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。

[1] Nolan T, Chen J, Yin Y. Cross-talk of brassinosteroid signaling in controlling growth and stress responses., 2017, 474(16): 2641–2661.

[2] Song XJ. Crop seed size: BR matters., 2017, 10(5): 668–669.

[3] Li XJ, Chen XJ, Guo X, Yin LL, Ahammed GJ, Xu CJ, Chen KS, Liu CC, Xia XJ, Shi K, Zhou J, Zhou YH, Yu JQ.overexpression induces alteration in phytohormone homeostasis, development, architecture and carotenoid accumulation in tomato., 2016, 14: 1021–1033.

[4] Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Li C, Ding Z. Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in., 2018, 14(1): e1007144.

[5] Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P. Overexpression of the brassinosteroid biosynthetic geneinsimultaneously increases seed yield and stress tolerance., 2016, 6: 28298.

[6] Yang J, Thames S, Best NB, Jiang H, Huang P, Dilkes BP, Eveland AL. Brassinosteroids modulate meristem fate and differentiation of unique inflorescence morphology in., 2018, 30(1): 48–66.

[7] Corvalán C, Choe S. Identification of brassinosteroid genes in., 2017, 17(1): 5.

[8] Kir G, Ye H, Nelissen H, Neelakandan AK, Kusnandar AS, Luo A, Inzé D, Sylvester AW, Yin Y, Becraft PW. RNA interference knockdown of BRASSINOSTEROID INSEN-SITIVE1 in maize reveals novel functions for brassin-osteroid signaling in controlling plant architecture., 2015, 169(1): 826–839.

[9] Belkhadir Y, Jaillais Y. The molecular circuitry of brassinosteroid signaling., 2015, 206(2): 522–540.

[10] Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. A new class of transcription factors mediates brassinosteroid- regulated gene expression in., 2005, 120(2): 249–259.

[11] Wang ZY, Bai MY, Oh E, Zhu JY. Brassinosteroid signaling network and regulation of photomorphogenesis., 2012, 46: 701–724.

[12] Yu H, Feng W, Sun F, Zhang YY, Qu JT, Liu B, Lu F, Yang L, Fu F, Li W. Cloning and characterization of BES1/ BZR1 transcription factor genes in maize., 2018, 86(2): 235–249.

[13] Oh E, Zhu JY, Wang ZY. Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses., 2012, 14(8): 802–809.

[14] Qiao S, Sun S, Wang L, Wu Z, Li C, Li X, Wang T, Leng L, Tian W, Lu T, Wang X. The RLA1/SMOS1 transcription factor functions with OsBZR1 to regulate brassinosteroid signaling and rice architecture., 2017, 29(2): 292–309.

[15] Ye H, Li L, Guo H, Yin Y. MYBL2 is a substrate of GSK3-like kinase BIN2 and acts as a corepressor of BES1 in brassinosteroid signaling pathway in., 2012, 109(49): 20142–20147.

[16] Bai XF, Huang Y, Hu Y, Liu HY, Zhang B, Smaczniak C, Hu G, Han ZM, Xing YZ. Duplication of an upstream silencer of FZP increases grain yield in rice., 2017, 3(11): 885–893.

[17] Jiang J, Zhang C, Wang X. A recently evolved isoform of the transcription factor BES1 promotes brassinosteroid signaling and development in., 2015, 27(2): 361–374.

[18] Martins S, Montiel-Jorda A, Cayrel A, Huguet S, Roux CP, Ljung K, Vert G. Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature., 2017, 8(1): 309.

[19] Salazar-Henao JE, Lehner R, Betegón-Putze I, Vilarrasa- Blasi J, Ca?o-Delgado AI. BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of theprimary root., 2016, 67(17): 4951–4961.

[20] Wang ZY, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, Chory J. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis., 2002, 2(4): 505–513.

[21] Yin Y, Wang ZY, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J. BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation., 2002, 109(2): 181–191.

[22] Kim TW, Guan S, Sun Y, Deng Z, Tang W, Shang J X, Sun Y, Burlingame A L, Wang ZY. Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors., 2009, 11(10): 1254–1260.

[23] Kim TW, Guan S, Burlingame AL, Wang ZY. The CDG1 kinase mediates brassinosteroid signal transduction from BRI1 receptor kinase to BSU1 phosphatase and GSK3-like kinase BIN2., 2011, 43(4): 561–571.

[24] He JX, Gendron JM, Sun Y, Gampala SSL, Gendron N, Sun CQ, Wang ZY. BZR1 is a transcriptional repressor with dual roles in brassinosteroid homeostasis and growth responses., 2005, 307(5715): 1634–1638.

[25] Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in., 2010, 19(5): 765–777.

[26] Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y. A brassinosteroid transcriptional network revealed by genome-wide identification of BES1 target genes in., 2011, 65(4): 634–646

[27] Bai MY, Zhang LY, Gampala SS, Zhu SW, Song WY, Chong K, Wang ZY. Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice., 2007, 104(34): 13839–13844.

[28] Manoli A, Trevisan S, Quaggiotti S, Varotto S. Identification and characterization of the BZR transcription factor family and its expression in response to abiotic stresses inL., 2018, 84(3): 423–436.

[29] Saha G, Park JI, Jung HJ, Ahmed NU, Kayum MA, Kang JG, Nou IS. Molecular characterization of BZR transcriptionfactor family and abiotic stress induced expression profiling in., 2015, 92: 92–104.

[30] Shu HM, Guo SQ, Gong YY, Jiang L, Zhu JW, Ni WC. Identification and expression analysis of the Brassinosteroid signal gene GhBES1 family in upland cotton., 2017, 32(4): 7–12.束紅梅, 郭書巧, 鞏元勇, 蔣璐, 朱靜雯, 倪萬潮. 陸地棉油菜素內(nèi)酯信號基因GhBES1家族的鑒定及表達分析. 華北農(nóng)學報, 2017, 32(4): 7–12.

[31] Guo XL, Lu P, Wang YY, Cai XY, Wang XX, Zhou ZL, Wang YH, Wang CY, Wang KB, Liu F. Genome-wide identification and expression analysis of the gene family encoding Brassinazole resistant transcription factors in cotton., 2017, 29(5): 415–427.郭新磊, 路普, 王園園, 蔡小彥, 王星星, 周忠麗, 王玉紅, 王春英, 王坤波, 劉方. 棉花BZR基因家族的全基因組鑒定及表達分析. 棉花學報, 2017, 29(5): 415–427.

[32] Fan C, Guo G, Yan H, Qiu Z, Liu Q, Zeng B. Characterization of Brassinazole resistant (BZR) gene family and stress induced expression in., 2018, 24(5): 821–831.

[33] Song X, Ma X, Li C, Hu J, Yang Q, Wang T, Wang L, Wang J, Guo D, Ge W, Wang Z, Li M, Wang Q, Ren T, Feng S, Wang L, Zhang W, Wang X. Comprehensive analyses of the BES1 gene family inand examination of their evolutionary pattern in representative species., 2018, 19: 346.

[34] Tao Y, Wang YG, Li HJ, Li WC, Fu FL. Upstream messengers of abscisic acid signaling pathway in plant., 2016, 30(9): 1722–1730.陶怡, 王盈閣, 李鴻杰, 李晚忱, 付鳳玲. 植物脫落酸信號轉導途徑的上游信使. 核農(nóng)學報, 2016, 30(9): 1722–1730.

[35] Raghavendra AS, Gonugunta VK, Christmann A, Grill E. ABA perception and signalling., 2010, 15(7): 395–401.

[36] Li HQ, Chen C, Chen RR, Song XW, Li JN, Zhu YM, Ding XD. Preliminary analysis of the role of.1 andin the ABA and alkaline stress response of the soybean using the CRISPR/Cas9-based gene double-knockout system., 2018, 40(6): 496–507.李慧卿, 陳超, 陳冉冉, 宋雪薇, 李佶娜, 朱延明, 丁曉東. 利用CRISPR/Cas9雙基因敲除系統(tǒng)初步解析大豆和對ABA及堿脅迫的響應.遺傳, 2018, 40(6): 496–507.

[37] Yang X, Bai Y, Shang J, Xin R, Tang W. The antagonistic regulation of abscisic acid-inhibited root growth by brassinosteroids is partially mediated via direct suppression of ABSCISIC ACID INSENSITIVE 5 expression by BRASSINAZOLE RESISTANT 1.,, 2016, 39(9): 1994–2003.

[38] Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH. ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination., 2002, 32(3): 317–328.

[39] Ryu H, Cho H, Bae W, Hwang I. Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3., 2014, 5: 4138.

[40] He JX, Gendron JM, Yang Y, Li J, Wang ZY. The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in., 2002, 99(15): 10185–10190.

[41] Zhang S, Cai Z, Wang X. The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling., 2009, 106(11): 4543–4548.

[42] Wang H, Tang J, Liu J, Hu J, Liu J, Chen Y, Cai Z, Wang X. Abscisic acid signaling inhibits Brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2.2017, 11(2): 315–325.

[43] Hu Y, Yu D. BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in., 2014, 26(11): 4394–4408.

[44] Jiang WB, Huang HY, Hu YW, Zhu SW, Wang ZY, Lin WH. Brassinosteroid regulates seed size and shape in., 2013, 162(4): 1965–1977.

[45] Lu X, Xiong Q, Cheng T, Li QT, Liu XL, Bi YD, Li W, Zhang WK, Ma B, Lai YC, Du WG, Man WQ, Chen SY, Zhang JS. A PP2C-1 allele underlying a quantitative trait locus enhances soybean 100-seed weight., 2017, 10(5): 670–684.

[46] Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S. BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in, 2017, 10(4): 545–559.

[47] Tang W, Yuan M, Wang R, Yang Y, Wang C, Oses-Prieto JA, Kim TW, Zhou HW, Deng Z, Gampala SS, Gendron JM, Jonassen EM, Lillo C, DeLong A, Burlingame AL, Sun Y, Wang ZY. PP2A activates brassinosteroid-responsive gene expression and plant growth by dephosphorylating BZR1., 2011, 13(2): 124–131.

[48] Gomez MD, Barro-Trastoy D, Escoms E, Saura-Sánchez M, Sánchez I, Briones-Moreno A, Vera-Sirera F, Carrera E, Ripoll JJ, Yanofsky MF, Lopez-Diaz I, Alonso JM, Perez-Amador MA. Gibberellins negatively modulate ovule number in plants., 2018, 145(13), doi: 10.1242/dev.163865.

[49] Vishal B, Kumar PP. Regulation of seed germination and abiotic stresses by gibberellins and abscisic acid., 2018, 9: 838.

[50] Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadí D, Blázquez MA. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in., 2012, 109(33): 13446–13451.

[51] Unterholzner SJ, Rozhon W, Papacek M, Ciomas J, Lange T, Kugler KG, Mayer KF, Sieberer T, Poppenberger B. Brassinosteroids are master regulators of gibberellin biosynthesis in., 2015, 27(8): 2261–2272.

[52] Allen HR, Ptashnyk M. Mathematical modelling and analysis of the brassinosteroid and gibberellin signalling pathways and their interactions., 2017, 432: 109–131.

[53] Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun TP, Wang ZY. Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in., 2012, 14(8): 810–817.

[54] Li QF, Wang C, Jiang L, Li S, Sun SS, He JX. An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in., 2012, 5(244): ra72.

[55] Li QF, He JX. Mechanisms of signaling crosstalk between brassinosteroids and gibberellins., 2013, 8(7): e24686.

[56] Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice., 2014, 26(11): 4376–4393.

[57] Liu L, Liu H, Li S, Zhang X, Zhang M, Zhu N, Dufresne CP, Chen S, Wang Q. Regulation of BZR1 in fruit ripening revealed by iTRAQ proteomics analysis., 2016, 6: 33635.

[58] Tang Y, Liu H, Guo S, Wang B, Li Z, Chong K, Xu Y. OsmiR396d affects gibberellin and brassinosteroid signaling to regulate plant architecture., 2018, 176(1): 946–959.

[59] Kami C, Lorrain S, Hornitschek P, Fankhauser C. Light-regulated plant growth and development., 2010, 91: 29–66.

[60] Luo XM, Lin WH, Zhu S, Zhu JY, Sun Y, Fan XY, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang ZY. Integration of light- and brassinosteroid- signaling pathways by a GATA transcription factor in., 2010, 19(6): 872–883.

[61] Li QF, He JX. BZR1 interacts with HY5 to mediate Brassinosteroid- and light-regulated cotyledon opening inin darkness., 2015, 9(1): 113–125.

[62] Chen M, Chory J. Phytochrome signaling mechanisms and the control of plant development., 2011, 21(11): 664–671.

[63] Leivar P, Quail PH. PIFs: pivotal components in a cellular signaling hub., 2011, 16(1): 19–28.

[64] Ibanez C, Delker C, Martinez C, Bürstenbinder K, Janitza P, Lippmann R, Ludwig W, Sun H, James GV, Klecker M, Grossjohann A, Schneeberger K, Prat S, Quint M. Brassinosteroids dominate hormonal regulation of plant thermosmorphogenesis via BZR1., 2018, 28(2): 303–310.

[65] Liang T, Mei S, Shi C, Yang Y, Peng Y, Ma L, Wang F, Li X, Huang X, Yin Y, Liu H. UVR8 interacts with BES1 and BIM1 to regulate transcription and photomorphogenesis in., 2018, 44(4): 512–523.e5.

[66] Wang W, Lu X, Li L, Lian HL, Mao ZL, Xu PB, Guo T, Xu F, Du SS, Cao XL, Wang S, Shen H, Yang HQ. Photoexcited CRYPTOCHROME1 interacts with dephosphorylated BES1 to regulate Brassinosteroid signaling and photomorphogenesis in., 2018, doi: 10.1105/tpc.17.00994.

[67] Li QF, Huang LC, Wei K, Yu JW, Zhang CQ, Liu QQ. Light involved regulation of BZR1 stability and phosphorylation status to coordinate plant growth in., 2017, 37(2), doi: 10.1042/ BSR20170069.

[68] Kim B, Jeong YJ, Corvalán C, Fujioka S, Cho S, Park T, Choe S. Darkness and gulliver2/phyB mutation decrease the abundance of phosphorylated BZR1 to activate brassinosteroid signaling in., 2014, 77(5): 737–747.

[69] Yang M, Li C, Cai Z, Hu Y, Nolan T, Yu F, Yin Y, Xie Q, Tang G, Wang X. SINAT E3 ligases control the light-mediated stability of the Brassinosteroid-activated transcription factor BES1 in., 2017, 41(1): 47–58.e4.

[70] Guo R, Qian H, Shen W, Liu L, Zhang M, Cai C, Zhao Y, Qiao J, Wang Q. BZR1 and BES1 participate in regulation of glucosinolate biosynthesis by brassinosteroids in., 2013, 64(8): 2401–2412.

[71] Miyaji T, Yamagami A, Kume N, Sakuta M, Osada H, Asami T, Arimoto Y, Nakano T. Brassinosteroid-related transcription factor BIL1/BZR1 increases plant resistance to insect feeding., 2014, 78(6): 960–968.

[72] Kang S, Yang F, Li L, Chen H, Chen S, Zhang J. Thetranscription factor BES1 is a direct substrate of MPK6 and regulates immunity., 2015, 167(3): 1076–1086.

[73] Singh AP, Fridman Y, Friedlander-Shani L, Tarkowska D, Strnad M, Savaldi-Goldstein S. Activity of the brassinosteroid transcription factors BRASSINAZOLE RESISTANT1 and BRASSINOSTEROID INSENSITIVE1-ETHYL METHA-NESULFONATE-SUPPRESSOR1/BRASSINAZOLE RE-SISTANT2 blocks developmental reprogramming in response to low phosphate availability., 2014, 166(2): 678–688.

[74] Chen J, Nolan TM, Ye H, Zhang M, Tong H, Xin P, Chu J, Chu C, Li Z, Yin Y.WRKY46, WRKY54, and WRKY70 Transcription factors are involved in brassinosteroid-regulated plant growth and drought responses., 2017, 29(6): 1425–1439.

[75] Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin HY, Li L, Wang Y, Tong H, Zhang M, Chu C, Li Z, Aluru M, Aluru S, Schnable PS, Yin Y. RD26 mediates crosstalk between drought and brassinosteroid signalling pathways., 2017, 8: 14573.

[76] Nolan TM, Brennan B, Yang M, Chen J, Zhang M, Li Z, Wang X, Bassham DC, Walley J, Yin Y. Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival., 2017, 41(1): 33–46.e7.

[77] Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY. Cell elongation is regulated through a central circuit of interacting transcription factors in thehypocotyl., 2014, 3, doi: 10.7554/eLife.03031.

[78] Liu K, Li Y, Chen X, Li L, Liu K, Zhao H, Wang Y, Han S. ERF72 interacts with ARF6 and BZR1 to regulate hypocotyl elongation in., 2018, 69(16): 3933–3947.

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)