物毛茛科耬斗菜()的也具有I類花粉功能，從而為I類SI單起源于真雙子葉植物的最近共同祖先提供了更加充分的證據(jù)[11]。

顯花植物在進(jìn)化過程中由于受到地理環(huán)境和種群繁衍的選擇壓力，其SI也會(huì)頻繁的丟失和重獲。Zhao等[11]提出顯花植物SI起源、丟失和重獲的高度動(dòng)態(tài)進(jìn)化過程主要包含3種丟失路徑(x: I類位點(diǎn)重復(fù); y:基因失活; z:位點(diǎn)缺失)和4種重獲路徑(a: 重復(fù)I類位點(diǎn)失活; b: 重復(fù)I類結(jié)構(gòu)刪除; c:基因再激活; d: 新位點(diǎn)的獲得)構(gòu)成[11]。研究發(fā)現(xiàn)，包括自交親和的耬斗菜和菜豆()在內(nèi)的多個(gè)真雙子葉植物基因組均具有2～3個(gè)I類位點(diǎn)，表明由于全基因組復(fù)制和路徑x所導(dǎo)致的I類SI丟失最為普遍。為了避免近交衰退，自交不親和的西班牙金魚草()、多毛番茄()和柚子()則在失活或刪除重復(fù)I類位點(diǎn)基礎(chǔ)上重獲I類SI。與之不同，自交親和的栽培金魚草()、栽培番茄()和擬南芥()均通過路徑y(tǒng)即分別失活S-RNase和SRK/SCR而丟失SI，十字花科、報(bào)春花科和時(shí)鐘花科在完全刪除I類位點(diǎn)即丟失古老的I類SI后又分別進(jìn)化出了新的II、IV和V類SI (路徑z和d)，菊科SI可能也是該進(jìn)化路徑。而罌粟科則在保留I類基礎(chǔ)上演化出新的III類，但前者的功能尚不清楚。

圖3 顯花植物自交不親和性的起源與演化

I～VI類自交不親和代表物種的科水平物種進(jìn)化樹。進(jìn)化樹由TimeTree (http://www.timetree.org/)生成。上方為地質(zhì)年代，下方數(shù)軸為演化時(shí)間軸，MYA (million years ago)為時(shí)間單位。不同顏色的圓圈及其對應(yīng)線條分別表示6類SI。橙色虛線表示古老I類結(jié)構(gòu)，綠色虛線代表無I類位點(diǎn)。

2 單子葉植物自交不親和性的分子與演化機(jī)制

2.1 VI類自交不親和性的分子機(jī)制

VI類SI由和雙位點(diǎn)控制，當(dāng)花粉的和單倍體型與雌蕊的和基因型均匹配時(shí)則為不親和[7～9]。雙位點(diǎn)控制的特性也使得不同來源的花粉給雌蕊授粉后可出現(xiàn)0、50%、75%和100%四種不同程度的親和現(xiàn)象[9](圖1)。SI在禾本科中分布非常廣泛，約16個(gè)屬表現(xiàn)為自交不親和。自20世紀(jì)50年代發(fā)現(xiàn)其由雙位點(diǎn)控制以來，研究人員嘗試在天藍(lán)虉草()、多年生黑麥草()、黑麥()、球莖大麥()和長雄蕊野生稻()等自交不親和物種中克隆和基因。盡管早期鑒定到一些分別能與和位點(diǎn)共分離的基因，但均未驗(yàn)證其遺傳學(xué)功能。Kakeda等[25]在球莖大麥中發(fā)現(xiàn)雌蕊特異表達(dá)的可與位點(diǎn)連鎖，將其作為候選雌蕊因子。在多年生黑麥草和黑麥中，和位點(diǎn)分別被定位至1號(hào)和2號(hào)染色體[28,93～96]。Rohner等[28]提出和位點(diǎn)具有相似的基因構(gòu)成，二者均可編碼兩個(gè)序列多態(tài)且花藥特異表達(dá)的含DUF247結(jié)構(gòu)域蛋白和一個(gè)雌蕊特異表達(dá)的分泌小肽，與Manzanares等[27]和Shinozuka等[26]分別將1個(gè)編碼DUF247結(jié)構(gòu)域蛋白的基因作為候選花粉和基因一致。在稻屬唯一自交不親和物種長雄蕊野生稻中，Lian等[24]通過序列相似性分析發(fā)現(xiàn)多個(gè)候選基因，其中花粉候選基因和與多年生黑麥草的類似，雌蕊候選基因與球莖大麥同源，并且發(fā)現(xiàn)其連鎖結(jié)構(gòu)與多年生黑麥草的位點(diǎn)共線。盡管如此，這些候選和基因的分子遺傳學(xué)功能均鮮有報(bào)道。直到近期，研究人員首次利用基因編輯技術(shù)證明敲除雌蕊基因-和花粉基因-可分別打破長雄蕊野生稻雌蕊和花粉的SI，且進(jìn)一步通過自交T1代基因型分析和互作檢測發(fā)現(xiàn)雌蕊分泌的HPS10-S與花粉跨膜蛋白DUF247I-S以自己識(shí)別為主，但其如何引起自交不親和反應(yīng)尚不明確[97](圖2)。Chen等[98]通過羊草()自交和異交授粉雌蕊的轉(zhuǎn)錄組分析，發(fā)現(xiàn)雌蕊對自交花粉的拒絕可能與鈣離子和植物激素相關(guān)信號(hào)引發(fā)的PCD有關(guān)。

2.2 單子葉植物自交不親和性的起源與演化

VI類SI是單子葉植物中已知分子機(jī)制的唯一SI系統(tǒng)。其中，VI類花柱因子-僅存在于禾本科的稻亞科、早熟禾亞科和黍亞科，而編碼DUF247結(jié)構(gòu)域的花粉同源基因則廣泛存在于裸子和被子植物[97]。此外，研究發(fā)現(xiàn)，與一樣能夠編碼FBA/FBK結(jié)構(gòu)域的-基因也可與i/ii類T2連鎖且該類結(jié)構(gòu)在顯花植物起源之初即已存在[11](圖3)。盡管目前并不清楚其是否參與SI，但該古老I類位點(diǎn)與禾本科VI類共存的現(xiàn)象與罌粟科中I類與III類共存較為相似，提示禾本科可能通過與真雙子葉植物x和d進(jìn)化路徑類似的方式在丟失了古老的I類SI后獲得了新的VI類SI系統(tǒng)，進(jìn)一步對其他單子葉植物SI分子機(jī)制及其與古老I類位點(diǎn)演化關(guān)系的研究有望為顯花植物SI的起源和演化提供新的知識(shí)和線索。

3 顯花植物自交不親和性的育種應(yīng)用

在生產(chǎn)實(shí)踐中，SI雖然可以通過限制自交省去人工去雄等工作，但是不利于自交制種和純系培育。目前已發(fā)現(xiàn)能夠克服SI的方法主要涉及物理、化學(xué)和分子3個(gè)層面。

物理法包括射線或高溫處理、外科技術(shù)等。其中，利用γ-或x-射線輻照花粉人工授粉可顯著改善自交不親和表型，常用于水果作物自交親和栽培種的創(chuàng)制[99,100]。Townsend[101]基于雜三葉草的研究提出高溫處理可使溫度敏感基因與自交不親和基因互作，從而誘發(fā)高溫自交親和性。在菊科植物中，35℃～40℃高溫處理 24～48 小時(shí)可通過影響花柱的SI使其獲得自交種，而花柱CLE45則通過在高溫下保護(hù)花粉管生長從而誘發(fā)自交親和[102]。對于自交不親和反應(yīng)發(fā)生于柱頭的植物，人們還嘗試切除或浸泡柱頭以阻斷其對自交花粉的識(shí)別[103]。此外，對于開花前花柱和花粉即已成熟的植物，剝蕾授粉也能促進(jìn)自交傳粉[104]。

與物理法相比，化學(xué)處理在打破SI中應(yīng)用更為廣泛。例如，施加乙醚、3%～5%的二氧化碳、氯化鈉、氫氧化鉀等可人為打破十字花科SI，其中最為有效的二氧化碳處理法已被廣泛應(yīng)用于十字花科蔬菜作物的自交種繁育[105]。在糙葉千里光中，用5%鹽溶液處理可產(chǎn)生假性自交親和個(gè)體[106]。授粉前使用赤霉素處理可改善梅()柱頭的生理環(huán)境使其更利于花粉萌發(fā)和花粉管生長并產(chǎn)生較高的結(jié)實(shí)率[107]。在菊花花期利用50 mg/L的赤霉素處理也可促進(jìn)自交結(jié)籽[108]。與之類似，外源噴施氨基酸、多胺、磷脂酸等可通過促進(jìn)花粉管生長導(dǎo)致自交親和，使用鈣離子通道和激酶抑制劑還可打破黑麥和多年生黑麥草的SI[109,110]。

隨著自交不親和控制基因的成功克隆及其分子作用機(jī)制的詳細(xì)解析，人們開始嘗試?yán)没蚓庉嫽蚋蓴_技術(shù)直接敲除或抑制基因或其他信號(hào)轉(zhuǎn)導(dǎo)因子來打破SI。例如，利用CRISPR/Cas9敲除-后成功獲得自交親和的二倍體馬鈴薯[111,112]，敲除長雄蕊野生稻基因后獲得穩(wěn)定遺傳的自交親和植株[97]。對于具有I類SI的物種，也可利用轉(zhuǎn)基因打破SI。但是，這些方法普遍受限于成熟的遺傳轉(zhuǎn)化和編輯體系，特別是在一些野生種和多倍體物種中。此外，人們先后發(fā)現(xiàn)一些親和位點(diǎn)并嘗試將其導(dǎo)入SI物種以創(chuàng)制自交系，例如從野生馬鈴薯()自交親和突變體中鑒定到的(-)已用于馬鈴薯的自交和雜交制 種[113～115]，在多年生黑麥草中也發(fā)現(xiàn)了和親和位點(diǎn)[116,117]。然而，通過漸滲引入親和位點(diǎn)往往具有耗時(shí)較長且易產(chǎn)生附加性狀等缺點(diǎn)。綜上，通過分子手段打破SI并有效應(yīng)用于現(xiàn)代育種仍面臨一定挑戰(zhàn)。

4 結(jié)語與展望

異交授粉為后代基因組變異提供了最大可能性，而廣泛分布的異交促進(jìn)機(jī)制SI則為種群物種多樣性的維持和適應(yīng)生存提供了保障。被子植物快速擴(kuò)張的原因一直備受關(guān)注，而SI的起源和演化可能是其物種分化和種群擴(kuò)張的一個(gè)重要驅(qū)動(dòng)力。SI不僅是一個(gè)有趣的生物學(xué)問題，由于其對自交系創(chuàng)制的嚴(yán)重限制，長期以來還受到園藝、飼草、作物學(xué)家等的廣泛重視，挖掘和解析SI的分子調(diào)控網(wǎng)絡(luò)對于解除現(xiàn)代育種瓶頸至關(guān)重要。

目前盡管對I～VI類SI的分子和演化機(jī)制有了一定認(rèn)識(shí)，但仍存在一些尚未解決的問題，主要包括自交不親和植物的遺傳轉(zhuǎn)化和基因編輯體系建立及基因的遺傳學(xué)功能驗(yàn)證、花柱和花粉因子如何特異識(shí)別以區(qū)分自交和異交花粉、單子葉和真雙子葉植物SI的起源和演化關(guān)系等。功能缺失和獲得實(shí)驗(yàn)是候選基因遺傳功能驗(yàn)證的必要方法，而大多數(shù)顯花植物的遺傳轉(zhuǎn)化和基因編輯技術(shù)仍不成熟，進(jìn)一步完善相關(guān)體系有望為顯花植物SI的分子機(jī)制提供新知識(shí)。隨著蛋白質(zhì)結(jié)構(gòu)解析及原位示蹤技術(shù)的發(fā)展，未來對因子復(fù)合體結(jié)構(gòu)及其動(dòng)態(tài)變化的體外重構(gòu)和體內(nèi)觀測有望提升人們對自己和異己識(shí)別及其信號(hào)轉(zhuǎn)導(dǎo)機(jī)制的理解和認(rèn)識(shí)。此外，目前僅對單子葉禾本科植物的分子和演化機(jī)制有所了解，進(jìn)一步對其他單子葉植物SI機(jī)制及其與真雙子葉植物SI起源和演化關(guān)系的研究將為SI與被子植物早期快速擴(kuò)張的關(guān)系提供新線索。

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Molecular and evolutionary mechanisms of self-incompatibility in angiosperms

Hong Zhao, Yongbiao Xue

As an intraspecific outcrossing mechanism, self-incompatibility (SI) widely adopted by hermaphroditic plants is usually controlled by a polymorphic multi-alleliclocus. Typically, six molecular types of SI have been found, including type-I controlled by the pistil-and pollens commonly spread in Plantaginaceae, Solanaceae, Rosaceae and Rutaceae, type-II byandin Brassicaceae, type-III byandin Papaveraceae, type-IV by----in Primulaceae, type-V by-in Turneraceae and type-VI by-and-in Poaceae, with type-I characterized as a non-self recognition system but types-II, -III and -VI self ones.Furthermore, remarkable progresses have been made in their origin and evolutionary mechanisms recently. Among them, type-I SI possessed a single origin in the most recent common ancestor of eudicots and types II-V dynamically evolved following its losses, while type-VI SI exclusively existed in monocot Poaceae may be regained after the loss of the ancient type-I. Here, we mainly review the molecular and evolutionary mechanisms of angiosperm SI systems, thus providing a helpful reference for their theoretical research and breeding application.

angiosperms; self-incompatibility; origin; evolution; inbred lines; crossbreeding

薛勇彪研究員主要從事植物分子遺傳學(xué)領(lǐng)域研究，在植物自交不親和性、重要基因功能解析和基因組分析等領(lǐng)域做出了重要科學(xué)發(fā)現(xiàn)，發(fā)表SCI論文150余篇，2020～2022年獲愛思唯爾生物學(xué)中國高被引學(xué)者，2007年獲國家自然科學(xué)二等獎(jiǎng)2項(xiàng)，分別為“顯花植物自交不親和性分子機(jī)理”和“水稻第四號(hào)染色體測序及功能分析”，曾任中國科學(xué)院遺傳與發(fā)育生物學(xué)研究所和北京基因組研究所(國家生物信息中心)所長、第十屆中國遺傳學(xué)會(huì)理事長、水稻功能基因組973項(xiàng)目和中國科學(xué)院A類先導(dǎo)專項(xiàng)首席科學(xué)家，()榮譽(yù)主編、、()、、()等雜志編委或顧問。

2023-12-01;

2023-12-29;

2024-01-01

國家自然科學(xué)基金項(xiàng)目(編號(hào)：32200273，32030007) 資助[Supported by the National Natural Science Foundation of China (Nos. 32200273, 32030007)]

趙洪，博士，副研究員，研究方向：顯花植物自交不親和性。E-mail: zhhong@genetics.ac.cn

薛勇彪，博士，研究員，研究方向：顯花植物自交不親和性。E-mail: ybxue@genetics.ac.cn

10.16288/j.yczz.23-300

(責(zé)任編委: 孔凡江)