E3泛素連接酶調控植物抗病分子機理研究進展

楊玖霞, 張 浩, 王志龍, 王旭麗, 王國梁*

(1.湖南農業(yè)大學農學院, 長沙 410128;2. 中國農業(yè)科學院植物保護研究所,植物病蟲害生物學國家重點實驗室, 北京 100193)

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E3泛素連接酶調控植物抗病分子機理研究進展

楊玖霞1,2, 張 浩1,2, 王志龍1, 王旭麗2*, 王國梁1,2*

(1.湖南農業(yè)大學農學院, 長沙 410128;2. 中國農業(yè)科學院植物保護研究所,植物病蟲害生物學國家重點實驗室, 北京 100193)

生物脅迫是影響我國農作物生產的重要因素,也是當前植物界研究方向涉及最為廣泛的領域之一。由泛素介導的降解途徑是生物體內最為精細的調控體系,涉及對生物體的生長發(fā)育以及生物體對周圍環(huán)境適應的調控等過程。E3泛素連接酶因對底物有特異性識別作用,被認為是泛素化過程中最重要的組成部分。依據(jù)其結構和功能的不同可以將E3泛素連接酶分為4個家族。越來越多的研究表明這些不同的E3家族成員可以參與植物抗病免疫反應的各個過程。本文在簡要概括E3泛素連接酶分類的基礎上綜述了目前E3泛素連接酶參與調控植物抗病害方面研究進展,并對今后研究方向進行了展望,以期對抗病機理解析及抗病品種研發(fā)提供新思路。

UPS; 泛素化; E3泛素連接酶; PTI; ETI

植物與病原物在長期相互作用過程中協(xié)同進化。寄主針對病原菌相關分子模式(pathogen-associated molecule pattern, PAMP)包括模式識別受體(pattern recognition receptor, PRR),誘導的免疫反應PTI (PAMP-triggered immunity)[1]阻止病原物的侵染。為了抵御寄主的PTI,病菌進一步分泌特異性的效應蛋白分子(effector),而植物則進化出專一的抗病(resistance, R)蛋白直接或間接識別病原菌特異擁有的效應蛋白,產生效應蛋白激活的免疫反應(effector-triggered immunity, ETI)[2],以抵御病原物的侵襲,其中過敏反應(hypersensitive response, HR)是最典型的一種表現(xiàn)[3]。植物PTI和ETI免疫反應中存在很多交叉相似的信號途徑,比如蛋白質的翻譯后修飾作用,JA(jasmonic acid)、SA(salicylic acid)、ET(ethylene)等信號分子的產生,活性氧和抗病相關基因的誘導。植物激素是系統(tǒng)性信號的重要組分,并且對植物防御病原物的抗性水平有極其重要的影響,植物與病原物相互作用的同時常伴隨著一些激素水平的明顯變化,已有大量試驗數(shù)據(jù)表明,這些變化及其相互之間的影響對植物抵抗生物脅迫至關重要[4]。

泛素/26S蛋白酶體(ubiquitin-26S proteasome system, UPS)途徑是真核生物細胞中一種重要的蛋白質翻譯后修飾作用,涉及對生物體的生長發(fā)育以及生物體對周圍環(huán)境適應性的精細調控[5-10]。該過程首先是靶蛋白被泛素分子(76個氨基酸所組成的多肽)修飾標記,然后被蛋白酶體識別和降解。其中,泛素對靶蛋白的修飾過程是由泛素活化酶(ubiquitin-activating enzyme, E1)、泛素結合酶(ubiquitin-conjugating enzyme, E2)和泛素連接酶(ubiquitin-ligating enzyme, E3)3個酶所介導的級聯(lián)反應共同催化完成[11]。E3泛素連接酶是一個種類繁多的大家族,主要負責對靶蛋白的特異性識別,進而對其進行泛素化修飾。近幾年,越來越多的研究證據(jù)表明E3泛素連接酶參與了各種抗病信號反應途徑的調控。本文綜述了E3泛素連接酶在植物免疫反應從最初病原物的識別到下游信號途徑等各個過程中所發(fā)揮的正調控或負調控作用。通過概括其參與植物抗病反應的分子機理,增加對病原菌與植物分子互作機理的認識,為重要農作物分子育種提供新思路。

1 E3泛素連接酶分類

UPS是植物細胞內蛋白質降解的主要途徑,參與細胞內80%以上蛋白質的降解,與各種應激反應都有關聯(lián)[9,12]。Lee[13]和Mazzucotelli[14]等研究發(fā)現(xiàn)擬南芥中超過1 600個基因可以編碼UPS(Ub/26S proteasome system)相關功能蛋白(超過全基因組總數(shù)的6%),其中有多于1 400個基因編碼E3泛素連接酶;水稻中E3泛素連接酶基因也有1 300多個[15],這些龐大的數(shù)字說明了E3泛素連接酶在植物生命周期中的重要性。

E3泛素連接酶根據(jù)結構的不同大致可以分為兩大類：單亞基類型和多亞基類型。其中前者又可分為HECT型(homologous to E6-associated protein C-terminus)、U-box型和RING型(really interesting new gene);常見的多亞基CRL復合體(Cullin-RING ligase)如SCF(Skp1, Cullin, F-box)類型連接酶[5,9,16]。HECT類型蛋白C端含有一個約350個氨基酸殘基結構域,此結構域包含有Ub-E2復合體的結合位點,其中保守的半胱氨酸位點可以用于接受Ub分子,在將底物泛素化之前首先以E3-Ub中間體形式存在[17]。而RING和U-box蛋白在結構上是十分相似的單一多肽,他們可以通過鋅螯合物和氫鍵或者鹽橋將泛素分子(Ub)從Ub-E2中間復合物轉移到靶標蛋白上[18-19]。RING結構域主要包括兩種構型,由半胱氨酸(C)和組氨酸(H)組成的8個氨基酸與鋅離子螯合而成的RING-H2和RING-HC構型;這種類型的泛素連接酶除了獨立發(fā)揮作用以外,還可以CRL復合體的一個多亞基單位來行使功能。CRL形式的E3泛素連接酶是指由Cullin、RING-box和靶標蛋白識別元件共同組成的一個復合體[9],常見的有SCF(Skp1, Cullin, F-box),BTB(bric-a-brac-tramtrack-broad complex),DDB(DNA damage-binding)[9]。其中DDB復合體可以調節(jié)DNA的修復、DNA復制以及轉錄,它可以被病毒所破壞。常見CRL復合體中,對底物的特異識別依賴于F-box蛋白,RING蛋白則與E2結合在一起[20]。這些不同類別的E3連接酶家族成員都先后被報道參與植物免疫反應過程。比如,通過細胞膜上的模式識別分子(PRR)調控植物對病原分子相關分子模式的識別,并調節(jié)細胞內的核苷酸綁定亮氨酸富集的免疫受體積累;另外E3泛素連接酶還可以一些囊泡運輸成分或核轉錄因子為靶蛋白來調控病原菌識別免疫反應下游的各種信號途徑。

2 E3泛素連接酶和植物的抗病性

2.1 E3泛素連接酶調控植物PTI免疫過程

目前,已有不少例證發(fā)現(xiàn)E3泛素連接酶可作為調節(jié)子參與植物細胞質膜PRRs(pattern-recognition receptors)識別病原菌PAMPs所介導的PTI免疫反應過程(表1)。其中研究較為深入的有,Lu等在研究擬南芥PRR蛋白FLS2(flagellin-sensing 2)識別PAMP因子flg22所誘導的抗病信號反應過程中發(fā)現(xiàn),在由受體蛋白FLS2和協(xié)同受體BAK1(brassinosteroid insensitive 1-associated kinase 1)形成復合體這一復雜的信號通路中,受flg22結合FLS2的誘導,U-box泛素連接酶PUB12和PUB13(plant U-box)可被協(xié)同受體BAK1磷酸化,進而引起PUB12和PUB13直接泛素化FLS2以促進其降解,從而負調控FLS2介導的PTI免疫反應,抑制過量或持續(xù)的免疫反應激活對植物所造成的傷害[21]。另一例發(fā)現(xiàn)為擬南芥中3個E3泛素連接酶PUB22、PUB23和PUB24的表達量受PAMP因子flg22和chitin以及病菌侵染的誘導表達,同時,Pseudomonassyringaepv.tomato經pub22/pub23/pub24突變體接種后,表現(xiàn)為對病菌的抗性增強、ROS含量增多、參與ROS形成相關基因RbohD表達量上調[22-23],以上結果表明這3個E3泛素連接酶負調控PAMPs誘導的PTI反應。另外,擬南芥中ATL9基因編碼一個RING-finger結構蛋白,具備E3泛素連接酶活性。表達模式分析發(fā)現(xiàn)ATL9基因的表達量與擬南芥防御白粉菌(Golovinomycescichoracearum)的基礎抗性呈正相關。chitin處理擬南芥后,檢測到ATL9受到明顯誘導,這表明該基因可能直接參與擬南芥抵抗白粉菌的PTI反應過程[24]。轉錄因子VpWRKY11可以激活JA相應相關基因AOS(allene oxide synthase)和LOX2(lipoxygenase 2),負調控植物免疫反應[53]。Yu等[39]在中國野葡萄(Vitispseudoreticulata)中發(fā)現(xiàn)RING型E3連接酶蛋白EIRP1通過降解VpWRKY11,正調控植物免疫。另外他們還發(fā)現(xiàn),在擬南芥中過表達EIRP1導致VpWRKY11、AOS和LOX2的基因表達下調,并提高轉基因植株對細菌和真菌的抗性,上述研究揭示了E3連接酶介導的蛋白降解途徑在調控植物抗病相關的轉錄因子介導的抗病信號中具有重要作用。

表1 植物免疫信號途徑中參與調控作用的E3泛素連接酶

續(xù)表1 Table 1(Continued)

物種SpeciesE3泛素連接酶E3ligase類型Type靶蛋白Target免疫過程作用Signalpathway引文References水稻RiceAPIP6RINGAvrPiz-t正調控PTI[41]水稻RiceSPL11U-boxSPIN6負調控PTI[42-43]水稻RicePUB44U-boxXopPxoo正調控ETI[44]水稻RiceXB3RINGXA21正調控ETI[45]水稻RiceOsDRF1F-box未知正調控抗病反應[46]煙草TobaccoCMPG1U-boxAVR3a正調控ETI[47]煙草TobaccoACRE276U-boxSRK1-likekinase正調控ETI[28,48]煙草TobaccoACRE74U-box未知正調控ETI[49]胡椒PepperCaRING1RING未知正調控HR反應[50]油菜BrassicaARC1U-boxSRK2-likekinase正調控免疫反應[51-52]

水稻EL5(riceN-acetylchitooligosaccharide elicitor-responsive gene)是一個RING-H2 finger型泛素連接酶,研究證明EL5和水稻E2結合酶基因OsUBC5b受到激發(fā)子N-乙酰幾丁寡糖誘導表達,該結果表明EL5可能與OsUBC5b一起參與病原菌引發(fā)的水稻PTI抗病反應[40]。在揭示水稻稻瘟病菌(Magnaportheoryzae)效應因子AvrPiz-t和其相對應的R基因Piz-t的相互作用機理的過程中,發(fā)現(xiàn)效應子AvrPiz-t互作蛋白APIP6是一個RING型E3泛素連接酶,在APIP6干擾的水稻轉基因株系中發(fā)現(xiàn)PAMP誘導的活性氧含量降低,抗病相關基因表達下調,對稻瘟病抗性明顯減弱。這表明E3泛素連接酶APIP6作為一個正調控因子參與水稻對稻瘟菌的PTI免疫過程[41]。另外,擬南芥PUB12/13在水稻中的同源蛋白SPL11被發(fā)現(xiàn)負調控植物細胞程序化死亡和基礎抗病性[42]。Liu等[43]最新研究發(fā)現(xiàn)SPL11通過泛素化降解Rho型小G蛋白激活酶SPIN6,從而調控小G蛋白OsRac1介導的防衛(wèi)反應信號。

2.2 E3泛素連接酶調控植物ETI抗病反應過程

病原菌為了抵御寄主的PTI免疫反應,進一步分泌特異性效應蛋白分子(effector),打破植物的第一道防線-PTI,而植物則進化出專一的抗病蛋白(resistance protein, R protein)直接或間接識別病原菌特異擁有的效應蛋白。目前為止，植物中已經有近百個R基因被克隆,其中一些基因所涉及的抗病信號途徑已被證明與泛素化相關[54]。

2.2.1 E3泛素連接酶直接作用于Avr和R蛋白

已有例證表明,E3泛素連接酶可直接作用于Avr和R蛋白,將其泛素化并經26S蛋白酶降解體系最終降解,從而達到對寄主R基因所介導的ETI抗病反應的調控。在動物界中已有相關報道,沙門氏菌(Salmonella)效應子SopE和SptP在病菌侵染過程的不同階段發(fā)揮各自的功能,但是研究發(fā)現(xiàn)哺乳動物Henle-407細胞可以通過體內UPS將這兩個效應子泛素化并降解,從而阻礙細菌的入侵[55]。近年來在植物中也發(fā)現(xiàn)有相似的調控過程,例如,擬南芥E3泛素連接酶CPR1可以與NB-LRR R蛋白SNC1和RPS2發(fā)生互作并將其泛素化,最終依賴UPS途徑降低這兩個抗病蛋白的積累,避免了植物免疫信號途徑過度激活帶給植物的過度耗能[25-26]。水稻中,OsPUB44已被研究發(fā)現(xiàn)可以與Xoo(Xanthomonasoryzaepv.oryzae)效應子XopPxoo發(fā)生互作,將OsPUB44沉默后發(fā)現(xiàn)PGN或chitin引發(fā)的免疫反應受到抑制,植物對Xoo防御反應減弱,這表明OsPUB44在水稻中對ETI過程起正調控作用[44]。

2.2.2 E3泛素連接酶作用于HR反應途徑

HR過敏反應是寄主抗病蛋白在識別病菌效應蛋白時所產生ETI反應中的最典型的一種反應,研究發(fā)現(xiàn)E3泛素連接酶可通過調節(jié)HR反應達到對ETI過程的調節(jié)。例如,擬南芥中NLR(LZ-NBS-LRR)抗性蛋白RPM1被發(fā)現(xiàn)接種丁香假單胞菌(P.syringae)后聚集在質膜附近,但在HR反應初期迅速消失[56]。深入研究發(fā)現(xiàn),兩個RING型E3連接酶蛋白RIN2和RIN3能夠與RPM1相互作用,表明泛素蛋白酶體降解途徑可能參與了RPM1介導的ETI抗病信號途徑。但rin2rin3雙突變體和野生型Col-0接種DC3000(AvrRpm1)后都可以檢測到RPM1的消失,表明RPM1的降解并不是由RIN2和RIN3直接引起的[27]。另外rin2rin3雙突變體植株也會發(fā)生HR反應,只是較野生型HR反應弱,并且突變體植物中依然存在病原菌的生長,由此可以看出RIN2/RIN3 E3泛素連接酶在植物對抗P.syringae的反應中可能只參與調控RPM1依賴的HR反應中的某個分支。

Gilroy等人發(fā)現(xiàn)U-box類型的泛素連接酶CMPG1參與介導無毒基因和其相應的抗性基因(Cf-9/Avr9, Cf-4/Avr4, Pto/AvrPto)之間的識別作用所誘導的寄主細胞壞死反應[47],即該蛋白作為正向調節(jié)子促進寄主對病菌的抗病反應,但其在HR反應過程中自身會被UPS系統(tǒng)所降解。隨后研究發(fā)現(xiàn)致病疫霉(Phytophthorainfestans)效應子AVR3a在活體營養(yǎng)階段可以與CMPG1發(fā)生互作,并改變CMPG1定位,以穩(wěn)定CMPG1的泛素連接酶活性,阻礙其被26S蛋白酶體途徑所降解;從而抑制INF-1所引發(fā)的細胞壞死抗病性反應的產生[47]。有意思的是,煙草中ACRE74與荷蘭芹(Petroselinumcrispum)CMPG1[57]和擬南芥PUB20/PUB21高度同源,因而又被命名為NtCMPG1。功能研究發(fā)現(xiàn),在具有Cf9抗性基因背景的煙草中超表達NtCMPG1后,轉基因植株對含有無毒效應子Avr9的菌株表現(xiàn)出更強的抗性并誘發(fā)植株強烈HR反應。反之,該研究團隊嘗試在番茄中干擾番茄同源基因CMPG1,結果發(fā)現(xiàn)番茄植株對黃枝孢霉(Cladosporiumfulvum)的抗性明顯降低[49]。同樣的,煙草中RNAi干擾ACRE276導致植株HR反應消失。番茄中干擾ACRE276同源基因后,降低了含抗性基因Cf-9的植株的抗病性[28,48]。進一步研究發(fā)現(xiàn),擬南芥中ACRE276同源基因PUB17也具有保守的功能,煙草中瞬時表達PUB17可以互補ACRE276干擾煙草的HR反應,而E3活性缺失的PUB17則不能互補該表型[28],表明U-box E3連接酶ACRE276和PUB17在調控ETI防御反應中起著保守的重要作用。XA21是一個RLK(receptor-like kinase)蛋白,研究發(fā)現(xiàn)在水稻中RING-type E3泛素連接酶XB3可以與XA21發(fā)生互作,參與調控水稻對Xoo的抗性。同時XA21的積累需要XB3的存在,XB3能夠被XA21磷酸化。在煙草表皮細胞過表達XB3蛋白能夠引起細胞壞死現(xiàn)象,而細胞壞死現(xiàn)象的發(fā)生則依賴XB3的E3酶活性,這些結果表明泛素蛋白酶降解途徑參與了XA21介導的抗病信號途徑[45,58]。

2.2.3 E3泛素連接酶作用于調控抗病相關基因的轉錄因子

擬南芥中RING型E3泛素連接酶MIEL1與轉錄因子MYB30在細胞核中可發(fā)生互作,并導致MYB30的降解,從而降低MYB30轉錄激活的抗病相關基因的表達,抑制植物免疫反應[29-30]。類似地,擬南芥中另一個RING型E3泛素連接酶BOI1(BOS1 interactor1)與R2R3型MYB轉錄因子BOS1(botrytis susceptible1)在植物細胞核中互作并可體外泛素化BOS1,從而負調控植物對病原菌的抗性。生物學功能研究表明,BOI1的RNAi植株對灰霉病的抗性減弱而且表現(xiàn)出更不耐鹽性。而在BOI1的RNAi植株中過表達BOS1會增加植物對活性氧的耐受性和灰霉病的抗性[31]。

2.3 E3泛素連接酶調控抗病相關信號途徑

水楊酸SA在調控活體營養(yǎng)或者半活體營養(yǎng)型病原菌抗性中發(fā)揮著重要的作用。CaRING1是來自胡椒的一種E3泛素連接酶,其蛋白序列中包含一個跨膜結構域和一個C端RING結構域,接種毒性辣椒瘡痂病菌(Xanthomonascampestrispv.vesicatoria)之后檢測到該基因表達受到誘導。功能研究發(fā)現(xiàn)病毒介導的CaRING基因沉默后,降低了植株的抗病性與抗病相關基因PR1的表達,并伴隨親和性細胞死亡發(fā)生。同時,葉片中SA水平顯著下降[50]。另外,BAH1也是一個RING型E3連接酶,擬南芥bah1-D(benzoic acid hypersensitive1-Dominant)突變體在接種病原菌后或者用SA前體處理后都可以積累大量的SA,并產生依賴SA的局部細胞死亡,表明BAH1通過SA信號轉導途徑抑制植物免疫反應[32]。

最近,Xie等[59]發(fā)現(xiàn)F-box類型E3泛素連接酶COI1參與JA信號途徑并調控植物抗病性。COI1作為JA信號途徑中一個重要的組成成分,也是SCF類型E3泛素連接酶中一個成員。最新研究發(fā)現(xiàn),茉莉酸ZIM結構域(JAZ)蛋白是SCF-COI1調控的泛素化作用底物。當SCF-COI1復合體識別茉莉酸-異亮氨酸信號以后,JAZ被SCF-COI1 E3復合體泛素化,并進入26S蛋白酶體使其降解,受抑制的轉錄激活因子被重新激活,JA信號途徑相關基因開始轉錄、表達[33-34]。OsDRF1是水稻中一個F-box類型E3連接酶,ABA處理水稻后檢測到OsDRF1表達量上調,在煙草中過表達OsDRF1,超表達植株表現(xiàn)出ABA敏感以及對病毒和細菌抗性的提高[46]。上述研究揭示了E3連接酶在抗病相關激素SA/JA/ABA信號途徑中發(fā)揮作用。

3 病原物效應因子作為E3泛素連接酶參與調控植物防御反應

E3泛素連接酶除了在植物抗病反應中發(fā)揮著重要作用以外,新近研究表明病原菌相關效應因子具有E3泛素連接酶的活性,以抑制寄主的PTI和ETI防衛(wèi)反應。例如,番茄假單胞菌(P.syringaepv.tomato)無毒蛋白AvrPtoB是一個TypeⅢ效應因子(T3E)[60]。AvrPtoB可以與番茄中的一個激酶Fen互作,以激活植物ETI反應。然后,最近研究發(fā)現(xiàn)AvrPtoB的C端含有一個Ring/U-box結構域[61],該結構域具有E3泛素連接酶活性。且接種敲除該結構域的AvrPtoB突變體菌株后,含F(xiàn)en基因的番茄植株表現(xiàn)出HR反應[62]。在擬南芥中,AvrPtoB可通過其N端結構域與模式識別受體FLS2及其共同受體BAK1在體內發(fā)生相互作用,并催化FLS2的激酶結構域被泛素化,以抑制植物PTI免疫過程[63-65];而在番茄中AvrPtoB可以特異性地泛素化Fen蛋白激酶,促進Fen蛋白被26S蛋白酶降解體系降解,從而減弱番茄植株對假單胞菌的抗性,促進病原菌的侵染和定殖[66]。

根瘤菌(Rhizobiumsp. strain NGR234)的效應子蛋白NopM (nodulation outer protein M)編碼一個NEL(novel E3 ubiquitin ligase)類似E3蛋白,煙草中異源表達該基因后,植物中活性氧積累受到明顯抑制,防御反應相關基因表達下調[67]。

最近的晶體結構分析發(fā)現(xiàn),黃單胞菌效應蛋白XopL編碼一種新型E3泛素鏈接酶,其在結構上與沙門氏菌和志賀氏菌的Type III效應蛋白高度同源。生物化學活性分析表明XopL能與植物E2結合酶發(fā)生特異互作并表現(xiàn)E3活性,這種E3泛素連接酶活性對細胞凋亡的誘導和植物免疫反應的抑制起著關鍵作用[68]。

4 總結與展望

過去10年期間,科學家對泛素蛋白酶體系在植物生物學中的研究已延伸至各個方面,大量證據(jù)表明即使在單一的信號反應途徑中UPS也有眾多的控制點,因此,一些特異的UPS系統(tǒng)組成元件比如E3泛素連接酶等的破壞、修飾或者重組都可以直接或者間接地對植物激素信號途徑、基因轉錄、形態(tài)發(fā)生、對周圍惡劣生長環(huán)境的抵御以及植物與病原物之間的競爭等過程的調控產生很大的阻力,從而影響到農業(yè)生產。另外,泛素分子還可以通過3種酶的共同作用完成一些蛋白的正確組裝和折疊并參與一些蛋白的活性調節(jié)。盡管近期的遺傳學研究使人類對UPS的功能有了初步的認識,但詳細的作用機理仍有待于探索。

植物中,所發(fā)現(xiàn)的編碼UPS相關蛋白的基因中,有很大部分都編碼E3泛素連接酶,研究E3與植物免疫的關聯(lián)有助于更好地理解植物與病原菌互作,但是有些E3泛素連接酶雖然發(fā)現(xiàn)其在宿主免疫抗病反應中參與調控,但是其具體的分子機理尚不是很清楚。比如擬南芥PUB22、PUB23和PUB24雖然已經證明可以抑制植物PTI免疫過程[22],但其中只有PUB22是通過UPS抑制植物免疫過程,而對于PUB23和PUB24,其具體的作用底物和所參與的上游信號途徑尚不清楚。故基于E3泛素連接酶基因在植物抗病反應中所起的重要作用,一些問題的解決迫在眉睫,比如E3泛素連接酶的作用底物是什么？它是如何識別底物蛋白的？這些底物蛋白有何特點？解決了這些問題,不僅可以闡明植物對抗病原菌免疫反應中錯綜復雜的互作關系,還可以增加人們對E3蛋白功能的認識;更清楚地解釋植物通過自身免疫防御反應對抗病原菌侵染機理,并為植物抗病新品種的改進提供新思路。

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(責任編輯：田 喆)

Recent progresses in the regulation mechanism of E3 ligases in plant disease resistance

Yang Jiuxia1,2, Zhang Hao1,2, Wang Zhilong1, Wang Xuli2, Wang Guoliang1,2

(1. College of Agronomy, Hunan Agriculture University, Changsha 410128, China; 2. State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing 100193, China)

Biotic stress is an important factor that affects crop production in China. It is also one of the most widely studied areas in plant sciences. Degradation mediated by the ubiquitin proteasome system (UPS) is one of the most sophisticated regulation systems in eukaryotes, which is involved in plant growth and development and in response to abiotic and biotic stresses. E3 ligase is considered as a key enzyme in the UPS due to its specific interactions with its substrates. Based on the differences in structure and function, E3 ligases can be divided into four main classes. In this paper, we review the recent progresses in the regulation mechanism of E3 ligases in plant disease resistance and propose new research directions.

UPS; ubiquitination; E3 ligase; PTI; ETI

專論與綜述Reviews

2015-02-09

2015-03-23

國家自然科學基金項目(31471737)

S 432.1

A

10.3969/j.issn.0529-1542.2015.04.001

* 通信作者 E-mail: lilywang0313@163.com；wang.620@osu.edu