轉錄因子BES1/BZR1調(diào)控植物生長發(fā)育及抗逆性

于好強，孫福艾，馮文奇，路風中，李晚忱，付鳳玲

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轉錄因子BES1/BZR1調(diào)控植物生長發(fā)育及抗逆性

于好強，孫福艾，馮文奇，路風中，李晚忱，付鳳玲

四川農(nóng)業(yè)大學玉米研究所，農(nóng)業(yè)部西南玉米生物學與遺傳育種重點實驗室，溫江 611130

油菜素內(nèi)酯(brassinosteroid, BR)是植物特有的甾體激素，在植物生長發(fā)育及逆境應答過程中起重要作用。轉錄因子BES1/BZR1(BRI1 EMS SUPPRESSOR 1/BRASSINAZOLE RESISTANT 1)是BR信號轉導的核心成員，被BR信號激活后，結合到下游靶基因啟動子區(qū)的E框(CANNTG)或BRRE元件(CGTGT/CG)，調(diào)節(jié)靶基因表達。除介導BR信號，BES1/BZR1還參與脫落酸、赤霉素及光等信號轉導途徑，協(xié)同調(diào)控植物的生長發(fā)育。最新研究發(fā)現(xiàn)，BES1/BZR1還參與調(diào)控植物的抗逆性。本文對轉錄因子BES1/BZR1通過信號轉導調(diào)控植物生長發(fā)育和抗逆性分子機制的新近研究進展進行了綜述，以期為相關研究提供參考。

油菜素內(nèi)酯；生長發(fā)育；信號轉導；抗逆性；BES1/BZR1轉錄因子

油菜素內(nèi)酯(brassinosteroid, BR)是植物特有的甾體激素，在生長發(fā)育及環(huán)境脅迫應答中起重要作用，其生理活性遠高于生長素(auxin, IAA)、赤霉素(gibberellins, GA)、細胞分裂素(cytokinin, CTK)、脫落酸(abscisic acid, ABA)和乙烯(ethylene, ET)[1,2]。BR合成基因過量表達或缺失對植物生長發(fā)育及產(chǎn)量、品質(zhì)等農(nóng)藝性狀育均產(chǎn)生嚴重影響[3~6]。BR信號轉導被阻斷的植物則顯現(xiàn)矮化、開花延遲、早衰等缺陷表型[7,8]。

BR被細胞膜上BRASSINOSTEROID INSEN-SITIVE 1 (BRI1)及BRI1-ASSOCIATED RECEPTOR KINASE1 (BAK1)等激酶接受后，通過信號轉導激活轉錄因子BRI1 EMS SUPPRESSOR 1 (BES1)及其同源蛋白BRASSINAZOLE RESISTANT 1 (BZR1)的活性[9,10]。BES1與BZR1氨基酸序列相似性達88%，N端結構域相似性高達97%[11]，編碼基因以家族形式存在，本課題組在前期研究中將其統(tǒng)一命名為BES1/BZR1[12]。被BR信號激活后，BES1/BZR1直接或與其他轉錄因子一起結合到生長發(fā)育相關基因啟動子的E框(CANNTG)或BRRE元件(CGTGT/ CG)，調(diào)節(jié)這些基因的表達[13~15]。例如，BES1/BZR1抑制葉腋分生組織發(fā)育基因表達，可促進小穗發(fā)育，增加水稻產(chǎn)量[16]。BES1/BZR1調(diào)節(jié)根尖分生組織發(fā)育相關基因表達，進而調(diào)控根發(fā)育[4,17~19]。除介導BR信號，BES1/BZR1還參與ABA、GA及光等信號轉導途徑，調(diào)控植物的生長發(fā)育以及抗凍、耐旱、抗病等抗逆性。

本文對轉錄因子BES1/BZR1通過信號轉導調(diào)控植物生長發(fā)育和抗逆性分子機制的新近研究進展進行了綜述，以期為相關研究提供參考。

1 BES1/BZR1介導BR信號轉導

2002年，Wang等[20]利用EMS誘變篩選到一個BR合成抑制突變體()，圖位克隆獲得基因，該基因編碼核蛋白且受BR誘導。同年，Yin等[21]利用EMS誘變篩選到BR受體抑制因子BES1，受BR誘導并在細胞核中積累。后經(jīng)證實BES1是一個BZR1類蛋白(BZR1- like protein)，二者具有高度的序列相似性，N端均有一個核定位信號(NLS)，C端均有22~24個絲氨酸或蘇氨酸殘基(S/TXXXS/T)，該殘基是BIN2、GSK-3等激酶磷酸化位點，磷酸化后進入細胞質(zhì)被14-3-4蛋白降解[16,20,21]。直至2005年，Yin等[10]進一步證實BES1/BZR1是植物中特有的新一類轉錄因子，也是BR信號轉導途徑的唯一轉錄因子。細胞膜上的BRI1、BKI1和BAK1等激酶接受BR信號后，自身磷酸化并催化BRASSINOSTEROID-SIGNALLING KINASE1 (BSK)和CONSTITUTIVE DIFFERENTIAL GROWTH1 (CDG1)磷酸化，BSK與CDG1進一步磷酸化BRI1-SUPPRESSOR1 (BSU1)，BSU1催化BRASSINOSTEROID INSENSITIVE2 (BIN2)去磷酸化，導致其自身被蛋白酶體降解，削弱BIN2對BES1/BZR1的磷酸化從而使其活性增加[9,10,21~23]，BES1/BZR1通過調(diào)節(jié)下游靶基因的表達，調(diào)控植物的生長發(fā)育(圖1A)。

BES1/BZR1成員N端均有一個bHLH結構域，可特異性結合到靶基因啟動子區(qū)的E框或BRRE元件[10,24~26]。此外，多數(shù)BES1/BZR1成員均含有能被BIN2等激酶磷酸化的絲氨酸(serine, S)富集位點，個別成員包含一個與蛋白穩(wěn)定性緊密相關的脯氨酸(proline, P)、谷氨酸(glutamic acid, E)、絲氨酸(serine, S)和蘇氨酸(threonine, T)富集區(qū)(PEST基序)[10]。目前，擬南芥()和水稻()BES1/BZR1基因家族已被全部鑒定：擬南芥AtBES1/BZR1基因家族有6個成員，且功能存在部分冗余[10,20,21]；水稻OsBES1/BZR1基因家族有4個成員[27]。玉米()ZmBES1/BZR1基因家族有11個成員[23,28]。此外，從白菜(ssp)、棉花()、油菜()和桉樹()中均鑒定出多個BES1/ BZR1基因家族成員[29~33](表1)。進一步研究證實，BES1/BZR1基因家族成員通過不同信號途徑調(diào)控植物生理代謝過程，進而調(diào)控植物生長發(fā)育及逆境響應。

：未知過程；：相互作用；：促進作用；：抑制作用

A：BES1/BZR1介導的BR信號轉導；B：BES1/BZR1參與的ABA信號途徑；C：BES1/BZR1參與的GA信號途徑；D：BES1/BZR1參與的光信號途徑；E：BES1/BZR1調(diào)控逆境應答途徑；F：BES1/BZR1參與的生長素、乙烯及其他信號途徑。BR：油菜素內(nèi)酯；BES1/BZR1：轉錄因子；BKI1、BRI1、BAK1、BSK1及CDG1：蛋白激酶；BSU1：BRI1抑制因子；ABA：脫落酸；GA：赤霉素；PP2C：2C型絲氨酸蘇//氨酸蛋白激酶；PP2A：2A型絲氨酸/蘇氨酸蛋白激酶；PYL：ABA受體；BIN2：磷酸激酶；ABI3與ABI5：ABA響應的bZIP轉錄因子；DELLA：赤霉素負調(diào)控轉錄因子；SINAT與COP1：E3泛素連接酶；GATA2與HY5：光形態(tài)建成相關轉錄因子；UVR8：紫外光受體；PIF4：光敏色素互作因子；CRY：隱花色素。RD26與WRKY26：干旱相關轉錄因子；REF：乙烯應答因子；MEK6：促細胞分裂原活化蛋白激酶；P：磷。

2 BES1/BZR1參與ABA信號途徑

ABA是植物體內(nèi)重要激素之一，通過其直接受體PYL (pyrabactin resistance 1-like protein)、第二信使2C型蛋白磷酸酶(PP2C)及第三信使蔗糖非酵解型蛋白激酶(SnRK)向下游進行信號傳遞，在植物生長發(fā)育及抗逆過程中扮演重要角色，如衰老、抗旱、耐鹽等[34~36]。研究發(fā)現(xiàn)，在突變體中，BZR1結合到ABA誘導型轉錄因子ABA INSENSITIVE 5 (ABI5)編碼基因的啟動子，抑制其表達，因而抑制突變體對ABA誘導的應答[37]。同時，BES1抑制ABA調(diào)節(jié)的轉錄因子ABI3編碼基因的表達，進而抑制ABI3對下游ABI5轉錄因子的激活，致使ABA信號轉導受阻，表現(xiàn)為苗期發(fā)育遲緩[38,39]。

表1 已鑒定的不同植物BES1/BZR1基因家族成員

此外，外源ABA不僅誘導基因表達，而且誘導BES1蛋白磷酸化，使其穩(wěn)定性降低，從而抑制BR信號轉導，此過程依賴于ABA第二信使PP2C成員ABI1和ABI2[12,29,40,41]。最新研究表明，ABI1、ABI2與BIN2激酶互作后催化BIN2去磷酸化，從而調(diào)控BES1活性。ABA還可促進BIN2磷酸化并抑制ABI2的活性[42]。在ABA存在時，BIN2磷酸化ABI5使其穩(wěn)定性增強，調(diào)控種子發(fā)育過程[43]。在大豆()中，PP2C-1與GmBZR1直接互作，催化GmBZR1去磷酸化以增強GmBZR1活性，促進種子大小相關基因()、()和()等表達，調(diào)控種子的大小與重量[44,45]。BZR1也可結合到ABA受體PYL6編碼基因的啟動子區(qū)，上調(diào)表達，從而參與PYL6介導的ABA信號轉導[46]。研究還發(fā)現(xiàn)，BZR1的PEST結構域與蛋白磷酸酶2A(PP2A)的B亞基直接互作，使BZR1被PP2A去磷酸化，激活BZR1介導的BR信號途徑，調(diào)控植物的生長發(fā)育[47](圖1B)。

3 BES1/BZR1參與GA信號途徑

作為植物體內(nèi)重要激素之一，GA在種子萌發(fā)、細胞分裂、胚珠形成等生長發(fā)育過程中起關鍵作用[48,49]。研究發(fā)現(xiàn)，在BR缺失的突變體中，GA合成關鍵基因表達顯著下調(diào)，而在突變體中，基因表達顯著上調(diào)。同時，在和突變體中，基因均受BR誘導，表達顯著上調(diào)。有研究表明，基因啟動子區(qū)不含BES1/BZR1轉錄因子的結合位點。研究人員通過電泳遷移實驗(electroph-oretic mobility shift assays, EMSA)和染色質(zhì)免疫共沉淀(chromatin immunoprecipitation, Chip)實驗證實，BES1/BZR1可結合基因啟動子區(qū)一個非E-Box且長度為12 bp的基序(Motif)[50,51]。此外，GA信號負調(diào)控因子DELLA家族蛋白(RGA、GAI、RGL1、RGL2和RGL3)可以和BES1/BZR1結合，阻止BES1/BZR1與靶基因的結合[50,52~55]。這些研究結果證實，DELLA蛋白降解可促使BES1/BZR1活性增強，BES1/BZR1結合GA合成相關基因啟動子，使其表達上調(diào)，促進GA積累。此外，GA可通過PP2A促進BES1/BZR1的去磷酸化[54]。

在水稻中，BR誘導GA合成基因表達，促使GA積累。外源GA又抑制BR合成及其信號轉導。進一步研究表明，GA合成關鍵基因、、和的啟動子均包含CATGTG、BRRE或G-box元件。BES1/BZR1與這類元件直接結合，調(diào)節(jié)下游基因的表達，進而影響GA合成[56]。在番茄()中過表達，GA合成關鍵酶之一的酮戊二酸脫氫酶2 (2-ODD2)蛋白水平在果實成熟期顯著增加，致使GA顯著積累促進果實成熟[57]。水稻OsBZR1能夠促進miR396d的積累，調(diào)控其靶基因()的表達，通過參與的GA合成及信號轉導途徑，調(diào)控水稻株高及葉夾角等形態(tài)建成[58](圖1C)。

4 BES1/BZR1參與光信號途經(jīng)

光是植物光合作用的能量之源，在調(diào)控植物生長發(fā)育中起關鍵作用，如光信號參與調(diào)控種子萌發(fā)、光形態(tài)建成和開花等[59]。轉錄因子GATA2、HY5正向調(diào)控植物光形態(tài)建成并受光誘導積累，黑暗促使其降解。研究發(fā)現(xiàn)，被BR激活的BZR1直接與GATA2互作，抑制轉錄，調(diào)控擬南芥幼苗下胚軸伸長[60,61]。黑暗條件下，HY5能特異地結合BZR1，抑制BZR1與子葉開閉相關基因的結合能力，調(diào)控光形態(tài)建成[61]。光敏色素互作因子(phytochrome interacting factor，PIF)是一類bHLH轉錄因子，在黑暗條件下，PIF大量積累，促進植物暗形態(tài)建成，但在光照條件下，PIF發(fā)生磷酸化后降解，促進植物光形態(tài)建成[62,63]。研究發(fā)現(xiàn)，BES1/BZR1與PIF 4相互作用，形成異源二聚體后作用于共同靶基因，其中80%靶基因受光誘導參與光形態(tài)建成[11]。此外，BZR1與PIF4共同作用的靶基因還受GA誘導，GA促進細胞伸長的過程依賴于BZR1和PIF4。DELLA- BZR1-PIF4復合體調(diào)控下游靶基因paclobutrazol resistance家族(PREs)表達，促進細胞伸長，調(diào)控光形態(tài)建成[11,53]。在高溫條件下，BZR1和PIF4相互作用，調(diào)控植物熱形態(tài)建成[64]。

最近研究發(fā)現(xiàn)，去磷酸化的BES1可與紫外光受體UVR8 (UV RESISTANCE LOCUS 8)互作，二者的復合體受紫外光(UV-B)誘導，并在細胞核大量積累。同時，UV-B不僅抑制BES1靶基因表達，其受體UVR8又抑制BES1與DNA的結合作用，最終控制植物光形態(tài)建成過程[65]。在藍光條件下，其受體隱花色素(cryptochrome, CRY) CRY1和CRY2特異性與去磷酸化的BES1互作，抑制BES1與DNA結合活性及其靶基因表達，最終抑制下胚軸伸長[66]。

綜上所述，BES1/BZR1參與光信號途徑調(diào)控植物的形態(tài)建成過程。此外，還有研究發(fā)現(xiàn)，植物體內(nèi)BES1/BZR1的磷酸化狀態(tài)及穩(wěn)定性也受光信號調(diào)控。黑暗條件促進BES1/BZR1去磷酸化以增強活性，而光照條件下，大多數(shù)BZR1被BIN2磷酸化以保持失活狀態(tài)[61,67,68]。Kim等[68]研究發(fā)現(xiàn)，黑暗條件下，E3泛素連接酶COP1催化磷酸化后的BZR1降解，去磷酸化的BZR1積累。同時，光照條件可誘導E3泛素連接酶SINAT積累，SINAT泛素化BES1促使其降解。相反，黑暗條件抑制SINAT的積累，從而阻止BES1降解[69](圖1D)。

5 BES1/BZR1調(diào)控植物抗逆性

BES1/BZR1除調(diào)控植物生長發(fā)育外，在響應生物和非生物逆境脅迫過程中也起重要作用。Guo等[70]研究發(fā)現(xiàn)，BES1/BZR1調(diào)控硫代糖苷合酶基因的表達，促進硫代糖苷合成，而硫代糖苷在植物與食草動物或與微生物互作中起重要作用。隨后，Miyaji等[71]發(fā)現(xiàn)BZR1可能參與茉莉酸信號途徑，增強植物抗蟲能力。此外，研究表明，病原物相關分子模式(pathogen-associated molecular pattern, PAMP)感知可促進BES1磷酸化，在PAMP誘導的免疫反應(PAMP-triggered immunity, PTI)過程中，BES1作為病原菌誘導的MITOGEN-ACTIVATED PROTEIN KINASE 6 (MPK6)的直接底物被其磷酸化，參與調(diào)控植物對病菌的免疫反應[72]。

Singh等[73]研究發(fā)現(xiàn)，低磷脅迫促進BES1/ BZR1由細胞核向細胞質(zhì)轉移，低磷條件下，BES1/ BZR1顯著積累，維持根系正常生長，賦予擬南芥對低磷脅迫的耐受性。研究表明，BES1/BZR1可促進轉錄因子CBF (C-repeat binding factor)、WRKY6以及ABA受體PYL6等編碼基因的表達，并與WRKY54轉錄因子直接互作，正調(diào)控擬南芥耐寒性，但負調(diào)控其耐旱性[46,74]。研究還發(fā)現(xiàn)，BES1/BZR1與NAC轉錄因子家族的RD26存在拮抗關系，BES1/ BZR1結合到基因啟動子，抑制表達，而RD26蛋白又與BES1/BZR1蛋白結合，抑制RD26干旱應答調(diào)節(jié)功能[75]。同時，在干旱和低碳脅迫下，BES1與泛素受體DSK2互作而被降解，參與脅迫誘導的自噬反應過程，調(diào)控植物適應逆境[76]。

此外，在擬南芥、油菜和桉樹中，BES1/BZR1基因的表達受鹽、干旱、熱和冷等脅迫的誘導或抑制[29,32,33]，表明該基因家族參與這些逆境脅迫響應過程(圖1E)。

6 BES1/BZR1參與的信號轉導網(wǎng)絡

BES1/BZR1是BR信號轉導途徑特異的轉錄因子，通過介導BR信號調(diào)控植物生長發(fā)育。但近年來研究發(fā)現(xiàn)，BES1/BZR1在ABA、GA、光及逆境信號中也發(fā)揮著重要作用，并且還參與IAA、ET等信號途徑。如BZR1直接與生長素誘導基因、的啟動子結合而抑制其表達，從而影響生長素的合成，調(diào)控植物生長發(fā)育[77]。BES1/BZR1通過下調(diào)乙烯合成關鍵酶基因、和表達，抑制乙烯合成，而且與乙烯響應因子ERF72互作調(diào)控其下游基因表達，最終影響植物生長發(fā)育過程[4,78](圖1F)。綜上所述，BES1/BZR1參與多種信號途徑，調(diào)控植物生長發(fā)育及逆境應答，其功能和作用機制表現(xiàn)出多樣性。但是，BES1/BZR1調(diào)控植物響應逆境脅迫方面的研究還不夠深入，除擬南芥外，在作物及其他植物中BES1/BZR1抗逆功能研究尚未見報道。因此，本文將BES1/BZR1參與的信號轉導網(wǎng)絡進行了歸納總結(圖1)，以期為后續(xù)相關研究提供參考。

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The BES1/BZR1 transcription factors regulate growth, development and stress resistance in plants

Haoqiang Yu, Fuai Sun, Wenqi Feng, Fengzhong Lu, Wanchen Li, Fengling Fu

Brassinosteroid (BR) is a class of plant-specific steroidal hormone and plays vital roles in plant growth, developmental and stress response. As the core component of BR signaling, the BES1/BZR1 transcription factors are activated by the BR signal, bind to the E-box (CANNTG) or BRRE element (CGTGT/CG) enriched in the promoter of downstream target genes and regulate their expression. Besides BR signal transduction, BES1/BZR1s are also involved in other signaling pathways such as abscisic acid, gibberellin and light to co-regulate plant growth and development. Recently, BES1/BZR1s were found to be related to stress resistance. In this review, we summarize recent advances of molecular mechanism of the BES1/BZR1 transcription factors regulating plant growth, development and stress resistance through signal transduction to provide a reference for related researches.

brassinosteroid; growth and development; signal transduction; stress resistance; BES1/BZR1 transcription factors

2018-09-07;

2019-02-20

四川省科技計劃應用基礎項目(編號：2018JY0470)資助[Supported by the Sichuan Science and Technology Program (No.2018JY0470)]

于好強，博士，講師，研究方向：植物分子生物學。E-mail: yhq1801@sicau.edu.cn

付鳳玲，博士，教授，研究方向：玉米遺傳育種與生物技術。E-mail: ffl@sicau.edu.cn

10.16288/j.yczz.18-253

2019/2/25 15:23:43

URI: http://kns.cnki.net/kcms/detail/11.1913.R.20190225.1523.004.html

(責任編委: 張憲省)