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

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;*通信聯系人,email: ezhiguo@caas.cn)

堿性亮氨酸拉鏈（basic leucine zipper, bZIP）是一類重要的轉錄調控因子，廣泛存在于真核生物中，因含有高度保守的bZIP結構域而得名。bZIP結構域由緊密相鄰的堿性區域和亮氨酸拉鏈區域兩部分組成。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，它們參與調節水稻生長發育、生物與非生物脅迫應答，包括種子休眠和萌發、成花轉變、光形態建成，以及脅迫和激素信號通路等。

水稻；堿性亮氨酸拉鏈蛋白；bZIP轉錄因子；基因功能

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

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%，產量接近糧食總產量的31.2%[2]。然而，水稻在種植過程中極易遭受惡劣環境影響和病蟲害襲擊，造成減產和品質下降，嚴重威脅糧食安全。因此，水稻的生長發育和脅迫抗性機制，一直是農學與生物學研究的熱點。本文對水稻bZIP轉錄因子的研究進展進行綜述，旨在為水稻功能基因組學研究提供參考。

1 bZIP蛋白結構

bZIP蛋白因含有一個保守的bZIP結構域而得名。在bZIP蛋白分子結構上（如圖1-A所示），bZIP域分為兩個緊密相鄰的部分，一個是堿性區域（藍色），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合DNA的N-X7-R/K基序；第二個是亮氨酸拉鏈區（灰色），由7個氨基酸殘基組成一個重復單位，亮氨酸或相關疏水氨基酸位于第7位，重復單元的數量則從3個到8個不等[3]。每個bZIP結構域形成一個連續的α螺旋，兩個bZIP蛋白的α螺旋因側鏈疏水性交錯對插，形成拉鏈結構（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進化樹等生物信息學分析，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結構域示意圖, 由堿性DNA結合區(藍色)和相鄰的亮氨酸拉鏈區(灰色)組成; B―bZIP二聚體的結構模型。

2 bZIP蛋白調控水稻生長發育

2.1 bZIP蛋白調控水稻成花轉變

成花素Hd3a和RFT1與14-3-3蛋白GF14c互作，形成復合物轉至核內，與轉錄因子OsFD1(即OsbZIP77)結合形成三元成花素激活復合物(florigen activation complex, FAC)，誘導表達，從而分別在短日照和長日照下啟動水稻的成花轉變[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植株均表現為遲抽穗。轉錄因子Ehd1能誘導成花素基因和表達，形成FAC，而FAC又能進一步增強表達[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合物在葉中能抑制表達，在頂端分生組織(SAM)中能抑制表達，從而推遲水稻的成花轉變[14]。研究還發現，HBF2(即OsbZIP09)在葉中的功能與HBF2冗余，也能抑制表達[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轉錄因子DHD4，能與14-3-3競爭性結合OsFD1，干擾OsFD1與14-3-3的互作，從而影響FAC的形成，導致和的表達量降低，最終延遲開花[103]。

OsRE1(即OsbZIP01)[7]、OsABF1(即OsbZIP12)[21]、OsbZIP65[76]和OsbZIP71[84]均負調控水稻的成花轉變。OsRE1、OsbZIP65和OsbZIP71各自能直接結合到的啟動子區并抑制其表達；OsABF1則是通過激活表達，間接抑制表達。過表達、或的轉基因植株均表現出晚花表型，而突變體和表現為早花表型。因OsABF1功能與OsbZIP40冗余，單突抽穗期無顯著變化，但利用RNAi同時敲減和會導致明顯的早花表型。OsRIP1能與OsRE1協作，通過精細調節的表達對抽穗期進行微調。

2.2 bZIP蛋白調控水稻種子休眠與萌發

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

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ABA缺失時，蛋白磷酸酶OsPP2C30或OsPP2C51與激酶SAPK2在核中互作形成復合體；ABA存在時，ABA受體OsPYL/RCAR5與OsPP2C30、OsPP2C51結合，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蛋白則進一步結合ABA應答元件(ABA-responsive elements, ABREs)，誘導ABA應答基因如、和等表達，抑制種子萌發[15-16]。OsPP2C51在蛋白水平上能對OsbZIP10去磷酸化使其失活[15]，AP2轉錄因子OsSAE1在轉錄水平上直接抑制的表達[17]，因此，OsPP2C51和OsSAE1都能促進水稻種子萌發。此外，GF14h能與OsbZIP10互作降低其轉錄活性，而OsMFT2又能與OREB1-GF14h形成三元復合物，并破除GF14h對OsbZIP10的抑制作用[18]。類似地，TRAB1(OsbZIP66)與ABREs特異結合，并依賴于OsVP1調節ABA誘導的轉錄，控制水稻胚的成熟與休眠[77]。SAPK10能磷酸化OsbZIP66并將其激活[78]。研究還發現，OsbZIP23、OsbZIP66和OsbZIP72這三者在促進中花11種子休眠中的作用冗余，它們均正調控ABA應答基因表達，抑制水稻種子萌發；OsMFT2能分別與這3個bZIP轉錄因子互作，增強它們與啟動子的結合[37]。過表達能清除敲除株系穗發芽的表型[37]；雙突材料的種子萌發提早，對ABA敏感性下降[79]。OsbZIP75和OsbZIP78能直接與啟動子結合誘導其表達，OsDOG1L-3進一步上調ABA合成和信號傳導相關基因表達，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轉錄因子

(+)和(-)分別代表正調控和負調控。

有研究發現，ABA對種子萌發的抑制效應部分依賴于JA生物合成。SAPK10能磷酸化修飾OsbZIP72并增強其穩定性，磷酸化修飾增強了bZIP72結合JA合成途徑關鍵基因啟動子的能力，促進后者轉錄，從而提高內源JA水平并抑制種子萌發。外施JA合成抑制劑可緩解ABA對種子萌發的抑制也證實了這一點[79]。在過表達的轉基因水稻中，茉莉酸水平也上調，這可能是因為OsbZIP81.1直接激活了基因表達所致[97]。

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

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

有意思的是，如上文所述，OsbZIP10、OsbZIP23和OsbZIP72正調控ABA信號抑制種子萌發[15, 37]，但在褪黑素、加速老化或淹水等非常規處理過程中，又能提高種子活力，表現出與常規條件下相反的作用。如低溫和鉻離子毒害會抑制種子萌發，而褪黑素處理能恢復種子活力。研究發現，OsbZIP10能增強褪黑素改善低溫和鉻離子脅迫下種子萌發的作用，褪黑素處理下，OsbZIP10通過直接上調過氧化氫酶基因和抗壞血酸過氧化物酶基因的表達，增加赤霉素合成，促進H2O2清除，從而提高低溫和絡離子毒害下的發芽率[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，內源ABA含量增加促進表達，OsbZIP23進而激活下游靶標過氧化物還原酶基因表達，PER1A通過清除種子內活性氧正調控種子活力。突變體和種子中的H2O2含量均顯著高于野生型，而過表達的Kasalath種子在加速老化處理15或18 d后發芽率顯著高于對照[38]。該研究還發現OsbZIP42正調控水稻種子活力，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，隨后產生更多參與酒精發酵和糖酵解途徑的NAD+、NADH和ATP，提供必要的能量儲備，促進水稻種子萌發和胚芽鞘伸長[88]。

2.3 bZIP蛋白調控水稻胚乳發育

粒重是決定水稻產量的重要性狀，轉錄因子OsbZIP47參與調控水稻粒形和粒重。過表達的轉基因植株籽粒細長，而突變體籽粒變寬。研究發現CC類谷氧還蛋白WG1能與OsbZIP47直接互作，并招募轉錄共抑制子ASP1來抑制OsbZIP47的轉錄活性；而E3泛素連接酶GW2可以泛素化WG1，并調控WG1的蛋白穩定性。因此，GW2-WG1-OsbZIP47構成了一個調控水稻種子發育的通路[53]。

OsCEN2-GF14f-OsFD2(即OsbZIP55)是另一個調控水稻籽粒發育的模塊。實驗表明OsCEN2能與GF14f發生互作，而GF14f能直接與OsFD2互作，OsFD2則通過控制穎殼中的細胞生長和分裂來影響水稻籽粒大小[65]。OsFD2還調控水稻葉片的發育，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]。研究還發現，OsbZIP58能直接與6個淀粉合成基因、、、、和的啟動子結合，調節其表達，從而調節胚乳中淀粉的生物合成。突變體種子形態異常，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自身無轉錄激活活性，但它能分別與核因子Y家族轉錄因子OsNF-YB1和OsNF-YB9互作，調控水稻胚乳發育，共同參與儲藏物質積累。突變體的胚乳細胞化進程提前，表現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蛋白調控水稻其他組織發育

發育良好的根系對于水稻有效吸水至關重要，特別是在干旱環境中。編碼OsbZIP01，其突變通過抑制生長素信號促進水稻根系發育。突變體的種子根伸長加快，此外，與野生型相比，短而細的側根數減少，而長而粗的側根數增加[8]。此外，ABL1(即OsbZIP46)通過影響含ABRE元件基因實現對ABA和生長素應答的雙重調控，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相關基因的表達量發生改變，且的表達能恢復擬南芥突變體的ABA 敏感性[52]。

支鏈氨基酸和5-羥色胺在植物生長發育方面發揮著重要作用。OsbZIP18通過直接與支鏈氨基酸生物合成基因和的啟動子結合，正調控支鏈氨基酸的合成[27]。OsbZIP18還能直接與、和的啟動子結合并激活表達，促進5-羥色胺的生物合成，5-羥色胺積累導致植株矮小、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)還能促進水稻在藍光下的光形態建成[29]。

OsbZIP48在光調節的發育中發揮多種作用，過表達全長的轉基因水稻，細胞分裂素水平升高，綠色期更長，半矮稈，節間長度和穗長縮短，莖稈薄；RNAi株系和T-DNA插入突變體表現為幼苗致死[54]。OsHY5(即OsbZIP48)還能與OsBBX14協同作用，直接激活或表達，精細調控花青素生物合成[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]。

OsbZIP84參與調控細胞伸長。上調表達導致植株變高，而表達量下調導致植株變矮，且這種矮化是由細胞變短造成。OsbZIP84可能通過調控赤霉素代謝路徑中的合成調控胞內赤霉素的含量，并進一步調控水稻的生長發育[98]。

3 bZIP蛋白調控水稻非生物脅迫應答

非生物脅迫是一種廣泛存在的環境脅迫，包括干旱、水澇、高溫、低溫、高鹽、重金屬和輻射等，嚴重威脅農作物生產。ABA是植物應答非生物脅迫的主要激素。環境脅迫能促進植物體內快速合成脫落酸，并激活ABA信號通路應答脅迫，從而增強植物的抗性[30]。bZIP轉錄因子被磷酸化激活后，通過與基因啟動子中ABREs結合，參與ABA介導的轉錄調控。

3.1 bZIP蛋白調控水稻高低溫脅迫應答

脫落酸和低溫能誘導OsbZIP73表達，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運到花粉，提高了水稻結實率和產量；此外，bZIP73Jap:bZIP71還正調控qLTG3-1的表達，而qLTG3-1過表達株系的生殖期耐寒性大大提高[87]。(即)和(即)的表達分別受低溫脅迫誘導和抑制。LIP19 沒有bZIP蛋白常見的同源二聚化和結合DNA的能力，但LIP19能與OsOBF1互作形成異源二聚體，且這種結合比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大量表達并形成同源二聚體結合到六聚體基序ACGTCA上從而誘導目標基因的表達；隨著溫度降低，OsOBF1 表達量下降而LIP19 表達量上升，至5℃時，LIP19大量表達而OsOBF1表達很低，LIP19和OsOBF1互作形成異源二聚體并結合到G/C序列上從而誘導耐冷性基因表達[45]。

內質網(endoplasmic reticulum, ER)內腔中未折疊或錯折疊蛋白的積累會導致ER脅迫，并引發未折疊蛋白反應(unfolded protein response, UPR)，包括減少翻譯以緩解新生蛋白質折疊的需求，降解未折疊蛋白以減輕損傷，增加細胞伴侶蛋白表達以協助蛋白質折疊。ER脅迫傳感因子IRE1通過介導一些特異響應ER脅迫的關鍵轉錄因子mRNA的非典型剪接，誘導它們的激活[57-58]。OsbZIP50(也稱)在水稻胚乳發育過程中通過激活分子伴侶基因表達，影響種子貯藏蛋白和淀粉的積累[59]。研究發現，常規剪接下，蛋白不能轉入細胞核，但ER脅迫或高溫脅迫下，mRNA保守的雙莖環結構被剪接，新產生的蛋白丟失了跨膜區，變成具有轉錄活性的核定位形式，從而將脅迫信號從內質網傳遞到細胞核，并調控脅迫應答基因表達。OsbZIP39功能和作用方式與OsbZIP50類似[46]。NAC轉錄因子OsNTL3能從質膜遷移到細胞核，直接與啟動子結合并調控其表達[60]。過表達UPR響應基因、、和導致不同程度堊白，說明UPR反應會促進堊白形成。進一步研究發現，OsbZIP60 (OPAQUE3)能通過維持胚乳發育過程中內質網穩態來抑制過度激活，進而保證胚乳正常發育[59]。OsbZIP60在熱脅迫和干旱脅迫應答中也具有重要作用，過量表達能增強水稻的抗熱和抗旱能力[71]。OPAQUE3在水稻胚乳發育，特別是高溫脅迫下胚乳的正常發育中起著核心的調控作用。自然高溫環境下，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、谷蛋白含量顯著降低，千粒重和單株產量均顯著降低[72]。

3.2 bZIP蛋白調控水稻干旱和鹽脅迫應答

干旱、鹽和脫落酸處理能改變(、、和的表達水平，表明參與依賴ABA的干旱和高鹽信號通路。過表達、或的轉基因水稻，顯著提高了對干旱和鹽脅迫的耐受性；而突變體、表現相反[22-23, 31-33, 85]。研究發現OsSAPK10能與OsbZIP20互作并將其磷酸化激活，OsbZIP20進而與啟動子的ABRE元件結合并誘導其轉錄，從而增強水稻的干旱和鹽脅迫抗性[31]。OsbZIP23與組蛋白修飾協同調控水稻脫水蛋白基因表達，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，脫水蛋白基因表達水平增加，而OsbZIP23與脫水蛋白基因啟動子的結合能力也提高；相反，突變體中的H3K4me3修飾和脫水蛋白基因表達水平均下調[34]。而SUMO蛋白酶OsOTS1能對OsbZIP23直接去SUMO化，影響其穩定性，從而負調控ABA依賴的干旱應答基因表達[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又通過正調控和的表達，對ABA的信號轉導和生物合成進行反饋調節(圖2)[36]。過表達導致水稻對ABA敏感性降低，轉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-環氧類胡蘿卜素雙加氧酶是控制ABA合成的關鍵酶。與OsbZIP23類似，OsbZIP86能與啟動子結合，在干旱條件下激活表達，通過上調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，正調控水稻對鹽和干旱脅迫的耐受性。與野生型相比，過表達的轉基因水稻限制了活性氧的積累，表現出更高的存活率和更有利的滲透參數[9-10]。

圖2?OsbZIP23參與調控ABA信號通路.

OsABF2(OsbZIP46)也是ABA 信號和非生物脅迫的正調控因子，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 結構域對激活活性有負效應。因此，過量表達對耐旱性沒有正效應，但過表達(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共抑制復合物互作來抑制OsbZIP46活性，下調OsbZIP46靶基因的組蛋白乙酰化水平；并通過與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結構域通過與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結合因子，在干旱脅迫應答中作為轉錄激活因子發揮正調控作用。如晚期胚胎富集蛋白基因正調控水稻的耐旱性，且不影響產量[104]；OsbZIP66和OsbZIP72通過直接與的啟動子結合，上調表達水平，從而正調控水稻耐旱性[81, 89]。OsMFT1作為輔助激活因子能協調并增強OsbZIP66活性[81]。與野生型相比，干旱處理數天再復水后，過表達、、或的轉基因水稻幼苗對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運蛋白基因的表達，參與ABA信號通路介導的耐鹽途徑[90]。

也有bZIP蛋白負調控水稻的干旱和鹽脅迫應答。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，表明負調控水稻的耐旱性[13]。水稻中過量表達后對鹽脅迫高度敏感，而抑制表達則提高了耐鹽性，但同時導致育性降低[17, 19]。

3.3 bZIP蛋白調控其他非生物脅迫應答

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能上調表達，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，形成分子內二硫鍵，進而激活OsbZIP68。GPX1和OsbZIP68之間的二硫鍵交換誘導OsbZIP68形成同源四聚體，從而通過調節滲透應答基因的表達調節滲透脅迫反應[82]。

OsbZIP88參與調控水稻對3種不同類型除草劑的抗性，過表達的轉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蛋白調控水稻生物脅迫應答

APIP5(即OsbZIP53)形成同源二聚體，與真菌效應子AvrPiz-t在細胞質中互作，AvrPiz-t能特異性抑制APIP5的轉錄活性。當宿主沒有Piz-t時，AvrPiz-t通過作用于APIP5，增強效應子觸發的壞死，幫助稻瘟菌進入死體營養階段。當宿主包含Piz-t時，Piz-t通過與APIP5互作，穩定APIP5蛋白積累以阻止細胞壞死的發生，從而抑制稻瘟菌從活體營養階段過渡到死體營養階段[61]。除此，APIP5還有多種調控防衛反應的機制。APIP5能直接與羥基肉桂酰基轉移酶基因/、、和的啟動子結合，抑制它們的轉錄，負調控酚胺代謝物和木質素積累[62-63]。APIP5也能結合到細胞壁相關激酶基因和細胞色素P450基因的啟動子上，抑制二者的表達；OsWAK5調節木質素積累，CYP72A1調控植保素合成和活性氧迸發，兩者均正調控水稻基礎免疫反應。有趣的是，APIP5能發生質核穿梭，并有RNA結合活性，稻瘟病菌侵染促使其在胞質RNA加工小體中富集，與細胞死亡和防衛相關基因和的3' UTR的poly(U)序列特異結合，促進和的mRNA降解，從而在轉錄后水平調控水稻基礎免疫反應[64]。

白葉枯病抗性。研究發現白葉枯病菌Ⅲ型效應子基因誘導表達，而的異位表達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制，正調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。OsTGAP1OsbZIP37能上調效應子誘發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蛋白是重要的轉錄因子，通過突變體表型分析、基因敲除(低)或過表達等技術，已從水稻中鑒定了45個bZIP 轉錄因子(表1)。它們廣泛參與調控水稻各器官組織的發生發育、病蟲害抗性和非生物脅迫應答等生物學過程。但是，這些進程的調節不是孤立的，需要上下游多個調控因子的參與。如我們發現OsbZIP76自身無轉錄激活活性，但它能分別與核因子Y家族轉錄因子OsNF-YB1和OsNF-YB9互作，調控水稻胚乳發育，共同參與儲藏物質積累[93]。另外，多個信號間往往形成交叉，相互影響，而部分bZIP蛋白扮演中心節點的作用，如 OsbZIP12正調整水稻的耐鹽耐旱性，也調節種子萌發、抽穗期以及D-阿洛糖誘導的生長抑制[21-25]，OsbZIP23/66/72既促進種子休眠，也調控干旱脅迫應答，以及多種脅迫下種子萌發(圖2)[37, 107]。因此，bZIP蛋白家族對水稻的生長發育和脅迫應答調控是復雜的，每個bZIP轉錄因子都扮演了調控網絡中的一個或多個節點，我們仍需要通過鑒定更多的bZIP蛋白及其互作因子，為最終繪制出整個遺傳網絡填上一塊塊拼圖。

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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。

浙江省自然科學基金探索項目(LY21C130004)；中央級公益性科研院所基本科研業務費專項(CPSIBRF-CNRRI-202202)；中國農業科學院科技創新工程資助項目(CAAS-ASTIP-2021-CNRRI)。