韓聰 何禹暢 吳麗娟 郟麗麗 王磊 鄂志國

水稻堿性亮氨酸拉鏈(bZIP)蛋白家族功能研究進展

韓聰 何禹暢 吳麗娟 郟麗麗 王磊 鄂志國*

(中國水稻研究所, 杭州 310006;*通信聯(lián)系人,email: ezhiguo@caas.cn)

堿性亮氨酸拉鏈（basic leucine zipper, bZIP）是一類重要的轉(zhuǎn)錄調(diào)控因子，廣泛存在于真核生物中，因含有高度保守的bZIP結(jié)構(gòu)域而得名。bZIP結(jié)構(gòu)域由緊密相鄰的堿性區(qū)域和亮氨酸拉鏈區(qū)域兩部分組成。粳稻基因組中注釋有89個bZIP基因，其中45個已得到功能驗證，它們參與調(diào)節(jié)水稻生長發(fā)育、生物與非生物脅迫應(yīng)答，包括種子休眠和萌發(fā)、成花轉(zhuǎn)變、光形態(tài)建成，以及脅迫和激素信號通路等。

水稻；堿性亮氨酸拉鏈蛋白；bZIP轉(zhuǎn)錄因子；基因功能

種子的休眠、萌發(fā)，植株的生長發(fā)育及生物與非生物脅迫應(yīng)答等生物學(xué)過程中，不同基因通常有著不同的時空表達(dá)特性和脅迫誘導(dǎo)反應(yīng)，它們的表達(dá)受轉(zhuǎn)錄因子精準(zhǔn)調(diào)控[1]。堿性亮氨酸拉鏈（basic leucine zipper, bZIP）蛋白是一類重要的轉(zhuǎn)錄因子，在植物中廣泛分布，參與調(diào)控植物各種生物學(xué)過程。

水稻是我國最重要的糧食作物之一，種植面積約占糧食作物面積的25.4%，產(chǎn)量接近糧食總產(chǎn)量的31.2%[2]。然而，水稻在種植過程中極易遭受惡劣環(huán)境影響和病蟲害襲擊，造成減產(chǎn)和品質(zhì)下降，嚴(yán)重威脅糧食安全。因此，水稻的生長發(fā)育和脅迫抗性機制，一直是農(nóng)學(xué)與生物學(xué)研究的熱點。本文對水稻bZIP轉(zhuǎn)錄因子的研究進展進行綜述，旨在為水稻功能基因組學(xué)研究提供參考。

1 bZIP蛋白結(jié)構(gòu)

bZIP蛋白因含有一個保守的bZIP結(jié)構(gòu)域而得名。在bZIP蛋白分子結(jié)構(gòu)上（如圖1-A所示），bZIP域分為兩個緊密相鄰的部分，一個是堿性區(qū)域（藍(lán)色），高度保守，約由20個氨基酸殘基組成，包含一個核定位信號和一個能結(jié)合DNA的N-X7-R/K基序；第二個是亮氨酸拉鏈區(qū)（灰色），由7個氨基酸殘基組成一個重復(fù)單位，亮氨酸或相關(guān)疏水氨基酸位于第7位，重復(fù)單元的數(shù)量則從3個到8個不等[3]。每個bZIP結(jié)構(gòu)域形成一個連續(xù)的α螺旋，兩個bZIP蛋白的α螺旋因側(cè)鏈?zhǔn)杷越诲e對插，形成拉鏈結(jié)構(gòu)（圖1-B）。bZIP蛋白形成同源或異源二聚體后，才能正常行使其功能。

通過全基因組相似性比對，Nijhawan等[4]和Ji等[5]分別從粳稻品種日本晴基因組中鑒定了89個bZIP位點，Corrêa等[6]報道了92個bZIP位點。這些基因的染色體分布和系統(tǒng)進化樹等生物信息學(xué)分析，前人文獻已有較透徹的闡述，本文不再贅述。本文聚焦于已報道的bZIP基因的功能，如表1所示。

A―bZIP結(jié)構(gòu)域示意圖, 由堿性DNA結(jié)合區(qū)(藍(lán)色)和相鄰的亮氨酸拉鏈區(qū)(灰色)組成; B―bZIP二聚體的結(jié)構(gòu)模型。

2 bZIP蛋白調(diào)控水稻生長發(fā)育

2.1 bZIP蛋白調(diào)控水稻成花轉(zhuǎn)變

成花素Hd3a和RFT1與14-3-3蛋白GF14c互作，形成復(fù)合物轉(zhuǎn)至核內(nèi)，與轉(zhuǎn)錄因子OsFD1(即OsbZIP77)結(jié)合形成三元成花素激活復(fù)合物(florigen activation complex, FAC)，誘導(dǎo)表達(dá)，從而分別在短日照和長日照下啟動水稻的成花轉(zhuǎn)變[14, 66, 94-95]。蛋白激酶OsCIPK3能磷酸化修飾OsFD1第192位的絲氨酸位點，促進含RFT1的FAC形成[95]。研究表明，OsFD7(即OsbZIP62)[73]、OsFD4(即OsbZIP69)[83]也能與成花素和14-3-3蛋白形成FAC，促進開花，突變體和RNAi植株均表現(xiàn)為遲抽穗。轉(zhuǎn)錄因子Ehd1能誘導(dǎo)成花素基因和表達(dá)，形成FAC，而FAC又能進一步增強表達(dá)[14]。有意思的是，HBF1(即OsbZIP42)能與Hd3a直接互作，也能通過GF14c間接與RFT1互作，這兩種互作形成的復(fù)合物在葉中能抑制表達(dá)，在頂端分生組織(SAM)中能抑制表達(dá)，從而推遲水稻的成花轉(zhuǎn)變[14]。研究還發(fā)現(xiàn)，HBF2(即OsbZIP09)在葉中的功能與HBF2冗余，也能抑制表達(dá)[12]。此外，一類RCN蛋白(RICE CENTRORADIALIS)能與Hd3a競爭，與14-3-3蛋白和OsFD1互作，形成成花抑制復(fù)合物(florigen repression complex, FRC)，阻止Hd3a正常行使功能，抑制水稻開花[101-102]。另一類CONSTANS轉(zhuǎn)錄因子DHD4，能與14-3-3競爭性結(jié)合OsFD1，干擾OsFD1與14-3-3的互作，從而影響FAC的形成，導(dǎo)致和的表達(dá)量降低，最終延遲開花[103]。

OsRE1(即OsbZIP01)[7]、OsABF1(即OsbZIP12)[21]、OsbZIP65[76]和OsbZIP71[84]均負(fù)調(diào)控水稻的成花轉(zhuǎn)變。OsRE1、OsbZIP65和OsbZIP71各自能直接結(jié)合到的啟動子區(qū)并抑制其表達(dá)；OsABF1則是通過激活表達(dá)，間接抑制表達(dá)。過表達(dá)、或的轉(zhuǎn)基因植株均表現(xiàn)出晚花表型，而突變體和表現(xiàn)為早花表型。因OsABF1功能與OsbZIP40冗余，單突抽穗期無顯著變化，但利用RNAi同時敲減和會導(dǎo)致明顯的早花表型。OsRIP1能與OsRE1協(xié)作，通過精細(xì)調(diào)節(jié)的表達(dá)對抽穗期進行微調(diào)。

2.2 bZIP蛋白調(diào)控水稻種子休眠與萌發(fā)

脫落酸(abscisic acid, ABA)和赤霉素(gibberellin, GA)是調(diào)控水稻種子休眠和萌發(fā)最重要的兩種激素。ABA誘導(dǎo)和維持種子休眠，抑制種子萌發(fā)及幼苗生長，而GA作用相反。種子休眠和萌發(fā)受這兩種內(nèi)源激素含量和種胚對它們的敏感性共同調(diào)控。此外，茉莉酸(jasmonic acid, JA)和褪黑素(melatonin, MT)也參與調(diào)控。

ABA信號通路促進種子休眠的分子機制已研究得相對清晰。當(dāng)ABA缺失時，蛋白磷酸酶OsPP2C30或OsPP2C51與激酶SAPK2在核中互作形成復(fù)合體；ABA存在時，ABA受體OsPYL/RCAR5與OsPP2C30、OsPP2C51結(jié)合，從而釋放出SAPK2，磷酸化的SAPK2與bZIP蛋白如OREB1(即OsbZIP10)互作并將其激活，bZIP蛋白則進一步結(jié)合ABA應(yīng)答元件(ABA-responsive elements, ABREs)，誘導(dǎo)ABA應(yīng)答基因如、和等表達(dá)，抑制種子萌發(fā)[15-16]。OsPP2C51在蛋白水平上能對OsbZIP10去磷酸化使其失活[15]，AP2轉(zhuǎn)錄因子OsSAE1在轉(zhuǎn)錄水平上直接抑制的表達(dá)[17]，因此，OsPP2C51和OsSAE1都能促進水稻種子萌發(fā)。此外，GF14h能與OsbZIP10互作降低其轉(zhuǎn)錄活性，而OsMFT2又能與OREB1-GF14h形成三元復(fù)合物，并破除GF14h對OsbZIP10的抑制作用[18]。類似地，TRAB1(OsbZIP66)與ABREs特異結(jié)合，并依賴于OsVP1調(diào)節(jié)ABA誘導(dǎo)的轉(zhuǎn)錄，控制水稻胚的成熟與休眠[77]。SAPK10能磷酸化OsbZIP66并將其激活[78]。研究還發(fā)現(xiàn)，OsbZIP23、OsbZIP66和OsbZIP72這三者在促進中花11種子休眠中的作用冗余，它們均正調(diào)控ABA應(yīng)答基因表達(dá)，抑制水稻種子萌發(fā)；OsMFT2能分別與這3個bZIP轉(zhuǎn)錄因子互作，增強它們與啟動子的結(jié)合[37]。過表達(dá)能清除敲除株系穗發(fā)芽的表型[37]；雙突材料的種子萌發(fā)提早，對ABA敏感性下降[79]。OsbZIP75和OsbZIP78能直接與啟動子結(jié)合誘導(dǎo)其表達(dá)，OsDOG1L-3進一步上調(diào)ABA合成和信號傳導(dǎo)相關(guān)基因表達(dá)，通過增強ABA信號通路促進水稻種子休眠[92]。

表1 已功能鑒定的水稻bZIP轉(zhuǎn)錄因子

(+)和(-)分別代表正調(diào)控和負(fù)調(diào)控。

有研究發(fā)現(xiàn)，ABA對種子萌發(fā)的抑制效應(yīng)部分依賴于JA生物合成。SAPK10能磷酸化修飾OsbZIP72并增強其穩(wěn)定性，磷酸化修飾增強了bZIP72結(jié)合JA合成途徑關(guān)鍵基因啟動子的能力，促進后者轉(zhuǎn)錄，從而提高內(nèi)源JA水平并抑制種子萌發(fā)。外施JA合成抑制劑可緩解ABA對種子萌發(fā)的抑制也證實了這一點[79]。在過表達(dá)的轉(zhuǎn)基因水稻中，茉莉酸水平也上調(diào)，這可能是因為OsbZIP81.1直接激活了基因表達(dá)所致[97]。

也有bZIP蛋白能抑制ABA積累和信號傳導(dǎo)，正調(diào)控種子萌發(fā)。如OsbZIP09能直接與ABA分解基因啟動子結(jié)合并增強其表達(dá)，降低ABA積累，也能直接與啟動子結(jié)合并抑制其表達(dá)，減弱ABA信號通路，最終促進水稻種子發(fā)芽。突變體穗發(fā)芽現(xiàn)象較少[13-14]。

與ABA作用相反，GA能破除種子休眠，促進萌發(fā)。OsABF1(即OsbZIP12)通過抑制GA合成，負(fù)調(diào)控水稻種子萌發(fā)和節(jié)間伸長。OsABF1與多梳家族成員OsEMF2b互作，招募多梳蛋白抑制復(fù)合體PRC2到GA20氧化酶基因的啟動子區(qū)域，實施H3K27me3甲基化，經(jīng)表觀修飾抑制的轉(zhuǎn)錄，進而維持水稻生長和種子萌發(fā)所需的GA平衡。過表達(dá)產(chǎn)生典型的GA缺失表型，半矮化和種子萌發(fā)遲緩，外施GA3可以恢復(fù)表型[25]。此外，C2C2型鋅指蛋白OsLOL1與OsbZIP58互作，并經(jīng)OsbZIP58激活貝殼杉烯氧化酶基因表達(dá)，促進GA生物合成，GA水平的上調(diào)促進了胚乳糊粉層細(xì)胞程序化死亡(programmed cell death, PCD)和種子萌發(fā)[70]。

有意思的是，如上文所述，OsbZIP10、OsbZIP23和OsbZIP72正調(diào)控ABA信號抑制種子萌發(fā)[15, 37]，但在褪黑素、加速老化或淹水等非常規(guī)處理過程中，又能提高種子活力，表現(xiàn)出與常規(guī)條件下相反的作用。如低溫和鉻離子毒害會抑制種子萌發(fā)，而褪黑素處理能恢復(fù)種子活力。研究發(fā)現(xiàn)，OsbZIP10能增強褪黑素改善低溫和鉻離子脅迫下種子萌發(fā)的作用，褪黑素處理下，OsbZIP10通過直接上調(diào)過氧化氫酶基因和抗壞血酸過氧化物酶基因的表達(dá)，增加赤霉素合成，促進H2O2清除，從而提高低溫和絡(luò)離子毒害下的發(fā)芽率[105-106]。相對濕度80%、42℃的加速老化處理也能降低種子活力，但在Kasalath種子中，內(nèi)源ABA含量增加促進表達(dá)，OsbZIP23進而激活下游靶標(biāo)過氧化物還原酶基因表達(dá)，PER1A通過清除種子內(nèi)活性氧正調(diào)控種子活力。突變體和種子中的H2O2含量均顯著高于野生型，而過表達(dá)的Kasalath種子在加速老化處理15或18 d后發(fā)芽率顯著高于對照[38]。該研究還發(fā)現(xiàn)OsbZIP42正調(diào)控水稻種子活力，但作用機制有待進一步研究[38]。在淹水條件下，OsbZIP72通過激活乙醇脫氫酶ADH1，隨后產(chǎn)生更多參與酒精發(fā)酵和糖酵解途徑的NAD+、NADH和ATP，提供必要的能量儲備，促進水稻種子萌發(fā)和胚芽鞘伸長[88]。

2.3 bZIP蛋白調(diào)控水稻胚乳發(fā)育

粒重是決定水稻產(chǎn)量的重要性狀，轉(zhuǎn)錄因子OsbZIP47參與調(diào)控水稻粒形和粒重。過表達(dá)的轉(zhuǎn)基因植株籽粒細(xì)長，而突變體籽粒變寬。研究發(fā)現(xiàn)CC類谷氧還蛋白WG1能與OsbZIP47直接互作，并招募轉(zhuǎn)錄共抑制子ASP1來抑制OsbZIP47的轉(zhuǎn)錄活性；而E3泛素連接酶GW2可以泛素化WG1，并調(diào)控WG1的蛋白穩(wěn)定性。因此，GW2-WG1-OsbZIP47構(gòu)成了一個調(diào)控水稻種子發(fā)育的通路[53]。

OsCEN2-GF14f-OsFD2(即OsbZIP55)是另一個調(diào)控水稻籽粒發(fā)育的模塊。實驗表明OsCEN2能與GF14f發(fā)生互作，而GF14f能直接與OsFD2互作，OsFD2則通過控制穎殼中的細(xì)胞生長和分裂來影響水稻籽粒大小[65]。OsFD2還調(diào)控水稻葉片的發(fā)育，但需要形成FAC，Hd3a與14-3-3的互作會促進含有OsFD2的FAC的核運輸。過表達(dá)會使水稻葉片變小，且先后兩個葉原基形成的間隔期縮短[66]。

RISBZ1(即OsbZIP58)在水稻灌漿過程中起重要作用，影響種子中游離賴氨酸含量和儲藏蛋白積累[67-68]。研究還發(fā)現(xiàn)，OsbZIP58能直接與6個淀粉合成基因、、、、和的啟動子結(jié)合，調(diào)節(jié)其表達(dá)，從而調(diào)節(jié)胚乳中淀粉的生物合成。突變體種子形態(tài)異常，總淀粉和直鏈淀粉含量降低，且支鏈淀粉的短鏈比例較高、中鏈比例較低[69]。

OsbZIP76自身無轉(zhuǎn)錄激活活性，但它能分別與核因子Y家族轉(zhuǎn)錄因子OsNF-YB1和OsNF-YB9互作，調(diào)控水稻胚乳發(fā)育，共同參與儲藏物質(zhì)積累。突變體的胚乳細(xì)胞化進程提前，表現(xiàn)出和突變體類似的籽粒變小和直鏈淀粉含量降低等表型[93]。

2.4 bZIP蛋白調(diào)控水稻其他組織發(fā)育

發(fā)育良好的根系對于水稻有效吸水至關(guān)重要，特別是在干旱環(huán)境中。編碼OsbZIP01，其突變通過抑制生長素信號促進水稻根系發(fā)育。突變體的種子根伸長加快，此外，與野生型相比，短而細(xì)的側(cè)根數(shù)減少，而長而粗的側(cè)根數(shù)增加[8]。此外，ABL1(即OsbZIP46)通過影響含ABRE元件基因?qū)崿F(xiàn)對ABA和生長素應(yīng)答的雙重調(diào)控，突變體對外源吲哚乙酸超敏感，一些與生長素代謝或信號傳導(dǎo)相關(guān)基因的表達(dá)量發(fā)生改變，且的表達(dá)能恢復(fù)擬南芥突變體的ABA 敏感性[52]。

支鏈氨基酸和5-羥色胺在植物生長發(fā)育方面發(fā)揮著重要作用。OsbZIP18通過直接與支鏈氨基酸生物合成基因和的啟動子結(jié)合，正調(diào)控支鏈氨基酸的合成[27]。OsbZIP18還能直接與、和的啟動子結(jié)合并激活表達(dá)，促進5-羥色胺的生物合成，5-羥色胺積累導(dǎo)致植株矮小、少分蘗、深棕色的表型，對中波紫外線(UV-B)抗性也下降[28]。此外，OsbZIP18(OsHY5L1)還能促進水稻在藍(lán)光下的光形態(tài)建成[29]。

OsbZIP48在光調(diào)節(jié)的發(fā)育中發(fā)揮多種作用，過表達(dá)全長的轉(zhuǎn)基因水稻，細(xì)胞分裂素水平升高，綠色期更長，半矮稈，節(jié)間長度和穗長縮短，莖稈??；RNAi株系和T-DNA插入突變體表現(xiàn)為幼苗致死[54]。OsHY5(即OsbZIP48)還能與OsBBX14協(xié)同作用，直接激活或表達(dá)，精細(xì)調(diào)控花青素生物合成[56]。OsbZIP48被OsRLCK160磷酸化后，還能促進水稻中類黃酮的積累，參與UV-B抗性[55]。

OsbZIP84參與調(diào)控細(xì)胞伸長。上調(diào)表達(dá)導(dǎo)致植株變高，而表達(dá)量下調(diào)導(dǎo)致植株變矮，且這種矮化是由細(xì)胞變短造成。OsbZIP84可能通過調(diào)控赤霉素代謝路徑中的合成調(diào)控胞內(nèi)赤霉素的含量，并進一步調(diào)控水稻的生長發(fā)育[98]。

3 bZIP蛋白調(diào)控水稻非生物脅迫應(yīng)答

非生物脅迫是一種廣泛存在的環(huán)境脅迫，包括干旱、水澇、高溫、低溫、高鹽、重金屬和輻射等，嚴(yán)重威脅農(nóng)作物生產(chǎn)。ABA是植物應(yīng)答非生物脅迫的主要激素。環(huán)境脅迫能促進植物體內(nèi)快速合成脫落酸，并激活A(yù)BA信號通路應(yīng)答脅迫，從而增強植物的抗性[30]。bZIP轉(zhuǎn)錄因子被磷酸化激活后，通過與基因啟動子中ABREs結(jié)合，參與ABA介導(dǎo)的轉(zhuǎn)錄調(diào)控。

3.1 bZIP蛋白調(diào)控水稻高低溫脅迫應(yīng)答

脫落酸和低溫能誘導(dǎo)OsbZIP73表達(dá)，說明OsbZIP73 參與依賴ABA的低溫信號通路。OsbZIP73Jap與OsbZIP71互作形成異源二聚體，抑制脫落酸生物合成，降低活性氧水平，從而提高水稻苗期對低溫的耐受性[86]。生殖生長期，bZIP73Jap:bZIP71不僅能抑制花藥中ABA水平，而且可促進可溶性糖從花藥轉(zhuǎn)運到花粉，提高了水稻結(jié)實率和產(chǎn)量；此外，bZIP73Jap:bZIP71還正調(diào)控qLTG3-1的表達(dá)，而qLTG3-1過表達(dá)株系的生殖期耐寒性大大提高[87]。(即)和(即)的表達(dá)分別受低溫脅迫誘導(dǎo)和抑制。LIP19 沒有bZIP蛋白常見的同源二聚化和結(jié)合DNA的能力，但LIP19能與OsOBF1互作形成異源二聚體，且這種結(jié)合比OsOBF1自身的互作要強。推測水稻中存在這樣的一個感溫模型：正常溫度如25℃時，OsOBF1大量表達(dá)并形成同源二聚體結(jié)合到六聚體基序ACGTCA上從而誘導(dǎo)目標(biāo)基因的表達(dá)；隨著溫度降低，OsOBF1 表達(dá)量下降而LIP19 表達(dá)量上升，至5℃時，LIP19大量表達(dá)而OsOBF1表達(dá)很低，LIP19和OsOBF1互作形成異源二聚體并結(jié)合到G/C序列上從而誘導(dǎo)耐冷性基因表達(dá)[45]。

內(nèi)質(zhì)網(wǎng)(endoplasmic reticulum, ER)內(nèi)腔中未折疊或錯折疊蛋白的積累會導(dǎo)致ER脅迫，并引發(fā)未折疊蛋白反應(yīng)(unfolded protein response, UPR)，包括減少翻譯以緩解新生蛋白質(zhì)折疊的需求，降解未折疊蛋白以減輕損傷，增加細(xì)胞伴侶蛋白表達(dá)以協(xié)助蛋白質(zhì)折疊。ER脅迫傳感因子IRE1通過介導(dǎo)一些特異響應(yīng)ER脅迫的關(guān)鍵轉(zhuǎn)錄因子mRNA的非典型剪接，誘導(dǎo)它們的激活[57-58]。OsbZIP50(也稱)在水稻胚乳發(fā)育過程中通過激活分子伴侶基因表達(dá)，影響種子貯藏蛋白和淀粉的積累[59]。研究發(fā)現(xiàn)，常規(guī)剪接下，蛋白不能轉(zhuǎn)入細(xì)胞核，但ER脅迫或高溫脅迫下，mRNA保守的雙莖環(huán)結(jié)構(gòu)被剪接，新產(chǎn)生的蛋白丟失了跨膜區(qū)，變成具有轉(zhuǎn)錄活性的核定位形式，從而將脅迫信號從內(nèi)質(zhì)網(wǎng)傳遞到細(xì)胞核，并調(diào)控脅迫應(yīng)答基因表達(dá)。OsbZIP39功能和作用方式與OsbZIP50類似[46]。NAC轉(zhuǎn)錄因子OsNTL3能從質(zhì)膜遷移到細(xì)胞核，直接與啟動子結(jié)合并調(diào)控其表達(dá)[60]。過表達(dá)UPR響應(yīng)基因、、和導(dǎo)致不同程度堊白，說明UPR反應(yīng)會促進堊白形成。進一步研究發(fā)現(xiàn)，OsbZIP60 (OPAQUE3)能通過維持胚乳發(fā)育過程中內(nèi)質(zhì)網(wǎng)穩(wěn)態(tài)來抑制過度激活，進而保證胚乳正常發(fā)育[59]。OsbZIP60在熱脅迫和干旱脅迫應(yīng)答中也具有重要作用，過量表達(dá)能增強水稻的抗熱和抗旱能力[71]。OPAQUE3在水稻胚乳發(fā)育，特別是高溫脅迫下胚乳的正常發(fā)育中起著核心的調(diào)控作用。自然高溫環(huán)境下，突變體籽粒灌漿速率降低，成熟籽粒中總淀粉、直鏈淀粉和總蛋白質(zhì)、谷蛋白含量顯著降低，千粒重和單株產(chǎn)量均顯著降低[72]。

3.2 bZIP蛋白調(diào)控水稻干旱和鹽脅迫應(yīng)答

干旱、鹽和脫落酸處理能改變(、、和的表達(dá)水平，表明參與依賴ABA的干旱和高鹽信號通路。過表達(dá)、或的轉(zhuǎn)基因水稻，顯著提高了對干旱和鹽脅迫的耐受性；而突變體、表現(xiàn)相反[22-23, 31-33, 85]。研究發(fā)現(xiàn)OsSAPK10能與OsbZIP20互作并將其磷酸化激活，OsbZIP20進而與啟動子的ABRE元件結(jié)合并誘導(dǎo)其轉(zhuǎn)錄，從而增強水稻的干旱和鹽脅迫抗性[31]。OsbZIP23與組蛋白修飾協(xié)同調(diào)控水稻脫水蛋白基因表達(dá)，干旱脅迫下，組蛋白H3上第4位的賴氨酸三甲基化(H3K4me3)修飾水平提高，脫水蛋白基因表達(dá)水平增加，而OsbZIP23與脫水蛋白基因啟動子的結(jié)合能力也提高；相反，突變體中的H3K4me3修飾和脫水蛋白基因表達(dá)水平均下調(diào)[34]。而SUMO蛋白酶OsOTS1能對OsbZIP23直接去SUMO化，影響其穩(wěn)定性，從而負(fù)調(diào)控ABA依賴的干旱應(yīng)答基因表達(dá)[35]。此外，SAPK2能磷酸化OsbZIP23從而將其激活，而OsPP2C49能與SAPK2互作使其失活從而抑制了OsbZIP23的激活，OsbZIP23又通過正調(diào)控和的表達(dá)，對ABA的信號轉(zhuǎn)導(dǎo)和生物合成進行反饋調(diào)節(jié)(圖2)[36]。過表達(dá)導(dǎo)致水稻對ABA敏感性降低，轉(zhuǎn)基因幼苗置于空氣中快速脫水，對干旱超敏感；而編碼的9-順式-環(huán)氧類胡蘿卜素雙加氧酶是控制ABA合成的關(guān)鍵酶。與OsbZIP23類似，OsbZIP86能與啟動子結(jié)合，在干旱條件下激活表達(dá)，通過上調(diào)ABA合成來提高水稻耐旱性[99]。通過維持葉綠素含量和提高抗氧化能力，正調(diào)控水稻對鹽和干旱脅迫的耐受性。與野生型相比，過表達(dá)的轉(zhuǎn)基因水稻限制了活性氧的積累，表現(xiàn)出更高的存活率和更有利的滲透參數(shù)[9-10]。

圖2?OsbZIP23參與調(diào)控ABA信號通路.

OsABF2(OsbZIP46)也是ABA 信號和非生物脅迫的正調(diào)控因子，純合T-DNA插入突變體與野生型相比對干旱、高鹽和氧化脅迫更敏感[49]。但OsbZIP46 含有的D 結(jié)構(gòu)域?qū)せ罨钚杂胸?fù)效應(yīng)。因此，過量表達(dá)對耐旱性沒有正效應(yīng)，但過表達(dá)(去除D域的OsbZIP46) 顯著提高了水稻對干旱和滲透的抗性[50]。有意思的是，MODD通過與OsTPR3-HDA702共抑制復(fù)合物互作來抑制OsbZIP46活性，下調(diào)OsbZIP46靶基因的組蛋白乙?；剑徊⑼ㄟ^與U-box型E3泛素連接酶OsPUB70互作，促進OsbZIP46降解。這一過程中，OsbZIP46的D結(jié)構(gòu)域通過與MODD的互作，參與了OsbZIP46的去活化和降解[51]。與OsbZIP46類似，其他多個bZIP蛋白，包括OsBZIP10[20]、OsbZIP16[26]、OsbZIP33[42]、EDT1OsbZIP40[47]、OsbZIP45[33]、OsbZIP62[74]、OsbZIP66[80-81]和OsbZIP72[89]等，也都是ABREs結(jié)合因子，在干旱脅迫應(yīng)答中作為轉(zhuǎn)錄激活因子發(fā)揮正調(diào)控作用。如晚期胚胎富集蛋白基因正調(diào)控水稻的耐旱性，且不影響產(chǎn)量[104]；OsbZIP66和OsbZIP72通過直接與的啟動子結(jié)合，上調(diào)表達(dá)水平，從而正調(diào)控水稻耐旱性[81, 89]。OsMFT1作為輔助激活因子能協(xié)調(diào)并增強OsbZIP66活性[81]。與野生型相比，干旱處理數(shù)天再復(fù)水后，過表達(dá)、、或的轉(zhuǎn)基因水稻幼苗對ABA超敏感、存活率顯著提高，抗旱性明顯增強[46-47]，而敲除株系的存活率顯著降低，突變體的蒸騰速率和氣孔導(dǎo)度顯著高于野生型中花11[20]。OsbZIP72還能直接激活高親和力鉀轉(zhuǎn)運蛋白基因的表達(dá)，參與ABA信號通路介導(dǎo)的耐鹽途徑[90]。

也有bZIP蛋白負(fù)調(diào)控水稻的干旱和鹽脅迫應(yīng)答。干旱脅迫下，RNAi株系的氣孔開度和失水率相比野生型降低，生理指標(biāo)如脯氨酸、葉綠素和丙二醛含量顯著改善，存活率得到大幅提高，表明負(fù)調(diào)控水稻的耐旱性[13]。水稻中過量表達(dá)后對鹽脅迫高度敏感，而抑制表達(dá)則提高了耐鹽性，但同時導(dǎo)致育性降低[17, 19]。

3.3 bZIP蛋白調(diào)控其他非生物脅迫應(yīng)答

OsbZIP20參與銨解毒和抗氧化。OsSAPK9能與OsbZIP20互作并將其磷酸化，從而激活OsbZIP20功能。高NH4+脅迫下，ABA能上調(diào)表達(dá)，OsSAPK9–OsbZIP20模塊通過增強NH4+同化和抗氧化活性，降低活性氧和游離銨水平，減輕水稻銨中毒。突變體和對高NH4+高度敏感，伴隨自由NH4+和H2O2在組織中積累[30]。

OsbZIP68參與調(diào)控滲透脅迫，且不依賴于ABA。GPX1作為氧化還原的傳感元件，在暴露于滲透脅迫后很快被氧化，形成分子內(nèi)二硫鍵，進而激活OsbZIP68。GPX1和OsbZIP68之間的二硫鍵交換誘導(dǎo)OsbZIP68形成同源四聚體，從而通過調(diào)節(jié)滲透應(yīng)答基因的表達(dá)調(diào)節(jié)滲透脅迫反應(yīng)[82]。

OsbZIP88參與調(diào)控水稻對3種不同類型除草劑的抗性，過表達(dá)的轉(zhuǎn)基因水稻對除草劑敏感性下降，而敲除株系的敏感性增加[100]。

4 bZIP蛋白調(diào)控水稻生物脅迫應(yīng)答

APIP5(即OsbZIP53)形成同源二聚體，與真菌效應(yīng)子AvrPiz-t在細(xì)胞質(zhì)中互作，AvrPiz-t能特異性抑制APIP5的轉(zhuǎn)錄活性。當(dāng)宿主沒有Piz-t時，AvrPiz-t通過作用于APIP5，增強效應(yīng)子觸發(fā)的壞死，幫助稻瘟菌進入死體營養(yǎng)階段。當(dāng)宿主包含Piz-t時，Piz-t通過與APIP5互作，穩(wěn)定APIP5蛋白積累以阻止細(xì)胞壞死的發(fā)生，從而抑制稻瘟菌從活體營養(yǎng)階段過渡到死體營養(yǎng)階段[61]。除此，APIP5還有多種調(diào)控防衛(wèi)反應(yīng)的機制。APIP5能直接與羥基肉桂?；D(zhuǎn)移酶基因/、、和的啟動子結(jié)合，抑制它們的轉(zhuǎn)錄，負(fù)調(diào)控酚胺代謝物和木質(zhì)素積累[62-63]。APIP5也能結(jié)合到細(xì)胞壁相關(guān)激酶基因和細(xì)胞色素P450基因的啟動子上，抑制二者的表達(dá)；OsWAK5調(diào)節(jié)木質(zhì)素積累，CYP72A1調(diào)控植保素合成和活性氧迸發(fā)，兩者均正調(diào)控水稻基礎(chǔ)免疫反應(yīng)。有趣的是，APIP5能發(fā)生質(zhì)核穿梭，并有RNA結(jié)合活性，稻瘟病菌侵染促使其在胞質(zhì)RNA加工小體中富集，與細(xì)胞死亡和防衛(wèi)相關(guān)基因和的3' UTR的poly(U)序列特異結(jié)合，促進和的mRNA降解，從而在轉(zhuǎn)錄后水平調(diào)控水稻基礎(chǔ)免疫反應(yīng)[64]。

白葉枯病抗性。研究發(fā)現(xiàn)白葉枯病菌Ⅲ型效應(yīng)子基因誘導(dǎo)表達(dá)，而的異位表達(dá)增加了水稻對白葉枯病的易感性[90]。rTGA2.1OsbZIP63[74]和OsbZIP1OsbZIP28[39]，也通過水楊酸途徑分別調(diào)控水稻的白葉枯病抗性和稻瘟病抗性。RF2aOsbZIP75和RF2bOsbZIP30通過抑制東格魯桿狀病毒的復(fù)制，正調(diào)控水稻對該病毒的抗性[40-41]。

萜類植保素具有廣譜抑菌活性，參與植物的生物防御響應(yīng)。OsTGAP1OsbZIP37能上調(diào)效應(yīng)子誘發(fā)的萜類植保素的積累[43-44]，而OsbZIP79能與OsbZIP37互作，抑制萜類植保素的積累[96]。

5 問題與展望

bZIP蛋白是重要的轉(zhuǎn)錄因子，通過突變體表型分析、基因敲除(低)或過表達(dá)等技術(shù)，已從水稻中鑒定了45個bZIP 轉(zhuǎn)錄因子(表1)。它們廣泛參與調(diào)控水稻各器官組織的發(fā)生發(fā)育、病蟲害抗性和非生物脅迫應(yīng)答等生物學(xué)過程。但是，這些進程的調(diào)節(jié)不是孤立的，需要上下游多個調(diào)控因子的參與。如我們發(fā)現(xiàn)OsbZIP76自身無轉(zhuǎn)錄激活活性，但它能分別與核因子Y家族轉(zhuǎn)錄因子OsNF-YB1和OsNF-YB9互作，調(diào)控水稻胚乳發(fā)育，共同參與儲藏物質(zhì)積累[93]。另外，多個信號間往往形成交叉，相互影響，而部分bZIP蛋白扮演中心節(jié)點的作用，如 OsbZIP12正調(diào)整水稻的耐鹽耐旱性，也調(diào)節(jié)種子萌發(fā)、抽穗期以及D-阿洛糖誘導(dǎo)的生長抑制[21-25]，OsbZIP23/66/72既促進種子休眠，也調(diào)控干旱脅迫應(yīng)答，以及多種脅迫下種子萌發(fā)(圖2)[37, 107]。因此，bZIP蛋白家族對水稻的生長發(fā)育和脅迫應(yīng)答調(diào)控是復(fù)雜的，每個bZIP轉(zhuǎn)錄因子都扮演了調(diào)控網(wǎng)絡(luò)中的一個或多個節(jié)點，我們?nèi)孕枰ㄟ^鑒定更多的bZIP蛋白及其互作因子，為最終繪制出整個遺傳網(wǎng)絡(luò)填上一塊塊拼圖。

[1] 王金英, 丁峰, 潘介春, 張樹偉, 楊亞涵, 黃幸, 范志毅, 李琳, 王穎. 植物bZIP轉(zhuǎn)錄因子家族的研究進展[J]. 熱帶農(nóng)業(yè)科學(xué), 2019, 39(6): 39-45.

Wang J Y, Ding F, Pan J C, Zhang S W, Yang Y H, Huang X, Fan Z Y, Li L, Wang Y. Research progress of bZIP lineage transcription factors in plant[J]., 2019, 39(6): 39-45.

[2] 國家統(tǒng)計局. 中國統(tǒng)計年鑒[G]. 北京: 中國統(tǒng)計出版社, 2022: 385-387, 428-430.

National Bureau of Statistics of the People's Republic of China. Chinese Statistical Yearbook[G]. Beijing: China Statistics Press, 2022: 385-387,428-430. (in Chinese)

[3] Dr?ge-Laser W, Snoek B L, Snel B, Weiste C. ThebZIP transcription factor family: An update[J]., 2018, 45: 36-49.

[4] Nijhawan A, Jain M, Tyagi A K, Khurana J P. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice[J]., 2008, 146(2): 333-350.

[5] Ji Q, Zhang L S, Wang Y F, Wang J. Genome-wide analysis of basic leucine zipper transcription factor families in,and[J]., 2009, 13(2): 174-182.

[6] Corrêa L G G, Ria?o-Pachón D M, Schrago C G, dos Santos R V, Mueller-Roeber B, Vincentz M. The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes[J]., 2008, 3: e2944.

[7] Chai J T, Zhu S S, Li C N, Wang C M, Cai M H, Zheng X M, Zhou L, Zhang H, Sheng P K, Wu M M, Jin X, Cheng Z J, Zhang X, Lei C L, Ren Y L, Lin Q B, Zhou S R, Guo X P, Wang J, Zhao Z C, Wan J M. OsRE1 interacts with OsRIP1 to regulate rice heading date by finely modulatingexpression[J]., 2021, 19(2): 300-310.

[8] Hasegawa T, Lucob-Agustin N, Yasufuku K, Kojima T, Nishiuchi S, Ogawa A, Takahashi-Nosaka M, Kano-Nakata M, Inari-Ikeda M, Sato M, Tsuji H, Wainaina C M, Yamauchi A, Inukai Y. Mutation of/, which encodes a member of the basic leucine zipper transcription factor family, promotes root development in rice through repressing auxin signaling[J]., 2021, 306: 110861.

[9] Lakra N, Nutan K K, Das P, Anwar K, Singla-Pareek S L, Pareek A. A nuclear-localized histone-gene binding protein from rice (OsHBP1b) functions in salinity and drought stress tolerance by maintaining chlorophyll content and improving the antioxidant machinery[J]., 2015, 176: 36-46.

[10] Das P, Lakra N, Nutan K K, Singla-Pareek S L, Pareek A. A unique bZIP transcription factor imparting multiple stress tolerance in rice[J]., 2019, 12: 58.

[11] 仝宇, 王聰, 趙利利, 連娟, 劉曉梅, 趙寶存. 轉(zhuǎn)錄因子OsbZIP5負(fù)調(diào)控水稻的耐旱性[J]. 中國生物化學(xué)與分子生物學(xué)報, 2021, 37(6): 798-810.

Tong Y, Wang C, Zhao L L, Lian J, Liu X M, Zhao B C. Transcription factor OsbZIP5 negatively regulates drought-tolerance in rice[J]., 2021, 37(6): 798-810. (in Chinese with English abstract)

[12] Brambilla V, Martignago D, Goretti D, Cerise M, Somssich M, de Rosa M, Galbiati F, Shrestha R, Lazzaro F, Simon R, Fornara F. Antagonistic transcription factor complexes modulate the floral transition in rice[J]., 2017, 29(11): 2801-2816.

[13] Zhu C C, Wang C X, Lu C Y, Wang J D, Zhou Y, Xiong M, Zhang C Q, Liu Q Q, Li Q F. Genome-wide identification and expression analysis of OsbZIP09 target genes in rice reveal its mechanism of controlling seed germination[J]., 2021, 22(4): 1661.

[14] Wang C X, Zhu C C, Zhou Y, Xiong M, Wang J D, Bai H, Lu C Y, Zhang C Q, Liu Q Q, Li Q F. OsbZIP09, a unique OsbZIP transcription factor of rice, promotes rather than suppresses seed germination by attenuating abscisic acid pathway[J]., 2021, 28(4): 358-367.

[15] Bhatnagar N, Min M K, Choi E H, Kim N, Moon S J, Yoon I, Kwon T, Jung K H, Kim B G. The protein phosphatase 2C clade A proteinpositively regulates seed germination by directly inactivating[J]., 2017, 93(4): 389-401.

[16] Kim H, Hwang H, Hong J W, Lee Y N, Ahn I P, Yoon I S, Yoo S D, Lee S, Lee S C, Kim B G. A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth[J]., 2012, 63(2): 1013-1024.

[17] Li Y X, Zhou J H, Li Z, Qiao J Z, Quan R D, Wang J, Huang R F, Qin H. SALT AND ABA RESPONSE ERF1 improves seed germination and salt tolerance by repressing ABA signaling in rice [J]., 2022, 189(2): 1110-1127.

[18] Yoshida H, Hirano K, Yano K, Wang F, Mori M, Kawamura M, Koketsu E, Hattori M, Ordonio R L, Huang P, Yamamoto E, Matsuoka M. Genome-wide association study identifies a gene responsible for temperature-dependent rice germination[J]., 2022, 13: 5665.

[19] Zou M J, Guan Y C, Ren H B, Zhang F, Chen F. A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance[J]., 2008, 66(6): 675-683.

[20] Li Q, Zhou L Y, Chen Y N, Xiao N, Zhang D P, Zhang M J, Wang W G, Zhang C Q, Zhang A N, Li H, Chen J M, Gao Y. Phytochrome interacting factor regulates stomatal aperture by coordinating red light and abscisic acid[J]., 2022, 34(11): 4293-4312.

[21] Zhang C Y, Liu J, Zhao T, Gomez A, Li C, Yu C S, Li H Y, Lin J Z, Yang Y Z, Liu B, Lin C T. A drought-inducible transcription factor delays reproductive timing in rice[J]., 2016, 171(1): 334-343.

[22] Joo J, Lee Y H, Song S I. Overexpression of the rice basic leucine zipper transcription factor OsbZIP12 confers drought tolerance to rice and makes seedlings hypersensitive to ABA[J]., 2014, 8(6): 431-441.

[23] Hossain M A, Lee Y, Cho J I, Ahn C H, S K, Jeon J S, Kang H, Lee C H, An G, Park P B. The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice[J]., 2010, 72(4-5): 557-566.

[24] Tang L Q, Xu H Y, Wang Y F, Wang H M, Li Z Y, Liu X X, Shu Y Z, Li G, Liu W N, Ying J Z, Tong X H, Yao J L, Xiao W F, Tang S Q, Ni S, Zhang J. OsABF1 represses gibberellin biosynthesis to regulate plant height and seed germination in rice (L.)[J]., 2021, 22(22): 12220.

[25] Fukumoto T, Kano A, Ohtani K, Inoue M, Yoshihara A, Izumori K, Tajima S, Shigematsu Y, Tanaka K, Ohkouchi T, Ishida Y, Nishizawa Y, Tada Y, Ichimura K, Gomi K, Yoo S D, Sheen J, Akimitsu K. Phosphorylation of d-allose by hexokinase involved in regulation ofexpression for growth inhibition inL.[J]., 2013, 237(5): 1379-1391.

[26] Chen H, Chen W, Zhou J L, He H, Chen L B, Chen H D, Deng X W. Basic leucine zipper transcription factor OsbZIP16 positively regulates drought resistance in rice[J]., 2012, 193-194: 8-17.

[27] Sun Y Y, Shi Y H, Liu G G, Yao F, Zhang Y Y, Yang C K, Guo H, Liu X Q, Jin C, Luo J. Natural variation in thepromoter contributes to branched-chain amino acid levels in rice[J]., 2020, 228(5): 1548-1558.

[28] Sun Y Y, Wang B, Ren J X, Zhou Y T, Han Y, Niu S Y, Zhang Y Y, Shi Y H, Zhou J J, Yang C K, Ma X M, Liu X Q, Luo Y H, Jin C, Luo J. OsbZIP18, a positive regulator of serotonin biosynthesis, negatively controls the UV-B tolerance in rice[J]., 2022, 23(6): 3215.

[29] Bai B, Lu N N, Li Y P, Guo S L, Yin H B, He Y N, Sun W, Li W, Xie X Z. OsBBX14 promotes photomorphogenesis in rice by activatingexpression under blue light conditions[J]., 2019, 284: 192-202.

[30] Sun L, Di D W, Li G J, Kronzucker H J, Wu X Y, Shi W M. Endogenous ABA alleviates rice ammonium toxicity by reducing ROS and free ammonium via regulation of the SAPK9-bZIP20 pathway[J]., 2020, 71(15): 4562-4577.

[31] Wang B X, Xu B, Liu Y, Li J F, Sun Z G, Chi M, Xing Y G, Yang B, Li J, Liu J B, Chen T M, Fang Z W, Lu B G, Xu D Y, Babatunde K B. A novel mechanisms of the signaling cascade associated with thesynergistic interaction to enhance tolerance of plant to abiotic stress in rice (L.)[J]., 2022, 323: 111393.

[32] Xiang Y, Tang N, Du H, Ye H, Xiong L. Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice[J]., 2008, 148(4): 1938-1952.

[33] Park Su H, Jeong J S, Lee K H, Kim Y S, Choi Y D, Kim J K. OsbZIP23 and OsbZIP45, members of the rice basic leucine zipper transcription factor family, are involved in drought tolerance[J]., 2015, 9(2): 89-96.

[34] Zong W, Yang J, Fu J, Xiong L. Synergistic regulation of drought-responsive genes by transcription factor OsbZIP23 and histone modification in rice[J]., 2020, 62(6): 723-729.

[35] Srivastava A K, Zhang C J, Caine R S, Gray J, Sadanandom A. Rice SUMO proteasetargets the transcription factor, OsbZIP23 to promote drought tolerance in rice[J]., 2017, 92(6): 1031-1043.

[36] Zong W, Tang N, Yang J, Peng L, Ma S, Xu Y, Li G, Xiong L. Feedback regulation of ABA signaling and biosynthesis by a bZIP transcription factor targets drought-resistance-related genes[J]., 2016, 171(4): 2810-2825.

[37] Song S, Wang G, Wu H, Fan X, Liang L, Zhao H, Li S, Hu Y, Liu H, Ayaad M, Xing Y. OsMFT2 is involved in the regulation of ABA signaling mediated seed germination through interacting with OsbZIP23/66/72 in rice[J]., 2020, 103(2): 532-546.

[38] Wang WQ, Xu DY, Sui YP, Ding XH, Song XJ. A multiomic study uncovers a bZIP23-PER1A–mediated detoxification pathway to enhance seed vigor in rice[J]., 2022, 119(9): e2026355119.

[39] Meng X B, Zhao W S, Lin R M, Wang M, Peng Y L. Identification of a novel rice bZIP-type transcription factor gene,, involved in response to infection of[J]., 2005, 23(3): 301-302.

[40] Dai S H, Zhang Z H, Chen S Y, Beachy R N. RF2b, a rice bZIP transcription activator, interacts with RF2a and is involved in symptom development of rice tungro disease[J]., 2004, 101(2): 687-692.

[41] Dai S H, Wei X P, Alfonso A A, Pei L P, Duque U G, Zhang Z H, Babb G M, Beachy R N. Transgenic rice plants that overexpress transcription factors RF2a and RF2b are tolerant to rice tungro virus replication and disease[J]., 2008, 105(52): 21012-21016.

[42] Chen H, Dai X J, Gu Z Y. OsbZIP33 is an ABA-dependent enhancer of drought tolerance in rice[J]., 2015, 55(4): 1673-1685.

[43] Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H. OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice[J]., 2009, 284(39): 26510-26518.

[44] Miyamoto K, Matsumoto T, Okada A, Komiyama K, Chujo T, Yoshikawa H, Nojiri H, Yamane H, Okada K. Identification of target genes of the bZIP transcription factor OsTGAP1, whose overexpression causes elicitor-induced hyperaccumulation of diterpenoid phytoalexins in rice cells[J]., 2014, 9(8): e105823.

[45] Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T. LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants., 2005, 46(10): 1623-1634.

[46] Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F. A rice transmembrane bZIP transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response[J]., 2012, 53(1): 144-153.

[47] Wu T, Zhang M X, Zhang H J, Huang K, Chen M J, Chen C, Yang X, Li Z, Chen H Y, Ma Z M, Zhang X M, Jiang W Z, Du X L. Identification and characterization ofconferring drought tolerance in rice[J]., 2019, 62: 39-47.

[48] Lilay G H, Castro P H, Guedes J G, Almeida D M, Campilho A, Azevedo H, Aarts M G M, Saibo N J M, Assun??o A G L. Rice F-bZIP transcription factors regulate the zinc deficiency response[J]., 2020, 71(12): 3664-3677.

[49] Hossain M A, Cho J I, Han M, Ahn C H, Jeon J S, An G, Park P B. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice[J]., 2010, 167(17): 1512-1520.

[50] Tang N, Zhang H, Li X H, Xiao J H, Xiong L Z. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice[J]., 2012, 158(4): 1755-1768.

[51] Tang N, Ma S, Zong W, Yang N, Lv Y, Yan C, Guo Z, Li J, Li X, Xiang Y, Song H, Xiao J, Li X, Xiong L. MODD mediates deactivation and degradation of OsbZIP46 to negatively regulate ABA signaling and drought resistance in rice[J]., 2016, 28(9): 2161-2177.

[52] Yang X, Yang Y N, Xue L J, Zou M J, Liu J Y, Chen F, Xue H W. Rice ABI5-Like1 regulates abscisic acid and auxin responses by affecting the expression of ABRE-containing genes[J]., 2011, 156(3): 1397-1409.

[53] Hao J Q, Wang D K, Wu Y B, Huang K, Duan P G, Li N, Xu R, Zeng D L, Dong G J, Zhang B L, Zhang L M, Inzé D, Qian Q, Li Y H. The GW2-WG1-OsbZIP47 pathway controls grain size and weight in rice[J]., 2021, 14(8): 1266-1280.

[54] Burman N, Bhatnagar A, Khurana J P. OsbZIP48, a HY5 transcription factor ortholog, exerts pleiotropic effects in light-regulated development[J]., 2018, 176(2): 1262-1285.

[55] Zhang F, Huang J C, Guo H, Yang C K, Li Y F, Shen S Q, Zhan C S, Qu L H, Liu X Q, Wang S C, Chen W, Luo J.contributes to flavonoid accumulation and UV-B tolerance by regulatingin rice[J]., 2022, 65(7): 1380-1394.

[56] Kim D H, Park S, Lee J Y, Ha S H, Lee J G, Lim S H. A rice B-box protein, OsBBX14, finely regulates anthocyanin biosynthesis in rice[J]., 2018, 19(8): 2190.

[57] Hayashi S, Wakasa Y, Takahashi H, Kawakatsu T, Takaiwa F. Signal transduction by IRE1-mediated splicing ofand other stress sensors in the endoplasmic reticulum stress response of rice[J]., 2012, 69(6): 946-956.

[58] Lu S J, Yang Z T, Sun L, Sun L, Song Z T, Liu J X. Conservation of IRE1-regulatedmRNA unconventional splicing in rice (L.) involved in ER stress responses[J]., 2012, 5(2): 504-514.

[59] Yang W, Xu P, Zhang J, Zhang S, Li Z, Yang K, Chang X, Li Y. OsbZIP60-mediated unfolded protein response regulates grain chalkiness in rice[J]., 2022, 49(5): 414-426.

[60] Liu X H, Lü Y S, Yang W, Yang Z T, Lu S J, Liu J X. A membrane-associated NAC transcription factor OsNTL3 is involved in thermotolerance in rice[J]., 2020, 18(5): 1317-1329.

[61] Wang R T, Ning Y S, Shi X T, He F, Zhang C Y, Fan J B, Jiang N, Zhang Y, Zhang T, Hu Y J, Bellizzi M, Wang G L. Immunity to rice blast disease by suppression of effector-triggered necrosis[J]., 2016, 26(18): 2399-2411.

[62] Fang H, Shen S Q, Wang D, Zhang F, Zhang C Y, Wang Z X, Zhou Q Q, Wang R Y, Tao H, He F, Yang C K, Peng M, Jing X Y, Hao Z Y, Liu X L, Luo J, Wang G L, Ning Y S. A monocot-specific hydroxycinnamoyl- putrescine gene cluster contributes to immunity and cell death in rice[J]., 2021, 66(23): 2381-2393.

[63] Fang H, Zhang F, Zhang C Y, Wang D, Shen S Q, He F, Tao H, Wang R Y, Wang M, Wang D B, Liu X L, Luo J, Wang G L, Ning Y S. Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to[J]., 2022, 49(8): 776-786.

[64] Zhang F, Fang H, Wang M, He F, Tao H, Wang R Y, Long J W, Wang J Y, Wang G L, Ning Y S. APIP5 functions as a transcription factor and an RNA-binding protein to modulate cell death and immunity in rice[J]., 2022, 50(9): 5064-5079.

[65] He Y, Li L Y, Shi W B, Tan J H, Luo X X, Zheng S Y, Chen W T, Li J, Zhuang C X, Jiang D G. Florigen repression complexes involving rice CENTRORADIALIS2 regulate grain size[J]., 2022, 190(2): 1260-1274.

[66] Tsuji H, Nakamura H, Taoka K I, Shimamoto K. Functional diversification of FD transcription factors in rice, components of florigen activation complexes[J]., 2013, 54(3): 385-397.

[67] Kawakatsu T, Yamamoto M P, Touno S M, Yasuda H, Takaiwa F. Compensation and interaction between RISBZ1 and RPBF during grain filling in rice[J]., 2009, 59(6): 908-920

[68] Kawakatsu T and Takaiwa F. Differences in transcriptional regulatory mechanisms functioning for free lysine content and seed storage protein accumulation in rice grain[J]., 2010, 51(12): 1964-1974

[69] Wang J C, Xu H, Zhu Y, Liu Q Q, Cai X L. OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm[J]., 2013, 64(11): 3453-3466.

[70] Wu J H, Zhu C F, Pang J H, Zhang X R, Yang C L, Xia G X, Tian Y C, He C Z. OsLOL1, a C2C2-type zinc finger protein, interacts with OsbZIP58 to promote seed germination through the modulation of gibberellin biosynthesis in[J]., 2014, 80(6): 1118-1130.

[71] 喻旭, 牛向麗, 楊盛慧, 李欲翔, 劉亮亮, 唐維, 劉永勝. 過量表達(dá)轉(zhuǎn)錄因子OsbZIP60對水稻抗熱和抗旱能力的研究[J]. 中國農(nóng)業(yè)科學(xué), 2011, 44(20): 4142-4149.

Yu X, Niu X L, Yang S Hu, Li Y X, Liu L L, Tang W, Liu Y S. Research on heat and drought tolerance in rice (L.) by overexpressing transcription factor OsbZIP60 [J]., 2011, 44(20): 4142-4149. (in Chinese with English abstract)

[72] Cao R J, Zhao S L, Jiao G A, Duan Y Q, Ma L Y, Dong N N, Lu F F, Zhu M D, Shao G N, Hu S K, Sheng Z H, Zhang J, Tang S Q, Wei X J, Hu P S., encoding a transmembrane bZIP transcription factor, regulates endosperm storage protein and starch biosynthesis in rice [J]., 2022, 3(6): 100463.

[73] Kaur A, Nijhawan A, Yadav M, Khurana J P. OsbZIP62/OsFD7, a functional ortholog of FLOWERING LOCUS D, regulates floral transition and panicle development in rice[J]., 2021, 72(22): 7826-7845.

[74] Yang S Q, Xu K, Chen S J, Li T F, Xia H, Chen L, Liu H Y, Luo L J. A stress-responsive bZIP transcription factorimproves drought and oxidative tolerance in rice[J]., 2019, 19: 260.

[75] Fitzgerald H A, Canlas P E, Chern M S, Ronald P C. Alteration of TGA factor activity in rice results in enhanced tolerance topv.[J]., 2005, 43(3): 335-347.

[76] Pan T T, He M L, Liu H L, Tian X J, Wang Z Y, Yu X L, Miao X F, Li X F. Transcription factor bZIP65 delays flowering via suppressingexpression in rice[J]., 2022, 42(10): 63.

[77] Hobo T, Kowyama Y, Hattori T. A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription[J]., 1999, 96(26): 15348-15353.

[78] Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T. Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors[J]., 2005, 44(6): 939-949.

[79] Wang Y, Hou Y, Qiu J, Wang H, Wang S, Tang L, Tong X, Zhang J. Abscisic acid promotes jasmonic acid biosynthesis via a ‘SAPK10-bZIP72-AOC’ pathway to synergistically inhibit seed germination in rice ()[J]., 2020, 228(4): 1336-1353.

[80] Yoon S, Lee D K, Yu I J, Kim Y S, Choi Y D, Kim J K. Overexpression of thetranscription factor enhances drought tolerance of rice plants[J]., 2017, 11(1): 53-62.

[81] Chen Y, Shen J, Zhang L, Qi H, Yang L, Wang H, Wang J, Wang Y, Du H, Tao Z, Zhao T, Deng P, Shu Q, Qian Q, Yu H, Song S. Nuclear translocation of OsMFT1 that is impeded by OsFTIP1 promotes drought tolerance in rice[J]., 2021, 14(8): 1297-1311.

[82] Zhou H, Zhang F, Zhai F C, Su Y, Zhou Y, Ge Z L, Tilak P, Eirich J, Finkemeier I, Fu L, Li Z M, Yang J, Shen W B, Yuan X X, Xie Y J. Rice GLUTATHIONE PEROXIDASE1-mediated oxidation of bZIP68 positively regulates ABA-independent osmotic stress signaling[J]., 2022, 15(4): 651-670.

[83] Cerise M, Giaume F, Galli M, Khahani B, Lucas J, Podico F, Tavakol E, Parcy F, Gallavotti A, Brambilla V, Fornara F. OsFD4 promotes the rice floral transition via florigen activation complex formation in the shoot apical meristem[J]., 2021, 229(1): 429-443.

[84] Li X, Tian X, He M, Liu X, Li Z, Tang J, Mei E, Xu M, Liu Y, Wang Z, Guan Q, Meng W, Fang J, Zhang J, Bu Q. bZIP71 delays flowering by suppressingexpression in rice[J]., 2022, 64(7): 1352-1363.

[85] Liu C T, Mao B G, Ou S J, Wang W, Liu L C, Wu Y B, Chu C C, Wang X P. OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice[J]., 2014, 84(1-2): 19-36.

[86] Liu C, Ou S, Mao B, Tang J, Wang W, Wang H, Cao S, Schl?ppi M R, Zhao B, Xiao G, Wang X, Chu C. Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates[J]., 2018, 9: 3302.

[87] Liu C, Schl?ppi M R, Mao B, Wang W, Wang A, Chu C. The bZIP73 transcription factor controls rice cold tolerance at the reproductive stage[J]., 2019, 17(9): 1834-1849.

[88] Wang S, Liu W, He Y, Adegoke T V, Ying J, Tong X, Li Z, Tang L, Wang H, Zhang J, Tian Z, Wang Y. bZIP72 promotes submerged rice seed germination and coleoptile elongation by activating ADH1[J]., 2021, 169: 112-118.

[89] Lu G, Gao C, Zheng X, Han B. Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice[J]., 2009, 229(3): 605-615.

[90] Wang B, Liu Y, Wang Y, Li J, Sun Z, Chi M, Xing Y, Xu B, Yang B, Li J, Liu J, Chen T, Fang Z, Lu B, Xu D, Babatunde K B.is involved in transcriptional gene-regulation pathway of abscisic acid signal transduction by activating rice high-affinity potassium transporter[J]., 2021, 28(3): 257-267.

[91] Sugio A, Yang B, Zhu T, White F F. Two type III effector genes ofpv.control the induction of the host genesandduring bacterial blight of rice[J]., 2007, 104(25): 10720-10725.

[92] Wang Q, Lin Q B, Wu T, Duan E C, Huang Y S, Yang C Y, Mou C L, Lan J, Zhou C L, Xie K, Liu X, Zhang X, Guo X P, Wang J, Jiang L, Wan J M.regulates seed dormancy through the abscisic acid pathway in rice[J]., 2020, 298: 110570.

[93] Niu B, Deng H, Li T, Sharma S, Yun Q, Li Q, E Z, Chen C. OsbZIP76 interacts with OsNF-YBs and regulates endosperm cellularization in rice ()[J]., 2020, 62(12): 1983-1996.

[94] Taoka K I, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri Y A, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen[J]., 2011, 476(7360): 332-335.

[95] Peng Q, Zhu C, Liu T, Zhang S, Feng S, Wu C. Phosphorylation of OsFD1 by OsCIPK3 promotes the formation of RFT1-containing florigen activation complex for long-day flowering in rice[J]., 2021, 14(7): 1135-1148.

[96] Miyamoto K, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K. Overexpression of the bZIP transcription factor OsbZIP79 suppresses the production of diterpenoid phytoalexin in rice cells[J]., 2015, 173: 19-27.

[97] Liu D, Shi S, Hao Z, Xiong W, Luo M. OsbZIP81, a homologue ofVIP1, may positively regulate JA levels by directly targetting the genes in JA signaling and metabolism pathway in rice[J]., 2019, 20(9): 2360.

[98] 劉德芳. 水稻B-bZIP轉(zhuǎn)錄因子亞家族成員OsbZIP81和OsbZIP84的功能分析[D]. 武漢: 華中農(nóng)業(yè)大學(xué), 2019.

Liu D F. Functional analysis of rice B-bZIP subfamily members OsbZIP81 and OsbZIP84[D]. Wuhan: Huazhong Agricultural University, 2019.

[99] Gao W W, Li M K, Yang S G, Gao C Z, Su Y, Zeng X, Jiao Z L, Xu W J, Zhang M Y, Xia K F. miR2105 and the kinase OsSAPK10 co-regulate OsbZIP86 to mediate drought-induced ABA biosynthesis in rice[J]., 2022, 189(2): 889-905.

[100]Zhang Y H, Gao H T, Fang J P, Wang H, Chen J Y, Li J, Dong L Y. Up-regulation oftranscription factor is involved in resistance to three different herbicides in bothand[J]., 2022, 73(19): 6916-6930.

[101]Kaneko-Suzuki M, Kurihara-Ishikawa R, Okushita-Terakawa C, Kojima C, Nagano-Fujiwara M, Ohki I, Tsuji H, Shimamoto K, Taoka K I. TFL1-like proteins in rice antagonize rice FT-like protein in inflorescence development by competition for complex formation with 14-3-3 and FD[J]., 2018, 59(3): 458-468.

[102]Wang Y, Lu Y, Guo Z, Ding Y, Ding C., a-like gene, responses to drought stress and regulates rice flowering transition[J]., 2020, 13: 70.

[103]Cai M H, Zhu S S, Wu M M, Zheng X M, Wang J C, Zhou L, Zheng T H, Cui S, Zhou S R, Li C N, Zhang H, Chai J T, Zhang X Y, Jin X, Cheng Z J, Zhang X, Lei C L, Ren Y L, Wan J M. DHD4, a CONSTANS-like family transcription factor, delays heading date by affecting the formation of the FAC complex in rice[J]., 2021, 14(2): 330-343.

[104]Xiao B, Huang Y, Tang N, Xiong L. Over-expression of agene in rice improves drought resistance under the field conditions[J]., 2007, 115(1): 35-46.

[105]Li R Q, Zheng W Y, Yang R F, Hu Q W, Ma L Y, Zhang H L. OsSGT1 promotes melatonin-ameliorated seed tolerance to chromium stress by affecting the OsABI5–OsAPX1 transcriptional module in rice[J]., 2022, 112(1): 151-171.

[106]Li R Q, Jiang M, Song Y, Zhang H L. Melatonin alleviates low-temperature stress via ABI5-mediated signals during seed germination in rice (L.)[J]., 2021, 12: 727596.

[107]Yang L J, Chen Y, Xu L, Wang J X, Qi H Y, Guo J Z, Zhang L, Shen J, Wang H Y, Zhang F, Xie L J, Zhu W J, Lü P T, Qian Q, Yu H, Song S Y. The OsFTIP6-OsHB22-OsMYBR57 module regulates drought response in rice[J]., 2022, 15(7): 1227-1242.

Research Progress in the Function of Basic Leucine Zipper (bZIP) Protein Family in Rice

HAN Cong, HE Yuchang, WU Lijuan, JIA Lili, WANG Lei, E Zhiguo*

(China National Rice Research Institute, Hangzhou 310006, China;*Corresponding author, email: ezhiguo@caas.cn)

As a largefamily of transcriptional regulators, basic leucine zipper (bZIP) proteins are widespread in eukaryotes. The bZIP proteins characteristically harbor a bZIP domain composed of two closely adjacent structural features: a DNA-binding basic region and the leucine zipper region. Annotations to eighty-nine bZIP transcription factor-encoding genes are available in therice genome, 45 of which are identified. They are involved in regulating rice growth and development and responses to biotic and abiotic stress, including seed dormancy and germination, floral transition, and photomorphogenesis, andstress and hormone signaling pathway, etc.

rice; basic leucine zipper protein; bZIP transcription factor; gene function

10.16819/j.1001-7216.2023.221018

2022-11-17；

2023-02-02。

浙江省自然科學(xué)基金探索項目(LY21C130004)；中央級公益性科研院所基本科研業(yè)務(wù)費專項(CPSIBRF-CNRRI-202202)；中國農(nóng)業(yè)科學(xué)院科技創(chuàng)新工程資助項目(CAAS-ASTIP-2021-CNRRI)。