植物礦質(zhì)養(yǎng)分吸收的長距離反饋調(diào)節(jié)研究進展

熊長明， 王 曄， 田曉莉

(中國農(nóng)業(yè)大學(xué)作物化學(xué)控制研究中心， 植物生理學(xué)與生物化學(xué)國家重點實驗室，北京 100193)

土壤礦質(zhì)養(yǎng)分的時空波動廣泛存在，植物已進化出精細(xì)的局部和長距離調(diào)節(jié)系統(tǒng)對此做出響應(yīng)，以維持體內(nèi)礦質(zhì)養(yǎng)分的穩(wěn)態(tài)。局部調(diào)節(jié)包括根毛和側(cè)根增生等根系形態(tài)結(jié)構(gòu)的變化[1-6]及一些養(yǎng)分運輸載體的誘導(dǎo)表達[7-9]。長距離調(diào)節(jié)則由根-冠調(diào)節(jié)和冠-根調(diào)節(jié)組成，根系感受到周圍介質(zhì)養(yǎng)分的波動后首先通過木質(zhì)部向地上部傳遞信號，并觸發(fā)一系列響應(yīng); 隨后地上部產(chǎn)生信號并由韌皮部向下運輸，對根系生長和養(yǎng)分吸收速率進行反饋調(diào)節(jié)，使根系的吸收能力與地上部的養(yǎng)分需求得以匹配[10]。

1 養(yǎng)分吸收的長距離反饋調(diào)節(jié)現(xiàn)象普遍存在

嫁接和分根是研究礦質(zhì)養(yǎng)分長距離反饋調(diào)節(jié)的常用方法，養(yǎng)分感受和信號系統(tǒng)發(fā)生缺陷的突變體也為探明養(yǎng)分穩(wěn)態(tài)的反饋調(diào)節(jié)提供了手段。

盡管有少量相反的報道[23]，但絕大多數(shù)研究證明礦質(zhì)養(yǎng)分吸收的長距離反饋調(diào)節(jié)現(xiàn)象是普遍存在的。

向部分根系供Pi，植株可能通過提高其養(yǎng)分吸收速率(與整根供Pi相比)部分或全部補償缺Pi部分根系的損失[26-27]。植株對Pi的需求通過供Pi部分根系得到滿足后，缺Pi部分根系Pi轉(zhuǎn)運蛋白的表達不再受低Pi誘導(dǎo)[28-30]。Mt4是蒺藜苜蓿根系的Pi-饑餓誘導(dǎo)基因(PSI)，在分根試驗中部分根系供Pi后發(fā)生系統(tǒng)下調(diào)[31]。pho1突變體根系的木質(zhì)部Pi載入發(fā)生缺陷，地上部的Pi水平較低[31]，導(dǎo)致其根系Mt4基因在充足供Pi時也不發(fā)生下調(diào)[32-33]。Grevilleacrithmifolia(銀樺)的排根起始和生長以及根系的Pi凈吸收速率也均受到系統(tǒng)反饋調(diào)節(jié)[34]。

分根試驗也廣泛用于研究缺Fe響應(yīng)的調(diào)節(jié)機制。車前草[40]、 黃瓜[41]、 擬南芥[42-43]、 番茄(Lycopersiconesculentum)[44]和木本植物小金海棠[45]等植物的部分根系處于缺Fe條件下時，可誘導(dǎo)另一部分供Fe根系的Fe(III)還原酶活性和/或質(zhì)子分泌增強。豌豆耐低鐵基因型(Santi)作為接穗可以誘導(dǎo)不耐低鐵基因型(Parafield)砧木的缺鐵響應(yīng)，使其Fe(III)還原酶活性維持在較高水平[46]。擬南芥frd3突變體的木質(zhì)部Fe裝載(由Fe(III)檸檬酸鹽螯合物介導(dǎo))發(fā)生缺陷，在充足供Fe條件下葉片仍處于缺Fe狀態(tài)[47]，此時根系中的缺鐵響應(yīng)也不能下調(diào)[48-50]，提示來自于地上部的缺Fe信號在持續(xù)調(diào)節(jié)根系吸鐵基因的表達。

植株去頂或去葉后，發(fā)現(xiàn)根系的一些缺素響應(yīng)減弱或消失[3, 41, 51, 56], 說明根系的吸收能力依賴于地上部對缺素的響應(yīng)，并受到冠-根信號的介導(dǎo)。

2 長距離反饋信號的作用模式尚不明確

雖然已經(jīng)證明了地上部可以發(fā)送長距離冠-根信號調(diào)控根系的缺素響應(yīng)，但地上部是在缺素條件下發(fā)出促進信號/需求信號、 還是在養(yǎng)分充足條件下發(fā)出抑制信號/供應(yīng)信號尚未得到一致的結(jié)論。

地上部控制根系缺Fe響應(yīng)的信號機制得到較多研究。Vert等(2003)曾提出擬南芥地上部調(diào)控根系Fe吸收機制的促進模型和抑制模型[43]。促進模型(the promotive model)是指在缺Fe條件下葉片產(chǎn)生促進信號傳遞至根系，誘導(dǎo)Fe吸收基因的表達，在Fe充足條件下則不產(chǎn)生信號; 抑制模型(the repressive model)是指在供Fe充足條件下地上部產(chǎn)生抑制信號，傳遞至根系后抑制Fe吸收響應(yīng)，在缺Fe條件下則不產(chǎn)生信號。

Grusak和Pezeshgi(1996)將豌豆突變體dgl(正常供鐵條件下根部缺鐵響應(yīng)機制仍然處于激活狀態(tài)，導(dǎo)致植株體內(nèi)的Fe 超量積累)和野生型DGV共同嫁接在野生型砧木上，發(fā)現(xiàn)充足供Fe時野生型砧木的Fe(III)還原速率也能在dgl突變體接穗的誘導(dǎo)下得到提高，他們認(rèn)為這種現(xiàn)象是由dgl突變體向下傳遞的促進信號所致[55]。Enomoto等(2007)的去葉試驗也證明地上部在缺Fe條件下向根系傳遞促進信號，他們發(fā)現(xiàn)煙草根系編碼Fe運輸載體的基因NtIRT1和編碼Fe(III)還原酶的基因NtFRO1在缺Fe條件下被誘導(dǎo)，但去掉葉片3 h后它們的表達快速下降，并逐漸降低到充足供Fe下的水平[56]。

擬南芥opt3-2突變體韌皮部中的肽-Fe螯合物運輸存在缺陷[57]。García等(2012)向處于缺Fe狀態(tài)的野生型植株葉面噴施FeSO4，發(fā)現(xiàn)根系的Fe(III)還原酶活性下降數(shù)倍，吸鐵基因的表達幾乎被阻斷; 但opt3-2突變體的Fe(III)還原酶活性和吸鐵基因表達仍然維持在與缺Fe處理相當(dāng)?shù)乃?。他們?jù)此推斷，葉面施Fe后產(chǎn)生了特異的抑制信號以阻止根系的缺Fe響應(yīng)，而非減弱或阻斷了地上部的促進信號向根系傳遞[58]。

Lucena等(2006)對Fe吸收反饋調(diào)節(jié)的促進模型和抑制模型進行了整合，提出地上部既可向根系發(fā)出促進信號(乙烯或促進乙烯合成的物質(zhì)，如生長素或乙烯前體ACC)，也可發(fā)出抑制信號(與韌皮部中的Fe有關(guān)); 根系可將兩類信號進行整合，最終決定是誘導(dǎo)還是抑制吸鐵基因的表達[59]。

3 長距離反饋信號的鑒定取得一定進展

3.1 養(yǎng)分或它們的同化物/代謝物信號

分根試驗表明，缺Pi側(cè)根系PSI基因的上調(diào)受到抑制，很可能由供Pi側(cè)運輸而來的Pi介導(dǎo)[28, 32, 70]。擬南芥PHO2基因編碼一個位于葉片韌皮部的Pi轉(zhuǎn)運蛋白，pho2突變體的Pi吸收能力和根-冠轉(zhuǎn)運能力提高，導(dǎo)致地上部的Pi過量積累，暗示Pi的負(fù)反饋調(diào)節(jié)功能缺失[71]。pho1突變體根系木質(zhì)部的Pi載入發(fā)生缺陷，地上部的Pi水平較低，其根系中PSI的下調(diào)同時受到破壞[32-33]。但Pi本身可能不負(fù)責(zé)這種系統(tǒng)下調(diào)，因為在蒺藜苜蓿的分根系統(tǒng)中，缺Pi部分根系Mt4的下調(diào)早于Pi濃度的上升，而且Pi流量的減少不影響系統(tǒng)抑制[32]。當(dāng)然，也可能是根系和地上部之間Pi的動態(tài)循環(huán)(而不是Pi濃度自身)為反饋調(diào)節(jié)提供了信號[35]。

充足供Fe的蓖麻植株，其葉片F(xiàn)e濃度和韌皮部中Fe復(fù)合物的水平高于缺Fe植株; 葉面供應(yīng)Fe-EDTA可降低根系的缺Fe響應(yīng)(質(zhì)子泌出和Fe(III)還原酶活性提高)。因此，韌皮部中的Fe復(fù)合物可能控制植物根系對Fe有效性的響應(yīng)[72]。擬南芥opt3-2突變可能影響韌皮部中Fe-肽螯合物的運輸[73]; 番茄chln突變導(dǎo)致煙草胺(NA，氨基羧酸類Fe螯合劑)無法合成[74]，而NA可以與Fe(II)形成穩(wěn)定的復(fù)合體在韌皮部運輸[75-77]; 豌豆dgl突變體在韌皮部中不形成野生型具有的Fe-肽螯合物[78-80]。上述這些突變體根系的缺Fe響應(yīng)在供Fe條件下均比較強，據(jù)此推測與肽或NA形成復(fù)合物的Fe可能作為韌皮部信號下調(diào)根系吸Fe基因的表達。最近的葉面57Fe標(biāo)記試驗表明，突變體opt3-2、chln和dgl根系中積累的57Fe與各自的野生型相似[58]，說明韌皮部中的總Fe含量不是根系缺Fe響應(yīng)的抑制信號，為上述Fe復(fù)合物作為信號物質(zhì)的推測提供了旁證。

3.2 地上部衍生的碳水化合物信號

Pitman(1972)的遮光試驗表明，K+自根系向地上部的運轉(zhuǎn)量與根系中的糖濃度有關(guān)，推測地上部可能通過向根系供應(yīng)能量來反饋調(diào)節(jié)K+向地上部的運輸[81]。

糖類物質(zhì)對Pi饑餓響應(yīng)的調(diào)節(jié)得到很多研究的肯定。根中糖濃度的增加早于磷脅迫響應(yīng)基因(PSR)的誘導(dǎo)[82]。在缺Pi條件下，采用黑暗或環(huán)割處理抑制蔗糖的生物合成和轉(zhuǎn)運，使根中PSI的表達降低[83]。pho3突變體的SUC2基因(編碼一個在韌皮部表達的蔗糖運輸載體)發(fā)生缺陷，在低Pi條件下其根系的酸性磷酸酶(ACP)活性和PSI基因表達減弱[84-85]。Lei等(2011)構(gòu)建了一個SUC2基因過表達的擬南芥突變體hps1，其在Pi吸收、 轉(zhuǎn)運和根系構(gòu)型等多方面表現(xiàn)出低Pi響應(yīng)[86]。缺Pi白羽扇豆排根中的幾個PSR以依賴光合作用的方式上調(diào)[82]。外源施用糖類物質(zhì)對根系形態(tài)和Pi運輸載體等PSR有放大作用[83-89]。

3.3 植物激素信號

有研究表明，CK可抑制Pi饑餓響應(yīng)[102]，但外源CK處理不能模擬恢復(fù)供Pi的抑制效應(yīng)[70]，因而對CK作為Pi長距離信號的作用提出了質(zhì)疑。

擬南芥lpr1(抗低Pi)突變體的側(cè)根形成在Pi饑餓條件下減少，而該突變體是Auxin極性運輸所需要的BIG的等位基因系[104]，表明自上而下運輸?shù)腁uxin可能也與根系的Pi饑餓響應(yīng)有關(guān)。應(yīng)用野生型和Auxin響應(yīng)突變體進行的研究發(fā)現(xiàn)，根系中Auxin的重新分布激發(fā)了Pi饑餓誘導(dǎo)的根系發(fā)育[105]。但其他不依賴于Auxin的信號途徑也參與了這些響應(yīng)[104]。

大量應(yīng)用突變體、 去頂(去除Auxin產(chǎn)生的主要源器官)、 環(huán)割(阻斷Auxin的向基運輸)、 添加Auxin及其極性運輸抑制劑的研究為Auxin作為系統(tǒng)信號參與缺Fe響應(yīng)提供了證據(jù)。擬南芥突變體aux1-7的生長素極性運輸有缺陷，該突變體的轉(zhuǎn)錄因子FIT及其靶標(biāo)基因Fe(III)還原酶的表達不受缺Fe誘導(dǎo)[106]。大豆缺Fe植株去掉莖頂端、 或在初生葉下方的莖部施用IAA運輸抑制劑CFM，根系的Fe(III)還原酶活性降低，恢復(fù)到與供Fe處理相當(dāng)?shù)乃絒41]。缺Fe導(dǎo)致紅三葉草根系的IAA積累和Fe(III)還原酶活性的提高，而在莖部施用IAA運輸抑制劑TIBA后根系的IAA積累減少，還原酶活性也受到顯著抑制[107]。最近Wu等(2012)的系列試驗證明，IAA自上而下的長距離運輸確實介導(dǎo)了根系的缺Fe響應(yīng)，如莖環(huán)割完全抑制了根系中的IAA積累，同時阻止了根系中質(zhì)子泌出和Fe(III)還原酶活性的上調(diào); 去掉莖尖抑制了根中的質(zhì)子泌出和Fe(III)還原酶活性的上調(diào)，但向去頂植株的頂端補充NAA可以恢復(fù)這兩種生理響應(yīng)[108]。

Auxin作為長距離冠-根信號調(diào)控根系缺Fe響應(yīng)也受到一些質(zhì)疑。去頂和施用CFM不能降低黃瓜缺Fe植株根系的Fe(III)還原酶活性[41]，煙草去頂不影響根系中NtIRT1和NtFRO1的表達[56]。Schmidt等(2000)應(yīng)用多種突變體的研究表明，主要植物激素(包括Auxin)均未參與擬南芥的缺Fe響應(yīng)[109]。Bacaicoa等(2011)則推測，IAA調(diào)節(jié)缺Fe響應(yīng)的作用可能是次級的，而且是非必需的[110]。

3.4 新的長距離信號物質(zhì)MicroRNA

在韌皮部汁液中鑒定出MicroRNAs(miRNAs)的事實，提示這類物質(zhì)具有作為長距離信號分子的潛力[111-112]。目前，幾種主要礦質(zhì)養(yǎng)分缺乏時均發(fā)現(xiàn)韌皮部中有miRNAs上調(diào)現(xiàn)象。miR395、 miR398和miR399的表達分別在S、 Cu和Pi缺乏時上調(diào)[113-116]。最近在油菜(Brassicarapus)韌皮部汁液中檢測到了miR395、 miR398和miR399，而且它們的豐度在植物分別處于S、 Cu和Pi饑餓時增加[108]。油菜缺Fe時韌皮部中的miR158b上調(diào)[117]，擬南芥中也發(fā)現(xiàn)同樣的現(xiàn)象[118]。借助谷氨酰合成酶抑制劑MSX，Gifford等(2008)鑒定出一個響應(yīng)有機N的miR167/ARF8調(diào)節(jié)模型，該模型調(diào)節(jié)側(cè)根起始和伸長，使根系與有機N進行匹配[66]。miR393/AFB3(生長素受體)模型則通過調(diào)節(jié)主根和側(cè)根的生長對N作出響應(yīng)[119]。但目前還沒有直接證據(jù)表明miR167或miR393可以從地上部運輸至根系。

miR399對Pi饑餓響應(yīng)的調(diào)節(jié)得到最系統(tǒng)和廣泛的研究。miR399在缺Pi組織中特異上調(diào)[114, 120-122]，直接引起一種泛素結(jié)合E2酶基因PHO2 mRNA的裂解，從而促進Pi吸收和向地上部的運輸。過表達miR399的擬南芥和水稻在地上部過量積累Pi，在充足供Pi條件下出現(xiàn)Pi中毒現(xiàn)象[120, 124]。由于在油菜和南瓜的韌皮部汁液中也檢測到miR399[123, 126]，因此推測長距離信號系統(tǒng)在不同植物種類中可能是保守的。采用嵌合基因(啟動子-報告基因)的分析表明，miR399和PHO2主要在維管組織中表達[121]。嫁接研究證明，野生型與過表達miR399的擬南芥或煙草互相嫁接，接穗中的miR399能通過嫁接位點向野生型砧木移動并抑制砧木中PHO2的表達，從而激活Pi的吸收和運輸[123, 127]。著生菌根的苜蓿植株，其葉片中成熟miR399及其前體含量均高于無菌根植株[125]，并且部分成熟miR399可被轉(zhuǎn)運至菌根中組成miR399-PHO2 信號途徑。

由于miR399既可以在地上部表達、 也可以在根系表達，它在冠-根之間移動的生物學(xué)意義曾受到質(zhì)疑。但時間動態(tài)分析表明，Pi缺乏條件下miR399在地上部的表達早于根系，因此它的系統(tǒng)移動確實屬于Pi缺乏的早期響應(yīng)[127]。

4 長距離反饋信號的作用靶標(biāo)得到初步研究

地上部產(chǎn)生的系統(tǒng)反饋信號需要由根系感受器接收，然后引發(fā)一系列生理生化反應(yīng)乃至根系形態(tài)變化對養(yǎng)分缺乏作出響應(yīng)。但反饋信號的調(diào)控靶標(biāo)、 相關(guān)調(diào)控網(wǎng)絡(luò)的上、 下游組分研究總體上比較薄弱，目前僅有一些初步進展。

上文提到的PHO2被鑒定為miR399的下游靶標(biāo)[121-122]。Pi缺乏條件下，miR399的上調(diào)抑制了PHO2的表達，解除了PHO2對Pi吸收的抑制。pho2突變體的Pi吸收和運輸受到促進，導(dǎo)致地上部過量積累Pi出現(xiàn)Pi中毒現(xiàn)象[71, 121]。已知miR399 在Pi饑餓信號途徑中的上游元件可能為轉(zhuǎn)錄因子PHR1[122]，同為反饋信號的蔗糖也位于miR399 的上游[128]。PHO2的下游分子元件尚不清楚，推測泛素介導(dǎo)的蛋白質(zhì)水解或功能修飾可能參與其中[13]。

5 研究展望

至今，人們對養(yǎng)分長距離反饋調(diào)節(jié)機制的了解還很有限。已知的養(yǎng)分/代謝物信號是直接調(diào)控根系吸收能力還是通過激發(fā)其他次級信號發(fā)揮調(diào)節(jié)作用尚不可知。此外，筆者推測抑制信號和促進信號共存比較接近反饋調(diào)節(jié)的本質(zhì)，但目前缺乏足夠的試驗證據(jù)。

因此，鑒定潛在的長距離信號物質(zhì)、 揭示其作用模式仍然是養(yǎng)分吸收反饋調(diào)節(jié)領(lǐng)域需要面對的長期挑戰(zhàn)，應(yīng)用養(yǎng)分感受或信號傳導(dǎo)途徑發(fā)生缺陷的突變體有望加快這方面的進展。另外，反饋信號的產(chǎn)生部位、 運輸機制、 作用靶標(biāo)及此后的調(diào)控網(wǎng)絡(luò)都是該領(lǐng)域未來的研究重點。

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