光敏色素的生物學(xué)功能及其調(diào)控

張?jiān)姁?，?娟,2，蘭海燕

(1.新疆大學(xué) 生命科學(xué)與技術(shù)學(xué)院，新疆生物資源基因工程重點(diǎn)實(shí)驗(yàn)室，烏魯木齊 830046；2.新疆農(nóng)業(yè)科學(xué)院經(jīng)濟(jì)作物研究所，烏魯木齊 830091)

光敏色素的生物學(xué)功能及其調(diào)控

張?jiān)姁?，王 娟1,2，蘭海燕1

(1.新疆大學(xué) 生命科學(xué)與技術(shù)學(xué)院，新疆生物資源基因工程重點(diǎn)實(shí)驗(yàn)室，烏魯木齊 830046；2.新疆農(nóng)業(yè)科學(xué)院經(jīng)濟(jì)作物研究所，烏魯木齊 830091)

光是影響植物生長(zhǎng)發(fā)育的重要因素，植物為感受光而進(jìn)化出光受體。光受體分為4類，其中光敏色素研究較為深入，它是紅光和遠(yuǎn)紅光受體，在光形態(tài)建成過程中發(fā)揮著重要作用。近年來的研究闡明了光敏色素的作用模式，以及由其介導(dǎo)的光信號(hào)轉(zhuǎn)導(dǎo)途徑和植物發(fā)育調(diào)節(jié)過程，如下胚軸延伸、莖分支、生物鐘及開花時(shí)間控制等?；谀壳暗难芯靠偨Y(jié)光敏色素的生物學(xué)功能及其介導(dǎo)的光信號(hào)轉(zhuǎn)導(dǎo)途徑，并展望其研究前景，以期為相關(guān)領(lǐng)域研究提供參考。

光敏色素; 光信號(hào)途徑; 生物學(xué)功能; 調(diào)控

植物在整個(gè)生命周期中一直處于變化的光環(huán)境下，光質(zhì)、光強(qiáng)及輻照度的改變均對(duì)植物生長(zhǎng)發(fā)育產(chǎn)生影響[1]。在長(zhǎng)期進(jìn)化過程中，植物在適應(yīng)光環(huán)境變化的同時(shí)，還能相互影響改變微生境，即植物能感受光信號(hào)也能產(chǎn)生光信號(hào)。光信號(hào)參與調(diào)控種子萌發(fā)、幼苗脫黃化、生物鐘節(jié)律和開花時(shí)間等生理過程[2]。植物通過不同種類光受體(photoreceptors)感知光的方向、波長(zhǎng)、強(qiáng)度以及光周期等信號(hào)，從而調(diào)控體內(nèi)相關(guān)基因的表達(dá)，光敏色素(phytochrome，phy)是目前研究最為深入的光受體，其生理作用非常廣泛，植物從種子萌發(fā)到開花、結(jié)果及衰老均受其影響[3]。

1 光敏色素的結(jié)構(gòu)和分類

1.1 光敏色素的發(fā)現(xiàn)

光敏色素是植物體內(nèi)普遍存在的紅光/遠(yuǎn)紅光受體。Flint等[4]首次發(fā)現(xiàn)紅光能促進(jìn)而遠(yuǎn)紅光則抑制種子萌發(fā)。隨后Butler等[5]發(fā)現(xiàn)在紅光/遠(yuǎn)紅光照射下蛋白提取液的吸收光譜有顯著差異。1960年植物學(xué)家Borthwick和物理化學(xué)家Hendricks將其正式命名為光敏色素[6]。

1.2 光敏色素的結(jié)構(gòu)特征

光敏色素是一種易溶于水的色素蛋白質(zhì)，相對(duì)分子質(zhì)量為2.5×105。一個(gè)光敏色素單體包含1個(gè)線性四吡咯生色團(tuán)和1個(gè)脫輔基蛋白分子，蛋白分子由2個(gè)分子質(zhì)量在120～127 ku 的多肽聚合而成。如圖1所示，光敏色素由2個(gè)結(jié)構(gòu)域構(gòu)成：一個(gè)是位于N末端的分子質(zhì)量為70 ku 的光感受域，另一個(gè)是 C 末端的分子質(zhì)量為 55 ku 的光調(diào)節(jié)域[7]。光敏色素中光感受區(qū)包括多個(gè)亞結(jié)構(gòu)域。在天然狀態(tài)下，光敏色素通過 C 末端的氨基酸殘基聚合成二聚體[8]。生色團(tuán)與高度保守的 GAF(cGMP-specific phosphodiesterase/adenylate cyclases/formate hydrogen lyase transcription)區(qū)域相結(jié)合，當(dāng)紅光或遠(yuǎn)紅光照射時(shí)，生色團(tuán)的線性四吡咯環(huán)發(fā)生光質(zhì)異構(gòu)化，從而形成紅光吸收型或遠(yuǎn)紅光吸收型光敏色素[9]。PHY(Phytochrome domain)區(qū)域緊鄰 GAF 區(qū)域的 C 端，是保持吸收光譜完整所必需的組分[10]。光調(diào)節(jié)區(qū)含有2個(gè) PAS(period circadian protein homolog 1 / aryl hydrocarbon nuclear translocator /single-minded gene)同源重復(fù)序列和1個(gè)組氨酸激酶相關(guān)結(jié)構(gòu)域HKRD(Histidine-kinase-related domain)，此結(jié)構(gòu)在光信號(hào)轉(zhuǎn)導(dǎo)中發(fā)揮重要作用[11]。

1.3 光敏色素的分類

光敏色素在植物中的存在和作用并不單一。1989年Sharrock和Quail首次獲得直接證據(jù)證明存在多種光敏色素基因[12]。隨后，Clack等[13]獲得光敏色素D(phyD)、光敏色素E(phyE)基因的序列。在玉米、水稻以及小麥中存在3類光敏色素，在松樹和銀杏中分別存在4種和3種光敏色素[9,14-16]。研究表明，光敏色素家族最早形成2個(gè)分支，其中一支很快分成光敏色素 A(phyA)和光敏色素C(phyC)，另一分支分為光敏色素 B(phyB)和phyE[11]。phyE在某些類群(如單子葉植物)中丟失，而phyD 則起源于phyB最近的一次基因復(fù)制事件[11]。不同種類光敏色素基因的進(jìn)化速率也不同，phyA、phyB 較保守，而phyC、phyE 的進(jìn)化速率是phyA、phyB 的1 133倍[17]。

光敏色素按其在光下的狀態(tài)可分為2類：光不穩(wěn)定型(如phyA)和光穩(wěn)定型(如phyB-phyE等)。其在植物中有2種存在形式，分別是紅光吸收型(Pr)和遠(yuǎn)紅光吸收型(Pfr)。一般把吸收紅光的光敏色素稱為Pr型光敏色素，其吸收紅光后即轉(zhuǎn)變成吸收遠(yuǎn)紅光的Pfr型光敏色素。在黑暗條件下，Pfr會(huì)逆轉(zhuǎn)為Pr，Pfr 濃度降低并被蛋白酶降解[18]。光敏色素主要有3種反應(yīng)方式，極低輻照度反應(yīng)(VLFR)、低輻照度反應(yīng)(LFR)和強(qiáng)輻射反應(yīng)(HIR)。不同種類光敏色素的反應(yīng)方式各不相同，其中phyA主要調(diào)節(jié)VLFR和HIR，phyB 則調(diào)節(jié) LFR[19]。

N端: N-terminus; 光感受區(qū): Photoreception region, 包括NTE. N-terminal extension, PAS. period circadian protein homolog 1 / aryl hydrocarbon nuclear translocator /single-minded gene; GAF: cGMP-specific phosphodiesterase/adenylate cyclases/formate hydrogen lyase transcription, PHY: Phytochrome domain; 光調(diào)節(jié)區(qū): Light regulatory region, 包括PAS1和PAS2: PAS (period circadian protein homolog 1 / aryl hydrocarbon nuclear translocator /single-minded gene) -related domains, HKRD: Histidine-kinase-related domain; 生色團(tuán): Chromophore; C端: C-terminus.

2 光敏色素的生物學(xué)功能

光敏色素感受光信號(hào)并參與調(diào)控的生理反應(yīng)包括種子萌發(fā)、幼苗光形態(tài)建成、避蔭作用、開花時(shí)間和晝夜節(jié)律響應(yīng)等[7](表1)。此外，近年研究還發(fā)現(xiàn)，光敏色素參與調(diào)控植物對(duì)非生物脅迫的抗性應(yīng)答[8]。

2.1 在種子萌發(fā)中的功能

Borthwick等[20]的研究首次證明紅光/遠(yuǎn)紅光受體能調(diào)節(jié)種子萌發(fā)。對(duì)擬南芥突變體的研究表明，至少有 3 種光敏色素(phyA、phyB、phyE)參與擬南芥種子萌發(fā)的調(diào)控。phyA在不同波長(zhǎng)的光照(紫外線、可見光和遠(yuǎn)紅光)下調(diào)控不可逆轉(zhuǎn)的VLFR反應(yīng)，而phyB則調(diào)控紅光/遠(yuǎn)紅光受體的LFRs反應(yīng)，2種反應(yīng)均能促進(jìn)種子萌發(fā)[21]。此外，在連續(xù)遠(yuǎn)紅光及強(qiáng)輻射條件下，phyA能促進(jìn)種子萌發(fā)[22]。phyE可能直接參與遠(yuǎn)紅光的光受體響應(yīng)，或協(xié)助phyA調(diào)控種子萌發(fā)[22]。有趣的是，環(huán)境溫度參與擬南芥種子萌發(fā)的光調(diào)控，不同光敏色素在溫度變化條件下其功能會(huì)相應(yīng)改變[23]。

2.2 幼苗去黃化

黑暗下生長(zhǎng)的幼苗發(fā)生黃化，且下胚軸伸長(zhǎng)、子葉不展開、原質(zhì)體發(fā)育成白色體。而光下幼苗則發(fā)生去黃化反應(yīng)，植株形態(tài)正常且原質(zhì)體發(fā)育為成熟的葉綠體。不同光敏色素(除phyE外)在幼苗去黃化過程中均起到一定作用[24]。

在白光和紅光下，phyA 缺失突變體表現(xiàn)為野生型光形態(tài)建成表型；而在連續(xù)遠(yuǎn)紅光照射時(shí)，該突變體表現(xiàn)為暗形態(tài)建成表型，表明 phyA 是感知和調(diào)節(jié)遠(yuǎn)紅光反應(yīng)的主要光受體[25]。此外，試驗(yàn)證明 phyA 在紅光處理下的快速調(diào)控基因表達(dá)響應(yīng)中起重要作用[26]。phyB 是主要調(diào)控去黃化的光敏色素。但紅光處理后，phyB 缺失突變體和野生型在轉(zhuǎn)錄水平表達(dá)差異不顯著[27]；phyA/phyB 雙突變體與 phyB 單突變體相比，下胚軸明顯增長(zhǎng)且子葉擴(kuò)張減少，進(jìn)一步揭示 phyA 在紅光下的作用。

在紅光照射下，phyC 也能調(diào)控幼苗去黃化反應(yīng)[28]。但 phyC/phyD 雙突變體表型與單突變體表型間無(wú)明顯差異；在遠(yuǎn)紅光下，phyC 則不能調(diào)控幼苗去黃化反應(yīng)[29]。

此外，phyD 在紅光下也能獨(dú)自調(diào)控幼苗去黃化作用[25]。而 phyE 在此過程中的作用則極其微弱。

2.3 避蔭反應(yīng)

植物發(fā)育的調(diào)控不僅跟光暗有關(guān)，還受光質(zhì)量的影響，特別是由其他植物的陰影帶來的光質(zhì)量變化[30]。因此，植物啟動(dòng)另一種策略即避蔭反應(yīng)，包括莖和葉柄的伸長(zhǎng)，開花時(shí)間提前，頂端優(yōu)勢(shì)增加等[30]。

phyB 是大多數(shù)避蔭反應(yīng)的光受體，而 phyA 是避蔭環(huán)境中光照輻照度變化的敏感感受器。根據(jù)對(duì)突變體的研究顯示，phyD 和 phyE 幫助 phyB 參與避蔭反應(yīng)。

表1 不同種光敏色素在植物生長(zhǎng)發(fā)育及應(yīng)對(duì)逆境脅迫中的作用

3 光敏色素的調(diào)控

目前，已知光信號(hào)轉(zhuǎn)導(dǎo)途徑的相關(guān)基因根據(jù)其作用可分為3類：

第1類，參與光敏色素核定位。光敏色素入核是其發(fā)揮作用、調(diào)控光信號(hào)的關(guān)鍵步驟。但不同光敏色素的核內(nèi)定位機(jī)制各不相同[45-46]。早期研究[47-48]顯示，持續(xù)照射紅光和藍(lán)光能有效誘導(dǎo)phyB-phyE 轉(zhuǎn)移到細(xì)胞核內(nèi)，并可以通過遠(yuǎn)紅光照射逆轉(zhuǎn)。近年來研究發(fā)現(xiàn)在由黑暗過渡到遠(yuǎn)紅光照射時(shí)，phyB 也能快速移位至細(xì)胞核內(nèi)[49]，與早期結(jié)果矛盾，其潛在原因仍需進(jìn)一步研究。與 phyB-phyE 不同，phyA 入核不僅需要光信號(hào)，還需要2個(gè)同源伴侶蛋白協(xié)助，即FHY1(Far-red elongated hypocotyl 1)和FHL(fhy1 like)[48, 50-51]。陳芳等[52]研究發(fā)現(xiàn)，F(xiàn)HY1是幫助phyA入核、轉(zhuǎn)錄因子互作、結(jié)合基因啟動(dòng)子等的輔助蛋白。Lin等[53]發(fā)現(xiàn)擬南芥中2種光反應(yīng)關(guān)鍵蛋白：FHY3( far-red elongated hypocotyl3)和FAR1(Far-red impaired response1)，兩者通過直接激活 FHY1/FHL基因的表達(dá)來共同調(diào)控 phyA 在核內(nèi)的積累。Genoud等[54]研究發(fā)現(xiàn)細(xì)胞核內(nèi)組成型的 phyA 彌補(bǔ)fhy3突變體的表型。擬南芥 phyA 這種特殊的入核調(diào)控方式可能與其適應(yīng)性進(jìn)化有關(guān)[55]。其他物種不同光敏色素的入核機(jī)理是否與擬南芥一致目前還不清楚。

第2類，參與光敏色素信號(hào)輸出。鄧興旺課題組[56-57]的遺傳試驗(yàn)篩選鑒定出一個(gè)光形態(tài)建成抑制因子，命名為COP/DET/FUS(CONSTITUTIVE PHOTOMORPHOGENESIS/DE- ETIOLATED/FUSCA)基因，這些因子的突變體在暗環(huán)境中呈現(xiàn)光形態(tài)建成表型。研究表明，HY5(ELONGATED HYPOCOTYL5)[58]、HYH(HY5 Homolog)[59]、LAF1(LONG AFTER FARRED LIGHT1)[60]以及HFR1(LONG HYPOCOTYL IN FAR-RED1)[61-63]等均促進(jìn)光形態(tài)建成蛋白的表達(dá)水平增高，進(jìn)而促進(jìn)光敏色素的活化，從而抑制 COP/DET/FUS 的活性。此外，這些因子可在植物體內(nèi)形成不同的復(fù)合體，參與泛素化途徑。其中 COP1-SPAs 復(fù)合體由 COP1及 SPAs(SUPPRESSOR OF PHYA1)家族成員構(gòu)成，其中 COP1是擬南芥光形態(tài)建成的關(guān)鍵抑制因子，在黑暗條件下，能作為E3泛素連接酶降解光形態(tài)建成的轉(zhuǎn)錄因子，但在光下 COP1活性被抑制且在核內(nèi)的豐度降低。SPAs 家族是 phyA 信號(hào)轉(zhuǎn)導(dǎo)中的另一個(gè)負(fù)調(diào)控因子，通過結(jié)合 COP1對(duì)目標(biāo)蛋白進(jìn)行水解，且作為一個(gè)共同作用因子調(diào)節(jié) COP1的功能[64]。CSN(COP9 signalosome)，由8個(gè)高度保守的不同亞基組成，是一個(gè)新的 E3泛素連接酶的調(diào)節(jié)因子，是細(xì)胞對(duì)外界刺激或脅迫產(chǎn)生響應(yīng)的調(diào)節(jié)成分[65-66]。CDD 復(fù)合體[COP10, DET1, DDB1 (DNA DAMAGE BINDING PROTEIN1)]的具體功能還不清楚。此外，光信號(hào)導(dǎo)致 COP/DET/FUS 失活的具體分子機(jī)制也有待進(jìn)一步研究。

第3類，直接調(diào)節(jié)光反應(yīng)。與光受體相互作用因子中，有一類重要的堿性螺旋環(huán)螺旋(basic helix-loop-helix, bHLH)類轉(zhuǎn)錄因子-PIFs(phytochrome interacting factor)家族蛋白，其主要功能是調(diào)節(jié)光敏色素介導(dǎo)的暗形態(tài)建成到光形態(tài)建成轉(zhuǎn)換過程中的信號(hào)轉(zhuǎn)導(dǎo)途徑[67]。目前，已知的PIFs家族成員有且僅有 PIF1和 PIF3可以與活化的 phyA 相互作用，且 PIF1與 phyA的結(jié)合能力比 PIF3強(qiáng)[68-69]。PIF3能與phyC和phyE分別形成異源二聚體[70]。研究發(fā)現(xiàn) PIF3和 phyB可以在體外結(jié)合至光響應(yīng)基因啟動(dòng)子的 G-box 區(qū)域，表明光敏色素可以將光信號(hào)直接靶向目的基因的啟動(dòng)子調(diào)控該基因表達(dá)[71-72]。研究證明，在轉(zhuǎn)錄因子 PIF3或HY5的協(xié)同作用下，phyA-FHY1復(fù)合物可以結(jié)合至編碼查爾酮合酶的CHS(CHALCONE SYNTHASE)基因啟動(dòng)子上，共同調(diào)控CHS的轉(zhuǎn)錄[73]。Chen等[74]證明在與 phyA 直接發(fā)生相互作用的靶基因啟動(dòng)子上存在大量供 PIFs 識(shí)別的順式作用元件。這一發(fā)現(xiàn)說明包括 PIFs和 HY5在內(nèi)的大量轉(zhuǎn)錄因子均能以直接或間接的方式在靶基因啟動(dòng)子上與phyA發(fā)生相互作用，對(duì)眾多下游基因進(jìn)行調(diào)控，從而對(duì)各種內(nèi)外信號(hào)作出快速反應(yīng)[75]。擬南芥其他類型的轉(zhuǎn)錄因子(如 ARR4、IAAs、ATHB23等)也能以上述方式與光敏色素發(fā)生相互作用[75-77]。此外，也有研究認(rèn)為phyB會(huì)阻礙PIFs結(jié)合至靶基因的啟動(dòng)子區(qū)域[78]，并通過一系列體外試驗(yàn)證明，PIF1和 PIF4與靶基因作用后不能與 phyB 或 phyA 同時(shí)結(jié)合[79-80]，其深層次的機(jī)理還有待進(jìn)一步試驗(yàn)證實(shí)。

基于以上分析，筆者繪制光敏色素與各相關(guān)因子互作的模式圖(圖2)。

Pr.紅光吸收型 Phytochrome red light-obsorbing form; Pfr.遠(yuǎn)紅光吸收型 Phytochrome far-red light-absorbing form; PHYA.Phytochrome A; PHYB.Phytochrome B; FHY1.Far-red elongated hypocotyl 1; PHY.Phytochrome; COP1/DET/FUS.Constitutive photomorphogenesis/de-etiolated/fusca; HY5:Long hypocotyl 5; LAF1:Long after farred light1;HFR1:Long hypocotyl in far-red1; HYH:HY5 Homolog; PIFs:Phytochrome interacting factors; CHS:Chalcone synthase; CCA1:Circadian clock-associated protein 1; ABA:Abscisic acid; CBF.CRT/DRE2 binding factor; STO.Salt tolerance protein;箭頭表示正調(diào)控作用, T型線表示負(fù)調(diào)控作用 Arrow represent positive regulation and T-type line represent negative regulation.

4 展 望

不同光敏色素的分子結(jié)構(gòu)和生理功能已得到系統(tǒng)的闡述，其信號(hào)傳導(dǎo)機(jī)制成為近年來研究的重點(diǎn)。目前，基于對(duì)光信號(hào)、溫度及多種植物內(nèi)源激素共同組成的信號(hào)網(wǎng)絡(luò)有系統(tǒng)認(rèn)識(shí)，一大批與光敏色素相互作用的因子被發(fā)現(xiàn)。但因該網(wǎng)絡(luò)的復(fù)雜性，其整體功能以及各信號(hào)分子在整個(gè)調(diào)控網(wǎng)絡(luò)中的作用還需深入研究。如何系統(tǒng)詮釋以光敏色素為中心的信號(hào)通路作用機(jī)制以及各通路間的相互關(guān)系，仍是亟待解決的關(guān)鍵問題。此外，光敏色素還是介導(dǎo)植物應(yīng)對(duì)各種非生物與生物脅迫的重要激素[32]，了解其體內(nèi)的作用方式將為培育適應(yīng)不同光環(huán)境尤其是弱光下的農(nóng)作物新品種提供有價(jià)值的理論參考依據(jù)。

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(責(zé)任編輯：顧玉蘭 Responsible editor:GU Yulan)

Biological Functions and Signaling Regulation Network of Phytochromes

ZHANG Shiyue1,WANG Juan1,2and LAN Haiyan1

(1.Xinjiang Key Laboratory of Biological Resources and Genetic Engineering,College of Life Science and Technology,Xinjiang University,Urumqi 830046,China; 2.Institute of Economic Crops,Xinjiang Academy of Agricultural Sciences,Urumqi 830091,China)

Light is essential for plant growth and development.Plants have evolved light receptors (LRs) to accept light signal.So far,four different kinds of LRs have been reported,among these,phytochromes have been well-studied,which act as red and far-red LR and play vital roles in photomorphogenesis.Currently,the action mode of phytochrome and light signal transduction pathway as well as modulation of plant development have been elucidated,e.g.the hypocotyl extension,stem branching,circadian rhythm and flowering time control,etc.In this review,we summarized the biological functions,regulation of phytochrome,and light signal transduction pathways in plant development,which may provide insight for further study in this field.

Phytochrome;Light signal pathways; Biological functions; Regulation

ZHANG Shiyue, female, master student. Research area:plant adversity molecular biology. E-mail: 496689512@qq.com

LAN Haiyan, female,Ph.D,professor.Research area:plant adversity molecular biology. E-mail:lanhaiyan@xju.edu.cn

日期：2017-05-22

2016-03-24

2016-08-08

國(guó)家自然科學(xué)基金 (31260037; 31460043); 新疆自治區(qū)優(yōu)秀青年科技人才培養(yǎng)項(xiàng)目(2013721013)；國(guó)家科技部基礎(chǔ)研究計(jì)劃973前期項(xiàng)目 (2012CB722204)。

張?jiān)姁?，女，碩士研究生，研究方向?yàn)橹参锟鼓娣肿由飳W(xué)。E-mail:496689512@qq.com

蘭海燕，女，博士，教授，研究方向?yàn)橹参锟鼓娣肿由飳W(xué)。E-mail: lanhaiyan@xju.edu.cn

Q945.43

A

1004-1389(2017)05-0657-08

網(wǎng)絡(luò)出版地址：http://kns.cnki.net/kcms/detail/61.1220.S.20170522.0856.004.html

Received 2016-03-24 Returned 2016-08-08

Foundation item National Natural Science Foundation of China(No.31260037,No.31460043);Project for Cultivating Young Talents of Xinjiang Uygur Autonomous Region (No.2013721013);Initial Project of 973 Program from the Ministry of Science and Technology of China(No.2012CB722204).