染色質(zhì)重塑及其參與植物病害防御應(yīng)答的研究進(jìn)展

洪　林,　魏召新,　魏文輝,　譚　平*

(1. 重慶市農(nóng)業(yè)科學(xué)院果樹研究所, 重慶　402260; 2. 中國農(nóng)業(yè)科學(xué)院油料作物研究所,農(nóng)業(yè)部油料作物生物學(xué)與遺傳育種重點實驗室, 武漢　430062)

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專論與綜述

染色質(zhì)重塑及其參與植物病害防御應(yīng)答的研究進(jìn)展

洪林1,魏召新1,魏文輝2,譚平1*

(1. 重慶市農(nóng)業(yè)科學(xué)院果樹研究所, 重慶402260; 2. 中國農(nóng)業(yè)科學(xué)院油料作物研究所,農(nóng)業(yè)部油料作物生物學(xué)與遺傳育種重點實驗室, 武漢430062)

轉(zhuǎn)錄相關(guān)因子與特異DNA位點結(jié)合受染色質(zhì)空間構(gòu)象變化的調(diào)節(jié),通過染色質(zhì)重塑機制可以解除染色質(zhì)高度緊密的折疊狀態(tài),改變組蛋白與DNA鏈間的作用力,控制基因的表達(dá)與沉默。ATP依賴的染色質(zhì)重塑復(fù)合物、組蛋白的乙?；?去乙?；图谆?去甲基化共價修飾等是染色質(zhì)修飾的主要類型,植物能通過染色質(zhì)重塑復(fù)合物和組蛋白修飾酶復(fù)合物直接或間接介導(dǎo)的染色質(zhì)重塑作用調(diào)控防御基因的轉(zhuǎn)錄,控制植物對病原體侵染的防御應(yīng)答。本文結(jié)合近年來的研究進(jìn)展,對植物染色質(zhì)重塑如何調(diào)控防御相關(guān)基因的表達(dá)及病原體蛋白T3SEs、6b和VirE等如何利用染色質(zhì)重塑干預(yù)植物防御系統(tǒng)的分子機制進(jìn)行了論述。

植物;核小體;染色質(zhì)重塑;防御應(yīng)答

真核生物基因組DNA通常由146 bp的染色質(zhì)DNA圍繞H2A、H2B、H3、H4形成的核心組蛋白八聚體包裝成核小體結(jié)構(gòu),組蛋白H1再結(jié)合于各核小體間的連接DNA上,最終形成串珠樣結(jié)構(gòu)[1]。染色質(zhì)高級結(jié)構(gòu)的組裝、維持及構(gòu)象改變則是通過核小體高度有序的自我調(diào)節(jié)來調(diào)控的,而核小體因其結(jié)構(gòu)的特殊性,能阻礙轉(zhuǎn)錄因子與染色質(zhì)上靶基因的特異識別位點結(jié)合并起始特定基因的表達(dá)。然而,真核生物能借助于一些具有酶活性的復(fù)合物的作用來改變?nèi)旧|(zhì)的結(jié)構(gòu)形態(tài),通過染色質(zhì)高級結(jié)構(gòu)的各種變化增加基礎(chǔ)轉(zhuǎn)錄裝置與啟動子的可接近性,對染色質(zhì)賦予的生物學(xué)功能進(jìn)行調(diào)控。

染色質(zhì)重塑是目前表觀遺傳領(lǐng)域的研究熱點之一,它能驅(qū)動核小體的置換或重新排列,改變?nèi)旧|(zhì)的空間構(gòu)象。組蛋白H3和H4的甲基化、乙酰化修飾,ATP依賴的染色質(zhì)構(gòu)象變化等是染色質(zhì)重塑的主要方式,均能使染色質(zhì)特定區(qū)域?qū)嗣傅姆€(wěn)定性發(fā)生變化,調(diào)控基因轉(zhuǎn)錄[2]。染色質(zhì)重塑在植物防御相關(guān)基因的表達(dá)調(diào)控中發(fā)揮著關(guān)鍵作用,病原體侵染植物組織后,組蛋白修飾酶、ATP依賴性染色質(zhì)重塑相關(guān)因子和其他一些調(diào)節(jié)蛋白被招募到防御相關(guān)基因的轉(zhuǎn)錄控制區(qū)域。參與染色質(zhì)重塑復(fù)合體形成的許多蛋白亞基影響MAPK級聯(lián)信號、SA信號轉(zhuǎn)導(dǎo)、ABA信號轉(zhuǎn)導(dǎo)等途徑,進(jìn)而由PTI(PAMP-triggered immunity) 和ETI(effector-triggered immunity)介導(dǎo)轉(zhuǎn)錄水平上的重編程,激活或抑制植物的防御系統(tǒng)[3-4]。本文就染色質(zhì)重塑的主要方式,染色質(zhì)重塑調(diào)控植物防御應(yīng)答的機制,病原體如何調(diào)控染色質(zhì)重塑干擾植物防御系統(tǒng)等方面予以綜述,并展望該領(lǐng)域存在的問題及未來發(fā)展方向。

1　染色質(zhì)重塑的方式

目前在動植物中發(fā)現(xiàn)至少有兩類高度保守的染色質(zhì)修飾類型。第一類是通過水解ATP提供能量形成ATP依賴的染色質(zhì)重塑復(fù)合物,進(jìn)而改變核小體的位置,增強DNA 序列與轉(zhuǎn)錄因子的相互作用程度,改變組蛋白與DNA鏈之間的空間構(gòu)象[5];第二類是組蛋白尾部賴氨酸的乙?；头核鼗?蘇氨酸和絲氨酸的磷酸化,精氨酸的甲基化,谷氨酸的多聚ADP 核糖基化等共價修飾形成組蛋白修飾酶復(fù)合物(histone-modifying complex),破壞了基因組DNA與核小體、組蛋白尾部間的結(jié)構(gòu),間接引起染色質(zhì)的重塑[6-7]。

1.1ATP依賴的復(fù)合物介導(dǎo)染色質(zhì)重塑過程

ATP依賴的染色質(zhì)重塑復(fù)合物為大分子量的多組分復(fù)合體,包含4～17個不同種類的亞基,且在真核生物中高度保守。ATPase亞基為其中一類最重要的蛋白質(zhì)成分,具有催化和轉(zhuǎn)位酶活性,屬于SNF2超家族,存在于已知的ATP依賴的染色質(zhì)重塑復(fù)合物中[8]。核心ATPase亞基的保守結(jié)構(gòu)域由DExx和HELICc組成,兩個保守基序被一段長度存在變異的連接序列所間隔,基于各自獨特結(jié)構(gòu)域?qū)TPase亞基至少可分為SWI/SNF(yeast mating-type switching/sucrose non-fermenting)、INO80、ISWI、CHD等4個亞家族,關(guān)于SWI/SNF復(fù)合物方面的研究最多[9](圖1)。

圖1　ATPase亞基家族的結(jié)構(gòu)域比較[9]Fig.1　The comparison of protein domains in ATPase family[9]

SWI/SNF復(fù)合物最早是從酵母(Saccharomycescerevisiae)中純化得到的[10]。該復(fù)合物由8～14個蛋白亞基組成,分子量約1.5 MDa[11]。酵母主要有SWI/SNF和RSC兩種復(fù)合物類型,前者以SWI2或SNF2為ATPase催化亞基,而后者為Sth1[10]。擬南芥(Arabidopsisthaliana) SWI/SNF的組成亞基主要有SPLAYED (SYD)、BRAHMA(BRM)、CHR12、CHR23、ATBRCA1、BRG1、ATSWI3A、ATSWI3B、ATSWI3C和ATSWI3D等[12]。果蠅(Drosophilamelanogaster)中也發(fā)現(xiàn)與酵母SWI/SNF具有較高同源性的BRAHMA結(jié)合相關(guān)蛋白BAP和溴區(qū)相關(guān)的BAP兩種形式的重塑復(fù)合物,BRAHMA、Moira、SNR1、BAP60、BAP55等5種亞基為共有的核心組分,OSA亞基、溴區(qū)(bromodomain)及BAP170亞基在兩類復(fù)合體間表現(xiàn)一定的特異性。此外,BAP111亞基盡管未在酵母中被鑒定出,但卻被認(rèn)為可能與果蠅染色質(zhì)的高級形態(tài)結(jié)構(gòu)相關(guān)聯(lián)[13]。人類SWI/SNF同源復(fù)合體為BAF和PBAF,分子量約為2 MDa,兩者同源性達(dá)到74%,BAF包含hBRM和BRG1兩個ATPase催化亞基,但PBAF的形成沒有hBRM亞基的參與,兩者在體外試驗中表現(xiàn)出相似的生化活性,但在許多細(xì)胞代謝途徑中發(fā)揮不同的功能[14]。目前關(guān)于BRG1及其同源基因的功能研究報道較多,BRG1結(jié)構(gòu)域包括一個進(jìn)化上保守的ATP水解酶活性區(qū)域、C端溴區(qū)、AT-hook基序及N端QLQ、HAS和BRK等。參與機體內(nèi)的多種生理和病理調(diào)控過程[15]。其中,C端溴區(qū)能夠特異性識別組蛋白H3和H4末端乙?；馁嚢彼醄16]?？傮w來看,真核細(xì)胞SWI/SNF 復(fù)合物基于SWI/SNF/BAP/BAF和RSC/PBAP/PBAF兩種模式而建立,可能還有特異性亞基和其他因子參與的多種形式共存。

關(guān)于SWI/SNF復(fù)合物調(diào)控染色質(zhì)的重塑機制仍未被闡明,科學(xué)家認(rèn)為重塑可能與啟動子特性、染色質(zhì)狀態(tài)、SWI/SNF復(fù)合物的濃度、DNA結(jié)合因子等有關(guān)。目前主要有以下3種假說:滑動模型、組蛋白突變體交換模型、重獲環(huán)模型[17-18]。

1.2組蛋白共價修飾參與染色質(zhì)重塑

組蛋白修飾是染色質(zhì)重塑的關(guān)鍵調(diào)控方式之一。乙?；?、甲基化、泛素化、磷酸化、蘇素化等多種共價修飾常發(fā)生在組蛋白N端,組蛋白H3和H4的共價修飾直接影響染色質(zhì)結(jié)構(gòu)。乙?；图谆亲钪饕男揎椃绞?且此過程是可逆的。

1.2.1組蛋白乙?；c去乙?；?/p>

乙?；揎椧鸬娜旧|(zhì)結(jié)構(gòu)重塑是基因轉(zhuǎn)錄調(diào)控的重要調(diào)節(jié)因素,組蛋白乙?；D(zhuǎn)移酶(HATs)和組蛋白去乙?；?HDACs)共同控制組蛋白末端的乙?；?激活或抑制基因轉(zhuǎn)錄。目前已經(jīng)發(fā)現(xiàn)的與真核生物染色質(zhì)重塑相關(guān)的HATs有GCN5、P300/CBP、TAFII250、MYST、PCAF等[19];HDACs主要有RPD3、HDAC1、HDAC2、HDAC3、HD1BI、HD1BII、HD2等,參與NCoR/SMRT、SIN3、NuRD及CoREST等HDACs復(fù)合物的組裝[20]。

核小體核心組蛋白的N末端尾部保守的賴氨酸(K)是組蛋白的乙酰化位點,組蛋白乙?；癄顟B(tài)呈多樣性,能使ATP依賴的重塑復(fù)合物更加緊密地與DNA模板結(jié)合。組蛋白N末端尾部的賴氨酸乙?；苤泻推湔姾?促使染色質(zhì)形成能與調(diào)控蛋白結(jié)合的特定結(jié)構(gòu),進(jìn)而引發(fā)轉(zhuǎn)錄起始[21]。研究發(fā)現(xiàn)單一的HAT能乙酰化游離組蛋白,然而核小體組蛋白的乙?；瘎t需要包含HAT的多蛋白復(fù)合物介導(dǎo)下才可能實現(xiàn),如FACT、HMG14等染色質(zhì)修飾因子也參與不同核心組蛋白賴氨酸的乙?；^程[22]。重組的GCN5僅乙?；揎椊M蛋白H3、H4單體,而含有GCN5的兩大復(fù)合物ADA和SAGA才能將核小體結(jié)構(gòu)中組蛋白H3、H4乙?；痆23],PRZ1能通過調(diào)節(jié)GCN5活性影響GCN5/HAG1復(fù)合物參與的染色質(zhì)重塑效率[24]。組蛋白乙?；c去乙?；芨淖兣R近組蛋白甲基化修飾狀態(tài),H3K9和H3K14的乙?；揎椏梢约訌娹D(zhuǎn)錄因子TFⅡD與H3K4me3間的作用[25]。ING4作為HBO1組蛋白乙酰轉(zhuǎn)移酶復(fù)合體的一個重要亞基,卻能與H3K4me3位點結(jié)合,招募HBO1復(fù)合體,乙?；揎棸谢騿幼訁^(qū)的組蛋白,改變?nèi)旧|(zhì)結(jié)構(gòu),影響特定基因的表達(dá)[26]。

1.2.2組蛋白甲基化與去甲基化

組蛋白甲基化修飾在基因轉(zhuǎn)錄調(diào)控中發(fā)揮十分重要的作用。賴氨酸和精氨酸(R)殘基為主要的修飾位點。H3K4、H3K9、H3K27、H3K36、H3K79、H4K20等位點甲基化修飾后參與染色質(zhì)結(jié)構(gòu)重塑和基因表達(dá)調(diào)控,其中H3K4、H3K36、H3K79的甲基化修飾激活基因轉(zhuǎn)錄,而H3K9、H3K27、H4K20甲基化修飾抑制轉(zhuǎn)錄;H3R2、H3R8、H3R17、H3R26、H4R3是精氨酸甲基化的修飾位點。此外同一位點可能分別有一甲基化(me1)、二甲基化(me2)、三甲基化(me3)三種方式[27]。組蛋白甲基化修飾也往往與組蛋白乙?；NA甲基化等其他表觀遺傳學(xué)修飾協(xié)同作用,共同調(diào)節(jié)染色質(zhì)結(jié)構(gòu),影響基因轉(zhuǎn)錄。

組蛋白的甲基化修飾由一類含SET結(jié)構(gòu)域的甲基轉(zhuǎn)移酶介導(dǎo)。目前已經(jīng)發(fā)現(xiàn)和證實真核生物中存在數(shù)十種組蛋白賴氨酸甲基轉(zhuǎn)移酶(HKMTs)和精氨酸甲基轉(zhuǎn)移酶(PRMTs),它們參與染色質(zhì)結(jié)構(gòu)的形成、基因組印記及轉(zhuǎn)錄調(diào)控等多種生理功能的執(zhí)行[28]。H3K9位點的甲基化修飾頻率較高,如Su(var)3-9可以特異地甲基化修飾H3K9,招募HP1與組蛋白H3結(jié)合,影響染色質(zhì)構(gòu)象[29],而SETDB1催化的H3的N末端甲基化可以增強HP1與H3的結(jié)合能力[30]。HP1和甲基化的染色質(zhì)相互作用,抑制基因轉(zhuǎn)錄[31],SET2、SET1、NSD1、PCG、Dot1等其他HKMTs也在染色質(zhì)表觀遺傳調(diào)控中起關(guān)鍵作用。

目前,已從真核生物中鑒定出約11種PRMTs。PRMT2、10和11不具有催化精氨酸甲基化的功能, PRMT1和PRMT4的甲基化修飾激活基因的轉(zhuǎn)錄,而PRMT5和PRMT6與轉(zhuǎn)錄抑制相關(guān)。PRMT5與PRMT1、PRMT4(也稱為CARM1)均能與染色質(zhì)重塑復(fù)合物發(fā)生作用,調(diào)節(jié)染色質(zhì)構(gòu)象變化[32]。PRMT1和CARM1結(jié)合組蛋白乙?；?并與染色質(zhì)重塑復(fù)合物發(fā)生相互作用,導(dǎo)致染色質(zhì)結(jié)構(gòu)的解體并激活轉(zhuǎn)錄,而PRMT5則募集組蛋白去乙?；窰DAC,降低轉(zhuǎn)錄效率[33]。

但去甲基化酶的數(shù)量仍然較少,已發(fā)現(xiàn)與精氨酸相關(guān)的有PADI4、JMJD6;與賴氨酸相關(guān)的有LSD1、JHDM1、JHDM2、JHDM3/JMJD2、JARID1[34]。是否存在其他特異酶參與組蛋白的去甲基化,去甲基化酶家族成員的多樣性,去甲基修飾后激活或抑制轉(zhuǎn)錄的機制等為未來工作的重點。

2　染色質(zhì)重塑調(diào)節(jié)植物的防御機制

2.1ATP依賴的染色質(zhì)重塑因子調(diào)控植物防御應(yīng)答

至今為止,科學(xué)家已從擬南芥中分離鑒定出42個SNF2家族ATP酶亞基,這些亞基聚類為24個不同的亞族。它們之中SNF2亞族的SPLAYED(SYD)和BRAHMA (BRM)、SWR1亞族的PIE1、LSH亞族的DDM1和AGO4等被認(rèn)為具有調(diào)節(jié)植物防御應(yīng)答的能力[35]。

SYD和BRM具有特異性和相同的防御相關(guān)基因靶位點,兩者均能與ATSWI3B和ATSWI3C互作,但僅SYD的N端能選擇性結(jié)合ATSWI3A。高通量轉(zhuǎn)錄組分析發(fā)現(xiàn),SYD和BRM調(diào)控擬南芥全基因組1%的基因表達(dá)[36]。SYD-2突變體受病原菌丁香假單胞菌番茄致病變種(Pseudomonassyringaepv. Tomato DC3000, Pst DC3000)侵染后促使SA應(yīng)答基因PR1的上調(diào)表達(dá),暗示SYD可能為SA信號途徑的負(fù)調(diào)控子,SYD結(jié)合特異性分子伴侶,以復(fù)合物形式參與防御相關(guān)基因的啟動子目標(biāo)區(qū)域的調(diào)節(jié)。SYD突變型植株仍能對PstDC3000的侵染作出防御應(yīng)答,這可能與PstDC3000分泌T3SEs有關(guān)[36]。PR1基因在BRM-101突變株中的表達(dá)增強,但仍然缺乏BRM直接參與植株抗性調(diào)節(jié)的證據(jù)。T3SS功能缺失突變的細(xì)菌性斑點病菌丁香假單胞菌(Pseudomonassyringae)可能是研究SYD和BRM在植物防御反應(yīng)中如何發(fā)揮作用的經(jīng)典試材,BRM能在體外與組蛋白H3和H4結(jié)合,BRM結(jié)構(gòu)域中包含有1個溴區(qū)及3個不同序列特征的DNA結(jié)合區(qū)域,缺少其中1個DNA結(jié)合區(qū)的突變體的表型介于野生型和完全突變型之間,進(jìn)一步表明BRM的完整生物學(xué)功能的實現(xiàn)依賴于3個特征DNA結(jié)合域[37]。許多染色質(zhì)重塑蛋白(CHR)結(jié)構(gòu)域中含有溴區(qū),可特異性識別組蛋白H3和H4末端乙?；馁嚢彼嵛稽c,通過乙酰化和隨后染色質(zhì)的組裝參與信號依賴性的、非基礎(chǔ)性的基因轉(zhuǎn)錄調(diào)控[38]。溴區(qū)直接介導(dǎo)組蛋白乙酰轉(zhuǎn)移酶相關(guān)的共激活子與組蛋白之間的互作,乙?；馁嚢彼釟埢鶠樘禺愋宰饔梦稽c[39]。進(jìn)一步深入研究溴區(qū)結(jié)構(gòu)域是否存在其他染色質(zhì)結(jié)合熱點對建立和闡明BRM在植物免疫反應(yīng)中的作用模式具有重要的指導(dǎo)意義。

PIE1是PstDC3000激發(fā)的植物防御應(yīng)答反應(yīng)過程中的負(fù)調(diào)節(jié)子。研究發(fā)現(xiàn)PIE1突變體的許多防御相關(guān)基因組成性表達(dá),通常病原體侵染后這些基因的轉(zhuǎn)錄被抑制[40]。PIE1與組蛋白變體H2A.Z的共價修飾有關(guān),且H2A.Z在染色質(zhì)PIE1調(diào)控位點的募集需要PIE1參與,PIE1或H2A.Z突變體均表現(xiàn)對PstDC3000的抗性增強,推測PIE1介導(dǎo)H2A.Z與防御相關(guān)的靶基因位點結(jié)合可能抑制染色質(zhì)轉(zhuǎn)錄狀態(tài)[40-41]。H2A.Z通常結(jié)合在核小體側(cè)翼轉(zhuǎn)錄起始位點,調(diào)節(jié)熱響應(yīng)基因的轉(zhuǎn)錄,控制不同環(huán)境溫度條件下植物的生長發(fā)育[42]。

DDM1包含一個保守的SNF2-ATP酶結(jié)構(gòu)域,至今未發(fā)現(xiàn)其含有SET結(jié)構(gòu)域或甲基轉(zhuǎn)移酶活性[43]。但是DDM1具有維持甲基化和轉(zhuǎn)座子沉默的能力[44],這可能是通過DDM1的染色質(zhì)重塑活性來調(diào)節(jié)甲基轉(zhuǎn)移酶和去甲基化酶結(jié)合染色質(zhì)轉(zhuǎn)錄區(qū)實現(xiàn)[45-46]。DDM1突變植株全基因組發(fā)生低甲基化,大大抑制基因沉默現(xiàn)象[47]。突變導(dǎo)致DDM1功能喪失,染色質(zhì)結(jié)構(gòu)改變,PR1和PR2組成性表達(dá),抗病基因SNC1表達(dá)上調(diào),因此DDM1表現(xiàn)為防御應(yīng)答的負(fù)調(diào)控因子[48]。至于植物DDM1基因調(diào)控病原激發(fā)的防御反應(yīng)機制仍有許多不明之處。此外,在擬南芥中還發(fā)現(xiàn)另外一種蛋白AGO4,該蛋白調(diào)節(jié)RNA介導(dǎo)的DNA甲基化(RdDM)和基因沉默,正調(diào)控植物對病原體的主動防御[49]。

2.2組蛋白甲基化介導(dǎo)的植物防御應(yīng)答

與乙?；啾?甲基化的效應(yīng)更加多樣化。組蛋白H3甲基化依賴于精氨酸和賴氨酸特定殘基的修飾能發(fā)揮激活或抑制轉(zhuǎn)錄的雙重作用[50]。植物中已報道的調(diào)節(jié)防御應(yīng)答的組蛋白甲基化修飾酶有ATX1(arabidopsis homolog of trithorax 1)和SDG8(SET domain group 8)兩種。

ATX1屬于Trithorax家族成員,含有非常保守的SET結(jié)構(gòu)域[51]。H3K4的低水平三甲基化會引起ATX1靶基因的表達(dá)整體下調(diào)[52],但ATX1本身只影響染色質(zhì)某些特定部位的核小體H3K4甲基化修飾[53]。研究發(fā)現(xiàn)擬南芥ATX1在PstDC3000的T3SS功能缺失突變體激發(fā)的植物基礎(chǔ)抗性系統(tǒng)中起正調(diào)控作用,ATX1激活WRKY70表達(dá),WRKY70是SA及JA/ET介導(dǎo)的防御信號途徑中的關(guān)鍵轉(zhuǎn)錄因子[54]。ChIP試驗結(jié)果表明WRKY70可能為ATX1執(zhí)行組蛋白甲基化酶功能的初級靶因子,SA應(yīng)答基因PR1、JA應(yīng)答基因THI2.1為次級靶因子,PR1和THI2.1維持染色質(zhì)相應(yīng)區(qū)域保持開放的修飾狀態(tài),促進(jìn)防御相關(guān)基因的轉(zhuǎn)錄[55]。SDG8在PstDC3000激發(fā)的植物防御反應(yīng)中扮演“分子開關(guān)”的角色,調(diào)節(jié)NB-LRR類基因的LAZ5和RPM1表達(dá),但不影響RPS2、RPS4等基因的轉(zhuǎn)錄。SDG8能特異性催化H3K36的二甲基化和三甲基化修飾[56],研究發(fā)現(xiàn)病原體侵染過程中染色體LAZ5區(qū)域H3K36三甲基化程度變高[57]。

植物組蛋白修飾突變體改變了自身的抵抗力,但對于防御相關(guān)基因靶位點的特異性和相關(guān)染色質(zhì)特征信號的研究仍不明確。組蛋白多樣性的修飾及時空組合與生物學(xué)功能的關(guān)系可作為一種重要的表觀標(biāo)志,即“組蛋白密碼”。組蛋白修飾以協(xié)同或漸進(jìn)的動態(tài)轉(zhuǎn)錄調(diào)控方式誘導(dǎo)植物特異的下游防御應(yīng)答。

2.3組蛋白去乙?；{(diào)控植物防御應(yīng)答

組蛋白H3和H4的乙?；揎椗c基因活化密切相關(guān)。乙?；负腿ヒ阴；高x擇性修飾使組蛋白乙?；奖３制胶鉅顟B(tài)[50]。

研究發(fā)現(xiàn)兩類HDACs在植物免疫調(diào)節(jié)中發(fā)揮作用,細(xì)菌性斑點病菌PstDC3000能增強HDA19的表達(dá),HDA19作為防御反應(yīng)的正調(diào)控因子,而轉(zhuǎn)錄因子WRKY38和WRKY62負(fù)調(diào)控病程相關(guān)基因PR的表達(dá),WRKY38和WRKY62募集HDA19形成復(fù)合物結(jié)合于水楊酸響應(yīng)位點(SArlc),降低組蛋白H3和H4的乙?；讲⒁种妻D(zhuǎn)錄。對HDA19催化突變體的研究發(fā)現(xiàn)去乙?；钚詫τ贖DA19介導(dǎo)的植物防御相關(guān)基因表達(dá)是關(guān)鍵條件[58-59]。

SRT2為擬南芥中發(fā)現(xiàn)的另外一種HDAC,抑制SA生物合成基因的轉(zhuǎn)錄活性,而SA是植物抵抗細(xì)菌性斑點病菌和活體營養(yǎng)性病原等反應(yīng)中的關(guān)鍵信號分子[60]。PstDC3000感染后誘導(dǎo)SRT2表達(dá)下調(diào),促進(jìn)SA合成和防御相關(guān)基因的轉(zhuǎn)錄[61]。

2.4其他參與植物防御應(yīng)答的染色質(zhì)相關(guān)蛋白

植物中還存在其他一些染色質(zhì)相關(guān)蛋白,這些蛋白也直接參與植物防御應(yīng)答?？茖W(xué)家通過遺傳篩查分析發(fā)現(xiàn)RAD51(SSN1)、SSN2、BRCA2(SSN3)等與植物抗性調(diào)節(jié)相關(guān)[62-63]。SSN2包含一個SWI2/SNF2和MuDR(SWIM)結(jié)構(gòu)域,主要定位于細(xì)胞核。敲除擬南芥SSN2基因會引起PR基因表達(dá)量降低,表現(xiàn)不抗P.syringae[64]。系統(tǒng)獲得性抗性(SAR)是植物從轉(zhuǎn)錄和DNA同源重組(HR)兩個水平上產(chǎn)生防御應(yīng)答的結(jié)果,SAR啟動植物基因組中10%的基因轉(zhuǎn)錄。SNI1負(fù)調(diào)節(jié)SAR和HR,而SSNs(suppressor of SNI1)抑制SNI1的表達(dá),RAD51D(RAD51的5種同源物之一)、SSN1和BRCA2A(BRCA2同源物)共同形成蛋白復(fù)合體在TGA轉(zhuǎn)錄因子的協(xié)同作用下與染色質(zhì)中PR基因的啟動子區(qū)相結(jié)合,調(diào)控基因轉(zhuǎn)錄[65]。擬南芥BRCA2和RAD51對遺傳毒性物質(zhì)和病原體感染非常敏感,通過基因組微列陣和CHIP-Seq技術(shù)證明BRCA2/RAD51復(fù)合物在植物防御應(yīng)答中發(fā)揮關(guān)鍵作用,認(rèn)為RAD51D、BRCA2A、SSN2可能參與染色質(zhì)重塑復(fù)合物調(diào)節(jié)SNI1和其他PR基因的轉(zhuǎn)錄事件[63]。

3　病原體通過染色質(zhì)重塑干預(yù)植物防御系統(tǒng)

病原體采用多種策略來干擾植物先天免疫系統(tǒng)最終侵染植物體,染色質(zhì)重塑復(fù)合物在進(jìn)化過程中相當(dāng)保守,這對于活體營養(yǎng)型和半活體營養(yǎng)型病原體在侵染初期維持穩(wěn)定的共生關(guān)系尤為重要。

最早報道的有玉米炭色旋孢腔菌,該菌能產(chǎn)生HC毒素,HC毒素抑制組蛋白去乙?；钚?導(dǎo)致組蛋白高度乙酰化,直接調(diào)節(jié)植物染色質(zhì)重塑過程[66]。HC毒素還原酶能削弱其毒性并恢復(fù)玉米對病原體的抗性[67],但有關(guān)組蛋白去乙?；钚缘囊种平閷?dǎo)病原體侵染的分子機制仍知之甚少。

3.1根癌農(nóng)桿菌毒性蛋白VirE和6b

擬南芥和根癌農(nóng)桿菌是研究病原體毒性因子如何與寄主染色質(zhì)相關(guān)蛋白互作的兩種模式生物。根癌農(nóng)桿菌能將自身的一段T-DNA整合到植物基因組中,T-DNA包含有生長素和細(xì)胞分裂素合成相關(guān)基因的編碼序列,促進(jìn)植物細(xì)胞分裂和生長。同時T-DNA還包含冠癭堿合成相關(guān)基因,冠癭堿為根癌農(nóng)桿菌提供營養(yǎng)來源[68]。研究證實核心組蛋白、組蛋白修飾酶、組蛋白分子伴侶、染色質(zhì)組裝蛋白等在T-DNA整合過程中發(fā)揮關(guān)鍵作用[69-70]。

根癌農(nóng)桿菌毒性蛋白VirE2具有調(diào)節(jié)染色質(zhì)結(jié)構(gòu)和促進(jìn)T-DNA整合的功能。擬南芥中,VirE2互作蛋白VIP1(VirE2-interacting protein 1)直接與H2A等核心組蛋白發(fā)生作用,VIP1增強VirE2與核小體之間的作用[71]。通過此途徑,VirE2指導(dǎo)T-DNA以復(fù)合物形式與寄主染色質(zhì)結(jié)合,從而整合到植物基因組中[72]。此外,VirE2互作蛋白VIP2 (VirE2-interacting protein 2)能調(diào)控組蛋白基因的轉(zhuǎn)錄[73]。研究發(fā)現(xiàn)植物通過上調(diào)許多組蛋白基因的表達(dá)來抵御根癌農(nóng)桿菌侵染[74]。VirE3已被證實具有轉(zhuǎn)錄激活子功能,它與pCsn5-1和pBrp兩種蛋白形成復(fù)合物,在GAL4-BD蛋白因子的協(xié)同下與DNA結(jié)合,改變?nèi)旧|(zhì)結(jié)構(gòu),調(diào)節(jié)寄主防御相關(guān)基因的轉(zhuǎn)錄[75]。是否存在其他的根癌農(nóng)桿菌毒性因子有待深入研究。

毒性蛋白6b是根癌農(nóng)桿菌誘發(fā)植物異常發(fā)育和冠癭瘤形成的關(guān)鍵因子,與組蛋白H3、micro RNA途徑相關(guān)蛋白等多種染色質(zhì)蛋白存在相互作用[76-77],6b可能為一種組蛋白分子伴侶,協(xié)同染色質(zhì)重塑因子影響核小體的組裝、組蛋白置換、基因特異性轉(zhuǎn)錄[76]。最近蛋白結(jié)構(gòu)分析發(fā)現(xiàn)6b還具有ADP核糖基化活性[77]。盡管6b與組蛋白H3之間確實存在聯(lián)系,但6b如何修飾H3及6b介導(dǎo)組蛋白H3可能發(fā)生的ADP核糖基化如何影響防御基因的轉(zhuǎn)錄仍知之甚少。

3.2Ⅲ型分泌效應(yīng)因子(Type Ⅲ secreted effectors,T3SEs)

Ⅲ型分泌效應(yīng)因子是一種目前研究較多的毒性蛋白。革蘭氏陰性菌借助于T3SEs進(jìn)入真核細(xì)胞,抑制寄主免疫反應(yīng)[78]。進(jìn)入細(xì)胞質(zhì)后,一方面與胞質(zhì)中合成的核蛋白發(fā)生作用;另一方面,T3SEs在核定位信號序列(NLS)的引導(dǎo)下進(jìn)行入核運輸,調(diào)節(jié)染色質(zhì)構(gòu)象的變化和基因轉(zhuǎn)錄。例如,黃單胞菌TAL(transcription activator-like)因子綁定特定啟動子序列位點,直接激活防御應(yīng)答負(fù)調(diào)控基因的表達(dá),加速病原體侵染和病癥表現(xiàn)的進(jìn)程[79]。目前,僅在黃單胞菌中發(fā)現(xiàn)TAL因子具有直接的基因轉(zhuǎn)錄調(diào)節(jié)作用,因此尚需發(fā)掘更多的能通過染色質(zhì)重塑改變基因轉(zhuǎn)錄狀態(tài)的其他T3SEs。

OspF蛋白為一種Ⅲ型分泌系統(tǒng)的后期效應(yīng)分子,能誘導(dǎo)組蛋白H3去磷酸化和去乙?；?重塑染色質(zhì),降低免疫應(yīng)答相關(guān)基因的表達(dá)水平[80],同時Rb(retinoblastoma)蛋白和OspF蛋白以復(fù)合體形式參與此分子調(diào)控網(wǎng)絡(luò)[81]。OspF蛋白還具有磷酸絲氨酸水解酶活性,不可逆地將MAPK通路中的蛋白去磷酸化[82],丁香假單胞菌能合成一種與OspF類似的效應(yīng)因子HopAI1,定位于細(xì)胞核,通過MPK3和MPK6的去磷酸化修飾干擾PAMP誘導(dǎo)的植物防御信號途徑[83],其是否參與植物組蛋白的修飾過程尚未得到試驗證實。

科學(xué)家從甘藍(lán)黑腐病黃單胞菌中鑒定出一種效應(yīng)分子XopD,XopD蛋白具有染色質(zhì)重塑活性和小泛素樣修飾蛋白(small ubiquitin-like modifier,SUMO)酶活性。通過擬南芥全基因組水平上的蛋白質(zhì)研究,已經(jīng)鑒定出多種SUMO底物,包括組蛋白修飾酶類、染色質(zhì)重塑復(fù)合物成分及免疫相關(guān)的轉(zhuǎn)錄因子[84-85]。SUMO E3連接酶SIZ1突變體內(nèi)免疫響應(yīng)基因呈組成型表達(dá),伴隨著SA積累的增加[86],暗示蘇素化(sumoylation)在免疫調(diào)節(jié)過程中扮演重要的角色。除具有SUMO蛋白酶活性,XopD還包含一個EAR基序,EAR基序富含亮氨酸,具有雙親性,是賦予轉(zhuǎn)錄因子抑制功能的一段保守序列,可以通過染色質(zhì)修飾、激活子調(diào)節(jié)等途徑實現(xiàn)對防御和衰老相關(guān)基因的抑制[87],EAR型轉(zhuǎn)錄抑制子為植物特有的一類轉(zhuǎn)錄抑制子,適配子蛋白SIN3和SAP18能增強EAR基序招募HDA19輔阻遏復(fù)合體的能力,使H3K9、H3K27、H4K5和H4K8位點發(fā)生去乙?；?促進(jìn)基因沉默[88],EAR基序是XopD蛋白實現(xiàn)抑制轉(zhuǎn)錄的生物學(xué)功能的必要條件,番茄中的研究表明EAR基序能將HDA19同源物招募至XopD綁定的基因啟動子區(qū),抑制特定基因的表達(dá)。HDA19為蘇素化(SUMO)底物之一,XopD蛋白利用SUMO蛋白酶活性作用降低HDA19自身的SUMO化水平,從而提高HDA19的去乙?；钚?重塑染色質(zhì)構(gòu)象,抑制植物防御應(yīng)答基因的轉(zhuǎn)錄[85]。

4　展望

染色質(zhì)構(gòu)象動態(tài)改變是基因功能調(diào)控的關(guān)鍵點。目前對染色質(zhì)重塑的修飾類型及機制的研究較多,特別是ATP依賴的重塑復(fù)合物、乙酰化、甲基化等,但欠缺系統(tǒng)性。大量的研究證據(jù)表明基于這些不同的染色質(zhì)重塑方式能直接或間接在植物防御應(yīng)答反應(yīng)中發(fā)揮重要作用,模式植物擬南芥SYD、BRM、PIE1、DDM1、AGO4等蛋白具有防御調(diào)節(jié)功能的ATP酶亞基已被成功鑒定出,但相對于SNF2超家族龐大數(shù)量的蛋白亞基而言,仍是冰山一角,尋找同源或新的與染色質(zhì)重塑有關(guān)的蛋白顯得尤為急切,重塑相關(guān)蛋白通過什么機制精確修飾植物染色質(zhì)仍需深入解析。組蛋白修飾對于病原體侵染激發(fā)的植物信號轉(zhuǎn)導(dǎo)來說也非常關(guān)鍵,但分離的組蛋白甲基化、乙?；嚓P(guān)因子的數(shù)量極其有限,發(fā)現(xiàn)的特異或保守的修飾位點數(shù)量較少,甲基化與乙?；裙矁r修飾如何通過修飾酶復(fù)合物的介導(dǎo)來調(diào)控染色質(zhì)結(jié)構(gòu)仍不明晰,病原體VirE、6b、T3SEs等蛋白分子如何與重塑復(fù)合物、乙?；揎棌?fù)合物等共同作用于植物免疫系統(tǒng)的分子機制知之甚少。因此,許多問題有待系統(tǒng)解決,今后的研究將更多地致力建立并完善染色質(zhì)層面上植物與病原體互作的信號傳導(dǎo)網(wǎng)絡(luò),為最終通過基因工程等技術(shù)提升植物抗病能力奠定基礎(chǔ)。

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(責(zé)任編輯：田喆)

Advances in chromatin remodeling and its regulation of plant defense response to diseases

Hong Lin1,Wei Zhaoxin1,Wei Wenhui2,Tan Ping1

(1. Fruit Research Institute, Chongqing Academy of Agricultural Sciences, Chongqing402260, China;2. Research Institute of Oil Crops, Chinese Academy of Agricultural Sciences, Key Laboratory of Oil Crop Biology and Genetic Breeding of the Ministry of Agriculture, Wuhan430062, China)

Transcription-related factors can be integrated into specific DNA sites, and this molecular process is regulated by the configuration changes of chromatin. However, highly condensed chromatin is relieved through chromatin remodeling of itself with the alteration of covalence power between histone and DNA chain, and this mechanism may control gene expression and silencing. There are at least two primary modification types which contain ATP-dependent chromatin remodeling complex and covalent modifications of histone tails by histone modification complexes; the later type is made up of methylation/demethylation and acetylation/ deacetylation of histone. Upon pathogen infection, the transcription of defense-related genes is regulated directly and indirectly by chromatin remodelers under the force given by chromatin remodeling in plants, and then the immune response becomes effective. This paper reviews the mechanisms by which plant chromatin remodeling regulates expression of defense-related gene and the three proteins T3SEs,6b,VirE evade plant immune system by the pathway of modifying the chromatin structure according to recent studies.

plant;nucleosome;chromatin remodeling;defense response

2015-09-06

2015-10-15

國家自然科學(xué)基金(30671312)；重慶市科委基本科研項目(2012CSTSJBJY00510)

E-mail: tanp_168@163.com

Q 993.2,S 432.2

A

10.3969/j.issn.0529-1542.2016.04.002

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