彭銹玲, 王劍豪, 楊松光

染色質(zhì)重塑因子在植物發(fā)育過程的功能

彭銹玲1,2, 王劍豪1,2, 楊松光1*

(1. 中國科學院華南植物園, 華南農(nóng)業(yè)植物分子分析與遺傳改良重點實驗室，廣州 510650; 2. 中國科學院大學, 北京 100049)

染色質(zhì)重塑復合體(chromatin remodeling complexes)通過具有ATPase活性的亞基水解ATP釋放能量，通過改變核小體“構(gòu)象”(包括核小體重定位、核小體滑動和核小體替換等)而改變DNA的“可及性”(accessibility)，進而影響特定的生理、生化過程。染色質(zhì)重塑復合體最早在酵母中發(fā)現(xiàn)，生化分析表明其至少含有13個亞基。目前植物染色質(zhì)重塑復合體的組成還未完全解析，但通過對其酵母同源亞基(染色質(zhì)重塑因子)的研究可從側(cè)面探究植物染色質(zhì)重塑復合體的功能。同時，還著重討論了近年來在植物染色質(zhì)重塑因子研究上取得的結(jié)果，以期為植物染色質(zhì)重塑的作用機制提供啟示。

染色質(zhì)重塑因子；表觀調(diào)控；功能；植物

1 染色質(zhì)重塑復合體

真核生物遺傳信息以核小體為基本單位，經(jīng)高度包裹壓縮存儲于染色質(zhì)中。因此真核生物在DNA復制、轉(zhuǎn)錄、重組和DNA修復等過程中首先要克服DNA與組蛋白之間的“緊密”結(jié)合。涉及該過程的蛋白主要包括兩類，即染色質(zhì)修飾酶(包括組蛋白修飾酶和DNA修飾酶)和依賴于ATP的染色質(zhì)重塑因子(ATP-dependent chromatin remodelers, ATPase)。前者通過添加或者移除組蛋白和DNA上的化學基團改變DNA的“可及性”[1]，而后者通過與其他蛋白組成染色質(zhì)重塑復合體水解ATP釋放能量，改變核小體“構(gòu)象”(positioning, occupancy and composition of nucleosomes)而改變DNA的“可及性”，進而影響特定的生理過程[2–3]。

染色質(zhì)重塑復合體最早從酵母()和(sucrose non-fermenting)突變體中分離鑒定。生化分析表明該復合體含有至少11個亞基(SWI1、SWI2/SNF2、SWI3、SNF5、SWP73、ARP7、ARP9、SWP82、SNF6、SNF11和TAF14)，其中SWI2/SNF2蛋白具有ATPases活性[4]，SWP82、SNF6、SNF11和TAF14為酵母所特有(表1)。根據(jù)ATPase亞基的結(jié)構(gòu)，可將染色質(zhì)重塑復合體分為4類(表1~3)，即SWI/SNF、ISWI、CHD和INO80/SWR1[2], 且不同復合體可能包括相同的亞基。研究表明，這4類染色質(zhì)重塑復合體ATPase亞基無論是在酵母、果蠅還是人類中均十分保守，含有保守的ATPase催化結(jié)構(gòu)域(SNF2-N結(jié)構(gòu)域)，該催化結(jié)構(gòu)域可進一步細分為DExx和HELICc兩部分(圖1)。除ATPase催化結(jié)構(gòu)域外，不同染色質(zhì)重塑復合體ATPase亞基還含有特異結(jié)構(gòu)，如SWI/SNF (matingtype switching/sucrose non-fermenting)復合體ATPase亞基N端含有HSA (helicase-SANT)結(jié)構(gòu)域而C端含有bromodomain結(jié)構(gòu)域[5–6]。bromodomain結(jié)構(gòu)域能識別組蛋白“尾巴”乙酰化的殘基，使SWI/SNF復合體結(jié)合在染色質(zhì)特定位點[7–8]。而ISWI (imitation switch)復合體ATPase亞基C端含有SANT和SLIDE結(jié)構(gòu)域，這二者形成一個核小體識別結(jié)構(gòu)與未修飾的組蛋白和DNA結(jié)合[9]。CHD (chromodomain helicase-DNA binding)復合體ATPase亞基N端有串聯(lián)的chromodomain結(jié)構(gòu)域[10]，能識別組蛋白H3K4的甲基化位點[11–12]。與其他三類ATPase亞基相比，INO80/SWR1 (inositol requiring 80)復合體ATPase亞基結(jié)構(gòu)域DExx與HELICc之間有一段較長的氨基酸殘基(圖1)，然而這并未影響其ATPase的活性[13]。

表1 不同物種的SWI/SNF復合體組成

表2 不同物種的ISWI、CHD復合體組成

表3 不同物種INO80/SWR1復合體組成

雖然不同染色質(zhì)重塑復合體ATPase亞基在結(jié)構(gòu)上較為保守，但不同染色質(zhì)重塑復合體具有特有的功能。如ISWI和CHD復合體主要參與DNA復制后染色質(zhì)的組裝[14]；而SWI/SNF復合體則影響染色質(zhì)的去組裝和核小體穩(wěn)定蛋白的替換[15–17]。INO80/SWR1復合體則介導組蛋白變體(histonevariant)的替換，其中INO80復合體介導H2A替換H2A.Z，而SWR1復合體則與之相反[18–20]。組蛋白H2A與組蛋白變體H2A.Z之間的互換對核小體結(jié)構(gòu)穩(wěn)定性至關(guān)重要[21–23]。

圖1 不同染色質(zhì)重塑復合體ATPase亞基結(jié)構(gòu)示意圖(引自Clapier[2])

目前對染色質(zhì)重塑復合體的作用機制并不十分清楚。一般認為，染色質(zhì)重塑復合體ATPase亞基與DNA易位酶(DNA translocases)具有相似之功能。當染色質(zhì)重塑復合體ATPase亞基與核小體結(jié)合后，其易位酶活性將核小體之間的連接DNA (linker)推向核小體核心結(jié)構(gòu)，使DNA形成一個環(huán)狀結(jié)構(gòu)(loop)，從而使DNA與組蛋白之間結(jié)合由“緊密”狀態(tài)變?yōu)椤八缮ⅰ睜顟B(tài)[24–27]。該過程可能同時產(chǎn)生很多環(huán)狀結(jié)構(gòu)，這些環(huán)狀結(jié)構(gòu)只需改變DNA與1~2個組蛋白的結(jié)合程度即可啟動核小體的滑動。然而，對形成的環(huán)狀結(jié)構(gòu)大小并不十分清楚, 目前的證據(jù)支持該環(huán)狀結(jié)構(gòu)可能由較多的堿基(約100 bp)組成[28]。而關(guān)于染色質(zhì)重塑是如何被精確調(diào)節(jié)的還知之甚少，該過程可能與組蛋白的翻譯后修飾有關(guān)。如H4尾巴第17~19位殘基乙?；芴岣唧蛤?) ISWI復合體催化活性[29–30],而H4K16ac則抑制其活性。對酵母yISW2 (ISWI復合體催化亞基)和yChd1 (CHD復合體催化亞基)而言，H4乙?；种破銩TPase活性而不響應(yīng)它與核小體結(jié)合，然而H4乙?；瘏s能提高酵母RSC復合體(SWI/SFN類)的重塑活性[31]。

2 植物染色質(zhì)重塑因子及功能

目前，植物染色質(zhì)重塑復合體組成尚未完全分離鑒定，然而遺傳和蛋白相互作用數(shù)據(jù)提示植物中也存在多種染色質(zhì)重塑復合體(表1~3)。因此通過對染色質(zhì)重塑復合體同源亞基的研究可從側(cè)面探究植物染色質(zhì)重塑復合體的功能。通過與酵母、果蠅和人的染色質(zhì)重塑復合體ATPase亞基的同源比對，擬南芥含41個ATPase結(jié)構(gòu)域(SNF2-like)基因，可分為Snf2-like、Swr1-like、Rad54-like、Rad5/16-like、SSO1653-like和SMARCAL1-like家族，每個家族又可細分為不同亞家族[32]，如Snf2-like家族可分為SWI2/SNF2、Lsh、Iswi、Chd1和Mi-2亞家族，而Swr1-like家族則可分為Ino80、Swr1和Etl1亞家族。遺傳和蛋白相互作用及IP-MS研究表明，擬南芥() SWI/SNF染色質(zhì)重塑復合體亞基核心組分與酵母和動物相似，但含有更多同源基因(如與酵母SWI3同源的SWI3A/B/C/D)，且有植物特有的亞基(圖2)。這提示植物染色質(zhì)重塑復合體可能具有與動物和酵母不同的功能。圍繞各組成亞基的研究表明，這些基因參與細胞分化、器官發(fā)育和激素信號轉(zhuǎn)導等多種生理過程(表4)。在擬南芥所有SNF2-N蛋白中Snf2-like (11個)和Swr1-like (4個)家族成員在序列上最有可能是植物染色質(zhì)重塑復合體催化亞基，圍繞這些基因所取得的研究成果也最豐富。在Snf2-like家族中，SWI2/SNF2亞家族(4個)、CHD1-Mi2亞家族(4個)、Iswi-Lsh亞家族(3個)和Swr1-like家族(4個)成員分別對應(yīng)于SWI/SNF、CHD、 ISWI和 INO80/SWR1復合體催化亞基(表1~3)。

圖2 植物SWI/SNF染色質(zhì)重塑復合體可能組成(修改自Jerzmanowski[33])

2.1 SWI/SNF復合體

2.1.1 SWI/SNF復合體催化亞基

SWI/SNF復合體最早從酵母()中分離鑒定，隨后發(fā)現(xiàn)該類復合體亦廣泛存在于動物如果蠅()、小鼠()和人類中。目前關(guān)于植物SWI/SNF復合體的具體組成還不十分清楚，但遺傳和蛋白相互作用數(shù)據(jù)顯示該復合體也存在于植物中。在擬南芥41個ATPase結(jié)構(gòu)域(SNF2-like)蛋白中，SWI2/SNF2亞家族成員AtBRM (BRAHMA)、AtSYD (SPLAYED)、AtCHR23 (CHROMATINREMODELL ING23)和AtCHR12 (CHROMATIN REMODELL ING 12)最有可能是植物SWI/SNF復合體催化亞基，其中AtBRM的可能性最大。首先，僅有AtBRM蛋白C-端具有與酵母SWI2/SNF2和果蠅BRAHMA蛋白一樣的bromo結(jié)構(gòu)域；其次，AtBRM蛋白N-端能與酵母SWI3同源蛋白AtSWI3B和AtSWI3C相互作用；最后和突變體具有相似表型[34]。

表4 擬南芥染色質(zhì)重塑因子的功能分析

續(xù)表(Continued)

主要在分生組織和幼嫩器官中表達，其功能缺失導致2 000余基因中的一半下調(diào)而另一半上調(diào)表達[104]，這表明具有雙重功能。敲減的植株矮小，在長日照下葉片卷曲，花器官發(fā)育異常；在長日照和短日照下均出現(xiàn)早花現(xiàn)象[33]。缺失突變體中，有相當一部分植株在短日照下不開花，這提示在擬南芥開花過程的作用十分復雜[35]。進一步研究表明，除了影響光周期響應(yīng)基因的表達外，還抑制和的表達[104–105]。在葉片中，AtBRM分別與TCP4和AN- GUSTIFOLIA3 (AN3)相互作用，共同調(diào)控葉片發(fā)育相關(guān)基因的表達[38–39]。我們的研究表明，在花序軸中AtBRM與轉(zhuǎn)錄因子BREVIPEDICELLUS (BP)相互作用，直接調(diào)節(jié)和的表達來調(diào)控花序軸發(fā)育[36]。在黑暗中，AtBRM與PHY-INTER- ACTING FACTOR 1 (PIF1)相互作用抑制()表達從而抑制葉綠素合成[40]。除轉(zhuǎn)錄因子外, AtBRM亦可與其他核蛋白相互作用。如熱脅迫記憶激活因子FORGETTER1 (FGT1)與AtBRM相互作用，維持下游熱脅迫相關(guān)基因處于轉(zhuǎn)錄激活狀態(tài)[42]。而植物H3K27去甲基化酶RELATIVE OF EARLY FLO- WERING 6 (REF6)通過招募AtBRM結(jié)合于下游基因CTCTGYTY基序降低其H3K27me3水平激活轉(zhuǎn)錄[41]。這與動物中BRM拮抗PcG蛋白(polycomb group proteins)的作用一致。PcG蛋白作為表觀遺傳抑制因子維持細胞內(nèi)非活化基因的抑制狀態(tài)，其分別通過與Polycomb Repressive Complex 1 (PRC1) 和PRC2復合體相互作用建立和維持染色質(zhì)抑制狀態(tài)。PRC2復合體與目標基因結(jié)合后，催化這些基因組蛋白H3K27me3修飾，從而抑制基因表達。這與我們在擬南芥主根發(fā)育過程觀察到AtBRM拮抗PcG蛋白影響生長素運輸?shù)鞍谆虮磉_，從而影響主根根冠干細胞微環(huán)境維持的結(jié)果一致[43]。最近研究表明，翻譯后修飾對染色質(zhì)重塑過程也起著重要作用，AtBRM作為ABA信號途徑核心組分SnRK (蔗糖非依賴1蛋白激酶)和PP2C (蛋白磷酸酶2C)的底物來調(diào)控ABA反應(yīng)[46]；我們亦觀察到，METHYL METHANE SULFONATE SENSITIVITY 21 (MMS21)通過SUMO化修飾AtBRM調(diào)節(jié)其蛋白穩(wěn)定性參與主根發(fā)育[43]。有趣的是，新的研究結(jié)果表明microRNA前體(pri-miRNAs)也能與AtBRM相互作用，AtBRM作為microRNA前體加工復合體SE (MICROPRO CESSOR COMPONENT SERRATE)組分改變microRNA前體二級結(jié)構(gòu)以便后續(xù)通過DCL1和HYL1進一步加工[47]。

對擬南芥SWI2/SNF2亞家族其他成員的研究表明，參與頂端分生組織(SAM)活性的維持。缺失突變體植株矮小，生長緩慢、葉片極性和SAM缺失。其作用機理是，通過途徑影響SAM的維持，因為AtSYD可與BARD1相互作用結(jié)合于啟動子直接結(jié)合而調(diào)節(jié)表達, 后者促進SAM中干細胞活性[48–49]。進一步研究還表明，AtSYD通過調(diào)控JA和ET信號相關(guān)基因參與植物的生物脅迫響應(yīng)[106]，而這種脅迫大部分是通過抑制(SUPPRESSOR OF NPR1, CONSTITU- TIVE 1)實現(xiàn)的[107]。對和在植物發(fā)育中的功能還不十分清楚。過表達和均抑制植物種子萌發(fā)[50]，在其他發(fā)育過程過表達顯著抑制植物生長，而過表達表型則不明顯[51]；但在脅迫方面, 二者表型相似[52–53]。

2.1.2 SWI/SNF復合體非催化亞基-SWI3類蛋白

擬南芥基因組編碼4個SWI3同源蛋白，分別為AtSWI3A、AtSWI3B、AtSWI3C和AtSWI3D, 在結(jié)構(gòu)上他們均含有SWIRM、SANT和Leucine Zipper 結(jié)構(gòu)域。進化分析表明植物SWI3類蛋白可明顯分為兩簇，即SWI3A/B和SWI3C/D，這也與AtSWI3A、AtSWI3B、AtSWI3C和AtSWI3D的生物學功能有所差異相符。與突變導致植物胚在早期發(fā)育過程異常，而和突變使得植物葉片和花器官發(fā)育異常[53]。有意思的是突變還導致植物主根發(fā)育異常，而其他3個突變體則未觀察到相應(yīng)表型[53]。酵母雙雜交結(jié)果表明，AtSWI3A可分別與AtSWI3A、AtSWI3B、AtSWI3C、BSH、AtSYD和FCA相互作用[53–54], 提示AtSWI3A、BSH和AtSYD可能形成1個復合體。然而關(guān)于AtSWI3A與其他蛋白相互作用的生物學意義目前并不清楚。對AtSWI3B而言，除分別可與AtSWI3A、AtSWI3B、AtSWI3C、AtSWI3D、BSH、AtSYD、AtBRM相互作用外, 還分別與type 2C類磷酸酶(phosphatase type 2C) HAB1 (HYPERSENSI- TIVE TO ABA1)和長鏈非編碼RNA結(jié)合蛋白IDN2相互作用，參與ABA信號和長鏈非編碼RNA形成[55–56]。進一步研究還表明，AtSWI3B (包括At- SWI3C和AtSWI3D)與MORC6 (microrchidia 6)、SUVH9 [SU(VAR)3-9 homolog]和IDN2形成復合體, 通過RNA指導的DNA甲基化(RdDM, RNA-directedDNA methylation)介導的途徑調(diào)控DNA的甲基化[57]。在葉片發(fā)育過程,通過調(diào)控生長素代謝酶基因(IAA carboxyl methyltransferase 1)的染色質(zhì)“構(gòu)象”調(diào)節(jié)其表達，從而參與葉片發(fā)育[58]。

AtSWI3C也分別與AtSWI3A、AtSWI3B、AtSYD和AtBRM相互作用，進一步研究表明其還可與轉(zhuǎn)錄因子AN3和酵母SWI/SNF復合體同源蛋白SWP73B以及ARP4/7 (actin-related protein4/7)相互作用調(diào)控葉片發(fā)育[39]。同時，AtSWI3C通過與DELLA蛋白RGL2和RGL3相互作用促進(GIBBERELLIN-INSENSITIVE DWARF1)和(GIBBERELLIN 3-OXIDASE)表達，參與GA信號轉(zhuǎn)導[59]。相對于其他3個AtSWI3蛋白，AtSWI3D的功能還知之甚少，其缺失植株的表型與和缺失突變體相似，出現(xiàn)葉片卷曲，花器官發(fā)育異常和育性降低等表型[53]。

2.1.3 SWI/SNF復合體非催化亞基-SNF5類蛋白

4.4.2 強化服務(wù)監(jiān)督，完善管理制度。進一步完善和優(yōu)化項目立項制、項目公示制、項目審計制、項目檢查驗收制、后續(xù)管護等制度，加強項目事中、事后監(jiān)督。

在酵母中，SNF5蛋白對染色質(zhì)的裝配和基因啟動子與SWI/SNF復合體的結(jié)合至關(guān)重要[108]，其C端保守的200個氨基酸殘基形成兩個重復結(jié)構(gòu)負責與SWI/SNF復合體其他亞基和其他因子如cyclin E/CDK2之間的相互作用。動物發(fā)生突變往往會導致癌癥。在擬南芥中，SNF5同源蛋白BSH(BUSHY GROWTH)僅由1個基因編碼，其可與AtSWI3A和AtSWI3B相互作用，且在酵母中異源表達，可互補酵母突變體表型[61]。利用反義RNA技術(shù)降低表達導致植物頂端分生組織減小且出現(xiàn)不育表型[61]。T-DNA插入突變體雖然導致種子貯存基因在幼苗中異位表達，然而植株卻未出現(xiàn)可以看到的表型[60]。這可能是由于T-DNA插入位置在BSH的C端，僅破壞BSH蛋白C端結(jié)構(gòu)使得BSH還保留部分功能。

2.1.4 SWI/SNF復合體非催化亞基SWP73類蛋白

酵母SWI/SNF復合體亞基SWP73對SWI/SNF復合體在轉(zhuǎn)錄過程的作用至關(guān)重要。在植物中，擬南芥基因組編碼兩個SWP73蛋白：SWP73A和SWP73B，二者氨基酸序列相似度高達83.7%。蛋白互作分析表明SWP73A僅可與AtSWI3C相互作用，而SWP73B不僅可以與AtSWI3C和AtSWI3D相互作用，還能與AtBRM和ARP4/7以及轉(zhuǎn)錄因子AN3相互作用[39]。生物學功能分析表明，和功能亦有所差異，突變植物未出現(xiàn)可見表型，而突變導致植物根[63]、葉片和花發(fā)育異常[62]和開花時間推遲[64]。進一步研究表明，通過促進根中細胞分裂素的合成促進根中分生組織的維持[63]；同時通過改變?nèi)旧|(zhì)組蛋白修飾水平和H2A.Z的替換影響表達從而參與植物成花控制[64]。最新的研究表明，SWP73B通過直接結(jié)合于下游基因的G-box區(qū)域調(diào)節(jié)其表達抑制下胚軸伸長，但與SWP73B直接結(jié)合的基因與PIF4結(jié)合的基因大部分是不同的[65]。在脅迫方面,還參與UV-B介導的DNA損傷修復，然而其作用機制還不清楚[66]。

2.1.5 SWI/SNF復合體非催化亞基ARP類蛋白

酵母和動物SWI/SNF類復合體均含有一類ARPs (actin-related proteins)蛋白。在酵母中，ARPs一共有10個(ARP1~10)，其序列與酵母actin相似性按編號遞減。在酵母所有ARPs中，ARP7和ARP9是SWI/SNF類(包括RSC)復合體組分，而ARP4、ARP5和ARP8為INO80/SWR1復合體組分。動物SWI/SNF類僅含有一個ARP (Baf53/BAP55)，與酵母ARP4同源。雖然在結(jié)構(gòu)上ARPs與actin相似均含有ATP/ADP-binding pocket (actin fold)結(jié)構(gòu)，但除ARP4外，其他所有ARPs均沒有像actin那樣的ATPase活性。生物界所有ARPs可分為11類，其中ARP4~ARP9家族成員大多定位于細胞核[107]。擬南芥基因組編碼9個ARPs (ARP2~ARP9，其中ARP4包含2個同源基因和)，其中ARP4~ ARP9定位于細胞核[111]。CoIP-MS分析表明在擬南芥所有ARPs中, ARP4和ARP7為SWI/SNF復合體組分[39]，而后續(xù)的研究表明ARP4也是INO80/ SWR1復合體的組分。

雖然在正常情況下，ARP4和ARP7定位于細胞核，但在有絲分裂過程，它們與染色質(zhì)組裝無關(guān),且也可以定位于細胞質(zhì)[109]。與相似，缺失突變導致植物不育，敲減突變體使植株生長發(fā)育受阻并出現(xiàn)早花、花衰老推遲和花器官發(fā)育異常等表型[67–68]。

2.2 INO80/SWR1復合體

基因最早從篩選調(diào)控酵母磷脂生物合成的突變體中分離，后續(xù)生化分析表明其與其他14個亞基組成復合體(表3)。隨后，同源基因亦在酵母中發(fā)現(xiàn)，其主要催化組蛋白變體Htz1與H2A之間的交換。進一步研究表明，也與其他蛋白形成復合體，其中Rvb1、Rvb2、Arp4和actin亞基與INO80復合體共有(表3)。擬南芥中編碼4個(包括PIE1、INO80、CHR19和CHR10)與INO80和Swr1類復合體催化亞基同源蛋白，目前僅對CHR19、INO80和PIE1的功能有所了解。

目前的研究認為擬南芥SWR1復合體最少由10個亞基組成(PIE1、SWC2、SWC4、SWC6、YAF9A、RVB1、RVB2A、RVB2B、ARP4和ARP6)，其中PIE1是催化亞基[73]，首先，PIE1可與SWC2、SWC6和ARP6以及組蛋白H2A相互作用調(diào)控植物開花和發(fā)育[73–74]；其次，與PIE1形成的復合體在植物調(diào)節(jié)基因表達過程中也負責H2A.Z變體的交換[75–77]。然而有意思的是，在植物免疫過程中，和突變導致植物基本抗性降低，而突變則增加抗性[76]，這提示在不同的生理過程中植物SWR1復合體亞基的功能可能是不一樣的。進一步研究表明，通過促進和表達，抑制二者目標基因表達參與植物發(fā)育[77]。

對植物INO80/SWR1復合體非催化亞基RVB1、RVB2A和RVB2B的功能還知之甚少，但質(zhì)譜鑒定表明，其能與SWC6形成復合體[75]。對SWC4的研究表明其參與植物雄配子和胚發(fā)育，且對葉片細胞的分化和伸長至關(guān)重要[75]，同時質(zhì)譜鑒定表明其與SWC6相互作用。利用SWC6-MYC融合蛋白進行CoIP結(jié)合質(zhì)譜分析，SWC6與PIE1、SWC2、SWC4、YAF9A、RVB1、RVB2A、RVB2B、ARP4和ARP6形成復合體[75]，其pre-messenger RNA通過Ski- interacting protein (SKIP)介導剪切調(diào)控、和表達參與植物開花時間決定[78]。ARP6除與PIE1和SWC6相互作用參與PIE1和SWC6相似功能外，還通過促進(DISRUPTED MEIOTIC cDNA1)表達促進雌配子的減數(shù)分裂[79], 進一步研究表明該過程是細胞色素P450基因(KLUH/ CYP78A5)通過促進表達而實現(xiàn)[80]。

擬南芥中有2個與酵母INO80/SWR1復合體亞基Yaf9同源的基因：和。和在功能上有部分冗余，其中能與SWC6相互作用，且通過提高組蛋白H4乙?；酱龠M其表達，從而降低和表達, 抑制開花[81]。最新的研究表明，和通過調(diào)節(jié)細胞伸長和分化來影響植株發(fā)育, 且其調(diào)控開花還存在一條獨立于的途徑[82], 雖然YAF9s可通過維持(并不促進) H2A.Z變體與基因區(qū)的結(jié)合和組蛋白H4乙酰化水平直接促進表達[82]。

2.3 CHD復合體

基因家族成員在結(jié)構(gòu)上除含有DEAD/H- related ATP酶結(jié)構(gòu)域外，其N端還含有一段串聯(lián)chromodomains結(jié)構(gòu)域。所有CHD蛋白分為3類:CHD1和CHD2在C端含有DNA結(jié)合區(qū)；CHD3和CHD4的C端缺少DNA結(jié)合區(qū)，其N端有一對PHD結(jié)構(gòu)；CHD5~CHD9的C端含有多余結(jié)構(gòu)。酵母基因組僅編碼1個CHD蛋白CHD1，其可與組蛋白乙酰轉(zhuǎn)移酶復合體的(SAGA and SLIK complexes)亞基相互作用，并通過其PHD結(jié)構(gòu)域識別H3K4me3位點并與轉(zhuǎn)錄激活區(qū)結(jié)合促進下游基因轉(zhuǎn)錄延伸和剪切。

除催化亞基外，對擬南芥CHD復合體的其他亞基我們還知之甚少。擬南芥基因組編碼4個CHD類催化亞基，分別為CHR5、PICKLE/CHR6、CHR4和CHR7。其中CHR5通過改變核小體“構(gòu)象”正調(diào)控表達參與植物抗病過程[84]。在種子發(fā)育過程CHR5通過結(jié)合于和啟動子促進二者表達，調(diào)控胚的發(fā)育[83]。有意思的是，在這個過程PICKLE拮抗CHR5的功能[83]，這也與PICKLE在萌發(fā)階段抑制種子胚性功能一致[112]。與AtBRM相似，PICKLE通過與拮抗PcG蛋白CLF (CURLY LEAF)的功能促進主根中分生組織的活性[83]，而通過IAA14介導抑制側(cè)根起始基因和表達抑制側(cè)根的起始[86]。除在根中外, PICKLE還在葉片和花器官的發(fā)育過程拮抗CLF, 使其調(diào)控基因水平降低[113]。然而在14 d的幼苗中, PICKLE卻促進其調(diào)控基因表達水平[87]，這提示在植物不同的發(fā)育階段PICKLE的功能不一樣。進一步研究表明，PICKLE可與MADS-Box轉(zhuǎn)錄因子SEP3相互作用，提示在PICKLE影響花器官發(fā)育可能還依賴于SEP3[90]。PICKLE通過影響孢子體和配子體發(fā)育，調(diào)控植物的生殖生長[114]，而HY5通過招募PICKLE提高下游細胞伸長基因H3K27me3水平抑制其表達，從而抑制下胚軸伸長[91]。另外, PICKLE分別通過與PIF3、BZR1和DELLAs相互作用參與暗形態(tài)建成、BR和GA信號傳導過程[93], 從而將后三者整合在一起。進一步研究表明, PICKLE通過抑制DELLAs的活性參與植物生長發(fā)育階段的轉(zhuǎn)化[89]。除GA信號外，PICKLE還通過直接促進/的H3K27me3水平抑制其表達從而促進植物營養(yǎng)階段轉(zhuǎn)變(vegetative phase change)(從童年到成熟)[90]。除調(diào)控H3K27me3水平外, PICKLE還通過參與RNA指導的DNA甲基化(RdDM, RNA-directed DNA methylation)抑制下游基因表達[88]。

2.4 ISWI 復合體

ISWI蛋白(imitation SWI)最早從果蠅胚胎細胞提取的核小體重塑活性過程中分離鑒定的，其為一類DEAD/H-related ATP酶，且還含有SANT和SLIDE結(jié)構(gòu)域。在體外加入模板，果蠅ISWI復合體促進轉(zhuǎn)錄，而在體內(nèi)ISWI復合體亞基突變穩(wěn)定抑制同源基因(homeotic gene)表達。目前對植物ISWI類復合體的組成還知之甚少，對催化亞基的研究表明其參與多種生理過程。其中CHR11和CHR17通過共同調(diào)控基因區(qū)(gene body)核小體之間的“距離”(nucleosome spacing)調(diào)節(jié)下游基因表達[99]。同時CHR11和CHR17還分別通過與含DDT結(jié)構(gòu)域蛋白RINGLET1 (RLT1)和RLT2相互作用調(diào)控開花時間和花器官發(fā)育[100]。對該家族另一個成員DECREASE IN DNA METHYLATION 1 (DDM1)的研究表明，其主要參與DNA的甲基化過程。DDM1通過與Methyl- CpG binding domains (MBDs)相互作用改變后者在染色質(zhì)上的定位影響DNA的甲基化[94]，而一般認為MBDs通過影響組蛋白的甲基化參與DNA的甲基化。與RdDM不同，DDM1參與的DNA甲基化主要由DNA甲基轉(zhuǎn)移酶CMT2介導[95]，二者通過提高異染色質(zhì)基因(如)不同區(qū)段的DNA甲基化水平維持基因沉默。事實上, DDM1是通過影響異染色質(zhì)H1構(gòu)象使CMT2更加容易結(jié)合于異染色質(zhì)DNA而實現(xiàn)DNA甲基化修飾的[95]。進一步研究表明，DDM1還可促進甲基化的DNA在核小體上纏繞形成更為緊密的染色質(zhì)結(jié)構(gòu)[96]。有意思的是,突變體在連續(xù)種植5代內(nèi)，其端粒大小與野生型相似，而在第6和以后的世代中端粒大小顯著減小[97]，這似乎說明在介導的端粒維持有一定的時間劑量效應(yīng)。同時突變體亦出現(xiàn)葉片延遲衰老的表型，提示還參與葉片發(fā)育，然而對于具體機制仍不清楚[98]。

2.5 其他Snf2-like蛋白

目前對其他Snf2-like蛋白的功能還不是十分清楚，根據(jù)同源性分析這些蛋白(41個中的大部分)并不能歸于以上復合體中的任意一種。但通過突變體表型分析表明某些成員也有重要的功能。Rad54- like家族成員DRD1/CHR35 (DEFECTIVE IN RNA- DIRECTED DNA METHYLATION1)與RDM1 (RNA-DIRECTED DNA METHYLATION 1)和DMS3 (DEFECTIVE IN MERISTEM SILENCIN G3)形成復合體(DDR complex)，通過polymerase V介導參與RdDM[101]。而該家族另一成員Rad54/CHR25則通過同源重組途徑參與DNA的修復[102]。

與擬南芥相比，其他物種僅有少數(shù)Snf2-like蛋白被研究。如水稻()同源基因和也參與DNA的甲基化[115]，而CHD3家族成員通過GA信號途徑調(diào)控水稻幼苗發(fā)育[116]。小番茄(‘Micro-Tom’)過表達基因()可抑制生長發(fā)育[117]。

3 結(jié)語

染色質(zhì)重塑作為表觀遺傳調(diào)控的重要內(nèi)容在真核生物DNA復制、轉(zhuǎn)錄、重組和DNA修復等過程中起到重要的作用。對植物染色質(zhì)重塑復合體亞基(染色質(zhì)重塑因子)的研究表明，它們參與細胞分化、器官發(fā)育和激素信號轉(zhuǎn)導等多種生理過程。然而相對于酵母和動物，植物染色質(zhì)重塑的研究還相對滯后，其作用機制并不十分清楚，最主要的問題是植物染色質(zhì)重塑是如何識別其作用位點的。在酵母和動物中的研究結(jié)果表明該過程與組蛋白的修飾有關(guān)，這就為我們后續(xù)研究植物染色質(zhì)重塑和組蛋白修飾之間的Cross-Talk指明了方向。同時綜上所述，染色質(zhì)重塑因子在不同的發(fā)育(或基因調(diào)節(jié))過程與不同的因子(包括轉(zhuǎn)錄因子和核蛋白等)相互作用以及染色質(zhì)重塑因子的翻譯后修飾將極大拓展其調(diào)控基因表達的內(nèi)涵。

[1] LI B, CAREY M, WORKMAN J L. The role of chromatin during transcription [J]. Cell, 2007, 128(4): 707–719. doi: 10.1016/j.cell.2007. 01.015.

[2] CLAPIER R, CAIRNS B R. The biology of chromatin remodeling complexes [J]. Annu Rev Biochem, 2009, 78(1): 273–304. doi: 10. 1146/annurev.biochem.77.062706.153223.

[3] HARGREAVES D C, CRABTREE G R. ATP-dependent chromatin remodeling: Genetics, genomics and mechanisms [J]. Cell Res, 2011, 21(3): 396–420. doi: 10.1038/cr.2011.32.

[4] SMITH C L, HOROWITZ-SCHERER R, FLANAGAN J F, et al. Structural analysis of the yeast SWI/SNF chromatin remodeling complex [J]. Nat Struct Biol, 2003, 10(2): 141–145. doi: 10.1038/nsb888.

[5] EISEN J A, SWEDER K S, HANAWALT P C. Evolution of the SNF2 family of proteins: Subfamilies with distinct sequences and functions [J]. Nucl Acids Res, 1995, 23(14): 2715–2723. doi: 10.1093/nar/23. 14.2715.

[6] KIDDER B L, PALMER S, KNOTT J G. SWI/SNF-brg1 regulates self- renewal and occupies core pluripotency-related genes in embryonic stem cells [J]. Stem Cells, 2009, 27(2): 317–328. doi: 10.1634/stem cells.2008-0710.

[7] KASTEN M, SZERLONG H, ERDJUMENT-BROMAGE H, et al. Tandem bromodomains in the chromatin remodeler RSC recognize acetylated histone H3 Lys14 [J]. EMBO J, 2004, 23(6): 1348–1359. doi: 10.1038/sj.emboj.7600143.

[8] ZHOU Y G, GRUMMT I. The PHD finger/bromodomain of NoRC interacts with acetylated histone H4K16 and is sufficient for rDNA silencing [J]. Curr Biol, 2005, 15(15): 1434–1438. doi: 10.1016/j.cub. 2005.06.057.

[9] BOYER L A, LATEK R R, PETERSON C L. The SANT domain: A unique histone-tail-binding module? [J]. Nat Rev Mol Cell Biol, 2004, 5(2): 158–163. doi: 10.1038/nrm1314.

[10] THOMPSON P M, GOTOH T, KOK M, et al., a new member of the chromodomain gene family, is preferentially expressed in the nervous system [J]. Oncogene, 2003, 22(7): 1002–1011. doi: 10.1038/sj. onc.1206211.

[11] PRAY-GRANT M G, DANIEL J A, SCHIELTZ D, et al. Chd1 chromo- domain links histone H3 methylation with SAGA- and SLIK- dependent acetylation [J]. Nature, 2005, 433(7024): 434–438. doi: 10. 1038/nature03242.

[12] FLANAGAN J F, MI L Z, CHRUSZCZ M, et al. Double chromo- domains cooperate to recognize the methylated histone H3 tail [J]. Nature, 2005, 438(7071): 1181–1185. doi: 10.1038/nature04290.

[13] BAO Y H, SHEN X T. INO80 subfamily of chromatin remodeling complexes [J]. Mutat Res, 2007, 618(1/2): 18–29. doi: 10.1016/j.mrf mmm.2006.10.006.

[14] CORONA D F V, TAMKUN J W. Multiple roles for ISWI in trans- cription, chromosome organization and DNA replication [J]. Biochim Biophys Acta, 2004, 1677(1/2/3): 113–119. doi: 10.1016/j.bbaexp. 2003.09.018.

[15] WHITEHOUSE I, FLAUS A, CAIRNS B R, et al. Nucleosome mobilization catalysed by the yeast SWI/SNF complex [J]. Nature, 1999, 400(6746): 784–787. doi: 10.1038/23506.

[16] PHELAN M L, SCHNITZLER G R, KINGSTON R E. Octamer transfer and creation of stably remodeled nucleosomes by human SWI- SNF and its isolated ATPases [J]. Mol Cell Biochem, 2000, 20(17): 6380–6389. doi: 10.1128/mcb.20.17.6380-6389.2000.

[17] LORCH Y, ZHANG M C, KORNBERG R D. Histone octamer transfer by a chromatin-remodeling complex [J]. Cell, 1999, 96(3): 389–392. doi: 10.1016/s0092-8674(00)80551-6.

[18] MIZUGUCHI G, SHEN X T, LANDRY J, et al. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex [J]. Science, 2004, 303(5656): 343–348. doi: 10.1126/science. 1090701.

[19] PAPAMICHOS-CHRONAKIS M, WATANABE S, RANDO O J, et al. Global regulation of H2A.Z localization by the INO80 chromatin- remodeling enzyme is essential for genome integrity [J]. Cell, 2011, 144(2): 200–213. doi: 10.1016/j.cell.2010.12.021.

[20] LUK E, RANJAN A, FITZGERALD P C, et al. Stepwise histone replacement by SWR1 requires dual activation with histone H2A.Z and canonical nucleosome [J]. Cell, 2010, 143(5): 725–736. doi: 10.1016/j. cell.2010.10.019.

[21] JIN C Y, FELSENFELD G. Nucleosome stability mediated by histone variants H3.3 and H2A.Z [J]. Genes Dev, 2007, 21(12): 1519–1529. doi: 10.1101/gad.1547707.

[22] JIN C Y, ZANG C Z, WEI G, et al. H3.3/H2A.Z double variant- containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions in the human genome [J]. Nat Genet, 2009, 41(8): 941–945. doi: 10.1038/ng.409.

[23] KUMAR S V, WIGGE P A. H2A.Z-containing nucleosomes mediate the thermosensory response in[J]. Cell, 2010, 140(1): 136–147. doi: 10.1016/j.cell.2009.11.006.

[24] FITZGERALD D J, DELUCA C, BERGER I, et al. Reaction cycle of the yeast Isw2 chromatin remodeling complex [J]. EMBO J, 2004, 23 (19): 3836–3843. doi: 10.1038/sj.emboj.7600364.

[25] SAHA A, WITTMEYER J, AIRNS B R. Chromatin remodelling: The industrial revolution of DNA around histones [J]. Nat Rev Mol Cell Biol, 2006, 7(6): 437–447. doi: 10.1038/nrm1945.

[26] ZOFALL M, PERSINGER J, KASSABOV S R, et al. Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome [J]. Nat Struct Mol Biol, 2006, 13(4): 339–346. doi: 10. 1038/nsmb1071.

[27] STROHNER R, WACHSMUTH M, DACHAUER K, et al. A ‘loop recapture’ mechanism for ACF-dependent nucleosome remodeling [J]. Nat Struct Mol Biol, 2005, 12(8): 683–690. doi: 10.1038/nsmb966.

[28] ZHANG Y L, SMITH C L, SAHA A, et al. DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC [J]. Mol Cell, 2006, 24(4): 559–568. doi: 10.1016/j.molcel.2006.10.025.

[29] CLAPIER C R, L?NGST G, CORONA D F V, et al. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI [J]. Mol Cell Biol, 2001, 21(3): 875–883. doi: 10.1128/mcb.21.3.875-883.2001.

[30] SHIBA T, KAKUDA S, OKA S, et al. Molecular mechanisms in acceptor substrate recognition of a human glucuronyltransferase, GlcAT-P, an enzyme critical in the biosynthesis of the carbohydrate epitope HNK-1 [J]. Seikagaku, 2005, 77(2): 153–158.

[31] FERREIRA H, FLAUS A, OWEN-HUGHES T. Histone modifications influence the action of Snf2 family remodelling enzymes by different mechanisms [J]. J Mol Biol, 2007, 374(3): 563–579. doi: 10.1016/j. jmb.2007.09.059.

[32] KNIZEWSKI L, GINALSKI K, JERZMANOWSKI A. Snf2 proteins in plants: Gene silencing and beyond [J]. Trends Plant Sci, 2008, 13 (10): 557–565. doi: 10.1016/j.tplants.2008.08.004.

[33] JERZMANOWSKI A. SWI/SNF chromatin remodeling and linker histones in plants [J]. BBA Gene Struct Expr,2007, 1769(5/6): 330– 345. doi: 10.1016/j.bbaexp.2006.12.003.

[34] FARRONA S, HURTADO L, BOWMAN J L, et al. Thethaliana SNF2 homolog AtBRM controls shoot development and flowering [J]. Development, 2004, 131(20): 4965–4975. doi: 10.1242/ dev.01363.

[35] HURTADO L, FARRONA S, REYES J C. The putative SWI/SNF complex subunit BRAHMA activates flower homeotic genes in[J]. Plant Mol Biol, 2006, 62(1/2): 291–304. doi: 10.1007/s11103-006-9021-2.

[36] ZHAO M L, YANG S G, CHEN C Y, et al.BREVI- PEDICELLUS interacts with the SWI2/SNF2 chromatin remodeling ATPase BRAHMA to regulateandexpression in control of inflorescence architecture [J]. PLoS Genet, 2015, 11(3): e1005125. doi: 10.1371/journal.pgen.1005125.

[37] WU M F, SANG Y, BEZHANI S, et al. SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors [J]. Proc Natl Acad Sci USA, 2012, 109(9): 3576–3581. doi: 10.1073/ pnas.1113409109.

[38] EFRONI I, HAN S K, KIM H J, et al. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses [J]. Dev Cell, 2013, 24(4): 438–445. doi: 10.1016/j.devcel.2013.01.019.

[39] VERCRUYSSEN L, VERKEST A, GONZALEZ N, et al. ANGUSTI- FOLIA3 binds to swi/snf chromatin remodeling complexes to regulate transcription duringleaf development [J]. Plant Cell, 2014, 26(1): 210–229. doi: 10.1105/tpc.113.115907.

[40] ZHANG D, LI Y H, ZHANG X Y, et al. The SWI2/SNF2 chromatin- remodeling ATPase BRAHMA regulates chlorophyll biosynthesis in[J]. Mol Plant, 2017, 10(1): 155–167. doi: 10.1016/j.molp. 2016.11.003.

[41] LI C L, GU L F, GAO L, et al. Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in[J]. Nat Genet, 2016, 48(6): 687–693. doi: 10.1038/ng.3555.

[42] BRZEZINKA K, ALTMANN S, CZESNICK H, et al.FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling [J]. Elife, 2016, 5: e17061. doi: 10.7554/elife. 17061.

[43] YANG S G, Li C L, ZHAO L M, et al. TheSWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly toand is required for root stem cell niche maintenance [J]. Plant Cell, 2015, 27(6): 1670–1680. doi: 10.1105/tpc.15.00091.

[44] ZHANG J J, LAI J B, WANG F G, et al. A SUMO ligase AtMMS21 regulates the stability of the chromatin remodeler BRAHMA in root development [J]. Plant Physiol, 2017, 173(3): 1574–1582. doi: 10. 1104/pp.17.00014.

[45] HAN S K, SANG Y, RODRIGUES A, et al. The SWI2/SNF2 chromatin remodeling ATPase BRAHMA represses abscisic acid responses in the absence of the stress stimulus in[J]. Plant Cell, 2012, 24 (12): 4892–4906. doi: 10.1105/tpc.112.105114.

[46] PEIRATS-LLOBET M, HAN S K, GONZALEZ-GUZMAN M, et al. A direct link between abscisic acid sensing and the chromatin-remodeling ATPase BRAHMA via core ABA signaling pathway components [J]. Mol Plant, 2016, 9(1): 136–147. doi: 10.1016/j.molp.2015.10.003.

[47] WANG Z Y, MA Z Y, CASTILLO-GONZáLEZ C, et al. SWI2/SNF2 ATPase CHR2 remodels pri-miRNAsserrate to impede miRNA production [J]. Nature, 2018, 557(7706): 516–521. doi: 10.1038/s415 86-018-0135-x.

[48] HAN P, LI Q, ZHU Y X. Mutation ofcauses meristem defects by failing to confineexpression to the organizing center [J]. Plant Cell, 2008, 20(6): 1482–1493. doi: 10. 1105/tpc.108.058867.

[49] KWON C S, CHEN C B, WAGNER D.is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in[J]. Genes Dev, 2005, 19(8): 992–1003. doi: 10. 1101/gad.1276305.

[50] LEEGGANGERS H A C F, FOLTA A, MURAS A, et al. Reduced seed germination inover-expressing SWI/SNF2 ATPase genes [J]. Physiol Plant, 2015, 153(2): 318–326. doi: 10.1111/ppl.12231.

[51] FOLTA A, SEVERING E I, KRAUSKOPF J, et al. Over-expression ofchromatin remodeling ATPase results in increased variability of growth and gene expression [J]. BMC Plant Biol, 2014, 14: 76. doi: 10.1186/1471-2229-14-76.

[52] MLYNáROVá L, NAP J P, BISSELING T. The SWI/SNF chromatin- remodeling genemediates temporary growth arrest inupon perceiving environmental stress [J]. Plant J, 2007, 51(5): 874–885. doi: 10.1111/j.1365-313x.2007.03185.x.

[53] SARNOWSKI T J, RIOS G, JASIK J, et al. SWI3 subunits of putative SWI/SNF chromatin-remodeling complexes play distinct roles duringdevelopment [J]. Plant Cell, 2005, 17(9): 2454–2472. doi: 10.1105/tpc.105.031203.

[54] BEZHANI S, WINTER C, HERSHMAN S, et al. Unique, shared, and redundant roles for theSWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED [J]. Plant Cell, 2007, 19(2): 403– 416. doi: 10.1105/tpc.106.048272.

[55] SAEZ A, RODRIGUES A, SANTIAGO J, et al. HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in[J]. Plant Cell, 2008, 20(11): 2972–2988. doi: 10.1105/tpc.107.056705.

[56] ZHU Y Y, ROWLEY M J, B?HMDORFER G, et al. A SWI/SNF chromatin-remodeling complex acts in noncoding RNA-mediated transcriptional silencing [J]. Mol Cell, 2013, 49(2): 298–309. doi: 10. 1016/j.molcel.2012.11.011.

[57] LIU Z W, ZHOU J X, HUANG H W, et al. Two components of the RNA-directed DNA methylation pathway associate with MORC6 and silence loci targeted by MORC6 in[J]. PLoS Genet, 2016, 12(5): e1006026. doi: 10.1371/journal.pgen.1006026.

[58] HAN W X, HAN D L, HE Z P, et al. The SWI/SNF subunit SWI3B regulates IAMT1 expressionchromatin remodeling inleaf development [J]. Plant Sci, 2018, 271: 127–132. doi: 10.1016/j. plantsci.2018.03.021.

[59] SARNOWSKA E A, ROLICKA A T, BUCIOR E, et al. DELLA-inter- acting SWI3C core subunit of switch/sucrose nonfermenting chromatin remodeling complex modulates gibberellin responses and hormonal cross talk in[J]. Plant Physiol, 2013, 163(1): 305–317. doi: 10.1104/pp.113.223933

[60] TANG X R, HOU A F, BABU M, et al. TheBRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves [J]. Plant Physiol, 2008, 147(3): 1143–1157. doi: 10.1104/pp.108.121996.

[61] BRZESKI J, PODSTOLSKI W, OLCZAK K, et al. Identification and analysis of thegene, a member of thegene family [J]. Nucl Acids Res, 1999, 27(11): 2393–2399. doi: 10. 1093/nar/27.11.2393.

[62] SACHAROWSKI S P, GRATKOWSKA D M, SARNOWSKA E A, et al. SWP73 subunits ofSWI/SNF chromatin remodeling complexes play distinct roles in leaf and flower development [J]. Plant Cell, 2015, 27(7): 1889–1906. doi: 10.1105/tpc.15.00233.

[63] JéGU T, DOMENICHINI S, BLEIN T, et al. A swi/snf chromatin remodelling protein controls cytokinin production through the regu- lation of chromatin architecture [J]. PLoS One, 2015, 10(10): e0138276. doi: 10.1371/journal.pone.0138276.

[64] JéGU T, LATRASSE D, DELARUE M, et al. The BAF60 subunit of the swi/snf chromatin-remodeling complex directly controls the formation of a gene loop atin[J]. Plant Cell, 2014, 26(2): 538–551. doi: 10.1105/tpc.113.114454.

[65] JéGU T, VELUCHAMY A, RAMIREZ-PRADO J S, et al. TheSWI/SNF protein BAF60 mediates seedling growth control by modulating DNA accessibility [J]. Genome Biol, 2017, 18: 114. doi: 10.1186/s13059-017-1246-7.

[66] CAMPI M, D’ANDREA L, EMILIANI J, et al. Participation of chromatin- remodeling proteins in the repair of ultraviolet-b-damaged DNA [J]. Plant Physiol, 2012, 158(2): 981–995. doi: 10.1104/pp.111.191452.

[67] KANDASAMY M K, DEAL R B, MCKINNEY E C, et al. Silencing the nuclear actin-related protein AtARP4 inhas multiple effects on plant development, including early flowering and delayed floral senescence [J]. Plant J, 2005, 41(6): 845–858. doi: 10.1111/j. 1365-313x.2005.02345.x.

[68] KANDASAMY M K, MCKINNEY E C, DEAL R B, et al.ARP7 is an essential actin-related protein required for normal embryo- genesis, plant architecture, and floral organ abscission [J]. Plant Physiol, 2005, 138(4): 2019–2032. doi: 10.1104/pp.105.065326.

[69] FRITSCH O, BENVENUTO G, BOWLER C, et al. The INO80 protein controls homologous recombination in[J]. Mol Cell, 2004, 16(3): 479–485. doi: 10.1016/j.molcel.2004.09.034.

[70] ZHANG C, CAO L, RONG L, et al. The chromatin-remodeling factor AtINO80 plays crucial roles in genome stability maintenance and in plant development [J]. Plant J, 2015, 82(4): 655–668. doi: 10.1111/ tpj.12840.

[71] HAN Y F, DOU K, MA Z Y, et al. SUVR2 is involved in trans- criptional gene silencing by associating with SNF2-related chromatin- remodeling proteins in[J]. Cell Res, 2014, 24(12): 1445– 1465. doi: 10.1038/cr.2014.156.

[72] DOKLáDAL L, BENKOVá E, HONYS D, et al. An armadillo- domain protein participates in a telomerase interaction network [J]. Plant Mol Biol, 2018, 97(4/5): 407–420. doi: 10.1007/s11103-018- 0747-4.

[73] CHOI K, PARK C, LEE J, et al.homologs of components of the SWR1 complex regulate flowering and plant development [J]. Development, 2007, 134(10): 1931–1941. doi: 10.1242/dev.001891.

[74] MARCH-DíAZ R, GARCIA-DOMíNGUEZ M, FLORENCIO F J, et al. SEF, a new protein required for flowering repression in, interacts with PIE1 and ARP6 [J]. Plant Physiol, 2007, 143(2): 893– 901. doi: 10.1104/pp.106.092270.

[75] GóMEZ-ZAMBRANO á, CREVILLéN P, FRANCO-ZORRILLA J M, et al.SWC4 binds DNA and recruits the SWR1 complex to modulate histone H2A.Z deposition at key regulatory genes [J]. Mol Plant, 2018, 11(6): 815–832. doi: 10.1016/j.molp.2018.03.014.

[76] BERRIRI S, GANGAPPA S N, KUMAR S V. SWR1 chromatin- remodeling complex subunits and H2A.Z have non-overlapping functions in immunity and gene regulation in[J]. Mol Plant, 2016, 9(7): 1051–1065. doi: 10.1016/j.molp.2016.04.003.

[77] CHOI K, KIM J, MULLER S Y, et al. Regulation of microRNA- mediated developmental changes by the SWR1 chromatin remodeling complex [J]. Plant Physiol, 2016, 171(2): 1128–1143. doi: 10.1104/pp. 16.00332.

[78] CUI Z B, TONG A Z, HUO Y Q, et al. SKIP controls flowering timethe alternative splicing ofpre-mRNA in[J]. BMC Biol, 2017, 15: 80. doi: 10.1186/s12915-017-0422-2.

[79] QIN Y, ZHAO L H, SKAGGS M I, et al. Actin-related protein6 regulates female meiosis by modulating meiotic gene expression in[J]. Plant Cell, 2014, 26(4): 1612–1628. doi: 10.1105/tpc. 113.120576.

[80] ZHAO L H, CAI H Y, SU Z X, et al.suppresses megasporocyte cell fate through SWR1-mediated activation ofexpression in[J]. Proc Natl Acad Sci USA, 2018, 115(3): E526-E535. doi: 10.1073/pnas.1716054115..

[81] ZACHARAKI V, BENHAMED M, POULIOS S, et al. Theortholog of the YEATS domain containing protein YAF9a regu- lates flowering by controlling H4 acetylation levels at thelocus [J]. Plant Sci, 2012, 196: 44–52. doi: 10.1016/j.plantsci.2012.07.010.

[82] CREVILLéN P, GóMEZ-ZAMBRANO á, LóPEZ J A, et al.YAF9 histone readers modulate flowering time through nuA4- complex-dependent H4 and H2A.Z histone acetylation atchromatin [J]. New Phytol, 2019, 222(4): 1893–1908. doi: 10.1111/nph.15737.

[83] SHEN Y, DEVIC M, LEPINIEC L, et al. Chromodomain, helicase and DNA-binding CHD1 protein, CHR5, are involved in establishing active chromatin state of seed maturation genes [J]. Plant Biotechnol J, 2015, 13(6): 811–820. doi: 10.1111/pbi.12315.

[84] ZOU B H, SUN Q, ZHANG W L, et al. Thechromatin- remodeling factor CHR5 regulates plant immune responses and nucleosome occupancy [J]. Plant Cell Physiol, 2017, 58(12): 2202– 2216. doi: 10.1093/pcp/pcx155.

[85] AICHINGER E, VILLAR C B R, DI MAMBRO R, et al. The CHD3 chromatin remodeler PICKLE and polycomb group proteins antago- nistically regulate meristem activity in theroot [J]. Plant Cell, 2011, 23(3): 1047–1060. doi: 10.1105/tpc.111.083352.

[86] FUKAKI H, TANIGUCHI N, TASAKA M. PICKLE is required for SOLITARY-ROOT/IAA14-mediated repression of ARF7 and ARF19 activity duringlateral root initiation [J]. Plant J, 2006, 48(3): 380–389. doi: 10.1111/j.1365-313x.2006.02882.x.

[87] ZHANG H, BISHOP B, RINGENBERG W, et al. The CHD3 remodeler PICKLE associates with genes enriched for trimethylation of histone H3 lysine 27 [J]. Plant Physiol, 2012, 159(1): 418–432. doi: 10.1104/pp.112.194878.

[88] YANG R, ZHENG Z M, CHEN Q, et al. The developmental regulator PKL is required to maintain correct DNA methylation patterns at RNA- directed DNA methylation loci [J]. Genome Biol, 2017, 18(1): 103. doi: 10.1186/s13059-017-1226-y.

[89] PARK J, OH D H, DASSANAYAKE M, et al. Gibberellin signaling requires chromatin remodeler PICKLE to promote vegetative growth and phase transitions [J]. Plant Physiol, 2017, 173(2): 1463–1474. doi: 10.1104/pp.16.01471.

[90] XU M L, HU T Q, SMITH M R, et al. Epigenetic regulation of vegetative phase change in[J]. Plant Cell, 2016, 28(1): 28–41. doi: 10.1105/tpc.15.00854.

[91] JING Y J, ZHANG D, WANG X, et al.chromatin remodeling factor PICKLE interacts with transcription factor HY5 to regulate hypocotyl cell elongation [J]. Plant Cell, 2013, 25(1): 242–256. doi: 10.1105/tpc.112.105742.

[92] SMACZNIAK C, IMMINK R G H, MUI?O J M, et al. Charac- terization of MADS-domain transcription factor complexes inflower development [J]. Proc Natl Acad Sci USA, 2012, 109(5): 1560–1565. doi: 10.1073/pnas.1112871109.

[93] ZHANG D, JING Y J, JIANG Z M, et al. The chromatin-remodeling factor PICKLE integrates brassinosteroid and gibberellin signaling during skotomorphogenic growth in[J]. Plant Cell, 2014, 26(6): 2472–2485. doi: 10.1105/tpc.113.121848.

[94] ZEMACH A, LI Y, WAYBURN B, et al. DDM1 bindsmethyl-CpG binding domain proteins and affects their subnuclear localization [J]. Plant Cell, 2005, 17(5): 1549–1558. doi: 10.1105/tpc. 105.031567

[95] ZEMACH A, KIM M Y, HSIEH P H, et al. Thenucleo- some remodeler DDM1 allows DNA methyltransferases to access h1- containing heterochromatin [J]. Cell, 2013, 153(1): 193–205. doi: 10. 1016/j.cell.2013.02.033.

[96] LYONS D B, ZILBERMAN D. DDM1 and lsh remodelers allow methylation of DNA wrapped in nucleosomes [J]. Elife, 2017, 6: e30 674. doi: 10.7554/eLife.30674.

[97] XIE X Y, SHIPPEN D E. DDM1 guards against telomere truncation in[J]. Plant Cell Rep, 2018, 37(3): 501–513. doi: 10.1007/ s00299-017-2245-6.

[98] CHO E J, CHOI S H, KIM J H, et al. A mutation in plant-specific swi2/snf2-like chromatin-remodeling proteins, DRD1 and DDM1, delays leaf senescence in[J]. PLoS One, 2016, 11(1): e0146826. doi: 10.1371/journal.pone.0146826.

[99] LI G, LIU S J, WANG J W, et al. ISWI proteins participate in the genome-wide nucleosome distribution in[J]. Plant J, 2014, 78(4): 706–714. doi: 10.1111/tpj.12499.

[100] LI G, ZHANG J W, LI J Q, et al. Imitation switch chromatin remo- deling factors and their interacting RINGLET proteins act together in controlling the plant vegetative phase in[J]. Plant J, 2012, 72(2): 261–270. doi: 10.1111/j.1365-313X.2012.05074.x.

[101] LAW J A, AUSIN I, JOHNSON L M, et al. A protein complex required for polymerase V transcripts and RNA-directed DNA methy- lation in[J]. Curr Biol, 2010, 20(10): 951–956. doi: 10. 1016/j.cub.2010.03.062.

[102] HIRAKAWA T, HASEGAWA J, WHITE C I, et al. RAD54 forms DNA repair foci in response to DNA damage in living plant cells [J]. Plant J, 2017, 90(2): 372–382. doi: 10.1111/tpj.13499.

[103] ARCHACKI R, BUSZEWICZ D, SARNOWSKI T J, et al. BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in[J]. PLoS One, 2013, 8(3): e58588. doi: 10.1371/journal.pone.0058588.

[104] FARRONA S, HURTADO L, MARCH-DíAZ R, et al. Brahma is required for proper expression of the floral repressorin[J]. PLoS One, 2011, 6(3): e17997. doi: 10.1371/journal.pone. 0017997.

[105] LI C L, CHEN C, GAO L, et al. Theswi2/snf2 chromatin remodeler BRAHMA regulates polycomb function during vegetative development and directly activates the flowering repressor gene[J]. PLoS Genet, 2015, 11(1): e1004944. doi: 10.1371/journal.pgen. 1004944.

[106] WALLEY J W, ROWE H C, XIAO Y M, et al. The chromatin remo- deler SPLAYED regulates specific stress signaling pathways [J]. PLoS Pathog, 2008, 4(12): e1000237. doi: 10.1371/journal.ppat.1000237.

[107] JOHNSON K C M, XIA S T, FENG X Q, et al. The chromatin remo- deler SPLAYED negatively regulates SNC1-mediated immunity [J]. Plant Cell Physiol, 2015, 56(8): 1616–1623. doi: 10.1093/pcp/pcv087.

[108] GENG F, CAO Y, LAURENT B C. Essential roles of snf5p in snf-swi chromatin remodeling[J]. Mol Cell Biol, 2001, 21(13): 4311– 4320. doi: 10.1128/MCB.21.13.4311-4320.2001.

[109] MULLER J, OMA Y, VALLAR L, et al. Sequence and comparative genomic analysis of actin-related proteins [J]. Mol Biol Cell, 2005, 16(12): 5736–5748. doi: 10.1091/mbc.e05-06-0508.

[110] KANDASAMY M K, DEAL R B, MCKINNEY E C, et al. Plant actin-related proteins [J]. Trends Plant Sci, 2004, 9(4): 196–202. doi: 10.1016/j.tplants.2004.02.004.

[111] KANDASAMY M K, MCKINNEY E C, MEAGHER R B. Cell cycle-dependent association ofactin-related proteins AtARP4 and AtARP7 with the nucleus [J]. Plant J, 2003, 33(5): 939– 948. doi: 10.1046/j.1365-313x.2003.01691.x.

[112] LI H C, CHUANG K, HENDERSON J T, et al. PICKLE acts during germination to repress expression of embryonic traits [J]. Plant J, 2005, 44(6): 1010–1022. doi: 10.1111/j.1365-313x.2005.02602.x.

[113] AICHINGER E, VILLAR C B R, FARRONR S, et al. CHD3 proteins and polycomb group proteins antagonistically determine cell identity in[J]. PLoS Genet, 2009, 5(8): e1000605. doi: 10.1371/ journal.pgen.1000605.

[114] CARTER B, HENDERSON J T, SVEDIN E, et al. Cross-Talk between sporophyte and gametophyte generations is promoted by CHD3 chromatin remodelers in[J]. Genetics, 2016, 203(2): 817–829. doi: 10.1534/genetics.115.180141

[115] HIGO H, TAHIR M, TAKASHIMA K, et al.(decrease in DNA methylation) genes in rice () [J]. Mol Genet Genom, 2012, 287(10): 785–792. doi: 10.1007/s00438-012-0717-5.

[116] MA X D, MA J, ZHAI H H, et al. CHR729 is a CHD3 protein that controls seedling development in rice [J]. PLoS One, 2015, 10(9): e0138934. doi: 10.1371/journal.pone.0138934.

[117] FOLTA A, BARGSTEN J W, BISSELING T, et al. Compact tomato seedlings and plants upon overexpression of a tomato chromatin remodelling ATPase gene [J]. Plant Biotechnol J, 2016, 14(2): 581– 591. doi: 10.1111/pbi.12400.

Functions of ATP-dependent Chromatin Remodeling Factors in Plant Development

PENG Xiu-ling1,2, WANG Jian-hao1,2, YANG Song-guang1*

(1. Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; 2.University of Chinese Academy of Sciences, Chinese Academy of Sciences,Beijing 100049, China)

In eukaryotic cells, the ATP-dependent chromatin remodeling complexes utilize the energy of ATP to disrupt nucleosome DNA contacts, move nucleosomes along DNA, and remove or exchange nucleosomes. They thus make DNA/chromatin available to proteins that need to access DNA or histones directly during cellular processes. The first chromatin remodeling complex was found in yeast, containing at least 11 subunits by biochemical analysis. However, the chromatin remodeling complexes in plants are less known. The studies on plant chromatin remodeling factors were reviewed, which would provide insights into the involvement of plant chromatin remodeling in development.

Chromatin remodeling factor; Epigenetic regulation; Function; Plant

10.11926/jtsb.4070

2019–03–25

2019–05–17

廣東省杰出青年基金項目(2016A030306047); 廣州市珠江科技新星項目(201610010138); 國家自然科學基金項目(31672161)資助

This work was supported by the Guangdong Natural Science Funds for Distinguished Young Scholars (Grant No. 2016A030306047); the Pearl River Science and Technology Nova Program of Guangzhou (Grant No. 201610010138), and the National Natural Science Foundation of China (Grant No. 31672161).

E-mail: yangsongguang@scbg.ac.cn