PPR蛋白在植物生長發(fā)育中的作用

王婉珍, 任育軍, 繆穎

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PPR蛋白在植物生長發(fā)育中的作用

王婉珍, 任育軍, 繆穎*

(福建農(nóng)林大學生命科學學院，福州 350002)

PPR蛋白陸生植物中屬于最大的蛋白家族之一，其成員種類和數(shù)量均十分龐大。PPR蛋白主要的功能是通過在多種細胞器中進行定位從而參與細胞核和細胞器中特異單鏈RNA的轉(zhuǎn)錄后修飾和編輯，在植物生長發(fā)育的多個階段均發(fā)揮著重要的作用。多數(shù)PPR蛋白編碼基因的突變體呈現(xiàn)異常的發(fā)育表型，如胚胎致死、發(fā)育遲緩及綠化延遲等。對近年來植物PPR蛋白的分類、定位、RNA修飾的機制及其對植物生長發(fā)育影響進行了綜述，并展望了植物PPR發(fā)揮功能區(qū)域和參與的調(diào)控網(wǎng)絡研究。

植物；生長發(fā)育；PPR蛋白；RNA修飾；發(fā)育表型；綜述

植物的生長發(fā)育被認為是一系列可識別的變化事件綜合的結(jié)果，導致植株的結(jié)構(gòu)發(fā)生量變和質(zhì)變的過程，如根的生長、葉的發(fā)育、花形態(tài)的建成、胚胎的發(fā)育和種子的形成等[1]。從發(fā)育生物學的角度來講，生長發(fā)育是生命現(xiàn)象的發(fā)展和延伸，是生物有機體自我構(gòu)建和自我組織的必然過程[2]。植物的生長和發(fā)育是不可分離的生命過程。植物的生長伴隨著細胞的膨大，數(shù)目增多，體積增長，是一個不可逆的過程。在植物生長的同時，發(fā)育也同時進行，從胚胎發(fā)育到植株衰退，遵循生命周期，完成個體的發(fā)育[3]。植物的生長發(fā)育是一個復雜的調(diào)控過程，由基因的精細表達和外在的環(huán)境因素共同調(diào)控。近年來，已報道大量與植物生長發(fā)育相關的蛋白，如擬南芥()的WHY蛋白(whirly1)，可以通過維持細胞器基因組的穩(wěn)定、抗病信號的轉(zhuǎn)導調(diào)節(jié)植物葉片的衰老[4]；高等植物CYCD3蛋白(cyclin D3)可以影響植物根的二級生長[5]；植物中鈣依賴蛋白激酶(Ca/calmodulin- dependent protein kinases, CDPK)在花粉管的伸長和脅迫反應中起重要作用[6]；此外還有其他蛋白也參與調(diào)控植物生長發(fā)育的過程[7–10]。隨著測序技術的發(fā)展，許多新的基因不斷被報道和研究。

編碼PPR蛋白的基因是2000年通過測序技術被報道且命名的，因其蛋白基序結(jié)構(gòu)與TPR基序結(jié)構(gòu)相似，均含有三角狀五肽而被命名為PPR (pentatricopeptide repeat)[11]。目前的研究表明PPR家族大量存在于陸生植物中，在擬南芥和水稻()基因組中均有超過400個成員[12–13]。在玉米()、油菜()和番茄()等植物中也相繼報道了PPR家族的存在[14–16]。PPR作為一類反式作用因子，主要涉及RNA的轉(zhuǎn)錄后修飾，從而調(diào)控植物生長發(fā)育相關基因的表達，在植物抗逆性和植物生長發(fā)育過程等方面起著重要的作用[17–18]。本文對近年來植物PPR蛋白的分類、定位、RNA修飾的機制及其對植物生長發(fā)育的影響進行綜述，并對植物PPR發(fā)揮功能區(qū)域和參與的調(diào)控網(wǎng)絡的研究進行了展望。

1 PPR蛋白家族的分類和定位

1.1 分類

PPR蛋白一般包含2~27個串聯(lián)重復的結(jié)構(gòu)域,每個結(jié)構(gòu)域有31~36個氨基酸殘基。利用計算機軟件預測PPR的基序結(jié)構(gòu)并進行分類，根據(jù)基序類型PPR主要可分為兩個亞家族[12](圖1)。經(jīng)典的PPR基序由串聯(lián)重復的35個氨基酸排列形成，稱為P模型(圖1: B)。在此基礎上又延伸出含有36個氨基酸殘基的L模型，以及含有31個氨基酸殘基的S模型[19]。均由經(jīng)典的P模型組成的PPR蛋白稱為P亞家族[20]，如水稻中的WSL4 (white stripe leaf 4)就屬于這一亞家族的成員[21]；由經(jīng)典P模型、L模型和S模型交替排列的為PLS亞家族(圖1: C)，如擬南芥GRS1蛋白(growing slowly 1)，參與RNA的編輯和植物的發(fā)育[15,22]。再根據(jù)羧基端結(jié)構(gòu)域的不同，還可對PLS亞家族進一步劃分。PPR蛋白每個重復基序通常會形成1個穩(wěn)定的螺旋-轉(zhuǎn)角-螺旋結(jié)構(gòu)[20](圖1: A)。還可以再進一步折疊形成超螺旋結(jié)構(gòu)，與相關蛋白發(fā)生互作；同時PPR還能夠結(jié)合在單鏈RNA上，對靶基因的轉(zhuǎn)錄本進行剪接及編輯，進而影響植物的生長發(fā)育[23–24]。擬南芥中的MTL1蛋白(mitochondrial translation factor1)可以剪接線粒體NADH脫氫酶7基因的轉(zhuǎn)錄本[25]；MORF9蛋白(multiple organellar RNA editing factor 9)與PLS類PPR蛋白共同作用在RNA編輯過程中，可以提高RNA編輯的效率[26]; CLB19 (chloroplast biogenesis 19)與MORF2相互作用，共同編輯RNA，突變體會使植物雌配子體不正常發(fā)育，植物的生長發(fā)育呈現(xiàn)異?，F(xiàn)象[27]。

1.2 定位

大多數(shù)PPR蛋白氨基端具有定位信號序列[28]。多數(shù)PPR蛋白主要定位在細胞內(nèi)的線粒體或葉綠體上，如擬南芥OTP43蛋白(organelle transcript pro- cessing 43)定位在線粒體上，參與基因內(nèi)含子的剪接[29]；OTP70 (organelle transcript processing 70)則定位在葉綠體上[30]。有少數(shù)PPR蛋白存在雙定位模式，如水稻OsPGL1蛋白(pale green leaf1)同時定位在葉綠體和線粒體上[31]，而擬南芥PNM1蛋白則同時定位于細胞核及線粒體上[32]。

2 PPR蛋白參與植物生長發(fā)育與脅迫反應的調(diào)節(jié)

2.1 PPR蛋白調(diào)節(jié)植物種子的發(fā)育

研究表明，PPR蛋白在種子發(fā)育過程中具有重要的調(diào)控作用。擬南芥基因(glutamine-rich protein 23)單插入雜合突變體的種子中，有四分之一的胚胎致死，認為缺失GRP23會造成胚胎發(fā)育受阻[33]。大多數(shù)的grp23突變體胚胎受阻發(fā)生在16細胞球形胚時期之前，并且有19%細胞分裂畸形。主要在胚胎發(fā)育時期表達且GRP23定位在根的細胞核中，可以與RNA聚合酶II發(fā)生互作[33], 還與植物下胚軸的分化相關[34]。玉米谷粒缺陷型植株雖然可以長出谷粒，但為營養(yǎng)不良型小谷粒，是延遲植物發(fā)育的經(jīng)典類型。研究表明，(defective kernel 2)和基因在玉米中分別編碼PPR家族中的1個成員，其中主要參與玉米線粒體轉(zhuǎn)錄本的剪接[35]，而則是通過編輯線粒體轉(zhuǎn)錄本從而影響玉米細胞線粒體的功能[36]。和突變體均能產(chǎn)生胚乳發(fā)育不全、小而有缺陷的谷粒[35–36]。最新的研究表明，突變體玉米中胚乳和胚芽的發(fā)育有明顯缺陷，后來證實DEK37蛋白(defective kernel 37)可以影響線粒體中第二類內(nèi)含子的剪接和玉米種子的正常發(fā)育[37]。除以上基因，(empty pericarp 11)和基因突變也會導致玉米種子發(fā)育異常，EMP16蛋白主要參與對線粒體內(nèi)含子4的剪接，EMP11蛋白則是剪接的內(nèi)含子，他們的基因突變均能導致種子發(fā)育不良，甚至造成空谷粒的現(xiàn)象[38–39]。這些表明PPR家族蛋白在植物種子發(fā)育的過程中起到重要的調(diào)節(jié)作用。

2.2 PPR蛋白參與指導胞質(zhì)雄性不育的育性恢復

細胞質(zhì)雄性不育是廣泛存在于高等植物中的一種自然現(xiàn)象，表現(xiàn)為母體遺傳、花粉敗育和雌蕊正常[40]。在研究水稻細胞質(zhì)雄性不育的過程中，基因(fertility restorer)被認為是一類育性恢復基因[41]。曾有報道水稻中、和基因為育性恢復基因且均編碼PPR蛋白[42–43]。并且，這3個基因編碼的蛋白以線粒體為目標，通過剪切和降解機制來阻礙線粒體ORF79蛋白(open reading frame 79)的累積，從而恢復水稻的育性[43]。水稻中基因也可恢復細胞質(zhì)雄性不育，距離基因170 kb的基因編碼1個PPR家族成員，PPR762指導恢復RT98類型水稻的部分雄性不育性狀，使結(jié)實率達到9.3%[44]。推測基因在恢復水稻細胞質(zhì)雄性不育中除需要基因的參與，可能還需要基因周圍區(qū)域其他基因的共同參與才能完全恢復水稻中RT98類型的雄性不育性狀[44]。除了上述PPR蛋白可以指導雄性不育的育性恢復，水稻中其他PPR蛋白也有相似的功能，如RF6、PPR592和PPR676等[45–47]。此外，歐洲的1個油菜品系中有1個定位在線粒體上的RFn蛋白可以恢復胞質(zhì)雄性不育，基因(fertility restorer nap)編碼1個PPR蛋白[14]。通過對棉花(spp.)進行全基因組分析表明，棉花中多數(shù)PLS亞族的PPR蛋白與胞質(zhì)雄性不育和恢復相關[48]。

2.3 PPR蛋白參與調(diào)控葉綠體的形成、葉的發(fā)育和根的生長

2.3.1 參與調(diào)控葉綠體的形成

葉綠體的主要作用是進行光合作用并合成植物生長所需的相關物質(zhì)。目前關于葉綠體的形成機制仍然處于比較模糊的狀態(tài)。全基因組分析擬南芥中的PPR家族，表明他們在葉綠體的形成中起著不可或缺的作用[49]。PPR家族中的THA8蛋白(thylakoid assembly 8)在剪接被子植物葉綠體編碼基因的第二類內(nèi)含子中是必不可少的。玉米突變體中，幼苗期類囊體蛋白和色素均受損，葉綠體形成不完善導致葉片顏色呈淺綠色[50]。玉米PPR4參與葉綠體(ribosomal protein s12)前體RNA內(nèi)含子1的反式剪接，敲除該基因會使質(zhì)體核糖體無法正常積累，導致玉米幼苗葉片黃化和白化[51]。擬南芥OTP51 (organelle transcript processing 51)參與質(zhì)體基因(hypothetical chloroplast open reading frame 3)內(nèi)含子2的順式剪接等，突變影響光系統(tǒng)I和光系統(tǒng)II的組裝，表現(xiàn)為葉綠體形成異常，植株葉片白化[52]。擬南芥ECB2蛋白(early chloroplast development 2)可以編輯質(zhì)體基因(acetyl coA carboxylase subunit D)和基因(nicotinamide adenine dinucleotide dehydrogenase subunit F)的轉(zhuǎn)錄本，基因突變會使植株出現(xiàn)白化和敗育性狀，突變體中和基因的編輯效率受到影響，且突變體葉片相對于野生型表現(xiàn)出延遲綠化表型[53]。廣泛篩選擬南芥葉片顏色異常突變體，找到1個定位于葉綠體且編碼PPR蛋白的基因(white to green 1)，敲除該基因會影響葉綠體的發(fā)育，阻礙葉片的早期綠化，光合作用不能正常進行，植株的生長受到抑制；恢復基因的表達則能使突變體恢復正常表型[54]。(early chloroplast development 1)編碼1個定位于葉綠體上的PPR蛋白，敲除會導致胚胎致死或不正常的胚胎發(fā)育[55]。利用RNAi技術使基因的表達減少，幼苗子葉出現(xiàn)白化但葉片形態(tài)正常,這種異常現(xiàn)象是葉綠體類囊體膜系統(tǒng)發(fā)育延遲引起的，認為ECD1是一個可以編輯基因轉(zhuǎn)錄本的轉(zhuǎn)錄因子以及調(diào)節(jié)葉綠體早期發(fā)育的蛋白[55]。除以上PPR蛋白外，水稻PPR6[56]、擬南芥SOT5 (suppressor of thylakoid formation 5)[57]、SOT1 (suppressor of thyla- koid formation 1)[58]和PDM1 (pigment deficient mutant 1)[59]也參與葉綠體的形成和調(diào)控相關基因的表達。

2.3.2 參與葉的發(fā)育

PPR蛋白在調(diào)控植物葉綠體的形成時，也會影響葉的發(fā)育。在植物生長發(fā)育過程中PPR家族對葉的發(fā)育起著不可或缺的作用。擬南芥OTP70是一個E類的PPR蛋白，缺失該蛋白會使基因(RNA polymerase beta’ chain 1)轉(zhuǎn)錄本剪接受損，葉片呈淡黃色，整體植株發(fā)育不良，較野生型更為矮小[30]。水稻基因在葉片發(fā)育早期，影響葉綠體的生成；突變體葉片出現(xiàn)白色條紋，葉綠素含量比野生型少，但葉片大小和植株生長沒有受到明顯的影響[20]。擬南芥PPR596是一個P亞族的PPR蛋白, 可以編輯線粒體的轉(zhuǎn)錄本，突變體和野生型的葉片顏色無明顯區(qū)別，但生長早期的突變體的葉片更小，突變體植株也比野生型小得多；到生長后期，突變體和野生型植株大小無明顯差異，但突變體葉片更為卷曲，呈不規(guī)則形狀[60]。PPR蛋白不僅與葉片的大小和形態(tài)建成相關，還與葉片衰老有一定的關系。擬南芥中的1個基因在某種程度上參與了一些衰老外源因素的誘導，從而負調(diào)控擬南芥葉片的衰老進程[61]。

2.3.3 調(diào)節(jié)根的生長

根作為植物的營養(yǎng)器官，通常位于地表以下,負責吸收和運輸水分及溶解于其中的無機鹽，并且具有支持、合成和貯存有機物質(zhì)的作用[62]。PPR蛋白除調(diào)控植物葉片發(fā)育外還影響根的生長。擬南芥SLO3蛋白定位在線粒體上，參與NADH脫氫酶亞基7編碼基因內(nèi)含子2的剪接；缺失該蛋白導致植物存在發(fā)育缺陷，種子萌發(fā)延緩、根的長度較野生型顯著縮短、葉片卷曲，抽苔遲緩等[63]。SLO3還與植物生長素信號通路作用相關，調(diào)節(jié)根尖分生組織的活性范圍[64]。同時，擬南芥中的SLO4蛋白涉及基因的編輯和內(nèi)含子1的剪接，突變體根的長度較野生型顯著縮短，影響植株的整體發(fā)育[65]。擬南芥SLG1蛋白影響線粒體RNA的編輯和植物發(fā)育，與野生型相比，突變體的根較短, 根尖分生組織較短且側(cè)根少，對ABA、NaCl和甘露醇更加敏感，且更耐受干旱脅迫[66]。

綜上所述，PPR蛋白可以通過剪接和編輯相關基因的轉(zhuǎn)錄本，影響這些目標基因的功能，從而參與葉和根的生長發(fā)育最終調(diào)控植物的生長(圖2)。

2.4 PPR蛋白參與植物響應脅迫反應

植物生長過程中會受到許多逆境因素的影響。近年來的研究表明PPR蛋白參與響應脅迫反應的功能[13,67–70]。擬南芥中WSL蛋白(white stripe leaf)在參與基因(ribosomal protein L2) 轉(zhuǎn)錄本剪接效率的同時，還響應脅迫反應；突變體相對于野生型對脫落酸、鹽和糖更加敏感，可以積累更多的過氧化氫[13]。擬南芥參與調(diào)節(jié)植株鹽、脫落酸和氧化應激反應，突變體對鹽、脫落酸和氧化應激均不敏感[71]?；?suppressor of the ABAR overexpressor 1)的表達下調(diào)會使植株對脫落酸反應敏感，上調(diào)表達則相反，說明基因在脫落酸信號通路中起負調(diào)控作用[72]。進一步研究表明，過表達可以增強植株對干旱、冷和鹽的耐受力[73]。運用計算機軟件從歐洲大葉楊()的全基因組中找到154個與脅迫相關的基因，冷處理時，大葉楊基因的表達顯著上調(diào)；鹽處理時，、和的表達水平顯著上調(diào)；茉莉酸甲酯處理時，基因的表達水平顯著上調(diào)[70]。這表明基因家族能夠響應植物生長發(fā)育過程不同的脅迫反應[13,70]。

3 PPR蛋白的作用機制

PPR家族作為一類反式作用因子參與基因的表達調(diào)控，主要是在轉(zhuǎn)錄后水平的RNA修飾中發(fā)揮作用[15,74–75]。目前的研究表明，PPR家族對RNA的修飾主要分為以下3種類型，第一種類型為PPR蛋白識別并結(jié)合在目標RNA上，阻礙RNA外切酶的活性,使其形成穩(wěn)定的單順反子進行表達[75–76]；第二種類型為PPR特異識別RNA編輯的順式作用元件并招募相關編輯因子共同起作用，把特定的胞嘧啶轉(zhuǎn)變成尿嘧啶或特定的尿嘧啶轉(zhuǎn)變成胞嘧啶，改變氨基酸的序列，創(chuàng)造新的翻譯起始位點或者終止位點[23,55]；第三種類型為DNA轉(zhuǎn)錄后的前體RNA含有豐富的內(nèi)含子，需要進行切除然后拼接為成熟RNA。剪接過程中，一般PPR蛋白結(jié)合在RNA上，幫助RNA正確折疊形成催化結(jié)構(gòu)，保護活性區(qū)域，并輔助RNA酶進行催化[63]。PPR蛋白通過對目的基因的轉(zhuǎn)錄本進行修飾，激活或者抑制基因的表達活性，進而調(diào)控植物的生長發(fā)育[77–78]。

4 展望

葉綠體和線粒體是提供植物細胞生長發(fā)育所需能量和養(yǎng)分的場所，并且能夠感知外界環(huán)境信號，調(diào)節(jié)植物的生長[79]。目前已報道的大多數(shù)PPR蛋白都定位于細胞的葉綠體和線粒體上，并且在植物生長發(fā)育中的作用也有了一定了解。以往的綜述文章主要是針對PPR蛋白的起源、分類定位以及在計算機軟件輔助下不斷發(fā)現(xiàn)新的PPR蛋白，預測和驗證功能區(qū)域。本文主要描述了PPR蛋白可以對細胞器特異基因的轉(zhuǎn)錄本進行修飾和加工，并且以某種方式參與調(diào)節(jié)植物生長發(fā)育和響應脅迫反應(表1)。但其具體的調(diào)控網(wǎng)絡和特異性還有待進一步的探究。PPR蛋白在調(diào)節(jié)植物生長發(fā)育是否存在時空性和組織特異性？PPR蛋白在發(fā)揮不同功能時，其結(jié)構(gòu)是否發(fā)生改變？PPR蛋白是如何特異識別并結(jié)合在RNA上的？有文獻曾報道，TPR蛋白的氨基端部分與蛋白自身的穩(wěn)定性、聚化狀態(tài)以及和其它蛋白之間相互作用的能力密切相關[80–81]。PPR蛋白的結(jié)構(gòu)與TPR蛋白的結(jié)構(gòu)相似[11]，其氨基端是否也存在相似的功能還不清楚。另外，以往的研究大多集中在PPR結(jié)合的特異RNA上，對與PPR共同作用的蛋白研究較少；對于這些未知的部分還有待于進一步研究。此外，關于PPR的功能研究目前多停留在理論層面，運用到農(nóng)業(yè)生產(chǎn)實踐中還相對較少。PPR蛋白可以恢復植物雄性不育性狀[48]；并能在逆境條件下，提高作物的質(zhì)量和產(chǎn)量[82]。在農(nóng)業(yè)生產(chǎn)中，是否可以利用相關PPR蛋白的育性恢復機制和抗逆性等功能，培育優(yōu)良的農(nóng)作物新品種。要解決這些問題，需要進一步深入研究家族的功能，進一步闡述植物PPR發(fā)揮功能區(qū)域以及明確參與的調(diào)控網(wǎng)絡。

表1 參與調(diào)節(jié)植物生長發(fā)育的部分PPR蛋白

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Roles of PPR Proteins in Plant Growth and Development

WANG Wan-zhen, REN Yu-jun, MIAO Ying*

(College of Life Sciences, Fujian Agriculture and Forestry University,Fuzhou, 350002, China)

PPR proteins are one of the largest protein families in terrestrial plants, both on category and volume. The main functions of PPRs were involved in post-transcriptional modifications and editing of specific single-stranded RNAs in the nucleus and organellestheir localization in various organelles. PPRs play important roles in series events of plant growth and development. Mutants of most PPR protein-encoding genes exhibit abnormal developmental phenotypes, such as embryonic lethality, developmental retardation, and greening delays. The recent research advances of PPRs in classification, localization, RNA modification mechanisms and their functions on regulating growth and development of plants were summarized, and the studies on functional area and participating regulatory network of PPR in plants was prospected.

Plant; Growth and development; PPR protein; RNA modification; Development phenotype; Review

10.11926/jtsb.3956

2018-06-04

2018-08-13

國家自然科學基金項目(31770318, 31400260)資助

This work was supported by the National Natural Science Foundation of China (Grant No. 31770318, 31400260).

王婉珍(1990~ )，女，碩士研究生，研究方向為分子細胞生物學。E-mail: 1150539007@fafu.edu.cn

E-mail: ymiao@fafu.edu.cn