谷曉勇，劉揚，劉利靜

綜 述

植物激素水楊酸生物合成和信號轉(zhuǎn)導(dǎo)研究進展

谷曉勇，劉揚，劉利靜

山東大學(xué)生命科學(xué)學(xué)院，青島 266237

植物激素水楊酸(salicylic acid，SA)是廣泛存在于植物體中的小分子酚類物質(zhì)，參與植物多種生理過程，特別是在植物免疫中發(fā)揮重要功能。植物免疫過程中體內(nèi)SA大量合成，SA信號通路被激活從而誘導(dǎo)抗病相關(guān)基因表達。近年來，隨著研究的不斷深入，SA生物合成和信號轉(zhuǎn)導(dǎo)都取得一系列重要進展：進一步完善了SA生物合成的異分支酸合酶(isochorismate synthase, ICS)和苯丙氨酸解氨酶(phenylalanine ammonia-lyase, PAL)途徑；明確了NPR1 (nonexpresser ofgenes 1)和其同源蛋白NPR3、NPR4是植物接收SA的受體；發(fā)現(xiàn)II類TGA (TGACG-binding factor)轉(zhuǎn)錄因子通過與不同SA受體互作激活或抑制下游基因表達等。本文系統(tǒng)介紹了SA生物合成和信號轉(zhuǎn)導(dǎo)領(lǐng)域的相關(guān)進展，以期為深入研究SA調(diào)控植物生長發(fā)育和環(huán)境脅迫響應(yīng)提供理論參考。

水楊酸；水楊酸生物合成；水楊酸受體；水楊酸信號轉(zhuǎn)導(dǎo)

水楊酸(salicylic acid, SA)是一種廣泛存在于細菌和植物體中的小分子酚類物質(zhì)。早在公元前4世紀，古蘇美爾人和古埃及人就已經(jīng)開始使用柳樹(L.)和楊樹(L.)的樹皮和樹葉來緩解眼疾、風(fēng)濕、分娩和發(fā)燒引起的疼痛[1]。直到1828年，德國科學(xué)家Johann Buchner提取出柳樹皮中有效成分，并以白柳的拉丁文學(xué)名將其命名為水楊苷(SA glycoside, SAG)。1838年，Raffaele Piria進一步分解水楊苷得到SA。1898年拜耳公司將乙酰水楊酸以阿司匹林商標上市，并迅速成為世界最暢銷藥物之一[2]。直到20世紀90年代初，人們才逐漸認識到SA在植物中的重要作用，并將其定義為植物激素[3]。

植物激素SA參與植物生長發(fā)育的多個過程，并在植物對環(huán)境脅迫響應(yīng)中發(fā)揮重要功能。SA調(diào)控植物種子萌發(fā)、出芽、開花、坐果和果實成熟等過程[4,5]。最新研究表明，SA通過抑制乙烯信號途徑影響植物出芽過程中頂端彎鉤的形成[6]。SA介導(dǎo)植物對非生物脅迫的抗性，如SA能改變植物對重金屬、熱、冷、干旱、高鹽等脅迫環(huán)境的適應(yīng)性[4]。SA是重要的免疫激素，目前對SA的研究主要集中在植物免疫領(lǐng)域[7,8]。植物先天免疫系統(tǒng)包括病原相關(guān)分子模式觸發(fā)的免疫反應(yīng)(pathogen associated molecular pattern-triggered immu-nity, PTI)和效應(yīng)子觸發(fā)的免疫反應(yīng)(effector-triggered immunity, ETI)，SA在這兩種免疫反應(yīng)中都發(fā)揮重要作用，如在SA合成突變體中，PTI和ETI對病原菌的生長抑制效果都被嚴重削弱[9,10]。SA對植物系統(tǒng)獲得性抗性(systemic acquired resistance, SAR)至關(guān)重要，SA積累或信號轉(zhuǎn)導(dǎo)缺失突變體不能正常產(chǎn)生SAR[11,12]。

SA對植物生長發(fā)育和環(huán)境脅迫響應(yīng)的調(diào)控是通過改變植物體內(nèi)SA濃度和SA下游基因表達強度來實現(xiàn)。在病原菌侵染時，植物體內(nèi)SA生物合成和信號轉(zhuǎn)導(dǎo)被增強，SA誘導(dǎo)抗病相關(guān)基因的表達從而提高植物抗病能力。因此，對SA生物合成和信號轉(zhuǎn)導(dǎo)過程的認知是探究植物自身發(fā)育和其與環(huán)境互作的重要前提[13]。異分支酸合酶(isochorismate synthase, ICS)途徑和苯丙氨酸解氨酶(phenylalanine ammonia-lyase, PAL)途徑是植物合成SA的主要方式，但參與這兩條途徑的部分酶類還未被解析[8]。NPR1 (nonexpresser of PR genes 1)是SA信號轉(zhuǎn)導(dǎo)的關(guān)鍵調(diào)控因子，但NPR1是否參與SA信號接收還存在爭論[13]。近幾年，科研人員在SA研究領(lǐng)域發(fā)表了多篇重量級論文，進一步完善了SA生物合成途徑，也使爭論多年的SA受體問題塵埃落定。鑒于此，本文系統(tǒng)介紹了SA生物合成和信號轉(zhuǎn)導(dǎo)研究的相關(guān)進展，以期為SA領(lǐng)域的相關(guān)研究提供借鑒和參考。

1 水楊酸的生物合成

植物通過兩條通路合成水楊酸：ICS途徑和PAL途徑。它們都起始于葉綠體，以分支酸(chorismate)為前體，并涉及多個酶促反應(yīng)(圖1)[8]。兩條途徑對SA合成的貢獻存在差異，在擬南芥()中，與免疫相關(guān)SA主要由ICS途徑產(chǎn)生[14]。

1.1 ICS途徑

ICS途徑起始于分支酸，經(jīng)異分支酸(isochori-smate)、異分支酸-9-谷氨酸(isochorismate-9-glutamate, IC-9-Glu)最終合成水楊酸[8]。在擬南芥中該途徑有3種酶參與，分別是ICS、PBS3 (avrPphB susceptible 3)和EPS1 (enhanced pseudomonas susceptibility 1)[8]。

1.1.1 ICS

ICS1是第一個被報道參與ICS途徑的酶類，它以分支酸為底物合成異分支酸。通過正向遺傳學(xué)的方法篩選病原菌處理后植物體內(nèi)SA積累減少的突變體，發(fā)現(xiàn)了(SA induction deficient 2)，其突變的基因位點就是[15]。擬南芥基因組編碼2個ICS——ICS1和ICS2，都定位于葉綠體。病原菌侵染或紫外線處理植物能誘導(dǎo)SA生物合成，而在突變體中SA積累大幅度降低，雙突變體完全喪失誘導(dǎo)合成SA的能力[16]。這些結(jié)果說明異分支酸的合成發(fā)生在葉綠體中，由ICS1和ICS2共同介導(dǎo)。

圖1 水楊酸合成示意圖

植物通過兩條途徑合成SA。一是ICS途徑：ICS催化分支酸產(chǎn)生異分支酸，異分支酸經(jīng)EDS5轉(zhuǎn)運至細胞質(zhì)后PBS3催化其與谷氨酸結(jié)合生成IC-9-Glu，IC-9-Glu自主分解或經(jīng)EPS1催化加速分解最終產(chǎn)生水楊酸；二是PAL途徑：分支酸經(jīng)催化產(chǎn)生苯丙氨酸，苯丙氨酸進入細胞質(zhì)后由PALs催化產(chǎn)生反式肉桂酸，反式肉桂酸進入過氧化物酶體后經(jīng)β-氧化產(chǎn)生苯甲酸，苯甲酸轉(zhuǎn)運至細胞質(zhì)后可能由BA2H羥化產(chǎn)生水楊酸。綠色箭頭所示為發(fā)生在葉綠體中的反應(yīng)；棕色箭頭所示為發(fā)生在過氧化物酶體中的反應(yīng)；藍色箭頭所示為細胞質(zhì)中的反應(yīng)過程。ICS：isochorismate synthase；EDS5：enhanced disease susceptibility 5；PBS3：avrPphB susceptible 3；EPS1：enhanced pseudomonas susceptibility 1；PAL：phenylalanine ammonia-lyase；AIM：abnormal inflorescence meristem 1；BA2H：benzoic acid 2-hydroxylase。

1.1.2 PBS3

植物中異分支酸如何進一步催化生成SA一直是科學(xué)界的未解之謎。雖然該過程在銅綠假單胞菌()中已被解析：異分支酸由異分支酸丙酮酸裂解酶(isochorismate pyruvate lyase, IPL)直接裂解為SA，但植物中沒有IPL的同源蛋白[17]。為了尋找這一謎題的答案，科研人員進一步探究低SA含量的擬南芥突變體，如和等[18,19]SA生物合成減少的機理。Rekhter等[20]在()雙突變體背景下突變。該雙突變體本身SA含量偏高，植物生長受阻。雖然突變并未恢復(fù)的生長表型，但是對突變體中SA及其前體和代謝物含量進行測定顯示，SA和SAG的含量在中顯著低于，而異分支酸的含量在二者之間沒有顯著區(qū)別[20]。這一結(jié)果說明PBS3作用于異分支酸下游介導(dǎo)SA的生物合成。而Torrens-Spence等[21]發(fā)現(xiàn)突變可以互補另一高SA含量雙突變體()()的植株矮小表型。編碼氨基轉(zhuǎn)移酶(aminotransferase)，體外生物化學(xué)實驗表明PBS3可以促進底物谷氨酸化[22]。Rekhter等[20]和Torrens-Spence等[21]都證明在ICS途徑中PBS3負責將谷氨酸加在異分支酸上合成IC-9-Glu，IC-9-Glu可以自我衰變?yōu)镾A。PBS3定位在細胞質(zhì)中，因此異分支酸合成后需從葉綠體轉(zhuǎn)運到細胞質(zhì)中才能參與后續(xù)SA生物合成過程[20]。Rekhter等[20]和Torrens-Spence等[21]的研究進一步完善了植物SA生物合成的ICS途徑。

PBS3的發(fā)現(xiàn)表明植物已經(jīng)進化出一種獨特的、不同于細菌的ICS途徑。PBS3存在于多種開花植物中，暗示該蛋白廣泛參與植物SA生物合成過程[23]。

1.1.3 EDS5

EDS5 (enhanced disease susceptibility 5)屬于多種藥物和毒素排出(multidrug and toxin extrusion, MATE)轉(zhuǎn)運蛋白家族，定位于葉綠體膜。突變體中SA含量降低，推測其介導(dǎo)SA或SA前體的轉(zhuǎn)運[24]。Serrano等[25]將原生質(zhì)體孵育在14C標記的SA溶液中，然后分離葉綠體，檢測葉綠體中SA含量，結(jié)果顯示EDS5可以介導(dǎo)SA在細胞質(zhì)和葉綠體之間的轉(zhuǎn)運。而在突變體中，人為改變PBS3細胞質(zhì)定位特性使之定位到葉綠體，植物能夠正常合成SA[20]。因此推測EDS5在PBS3上游發(fā)揮作用，負責異分支酸從葉綠體到細胞質(zhì)的運輸。

1.1.4 EPS1

EPS1是BAHD (BEAT、AHCT、HCBT和DAT)乙酰轉(zhuǎn)移酶家族蛋白，突變體在丁香假單胞菌()侵染后植物體內(nèi)SA積累少于野生型，對病原菌的抗性降低[19]。突變可以互補雙突變體植株矮小表型，暗示其參與SA生物合成過程[21]。EPS1具有異羥甲基-谷氨酸A丙酮酰谷氨酸裂解酶(isochorismoyl-glutamate A py-ruvoylglutamate lyase)活性，催化IC-9-Glu裂解產(chǎn)生SA。在體外反應(yīng)中加入EPS1可以加快IC-9-Glu裂解產(chǎn)生SA的速度[21]。EPS1僅存在于十字花科植物中，表明其他科植物SA的合成可能依賴于IC-9-Glu自發(fā)衰變，或進化出了其他酶類來輔助該過程[21]。

1.2 PAL途徑

通過同位素標記實驗發(fā)現(xiàn)在煙草(L.)中苯丙氨酸(phenylalanine, Phe)可以經(jīng)反式肉桂酸(trans-cinnamic acid, t-CA)、苯甲酸(benzoic acid)進而合成SA[26]。已知PAL和AIM (abnormal inflorescence meristem 1)分別是催化合成反式肉桂酸和苯甲酸的關(guān)鍵酶類，而苯甲酸可能被BA2H (benzoic acid 2-hydroxylase)羥基化產(chǎn)生SA，但在植物體內(nèi)編碼BA2H的基因尚未被解析[27]。

1.2.1 PAL

大麥()的PAL最早被分離，并被證實具有苯丙氨酸脫氨酶活性[28]。擬南芥基因組中含有4個基因(~)。相比于野生型，四突變體中基礎(chǔ)PAL活性降低90%，正常生長狀況下SA積累減少75%，病原菌侵染后突變體SA積累減少50%，說明PAL途徑影響植物正常生長和病原菌侵染時SA的生物合成[29]。這也解釋了為什么在雙突變體中仍可以檢測到SA[14]。

水稻(L)PAL蛋白家族包括9個成員(OsPAL1~OsPAL9)，大多數(shù)在水稻中的表達受病原菌和昆蟲誘導(dǎo)。高表達增強水稻對病原菌和昆蟲的抗性，說明PAL途徑介導(dǎo)的SA生物合成對水稻免疫至關(guān)重要[30~33]。在此之前，對PAL的研究主要集中在植物抗菌領(lǐng)域，He等[33]研究發(fā)現(xiàn)PAL的抗蟲功能，增強了對PAL和SA功能的認知，具有重要的科學(xué)意義。

1.2.2 AIM1

反式肉桂酸可以通過β氧化途徑在過氧化物酶體中合成苯甲酸。已知有3類酶參與該過程，分別是肉桂酸:輔酶A連接酶(cinnamate: CoA ligase)、羥酰輔酶A水解酶(hydroxyacyl-CoA hydrolyase)和3-酮?；o酶A硫醇酶(3-ketoacyl CoA thiolase, KAT1)[34~36]。編碼羥酰輔酶A水解酶，是擬南芥種子中合成苯甲酸代謝物的重要酶類[37]。在水稻突變體中，肉桂酸含量升高，苯甲酸和SA含量大幅度降低，說明AIM1參與反式肉桂酸到苯甲酸的β氧化過程[38]。

綜上所述，植物SA生物合成的ICS途徑已基本被解析，PAL途徑也進一步被完善，但PAL途徑的部分反應(yīng)過程，如苯甲酸如何羥基化形成SA等還有待進一步探究。雖然SA生物合成過程的大部分酶類是在擬南芥和水稻中發(fā)現(xiàn)的，但在煙草、番茄(Mill.)、楊樹、紅花(L.)和黃瓜(L.)中同樣發(fā)現(xiàn)SA經(jīng)由ICS或PAL途徑合成，表明這兩種SA生物合成途徑在進化上具有保守性[39~42]。擬南芥中病原菌侵染時SA生物合成主要依賴于ICS途徑，但在煙草感染病毒后，體內(nèi)苯甲酸和SA大量合成，暗示煙草中病原體誘導(dǎo)的SA主要通過PAL途徑產(chǎn)生[43]。因此這兩種途徑在不同植物中對SA生物合成的貢獻具有物種特異性。

1.3 水楊酸的合成調(diào)控

在病原菌侵染時SA生物合成途徑中的基因，如被誘導(dǎo)表達，促進SA積累進而增強植物抗病性[15]。迄今為止，已有多個正調(diào)控表達的轉(zhuǎn)錄因子被報道，包括TCP (teosinte branched1/cyc-loidea/pcf)、WRKY (WRKY DNA binding protein)和CBP60 (CaM-binding protein 60)類蛋白等[44~46]。其中，對CBP60類蛋白SARD1(SAR-deficient 1)和CBP60g的研究較為深入[47]。病原菌通過TGA1 (TGACG-binding factor 1)和TGA4誘導(dǎo)和表達[48]。ChIP-Seq (chromatin immunopre-cipitation-sequencing)分析顯示SARD1和CBP60g能夠結(jié)合、和等SA合成相關(guān)基因的啟動子序列[49]。Wang等[50]研究顯示，病原菌誘導(dǎo)的高表達和SA積累在雙突變體中被阻斷，而相對于野生型，過表達植株中積累更多SA。這些結(jié)果表明SARD1和CBP60g是誘導(dǎo)SA合成的關(guān)鍵因子。

丁香假單胞菌通過冠菌素(coronatine)抑制植物體內(nèi)SA的合成[51]。冠菌素是一種茉莉酸類似物，被茉莉酸受體COI1 (coronatine insensitive 1)接收，并通過茉莉酸信號通路發(fā)揮功能[51]。Zheng等[51]研究發(fā)現(xiàn)冠菌素通過MYC2激活A(yù)NAC (abscisic acid-responsive NAC)類轉(zhuǎn)錄因子ANAC019、ANAC055和ANAC072進而抑制的表達，減少SA的合成從而降低植物的抗病能力。其他轉(zhuǎn)錄因子如WRKY54、WRKY70、EIN3 (ethylene insen-sitive 3)和CBP60a等也是ICS1表達的抑制子[52~54]。

2 水楊酸信號接收

2.1 NPR1

植物識別病原菌后內(nèi)源SA被誘導(dǎo)合成從而增強抗病相關(guān)基因表達。為了解析SA信號轉(zhuǎn)導(dǎo)過程，科研人員通過多個正向遺傳學(xué)篩選尋找SA不敏感突變體，發(fā)現(xiàn)()和()這3個突變體突變同一個基因[11,55~57]。突變使植物喪失SA誘導(dǎo)下游基因高表達和抗病性[55]。Wang等[52]研究表明，SA調(diào)控2280個基因的表達，其中2248個基因表達改變依賴于NPR1。這些數(shù)據(jù)表明NPR1是SA信號通路的關(guān)鍵調(diào)控因子。SA通過多種蛋白修飾影響NPR1的轉(zhuǎn)錄激活活性從而調(diào)控下游基因表達[58,59]。當植物體內(nèi)SA含量較少時，NPR1形成多聚體并定位于細胞質(zhì)中。NPR1第55和59位絲氨酸被磷酸化，抑制NPR1的轉(zhuǎn)錄激活活性。當SA積累時NPR1從多聚體還原為單體并轉(zhuǎn)移到細胞核中。在細胞核中NPR1被相素化，進而促進11和15位絲氨酸磷酸化，增強NPR1轉(zhuǎn)錄激活活性，促進SA下游基因表達。對NPR1的泛素化修飾導(dǎo)致其被26S蛋白酶體降解，一方面降低NPR1含量，另一方面使新的NPR1蛋白被募集到轉(zhuǎn)錄位點，增強下游基因表達[59]。

2012年Wu等[60]通過平衡透析配體結(jié)合實驗發(fā)現(xiàn)NPR1結(jié)合SA，Ding等[61]通過常規(guī)的受體-配體結(jié)合實驗進一步證實了該結(jié)論。Wu等[60]研究顯示NPR1通過其羧基端第521和529位半胱氨酸結(jié)合金屬銅和SA；通過螯合作用去除金屬將解除NPR1和SA的結(jié)合；SA結(jié)合導(dǎo)致NPR1羧基端反式激活結(jié)構(gòu)域構(gòu)象發(fā)生改變，從而使其從NPR1氨基端具有抑制功能的BTB/POZ (broad-complex, tramtrack and bric a brac/poxvirus and zinc finger)結(jié)構(gòu)域中釋放出來，誘導(dǎo)下游基因轉(zhuǎn)錄。而Ding等[61]研究顯示NPR1的第432位精氨酸在結(jié)合SA過程中發(fā)揮重要作用，將其突變?yōu)楣劝滨０穼⒋蠓冉档蚇PR1結(jié)合SA的能力。雖然這兩篇文章關(guān)注的氨基酸位點不同，但都證明NPR1羧基端在SA接收中的重要性。

2.2 NPR3和NPR4

NPR3和NPR4 (NPR3/4)是NPR1的同源蛋白，二者功能冗余，共同抑制植物對丁香假單胞菌的抗性[62]。2012年Fu等[63]研究指出NPR3/4是SA受體。通過常規(guī)受體-配體結(jié)合實驗，他們發(fā)現(xiàn)NPR3/4結(jié)合SA，NPR4具有較高的SA結(jié)合能力，NPR3結(jié)合能力弱于NPR4；SA的結(jié)合促進NPR3與NPR1相互作用，抑制NPR4與NPR1互作；NPR3/4含有BTB結(jié)構(gòu)域，直接與CUL3 (culin3)互作形成E3復(fù)合體促進NPR1降解；遺傳學(xué)證據(jù)表明NPR3/4對植物免疫反應(yīng)ETI的調(diào)控依賴于NPR1。因此他們提出假說，NPR3和NPR4分別感受植物體內(nèi)不同濃度SA，通過促進NPR1降解介導(dǎo)植物對SA的響應(yīng)。當植物體內(nèi)SA濃度很低時，NPR4介導(dǎo)NPR1降解(正常生長狀態(tài)下)。植物體內(nèi)SA濃度很高時(ETI)，NPR3介導(dǎo)NPR1降解。只有植物體內(nèi)SA濃度處于中等水平時(SAR)，SA足以干擾NPR4和NPR1互作，但不足以促進NPR3和NPR1互作，NPR1在植物體內(nèi)積累，促進下游基因表達[64]。

2018年Ding等[61]進一步證實NPR3/4是SA受體。與Fu等[63]研究結(jié)果一致，該研究同樣發(fā)現(xiàn)NPR4與SA的結(jié)合能力高于NPR3。但該研究提出不同的NPR3/4作用模型。通過篩選的抑制子，Ding等[61]發(fā)現(xiàn)一個NPR4功能獲得性突變形式npr4-4D；npr4-4D的突變位點是NPR4蛋白第419位精氨酸，該位點是NPR4結(jié)合SA的關(guān)鍵位點；SA結(jié)合NPR4解除其轉(zhuǎn)錄抑制活性，而npr4-4D不能與SA結(jié)合，持續(xù)抑制SA下游基因表達，使植物對丁香假單胞菌抗性減弱。由于和突變體對SA下游基因表達和植物抗病性具有疊加效應(yīng)，因此Ding等[61]認為SA下游有兩條平行的信號通路：一方面，當植物體內(nèi)SA濃度很低時，NPR3和NPR4抑制SA下游基因表達，當病原菌侵染導(dǎo)致SA濃度升高后，NPR3/4活性被抑制，其對SA下游基因轉(zhuǎn)錄抑制作用被解除；另一方面，植物體內(nèi)SA積累激活NPR1轉(zhuǎn)錄激活活性，進一步誘導(dǎo)SA下游抗病相關(guān)基因表達[65]。兩種不同模型的存在可能是由于NPR3/4有多個底物，而NPR1也受多種蛋白調(diào)控所致[58,66,67]。

2.3 SABPs

雖然現(xiàn)有研究證明NPR1和NPR3/4是SA主要受體，但事實上植物中有多個SA結(jié)合蛋白(SA-binding protein, SABP)[68]。如NPR1同源蛋白NPR2能夠結(jié)合SA并互補NPR1的功能，另外兩個NPR1同源蛋白BOP1 (block of cell proliferation 1)和BOP2也與SA有弱的結(jié)合能力[68,69]。長期以來，科研人員一直試圖通過生物化學(xué)方法尋找SA受體，并陸續(xù)鑒定出多個SABPs，如過氧化氫酶(SABP1)、水楊酸甲酯酯化酶(SABP2)和葉綠體碳酸酐酶(SABP3)等[70]。雖然這些SABPs缺乏作為SA受體的遺傳學(xué)證據(jù)，但它們確實參與特定SA代謝或信號轉(zhuǎn)導(dǎo)過程，例如SABP2以水楊酸甲酯為底物并將其轉(zhuǎn)化為SA[71]。在這些SABPs中，對SABP1同源蛋白過氧化氫酶2 (Catalase 2, CAT2)的功能解析近年獲得了新進展[72]。

煙草SABP1是最早報道的SA結(jié)合蛋白，其編碼過氧化氫酶催化過氧化氫分解成水和氧氣[73,74]。SA與SABP1結(jié)合抑制它的酶活性，導(dǎo)致植物體內(nèi)過氧化氫積累和SA下游基因誘導(dǎo)表達。CAT2是擬南芥中SABP1的同源蛋白，與SABP1具有78%序列同源性。SA抑制CAT2酶活性，導(dǎo)致病原菌侵染后植物體內(nèi)過氧化氫增加[72]。過氧化氫增加促進色氨酸合成酶亞基1 (tryptophan synthetase subunit 1, TSB1)第308位半胱氨酸磺基化(sulfenylation)，導(dǎo)致其活性受到抑制，減少生長素合成從而解除其對SA介導(dǎo)免疫反應(yīng)的抑制作用。同時，SA解除CAT2對茉莉酸生物合成過程中乙酰輔酶A氧化酶(acyl-CoA oxidases)活性的促進作用，抑制茉莉酸合成，解除茉莉酸對SA介導(dǎo)免疫反應(yīng)的負調(diào)控效應(yīng)[72]。這些結(jié)果表明CAT2特異性地調(diào)控SA信號轉(zhuǎn)導(dǎo)的特定過程。由于NPR類SA受體與該過程的關(guān)系還未被探究，所以CAT2在SA信號轉(zhuǎn)導(dǎo)中是否不依賴于NPRs獨立發(fā)揮功能還有待新的實驗證據(jù)。

3 水楊酸信號通路的轉(zhuǎn)錄因子

NPR類蛋白和CAT2都不具備直接結(jié)合DNA的能力，因此需要通過轉(zhuǎn)錄因子(transcription factor, TF)來調(diào)控SA下游基因表達。參與SA信號通路的TF包括TGA、WRKY和NIMIN(NIM1 interacting)等[75,76]。

3.1 TGA

由于NPR1在SA信號轉(zhuǎn)導(dǎo)中的重要作用，科研人員通過篩選其互作蛋白以期解析SA信號通路。酵母雙雜交實驗結(jié)果顯示NPR1與bZIP (basic leucine zipper protein)類轉(zhuǎn)錄因子TGA家族蛋白互作[77~79]。TGA結(jié)合的順式作用元件存在于多個SA調(diào)控基因啟動子序列中[78]。擬南芥TGA家族由10個蛋白(TGA1~TGA10)組成，其中TGA1~ TGA7與NPR1互作。這7個TGA分為3個亞家族，分別是TGA1和TGA4(I)，TGA2、TGA5和TGA6(II)以及TGA3和TGA7(III)。其中II類TGA負調(diào)控SA下游基因基礎(chǔ)表達和介導(dǎo)病原菌侵染時SA對下游基因的誘導(dǎo)表達，在植物響應(yīng)SA信號中發(fā)揮關(guān)鍵作用[80]。II類TGA不僅與NPR1互作，也與另外兩個SA受體NPR3/4互作[61]。正常生長狀態(tài)下三突變體中SA下游基因()的表達量高于野生型，但該三突變體完全喪失SA誘導(dǎo)表達的能力，植物不能產(chǎn)生SAR[80]。Ding等[61]研究發(fā)現(xiàn)II類TGA轉(zhuǎn)錄因子對SA信號響應(yīng)由NPR1和NPR3/4共同調(diào)控。在正常生長狀態(tài)下NPR3/4和II類TGA互作抑制SA下游基因轉(zhuǎn)錄，而在SA積累時這種抑制作用解除。同時NPR1與組蛋白乙酰轉(zhuǎn)移酶HACs (histone acetyltransferases)形成的協(xié)同激活因子復(fù)合物與II類TGA結(jié)合，通過組蛋白乙酰化介導(dǎo)的表觀遺傳重編程激活下游基因轉(zhuǎn)錄[61,81]。由此可見，II類TGA對SA信號的調(diào)控取決于和其互作的SA受體蛋白。

3.2 NIMIN

通過酵母雙雜交還發(fā)現(xiàn)另一類受SA誘導(dǎo)表達的NPR1互作蛋白——NIMIN蛋白家族[82]。擬南芥中該家族由3個成員(NIMIN1~NIMIN3)組成，其中NIMIN1和NIMIN2與NPR1的羧基端互作，而NIMIN3與NPR1的羥基端互作[82]。過表達植株對病原菌敏感性增強，降低SA誘導(dǎo)的免疫反應(yīng)和下游基因表達，而敲除突變體在SA誘導(dǎo)后表達水平高于野生型[83]。酵母三雜交顯示NIMIN與NPR1和II類TGA蛋白形成復(fù)合體抑制SA下游基因表達。NIMIN蛋白含有EAR (ERF- associated amphiphilic repression)結(jié)構(gòu)域，可能通過結(jié)合TPL(topless)介導(dǎo)對基因表達的抑制作用[83]。在正常生長的植物中，NIMIN3發(fā)揮主要作用。病原菌侵染或SA處理后，和被快速誘導(dǎo)，NIMIN1防止植物免疫反應(yīng)被過早激活，而NIMIN2不參與抑制基因表達，在早期SA反應(yīng)中作用未知[84]。

3.3 WRKY

Maleck等[85]通過轉(zhuǎn)錄組分析發(fā)現(xiàn)并非所有SA調(diào)控基因啟動子中都含有TGA結(jié)合位點。相反，特異性結(jié)合WRKY轉(zhuǎn)錄因子的W-box順式元件在這些基因啟動子中更為常見，表明WRKY家族轉(zhuǎn)錄因子可能在SA信號通路中具有重要作用。擬南芥WRKY家族有74個成員，其中43個參與病原菌脅迫反應(yīng)或響應(yīng)SA信號[86~88]。Wang等[52]通過轉(zhuǎn)錄組數(shù)據(jù)分析得到8個NPR1直接轉(zhuǎn)錄調(diào)控的WRKY蛋白，其中的突變使植物對病原菌敏感性增加并減弱SA誘導(dǎo)的獲得性抗性，而突變增強對病原菌的抗性和對SA誘導(dǎo)免疫的響應(yīng)。WKRY18與NPR1和CDK8互作使RNA聚合酶II結(jié)合到NPR1和SA下游基因的啟動子區(qū)，調(diào)控和約20% SA響應(yīng)基因的表達[52,89]。WRKY不僅識別啟動子區(qū)的W-box，WRKY50結(jié)合在啟動子位于TGA轉(zhuǎn)錄因子結(jié)合位點附近的非W-box位點，通過與II類TGA相互作用協(xié)同促進表達[90]。

綜上所述，植物SA信號轉(zhuǎn)導(dǎo)是一個復(fù)雜網(wǎng)路，通過多個轉(zhuǎn)錄因子促進或抑制SA下游基因表達，將植物對SA的響應(yīng)控制在合理范圍內(nèi)，防止其過度激活導(dǎo)致植物生長受阻[91]。

4 結(jié)語與展望

目前，人們對SA生物合成和信號轉(zhuǎn)導(dǎo)的認知已經(jīng)有了長足進步。SA生物合成涉及兩個代謝途徑：ICS途徑和PAL途徑。迄今為止ICS途徑已基本被解析，PAL途徑也被進一步完善。SA信號轉(zhuǎn)導(dǎo)過程中植物主要通過NPR1和其同源蛋白NPR3/4接收SA信號，進而調(diào)控TGA、NIMIN和WRKY等多種轉(zhuǎn)錄因子改變下游基因的表達模式。但在SA生物合成和信號轉(zhuǎn)導(dǎo)領(lǐng)域仍有一些問題有待進行深入探究：(1)在不同物種中兩條SA生物合成途徑對合成SA的貢獻尚不明確；(2)雖然已發(fā)現(xiàn)到一些SA合成調(diào)控因子，但從生長發(fā)育或/和環(huán)境信號到SA生物合成還存在許多未知過程；(3) NPR1和NPR3/4之間是否以及何時存在上下游關(guān)系仍需進一步驗證；(4)雖然已鑒定出一些SA下游作用分子和轉(zhuǎn)錄因子，但已有知識還無法形成一個完善的體系，對SA信號轉(zhuǎn)導(dǎo)的理解還有待加強。進一步探索SA生物合成、信號轉(zhuǎn)導(dǎo)及其功能研究將加深人們對植物免疫系統(tǒng)分子機制的理解，并開辟新的研究領(lǐng)域，如SA對生長發(fā)育的調(diào)控機理以及對生長免疫平衡的影響等。更重要的是，這些研究成果還將為作物標記輔助選擇和分子設(shè)計育種提供新目標，從而促進現(xiàn)代農(nóng)業(yè)的可持續(xù)性發(fā)展。

[1] Norn S, Permin H, Kruse PR, Kruse E. From willow bark to acetylsalicylic acid, 2009, 37: 79–98.

[2] Sneader W. The discovery of aspirin: a reappraisal, 2000, 321(7276): 1591–1594.

[3] Raskin I. Salicylate, a new plant hormone, 1992, 99(3): 799–803.

[4] Koo YM, Heo AY, Choi HW. Salicylic acid as a safe plant protector and growth regulator, 2020, 36(1): 1–10.

[5] Zou LP, Pan C, Wang MX, Cui L, Han BY. Progress on the mechanism of hormones regulating plant flower formation., 2020, 42(8): 739–751.鄒禮平, 潘鋮, 王夢馨, 崔林, 韓寶瑜. 激素調(diào)控植物成花機理研究進展. 遺傳, 2020, 42(8): 739–751.

[6] Huang PX, Dong Z, Guo PR, Zhang X, Qiu YP, Li BS, Wang YC, Guo HW. Salicylic acid suppresses apical hook formation via NPR1-mediated repression of EIN3 and EIL1 in, 2020, 32(3): 612–629.

[7] White RF. Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco, 1979, 99(2): 410–412.

[8] Zhang YL, Li X. Salicylic acid: Biosynthesis, perception, and contributions to plant immunity, 2019, 50: 29–36.

[9] Jones JDG, Dangl JL. The plant immune system, 2006, 444(7117): 323–329.

[10] Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F. Network properties of robust immunity in plants, 2009, 5(12): e1000772.

[11] Cao H, Glazebrook J, Clarke JD, Volko S, Dong X. Thegene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats, 1997, 88(1): 57–63.

[12] Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J. Requirement of salicylic acid for the induction of systemic acquired resistance, 1993, 261(5122): 754–756.

[13] Seyfferth C, Tsuda K. Salicylic acid signal transduction: The initiation of biosynthesis, perception and transcriptional reprogramming, 2014, 5: 697.

[14] Garcion C, Lohmann A, Lamodiere E, Catinot J, Buchala A, Doermann P, Metraux JP. Characterization and biological function of thegene of, 2008, 147(3): 1279–1287.

[15] Wildermuth MC, Dewdney J, Wu G, Ausubel FM. Isochorismate synthase is required to synthesize salicylic acid for plant defence, 2001, 414(6863): 562–565.

[16] Macaulay KM, Heath GA, Ciulli A, Murphy AM, Abell C, Carr JP, Smith AG. The biochemical properties of the twoisochorismate synthases, 2017, 474(10): 1579–1590.

[17] Serino L, Reimmann C, Baur H, Beyeler M, Visca P, Haas D. Structural genes for salicylate biosynthesis from chorismate in pseudomonas aeruginosa, 1995, 249(2): 217–228.

[18] Jagadeeswaran G, Raina S, Acharya BR, Maqbool SB, Mosher SL, Appel HM, Schultz JC, Klessig DF, Raina R.GH3-LIKE DEFENSE GENE 1 is required for accumulation of salicylic acid, activation of defense responses and resistance to pseudomonas syringae, 2007, 51(2): 234–246.

[19] Zheng ZY, Qualley A, Fan BF, Dudareva N, Chen ZX. An important role of a BAHD acyl transferase-like protein in plant innate immunity, 2009, 57(6): 1040–1053.

[20] Rekhter D, Lüdke D, Ding YL, Feussner K, Zienkiewicz K, Lipka V, Wiermer M, Zhang YL, Feussner I. Isochorismate- derived biosynthesis of the plant stress hormone salicylic acid, 2019, 365(6452): 498–502.

[21] Torrens-Spence MP, Bobokalonova A, Carballo V, Glin-kerman CM, Pluskal T, Shen A, Weng JK. PBS3 and EPS1 complete salicylic acid biosynthesis from isochorismate in, 2019, 12(12): 1577–1586.

[22] Okrent RA, Brooks MD, Wildermuth MC.GH3.12 (PBS3) conjugates amino acids to 4-substituted benzoates and is inhibited by salicylate, 2009, 284(15): 9742–9754.

[23] Okrent RA, Wildermuth MC. Evolutionary history of the GH3 family of acyl adenylases in rosids, 2011, 76(6): 489–505.

[24] Nawrath C, Heck S, Parinthawong N, Metraux JP. EDS5, an essential component of salicylic acid-dependent signa-ling for disease resistance in, is a member of the mate transporter family, 2002, 14(1): 275–286.

[25] Serrano M, Wang BJ, Aryal B, Garcion C, Abou-Mansour E, Heck S, Geisler M, Mauch F, Nawrath C, Metraux JP. Export of salicylic acid from the chloroplast requires the multidrug and toxin extrusion-like transporter EDS5, 2013, 162(4): 1815–1821.

[26] Ribnicky DM, Shulaev V, Raskin II. Intermediates of salicylic acid biosynthesis in tobacco, 1998, 118(2): 565–572.

[27] Leon J, Yalpani N, Raskin I, Lawton MA. Induction of benzoic acid 2-hydroxylase in virus-inoculated tobacco, 1993, 103(2): 323–328.

[28] Koukol J, Conn EE. The metabolism of aromatic compounds in higher plans. IV. Purification and properties of the phenylalanine deaminase of hordeum vulgare, 1961, 236(10): 2692–2698.

[29] Huang JL, Gu M, Lai ZB, Fan BF, Shi K, Zhou YH, Yu JQ, Chen ZX. Functional analysis of thePAL gene family in plant growth, development, and response to environmental stress, 2010, 153(4): 1526–1538.

[30] Tonnessen BW, Manosalva P, Lang JM, Baraoidan M, Bordeos A, Mauleon R, Oard J, Hulbert S, Leung H, Leach JE. Rice phenylalanine ammonia-lyase geneis associated with broad spectrum disease resistance, 2015, 87(3): 273–286.

[31] Zhou XG, Liao HC, Chern M, Yin JJ, Chen YF, Wang JP, Zhu XB, Chen ZX, Yuan C, Zhao W, Wang J, Li WT, He M, Ma B, Wang JC, Qin P, Chen WL, Wang YP, Liu JL, Qian YW, Wang WM, Wu XJ, Li P, Zhu LH, Li SG, Ronald PC, Chen XW. Loss of function of a rice TPR- domain RNA-binding protein confers broad-spectrum disease resistance, 2018, 115(12): 3174–3179.

[32] Ning Y, Wang GL. Breeding plant broad-spectrum resistance without yield penalties, 2018, 115(12): 2859–2861.

[33] He J, Liu YQ, Yuan DY, Duan MJ, Liu YL, Shen ZJ, Yang CY, Qiu ZY, Liu DM, Wen PZ, Huang J, Fan DJ, Xiao SZ, Xin YY, Chen XN, Jiang L, Wang HY, Yuan LP, Wan JM. An R2R3 MYB transcription factor confers brown planthopper resistance by regulating the phenylalanine ammonia-lyase pathway in rice, 2020, 117(1): 271–277.

[34] Colquhoun TA, Marciniak DM, Wedde AE, Kim JY, Schwieterman ML, Levin LA, Moerkercke AV, Schuurink RC, Clark DG. A peroxisomally localized acyl-activating enzyme is required for volatile benzenoid formation in a petuniaxhybrida cv. 'Mitchell diploid' flower, 2012, 63(13): 4821–4833.

[35] Moerkercke AV, Schauvinhold I, Pichersky E, Haring MA, Schuurink RC. A plant thiolase involved in benzoic acid biosynthesis and volatile benzenoid production, 2009, 60(2): 292–302.

[36] Klempien A, Kaminaga Y, Qualley A, Nagegowda DA, Widhalm JR, Orlova I, Shasany AK, Taguchi G, Kish CM, Cooper BR, D'Auria JC, Rhodes D, Pichersky E, Dudareva N. Contribution of CoA ligases to benzenoid biosynthesis in petunia flowers, 2012, 24(5): 2015–2030.

[37] Bussell JD, Reichelt M, Wiszniewski AAG, Gershenzon J, Smith SM. Peroxisomal ATP-binding cassette transporter comatose and the multifunctional protein abnormal inflo-rescence meristem are required for the production of benzoylated metabolites inseeds, 2014, 164(1): 48–54.

[38] Xu L, Zhao HY, Ruan WY, Deng MJ, Wang F, Peng JR, Luo J, Chen ZX, Yi KK. Abnormal inflorescence meristem1 functions in salicylic acid biosynthesis to maintain proper reactive oxygen species levels for root meristem activity in rice, 2017, 29(3): 560– 574.

[39] Sadeghi M, Dehghan S, Fischer R, Wenzel U, Vilcinskas A, Kavousi HR, Rahnamaeian M. Isolation and characteri-zation of isochorismate synthase and cinnamate 4-hydro-xylase during salinity stress, wounding, and salicylic acid treatment in carthamus tinctorius, 2013, 8(11): e27335.

[40] Uppalapati SR, Ishiga Y, Wangdi T, Kunkel BN, Anand A, Mysore KS, Bender CL. The phytotoxin coronatine contributes to pathogen fitness and is required for sup-pression of salicylic acid accumulation in tomato inocu-lated with pseudomonas syringae pv. Tomato DC3000, 2007, 20(8): 955–965.

[41] Meuwly P, Molders W, Buchala A, Metraux JP. Local and systemic biosynthesis of salicylic acid in infected cucumber plants, 1995, 109(3): 1107–1114.

[42] Yuan YN, Chung JD, Fu XY, Johnson VE, Ranjan P, Booth SL, Harding SA, Tsai CJ. Alternative splicing and gene duplication differentially shaped the regulation of isochorismate synthase in populus and, 2009, 106(51): 22020–22025.

[43] Yalpani N, Leon J, Lawton MA, Raskin I. Pathway of salicylic acid biosynthesis in healthy and virus-inoculated tobacco, 1993, 103(2): 315–321.

[44] Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J.CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against pseudomonas syringae, 2009, 5(2): e1000301.

[45] van Verk MC, Bol JF, Linthorst HJM. WRKY transcription factors involved in activation of SA biosynthesis genes, 2011, 11: 89.

[46] Wang XY, Gao J, Zhu Z, Dong X, Wang XX, Ren GD, Zhou X, Kuai BK. TCP transcription factors are critical for the coordinated regulation ofexpression in, 2015, 82(1): 151–162.

[47] Zhang YX, Xu SH, Ding PT, Wang DM, Cheng YT, He J, Gao MH, Xu F, Li Y, Zhu ZH, Li X, Zhang YL. Control of salicylic acid synthesis and systemic acquired resistance by two members of a plant-specific family of transcription factors, 2010, 107(42): 18220– 18225.

[48] Sun TJ, Busta L, Zhang Q, Ding PT, Jetter R, Zhang YL. TGACG-binding factor 1 (TGA1) and TGA4 regulate salicylic acid and pipecolic acid biosynthesis by modulating the expression of systemic acquired resistance deficient 1 (SARD1) and calmodulin-binding protein 60g (CBP60g), 2018, 217(1): 344–354.

[49] Sun TJ, Zhang YX, Li Y, Zhang Q, Ding YL, Zhang YL. ChIP-seq reveals broad roles of SARD1 and CBP60g in regulating plant immunity, 2015, 6: 10159.

[50] Wang L, Tsuda K, Truman W, Sato M, Nguyen LV, Katagiri F, Glazebrook J. CBP60g and SARD1 play partially redundant critical roles in salicylic acid signaling, 2011, 67(6): 1029–1041.

[51] Zheng XY, Spivey NW, Zeng WQ, Liu PP, Fu ZQ, Klessig DF, He SY, Dong XN. Coronatine promotes pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation, 2012, 11(6): 587–596.

[52] Wang D, Amornsiripanitch N, Dong XN. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants, 2006, 2(11): e123.

[53] Truman W, Sreekanta S, Lu Y, Bethke G, Tsuda K, Katagiri F, Glazebrook J. The calmodulin-binding protein60 family includes both negative and positive regulators of plant immunity, 2013, 163(4): 1741–1751.

[54] Chen HM, Xue L, Chintamanani S, Germain H, Lin HQ, Cui HT, Cai R, Zuo JR, Tang XY, Li X, Guo HW, Zhou JM. Ethylene insensitive3 and ethylene insensitive3-like1 repress salicylic acid induction deficient2 expression to negatively regulate plant innate immunity in, 2009, 21(8): 2527–2540.

[55] Cao H, Bowling SA, Gordon AS, Dong X. Charac-terization of anmutant that is nonresponsive to inducers of systemic acquired resistance, 1994, 6(11): 1583–1592.

[56] Delaney TP, Friedrich L, Ryals JA.signal transduction mutant defective in chemically and biolo-gically induced disease resistance, 1995, 92(14): 6602–6606.

[57] Shah J, Tsui F, Klessig DF. Characterization of a salicylic acid-insensitive mutant () ofthaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene, 1997, 10(1): 69–78.

[58] Withers J, Dong XN. Posttranslational modifications of NPR1: A single protein playing multiple roles in plant immunity and physiology, 2016, 12(8): e1005707.

[59] Saleh A, Withers J, Mohan R, Marqueés J, Gu YN, Yan SP, Zavaliev R, Nomoto M, Tada Y, Dong XN. Posttrans-lational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses, 2015, 18(2): 169–182.

[60] Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Després C. TheNPR1 protein is a receptor for the plant defense hormone salicylic acid., 2012, 1(6): 639–647.

[61] Ding YL, Sun TJ, Ao K, Peng YJ, Zhang YX, Li X, Zhang YL. Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity, 2018, 173(6): 1454–1467.e15.

[62] Zhang YL, Cheng YT, Qu N, Zhao QG, Bi DL, Li X. Negative regulation of defense responses inby two NPR1 paralogs, 2006, 48(5): 647–656.

[63] Fu ZQ, Yan SP, Saleh A, Wang W, Ruble J, Oka N, Mohan R, Spoel SH, Tada Y, Zheng N, Dong XN. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants, 2012, 486(7402): 228–232.

[64] Yan S, Dong X. Perception of the plant immune signal salicylic acid, 2014, 20: 64–68.

[65] Ding PT, Ding YL. Stories of salicylic acid: A plant defense hormone, 2020, 25(6): 549–565.

[66] Liu LJ, Sonbol FM, Huot B, Gu YN, Withers J, Mwimba M, Yao J, He SY, Dong XN. Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity, 2016, 7: 13099.

[67] Chang M, Zhao JP, Chen H, Li GY, Chen J, Li M, Palmer IA, Song JQ, Alfano JR, Liu FQ, Fu ZQ. PBS3 protects EDS1 from proteasome-mediated degradation in plant immunity, 2019, 12(5): 678–688.

[68] Manohar M, Tian MY, Moreau M, Park SW, Choi HW, Fei ZJ, Friso G, Asif M, Manosalva P, von Dahl CC, Shi K, Ma SS, Dinesh-Kumar SP, O'Doherty I, Schroeder FC, van Wijk KJ, Klessig DF. Identification of multiple salicylic acid-binding proteins using two high throughput screens, 2015, 5: 777.

[69] Castelló MJ, Medina-Puche L, Lamilla J, Tornero P. NPR1 paralogs ofand their role in salicylic acid perception, 2018, 13(12): e0209835.

[70] Pokotylo I, Kravets V, Ruelland E. Salicylic acid binding proteins (SABPs): The hidden forefront of salicylic acid signalling, 2019, 20(18): 4377.

[71] Forouhar F, Yang Y, Kumar D, Chen Y, Fridman E, Park SW, Chiang YW, Acton TB, Montelione GT, Pichersky E, Klessig DF, Tong L. Structural and biochemical studies identify tobacco SABP2 as a methyl salicylate esterase and implicate it in plant innate immunity, 2005, 102(5): 1773–1778.

[72] Yuan HM, Liu WC, Lu YT. Catalase2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses, 2017, 21(2): 143–155.

[73] Chen Z, Klessig DF. Identification of a soluble salicylic acid-binding protein that may function in signal transduction in the plant disease-resistance response, 1991, 88(18): 8179–8183.

[74] Chen Z, Ricigliano JW, Klessig DF. Purification and characterization of a soluble salicylic acid-binding protein from tobacco, 1993, 90(20): 9533–9537.

[75] Backer R, Naidoo S, van den Berg N. The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: Mechanistic insights in plant disease resistance, 2019, 10: 102.

[76] Zhang JY, Wang QJ, Guo ZR. Progresses on plant AP2/ERF transcription factors., 2012, 34(7): 835–847.張計育, 王慶菊, 郭忠仁. 植物AP2/ERF類轉(zhuǎn)錄因子研究進展. 遺傳, 2012, 34(7): 835–847.

[77] Zhang Y, Fan W, Kinkema M, Li X, Dong X. Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of thegene, 1999, 96(11): 6523–6528.

[78] Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF. NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of thegene required for induction by salicylic acid, 2000, 13(2): 191–202.

[79] Després C, DeLong C, Glaze S, Liu E, Fobert PR. TheNPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors, 2000, 12(2): 279–290.

[80] Kesarwani M, Yoo J, Dong XN. Genetic interactions of TGA transcription factors in the regulation of patho-genesis-related genes and disease resistance in, 2007, 144(1): 336–346.

[81] Jin HS, Choi SM, Kang MJ, Yun SH, Kwon DJ, Noh YS, Noh B. Salicylic acid-induced transcriptional reprogram-ming by the HAC-NPR1-TGA histone acetyltransferase complex in, 2018, 46(22): 11712–11725.

[82] Weigel RR, B?uscher C, Pfitzner AJ, Pfitzner UM. NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins fromthat interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants, 2001, 46(2): 143–160.

[83] Weigel RR, Pfitzner UM, Gatz C. Interaction of NIMIN1 with NPR1 modulates PR gene expression in, 2005, 17(4): 1279–1291.

[84] Hermann M, Maier F, Masroor A, Hirth S, Pfitzner AJP, Pfitzner UM. TheNIMIN proteins affect NPR1 differentially, 2013, 4: 88.

[85] Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA. The transcriptome ofthaliana during systemic acquired resistance, 2000, 26(4): 403–410.

[86] Dong JX, Chen CH, Chen ZX. Expression profiles of thegene superfamily during plant defense response, 2003, 51(1): 21–37.

[87] Ulker B, Somssich IE. WRKY transcription factors: From DNA binding towards biological function, 2004, 7(5): 491–498.

[88] Pandey SP, Somssich IE. The role of WRKY transcription factors in plant immunity, 2009, 150(4): 1648–1655.

[89] Chen J, Mohan R, Zhang YQ, Li M, Chen H, Palmer IA, Chang M, Qi G, Spoel SH, Mengiste T, Wang DW, Liu FQ, Fu ZQ. NPR1 promotes its own and target gene expression in plant defense by recruiting CDK8, 2019, 181(1): 289–304.

[90] Hussain RMF, Sheikh AH, Haider I, Quareshy M, Linthorst HJM.WRKY50 and TGA transcription factors synergistically activate expression of, 2018, 9: 930.

[91] Xu GY, Yuan M, Ai CR, Liu LJ, Zhuang E, Karapetyan S, Wang SP, Dong XN. uORF-mediated translation allows engineered plant disease resistance without fitness costs, 2017, 545(7655): 491–494.

Progress on the biosynthesis and signal transduction of phytohormone salicylic acid

Xiaoyong Gu, Yang Liu, Lijing Liu

The phenolic phytohormone salicylic acid (SA) is widely produced in plants, and is a key player in many processes of plant physiology, especially in plant immunity. During pathogen infection, SA is accumulated and the SA signaling pathway is activated to induce the expression of defense-related genes. Recently, a series of SA-related studies have been published. These researches filled gaps in the two SA biosynthesis pathways: the isochorismate synthase (ICS) pathway and the phenylalanine ammonia-lyase (PAL) pathway. The NPR1 (nonexpresser ofgenes 1) and its paralogs, NPR3 and NPR4, were identified as SA receptors. The effect of type II TGAs (TGACG-binding factor) on SA downstream genes was shown to depend on the SA receptor they interacted with. This review will systematically introduce the progress on SA biosynthesis and signal transduction, aiming to provide a theoretical reference for in-depth study of SA regulation on plant development and defense responses.

salicylic acid; salicylic acid biosynthesis; salicylic acid receptors; salicylic acid signal transduction

2020-06-12;

2020-07-14

山東大學(xué)齊魯青年學(xué)科建設(shè)經(jīng)費項目(編號:11200087963080)資助[Supported by the Qilu Scholarship from Shandong University (No. 11200087963080)]

谷曉勇，碩士，助理實驗師，研究方向：植物免疫。E-mail: guxy18@sdu.edu.cn

劉利靜，博士，教授，研究方向：植物免疫。E-mail: ljliu@sdu.edu.cn

10.16288/j.yczz.20-173

2020/8/31 10:02:37

URI: https://kns.cnki.net/kcms/detail/11.1913.r.20200907.1316.001.html

(責任編委: 儲成才)