光敏色素的生物學功能及其調控

張詩悅，王 娟,2，蘭海燕

(1.新疆大學 生命科學與技術學院，新疆生物資源基因工程重點實驗室，烏魯木齊 830046；2.新疆農業科學院經濟作物研究所，烏魯木齊 830091)

光敏色素的生物學功能及其調控

張詩悅1，王 娟1,2，蘭海燕1

(1.新疆大學 生命科學與技術學院，新疆生物資源基因工程重點實驗室，烏魯木齊 830046；2.新疆農業科學院經濟作物研究所，烏魯木齊 830091)

光是影響植物生長發育的重要因素，植物為感受光而進化出光受體。光受體分為4類，其中光敏色素研究較為深入，它是紅光和遠紅光受體，在光形態建成過程中發揮著重要作用。近年來的研究闡明了光敏色素的作用模式，以及由其介導的光信號轉導途徑和植物發育調節過程，如下胚軸延伸、莖分支、生物鐘及開花時間控制等?；谀壳暗难芯靠偨Y光敏色素的生物學功能及其介導的光信號轉導途徑，并展望其研究前景，以期為相關領域研究提供參考。

光敏色素; 光信號途徑; 生物學功能; 調控

植物在整個生命周期中一直處于變化的光環境下，光質、光強及輻照度的改變均對植物生長發育產生影響[1]。在長期進化過程中，植物在適應光環境變化的同時，還能相互影響改變微生境，即植物能感受光信號也能產生光信號。光信號參與調控種子萌發、幼苗脫黃化、生物鐘節律和開花時間等生理過程[2]。植物通過不同種類光受體(photoreceptors)感知光的方向、波長、強度以及光周期等信號，從而調控體內相關基因的表達，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，植物從種子萌發到開花、結果及衰老均受其影響[3]。

1 光敏色素的結構和分類

1.1 光敏色素的發現

光敏色素是植物體內普遍存在的紅光/遠紅光受體。Flint等[4]首次發現紅光能促進而遠紅光則抑制種子萌發。隨后Butler等[5]發現在紅光/遠紅光照射下蛋白提取液的吸收光譜有顯著差異。1960年植物學家Borthwick和物理化學家Hendricks將其正式命名為光敏色素[6]。

1.2 光敏色素的結構特征

光敏色素是一種易溶于水的色素蛋白質，相對分子質量為2.5×105。一個光敏色素單體包含1個線性四吡咯生色團和1個脫輔基蛋白分子，蛋白分子由2個分子質量在120～127 ku 的多肽聚合而成。如圖1所示，光敏色素由2個結構域構成：一個是位于N末端的分子質量為70 ku 的光感受域，另一個是 C 末端的分子質量為 55 ku 的光調節域[7]。光敏色素中光感受區包括多個亞結構域。在天然狀態下，光敏色素通過 C 末端的氨基酸殘基聚合成二聚體[8]。生色團與高度保守的 GAF(cGMP-specific phosphodiesterase/adenylate cyclases/formate hydrogen lyase transcription)區域相結合，當紅光或遠紅光照射時，生色團的線性四吡咯環發生光質異構化，從而形成紅光吸收型或遠紅光吸收型光敏色素[9]。PHY(Phytochrome domain)區域緊鄰 GAF 區域的 C 端，是保持吸收光譜完整所必需的組分[10]。光調節區含有2個 PAS(period circadian protein homolog 1 / aryl hydrocarbon nuclear translocator /single-minded gene)同源重復序列和1個組氨酸激酶相關結構域HKRD(Histidine-kinase-related domain)，此結構在光信號轉導中發揮重要作用[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最近的一次基因復制事件[11]。不同種類光敏色素基因的進化速率也不同，phyA、phyB 較保守，而phyC、phyE 的進化速率是phyA、phyB 的1 133倍[17]。

光敏色素按其在光下的狀態可分為2類：光不穩定型(如phyA)和光穩定型(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，其吸收紅光后即轉變成吸收遠紅光的Pfr型光敏色素。在黑暗條件下，Pfr會逆轉為Pr，Pfr 濃度降低并被蛋白酶降解[18]。光敏色素主要有3種反應方式，極低輻照度反應(VLFR)、低輻照度反應(LFR)和強輻射反應(HIR)。不同種類光敏色素的反應方式各不相同，其中phyA主要調節VLFR和HIR，phyB 則調節 LFR[19]。

N端: N-terminus; 光感受區: 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; 光調節區: 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: Chromophore; C端: C-terminus.

2 光敏色素的生物學功能

光敏色素感受光信號并參與調控的生理反應包括種子萌發、幼苗光形態建成、避蔭作用、開花時間和晝夜節律響應等[7](表1)。此外，近年研究還發現，光敏色素參與調控植物對非生物脅迫的抗性應答[8]。

2.1 在種子萌發中的功能

Borthwick等[20]的研究首次證明紅光/遠紅光受體能調節種子萌發。對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的調控。phyA在不同波長的光照(紫外線、可見光和遠紅光)下調控不可逆轉的VLFR反應，而phyB則調控紅光/遠紅光受體的LFRs反應，2種反應均能促進種子萌發[21]。此外，在連續遠紅光及強輻射條件下，phyA能促進種子萌發[22]。phyE可能直接參與遠紅光的光受體響應，或協助phyA調控種子萌發[22]。有趣的是，環境溫度參與擬南芥種子萌發的光調控，不同光敏色素在溫度變化條件下其功能會相應改變[23]。

2.2 幼苗去黃化

黑暗下生長的幼苗發生黃化，且下胚軸伸長、子葉不展開、原質體發育成白色體。而光下幼苗則發生去黃化反應，植株形態正常且原質體發育為成熟的葉綠體。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 缺失突變體表現為野生型光形態建成表型；而在連續遠紅光照射時，該突變體表現為暗形態建成表型，表明 phyA 是感知和調節遠紅光反應的主要光受體[25]。此外，試驗證明 phyA 在紅光處理下的快速調控基因表達響應中起重要作用[26]。phyB 是主要調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錄水平表達差異不顯著[27]；phyA/phyB 雙突變體與 phyB 單突變體相比，下胚軸明顯增長且子葉擴張減少，進一步揭示 phyA 在紅光下的作用。

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

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

2.3 避蔭反應

植物發育的調控不僅跟光暗有關，還受光質量的影響，特別是由其他植物的陰影帶來的光質量變化[30]。因此，植物啟動另一種策略即避蔭反應，包括莖和葉柄的伸長，開花時間提前，頂端優勢增加等[30]。

phyB 是大多數避蔭反應的光受體，而 phyA 是避蔭環境中光照輻照度變化的敏感感受器。根據對突變體的研究顯示，phyD 和 phyE 幫助 phyB 參與避蔭反應。

表1 不同種光敏色素在植物生長發育及應對逆境脅迫中的作用

3 光敏色素的調控

目前，已知光信號轉導途徑的相關基因根據其作用可分為3類：

第1類，參與光敏色素核定位。光敏色素入核是其發揮作用、調控光信號的關鍵步驟。但不同光敏色素的核內定位機制各不相同[45-46]。早期研究[47-48]顯示，持續照射紅光和藍光能有效誘導phyB-phyE 轉移到細胞核內，并可以通過遠紅光照射逆轉。近年來研究發現在由黑暗過渡到遠紅光照射時，phyB 也能快速移位至細胞核內[49]，與早期結果矛盾，其潛在原因仍需進一步研究。與 phyB-phyE 不同，phyA 入核不僅需要光信號，還需要2個同源伴侶蛋白協助，即FHY1(Far-red elongated hypocotyl 1)和FHL(fhy1 like)[48, 50-51]。陳芳等[52]研究發現，FHY1是幫助phyA入核、轉錄因子互作、結合基因啟動子等的輔助蛋白。Lin等[53]發現擬南芥中2種光反應關鍵蛋白：FHY3( far-red elongated hypocotyl3)和FAR1(Far-red impaired response1)，兩者通過直接激活 FHY1/FHL基因的表達來共同調控 phyA 在核內的積累。Genoud等[54]研究發現細胞核內組成型的 phyA 彌補fhy3突變體的表型。擬南芥 phyA 這種特殊的入核調控方式可能與其適應性進化有關[55]。其他物種不同光敏色素的入核機理是否與擬南芥一致目前還不清楚。

第2類，參與光敏色素信號輸出。鄧興旺課題組[56-57]的遺傳試驗篩選鑒定出一個光形態建成抑制因子，命名為COP/DET/FUS(CONSTITUTIVE PHOTOMORPHOGENESIS/DE- ETIOLATED/FUSCA)基因，這些因子的突變體在暗環境中呈現光形態建成表型。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]等均促進光形態建成蛋白的表達水平增高，進而促進光敏色素的活化，從而抑制 COP/DET/FUS 的活性。此外，這些因子可在植物體內形成不同的復合體，參與泛素化途徑。其中 COP1-SPAs 復合體由 COP1及 SPAs(SUPPRESSOR OF PHYA1)家族成員構成，其中 COP1是擬南芥光形態建成的關鍵抑制因子，在黑暗條件下，能作為E3泛素連接酶降解光形態建成的轉錄因子，但在光下 COP1活性被抑制且在核內的豐度降低。SPAs 家族是 phyA 信號轉導中的另一個負調控因子，通過結合 COP1對目標蛋白進行水解，且作為一個共同作用因子調節 COP1的功能[64]。CSN(COP9 signalosome)，由8個高度保守的不同亞基組成，是一個新的 E3泛素連接酶的調節因子，是細胞對外界刺激或脅迫產生響應的調節成分[65-66]。CDD 復合體[COP10, DET1, DDB1 (DNA DAMAGE BINDING PROTEIN1)]的具體功能還不清楚。此外，光信號導致 COP/DET/FUS 失活的具體分子機制也有待進一步研究。

第3類，直接調節光反應。與光受體相互作用因子中，有一類重要的堿性螺旋環螺旋(basic helix-loop-helix, bHLH)類轉錄因子-PIFs(phytochrome interacting factor)家族蛋白，其主要功能是調節光敏色素介導的暗形態建成到光形態建成轉換過程中的信號轉導途徑[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的結合能力比 PIF3強[68-69]。PIF3能與phyC和phyE分別形成異源二聚體[70]。研究發現 PIF3和 phyB可以在體外結合至光響應基因啟動子的 G-box 區域，表明光敏色素可以將光信號直接靶向目的基因的啟動子調控該基因表達[71-72]。研究證明，在轉錄因子 PIF3或HY5的協同作用下，phyA-FHY1復合物可以結合至編碼查爾酮合酶的CHS(CHALCONE SYNTHASE)基因啟動子上，共同調控CHS的轉錄[73]。Chen等[74]證明在與 phyA 直接發生相互作用的靶基因啟動子上存在大量供 PIFs 識別的順式作用元件。這一發現說明包括 PIFs和 HY5在內的大量轉錄因子均能以直接或間接的方式在靶基因啟動子上與phyA發生相互作用，對眾多下游基因進行調控，從而對各種內外信號作出快速反應[75]。擬南芥其他類型的轉錄因子(如 ARR4、IAAs、ATHB23等)也能以上述方式與光敏色素發生相互作用[75-77]。此外，也有研究認為phyB會阻礙PIFs結合至靶基因的啟動子區域[78]，并通過一系列體外試驗證明，PIF1和 PIF4與靶基因作用后不能與 phyB 或 phyA 同時結合[79-80]，其深層次的機理還有待進一步試驗證實。

基于以上分析，筆者繪制光敏色素與各相關因子互作的模式圖(圖2)。

Pr.紅光吸收型 Phytochrome red light-obsorbing form; Pfr.遠紅光吸收型 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;箭頭表示正調控作用, T型線表示負調控作用 Arrow represent positive regulation and T-type line represent negative regulation.

4 展 望

不同光敏色素的分子結構和生理功能已得到系統的闡述，其信號傳導機制成為近年來研究的重點。目前，基于對光信號、溫度及多種植物內源激素共同組成的信號網絡有系統認識，一大批與光敏色素相互作用的因子被發現。但因該網絡的復雜性，其整體功能以及各信號分子在整個調控網絡中的作用還需深入研究。如何系統詮釋以光敏色素為中心的信號通路作用機制以及各通路間的相互關系，仍是亟待解決的關鍵問題。此外，光敏色素還是介導植物應對各種非生物與生物脅迫的重要激素[32]，了解其體內的作用方式將為培育適應不同光環境尤其是弱光下的農作物新品種提供有價值的理論參考依據。

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(責任編輯：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

國家自然科學基金 (31260037; 31460043); 新疆自治區優秀青年科技人才培養項目(2013721013)；國家科技部基礎研究計劃973前期項目 (2012CB722204)。

張詩悅，女，碩士研究生，研究方向為植物抗逆分子生物學。E-mail:496689512@qq.com

蘭海燕，女，博士，教授，研究方向為植物抗逆分子生物學。E-mail: lanhaiyan@xju.edu.cn

Q945.43

A

1004-1389(2017)05-0657-08

網絡出版地址：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).