激素調(diào)控植物成花機(jī)理研究進(jìn)展

鄒禮平，潘鋮，王夢馨，崔林，韓寶瑜

綜 述

激素調(diào)控植物成花機(jī)理研究進(jìn)展

鄒禮平，潘鋮，王夢馨，崔林，韓寶瑜

中國計(jì)量大學(xué)，浙江省生物計(jì)量及檢驗(yàn)檢疫技術(shù)重點(diǎn)實(shí)驗(yàn)室，杭州 310018

開花是植物對環(huán)境的適應(yīng)性表現(xiàn)，是在多種外源和內(nèi)源信號(hào)形成的復(fù)雜成花調(diào)控網(wǎng)絡(luò)下完成。植物激素作為最重要的內(nèi)源信號(hào)參與者，在成花進(jìn)程中扮演著重要角色。近年來，光周期等成花途徑和表觀遺傳調(diào)控中激素的作用機(jī)理不斷被解析。研究發(fā)現(xiàn)激素間存在協(xié)同和拮抗作用，并證實(shí)多種激素參與赤霉素(gibberellins, GA)途徑中DELLA蛋白介導(dǎo)的多種成花調(diào)控途徑。本文主要綜述了GA在植物成花中的調(diào)控機(jī)理，同時(shí)探討了脫落酸(abscisic acid, ABA)、生長素(auxin, IAA)、細(xì)胞分裂素(cytokinin, CTK)、水楊酸(salicylic acid, SA)、茉莉酸(jasmonic acid, JA)和乙烯(ethylene, ET)等其他內(nèi)源激素在成花中的作用及其與DELLA、miRNAs和轉(zhuǎn)錄因子(transcription factor, TFs)等通路串聯(lián)調(diào)控，為全面解析激素調(diào)控植物成花的網(wǎng)絡(luò)提供參考。

植物激素；花芽分化；成花調(diào)控；信號(hào)傳導(dǎo)

開花是植物對環(huán)境的適應(yīng)性表現(xiàn)，是植物從營養(yǎng)生長向生殖發(fā)育的轉(zhuǎn)變，是決定植物繁殖成功與否的重要環(huán)節(jié)，本質(zhì)是莖頂端分生組織(shoot apical meristem, SAM)由營養(yǎng)生長時(shí)期分化產(chǎn)生葉片轉(zhuǎn)變?yōu)樯嘲l(fā)育時(shí)期形成花、果實(shí)和種子的過程[1]。植物成花過程可分為花的誘導(dǎo)、花芽分化和花器官的發(fā)育3個(gè)階段，此過程與開花時(shí)間、開花數(shù)量、開花質(zhì)量和花期長短密切相關(guān)，同時(shí)還對植物的觀賞、食用和藥用的經(jīng)濟(jì)價(jià)值產(chǎn)生直接影響[2]。成花過程是一個(gè)復(fù)雜的生理過程，該過程受外部和內(nèi)部因素的共同調(diào)控，如光周期、溫度以及內(nèi)源激素介導(dǎo)的多種途徑調(diào)控[2~4]。在過去幾十年，通過對擬南芥()的成花生理和分子機(jī)制的研究，發(fā)現(xiàn)光周期途徑、春化途徑和環(huán)境溫度途徑主要傳遞光和溫度等外部信號(hào)；而自主途徑、赤霉素途徑和年齡途徑在很大程度上以內(nèi)源信號(hào)為主[1,2,5~7]?？梢?，在自然狀態(tài)下植物成花是對多種環(huán)境和內(nèi)源信號(hào)識(shí)別和整合后作出的應(yīng)答。

植物內(nèi)源激素(plant endogenous hormones)參與植物的整個(gè)生命過程，通過在植物體內(nèi)構(gòu)建復(fù)雜完整的信號(hào)網(wǎng)絡(luò)，傳遞外源或內(nèi)源信號(hào)來調(diào)控植物的生長發(fā)育。因此，激素信號(hào)對于成花的影響非常重要[8,9]。在特定的條件下，激素信號(hào)的調(diào)控往往是將不同激素信號(hào)匯集后通過改變關(guān)鍵成花基因的表達(dá)水平來實(shí)現(xiàn)[10]。赤霉素(gibberllins, GA)作為赤霉素途徑中主要的信號(hào)因子，在成花過程必然發(fā)揮著關(guān)鍵性的作用，但其他激素如脫落酸(abscisic acid, ABA)、生長素(auxin, IAA)、細(xì)胞分裂素(cytokinin, CTK)、水楊酸(salicylic acid, SA)、茉莉酸(jasmonic acid, JA)和乙烯(ethylene, ET)等，也是參與激素調(diào)控網(wǎng)絡(luò)不可缺少的部分[3,11]。對于溫室種植或精細(xì)化管理的作物而言，通過光周期和溫度等控制外部信號(hào)可實(shí)現(xiàn)對成花的調(diào)控；但是對于大田種植的作物而言，則存在易被干擾、成本較高和可操作性差等缺點(diǎn)。因此，研究成花過程中激素的調(diào)控作用，解析植物體內(nèi)信號(hào)調(diào)控網(wǎng)絡(luò)，可為大田作物生產(chǎn)提供指導(dǎo)借鑒。本文主要對激素調(diào)控植物成花的機(jī)理研究進(jìn)行了綜述，并總結(jié)出部分激素互作通路模式圖(圖1)，以期為更好地研究植物花的誘導(dǎo)、花芽分化和花器官發(fā)育中激素作用機(jī)理和調(diào)控機(jī)制提供參考。

1 赤霉素途徑

GA是一類四環(huán)二萜類化合物，在植物生長發(fā)育過程中起著重要的調(diào)節(jié)作用。迄今為此，自然界中發(fā)現(xiàn)的GA形態(tài)結(jié)構(gòu)超過136種，但是只有GA1、GA3、GA4和GA7少數(shù)形態(tài)具有生理活性[12]。近年來，隨著分子遺傳學(xué)和功能基因組學(xué)的不斷發(fā)展，GA調(diào)控植物生長發(fā)育的模式被解析的十分透徹[13,14]。越來越多的研究表明，GA在去抑制和信號(hào)轉(zhuǎn)導(dǎo)等方面發(fā)揮著重要的作用[14,15]。GA信號(hào)轉(zhuǎn)導(dǎo)主要借助于GID1 (GA insensitive dwarf 1)、DELLA蛋白和介導(dǎo)DELLA蛋白降解的其他調(diào)控因子實(shí)現(xiàn)，可見DELLA蛋白是GA合成及其信號(hào)轉(zhuǎn)導(dǎo)過程中的核心因子，在GA合成以及其信號(hào)轉(zhuǎn)導(dǎo)中發(fā)揮著重要作用。

1.1 GA與植物成花

赤霉素途徑調(diào)控成花是最早被發(fā)現(xiàn)的4條成花途徑之一，擬南芥內(nèi)源GA合成受阻或者破壞GA在體內(nèi)的信號(hào)轉(zhuǎn)導(dǎo)過程，成花進(jìn)程均會(huì)受到影響[16]。GA信號(hào)轉(zhuǎn)導(dǎo)是由活性GA激活的，而GA作為可移動(dòng)的分子，可通過細(xì)胞膜在細(xì)胞間進(jìn)行運(yùn)輸[17]。細(xì)胞間GA的動(dòng)態(tài)平衡主要由GA合成途徑中關(guān)鍵限速酶基因和、失活和降解途徑中氧化酶基因調(diào)控。GA信號(hào)轉(zhuǎn)導(dǎo)依賴一類核蛋白DELLA的介導(dǎo)[18]，DELLA蛋白被認(rèn)為是植物生長發(fā)育和成花的抑制因子。水稻(L)中僅存在一個(gè)基因編碼DELLA蛋白[19,20]，而擬南芥存在5個(gè)特異性的基因，包括(GA insen-sitive)、(repressor of GAL-3)和3個(gè)gal-3-like蛋白的抑制基因(、和)，這些基因既存在功能的冗余又具有特異性[8,21]。擬南芥突變體在短日照下不開花，在長日照下呈現(xiàn)中度晚花現(xiàn)象[22]。該現(xiàn)象揭示赤霉素途徑調(diào)控低于光周期調(diào)控，當(dāng)光周期調(diào)控不起主導(dǎo)作用時(shí)，赤霉素途徑的重要性被凸顯出來。但是近期研究發(fā)現(xiàn)，無論光周期調(diào)控信號(hào)是否存在，GA都具有獨(dú)特的調(diào)控模式促進(jìn)成花。Porri等[23]發(fā)現(xiàn)長日照下GA也可以上調(diào)FT (flowering locus T)和TSF (twin sister of FT)蛋白的表達(dá)水平促進(jìn)成花。Galv?o等[24]發(fā)現(xiàn)環(huán)境溫度途徑誘導(dǎo)擬南芥成花需要借助GA信號(hào)轉(zhuǎn)導(dǎo)，DELLA在長日照下可沉默葉片中miR172和莖尖的基因參與自主途徑抑制成花[25]，DELLA也下調(diào)年齡途徑中miR156的靶基因(squamosa promoter bi-nding protein-like)參與成花[22]?？梢奊A信號(hào)參與年齡、自主和環(huán)境溫度等途徑的調(diào)控[22,24,26~28]。FT蛋白的合成部位在葉片，但其被運(yùn)送至SAM中才發(fā)揮作用[11]，因此GA調(diào)控成花的作用部位分為葉片和SAM。

成花途徑關(guān)鍵基因用黃色高亮標(biāo)記，紅色和綠色分別代表激素的作用，紅色代表促進(jìn)、綠色代表抑制；虛線箭頭代表遷移，→代表正調(diào)控，┤代表負(fù)調(diào)控，雙向符號(hào)代表互相作用。GA：赤霉素；ABA：脫落酸；IAA：生長素；CTK：細(xì)胞分裂素；SA：水楊酸；JA：茉莉酸；ET：乙烯。CO: constans; FT: flowering locus T; AP1: apetala 1; SOC1: suppressor of overexpression of constans; LFY: leafy; SPLs: squamosa promoter binding protein-like; BOIs: botrytis susceptible1 interactors; PIFs: phytochrome interacting factor; AREB: ABA responsive element binding protein; ABI: abscisic acid-insensitive; HDA6: histone deacetylase 6; FLC: flowering locus C; SVP: short vegetative phase; MYC: myelocytomatosis proteins; JAZ: jasmonate ZIM-domain protein; MYB33: MYB domain protein 33; TFL: terminal flower。

1.2 葉片中的GA調(diào)控

眾多的研究表明，當(dāng)植物體內(nèi)GA含量較低或者GA信號(hào)傳遞受阻的情況下，基因表達(dá)水平處于較低水平；而當(dāng)葉面上外源噴灑GA或恢復(fù)GA信號(hào)傳遞時(shí)，基因表達(dá)水平上調(diào)[23,24,27~29]。這些結(jié)果支持長日照下GA可增強(qiáng)基因的轉(zhuǎn)錄活性這一觀點(diǎn)。但也有研究發(fā)現(xiàn)葉面噴灑GA既不能改變野生型植株在短日照下基因的轉(zhuǎn)錄水平，也不能改變長日照下突變體基因的轉(zhuǎn)錄水平[29,30]。所以，長日照下GA是否調(diào)控基因的表達(dá)量還需要更多的研究來驗(yàn)證。

GA可通過多種機(jī)制調(diào)節(jié)基因的表達(dá)水平實(shí)現(xiàn)成花調(diào)控[23,24,27,28]。AP2 (apetala 2)類蛋白負(fù)調(diào)節(jié)葉片中基因的轉(zhuǎn)錄活性，而葉片中DELLA可抑制miR172的表達(dá)，實(shí)現(xiàn)對miR172靶基因的上調(diào)[31~33]。Yu等[27]也發(fā)現(xiàn)GA對miR172的調(diào)控是借助于DELLA和miR172的正調(diào)控因子SPLs來實(shí)現(xiàn)。當(dāng)然部分(如)基因編碼序列可直接與基因序列結(jié)合，并激活基因轉(zhuǎn)錄[34]。Yu等[27]還指出DELLA組成型激活表達(dá)后，miR172的表達(dá)量被顯著下調(diào)，可能是由于DELLA與SPLs蛋白結(jié)合引起的，同時(shí)會(huì)引起基因轉(zhuǎn)錄水平下調(diào)。在突變體中過表達(dá)miR172可改善其晚花現(xiàn)象[31]，這也證明DELLA可能是通過調(diào)控模式增強(qiáng)對的轉(zhuǎn)錄抑制。

DELLA除了可激活基因的抑制因子外，還會(huì)干擾關(guān)鍵轉(zhuǎn)錄激活因子CO (constans)蛋白的功能。DELLA可與CO或含有CO結(jié)構(gòu)域的類似物結(jié)合，使其與DNA互作而喪失功能[35,36]。因此，不論是GA含量降低還是增強(qiáng)DELLA蛋白水平，其最終結(jié)果都是導(dǎo)致和的轉(zhuǎn)錄水平降低，這與CO蛋白的穩(wěn)定性恰好一致[23,30]。體外研究發(fā)現(xiàn)，DELLA可阻止CO和NFYB(nuclear transcription factor Y subunit B)互相結(jié)合，從而使CO失去激活的功能[35,37]。CO與NFY (nuclear transcription factor Y)復(fù)合物的主要功能是維持染色體上位點(diǎn)的特異性結(jié)構(gòu)，從而有利于的轉(zhuǎn)錄激活[38]。因此，DELLA可通過降低CO蛋白功能來阻止染色體上位點(diǎn)的特異性結(jié)構(gòu)的形成[30]。但是，Hou等[28]提出DELLA與NFYB和NFYC也可以互相結(jié)合，所以DELLA的調(diào)控機(jī)制可能更為復(fù)雜。

DELLA蛋白可與多種轉(zhuǎn)錄因子結(jié)合同時(shí)抑制CO蛋白功能和基因的轉(zhuǎn)錄激活，其本質(zhì)是通過與轉(zhuǎn)錄因子結(jié)合互作的方式降低與DNA的結(jié)合能力[39]。如光敏色素互作因子(phytochrome interacting factor 4)是的激活因子，在溫敏途徑中CO蛋白也可被互作激活。DELLA與結(jié)合后，的功能被抑制[40~42]?？梢姡珿A利用DELLA與PIF4或PIFs類轉(zhuǎn)錄因子的互作機(jī)制調(diào)控植物成花時(shí)間[43]。

除了結(jié)合互作的方式外，DELLA還可通過其他機(jī)制影響轉(zhuǎn)錄因子[39]。Li等[44]研究發(fā)現(xiàn)，DELLA與轉(zhuǎn)錄因子的結(jié)合，不但產(chǎn)生“隔離”的作用，還能降解。DELLA還可以引導(dǎo)轉(zhuǎn)錄抑制因子作用于特定的基因位點(diǎn)，如BOIs (botrytis susce-ptible1 interactors)蛋白[45]。BOIs蛋白在花芽分化期富集，但需要依賴于DELLA才能被引導(dǎo)至啟動(dòng)子區(qū)域富集并與位點(diǎn)結(jié)合，抑制的轉(zhuǎn)錄[46]。除了依賴于DELLA的方式外，BOIs蛋白也可通過其CCT結(jié)構(gòu)域與CO蛋白結(jié)合，干擾CO與DNA的識(shí)別機(jī)制[46]。同樣，DELLA蛋白還可與FLC (flowering locus C)形成復(fù)合物阻礙基因的轉(zhuǎn)錄激活[47]。

1.3 SAM中的GA調(diào)控

SAM是GA調(diào)控成花的另一個(gè)作用部位。外源噴灑GA不能激活短日照下葉片內(nèi)基因的表達(dá)，但卻可以促進(jìn)野生型、突變體和突變體成花[23,29,48,49]。非成花條件下，葉片中高含量GA誘導(dǎo)SAM成花，因此Hisamatsu和King[29]提出GA成花調(diào)控途徑不借助于葉片中的成花基因。這可能是葉片中合成的GA被運(yùn)輸至SAM才激活成花基因表達(dá)，也可能是GA擁有不依賴于葉片中FT蛋白的調(diào)控機(jī)制[17]。Zhu等[50]發(fā)現(xiàn)葉片中合成FT蛋白在NaKR1 (sodium potassium root defective 1)蛋白作用下被運(yùn)輸至SAM中發(fā)揮作用。雖然GA在植物體內(nèi)的精準(zhǔn)分布情況還缺乏研究，但是GA可在細(xì)胞間被主動(dòng)運(yùn)輸已被廣泛認(rèn)可[51,52]。研究發(fā)現(xiàn)GA4含量會(huì)在SAM花芽分化期急劇上升，與成花進(jìn)程密切相關(guān)；但是通過分子水平的研究發(fā)現(xiàn)，該階段SAM中與GA4生物合成相關(guān)基因并未提前呈現(xiàn)上調(diào)趨勢，因此GA4含量的增加是由于SAM以外的部位運(yùn)輸補(bǔ)充[17]。NFL (no flowering in short day)轉(zhuǎn)錄因子是短日照下GA穩(wěn)態(tài)的關(guān)鍵調(diào)控因子，突變體的SAM中GA生物合成和分解代謝相關(guān)基因相對野生型分別呈現(xiàn)下調(diào)和上調(diào)的現(xiàn)象，這表明該突變體的SAM中GA呈現(xiàn)低活性狀態(tài)；但在長日照條件下，突變體與野生型類似，表現(xiàn)為開花表型，因此NFL及其靶基因的調(diào)控與光周期調(diào)控也密切相關(guān)[53]。

SAM中GA含量變化受到多種成花基因的影響。Andrés等[54]發(fā)現(xiàn)長日照下SAM中GA合成關(guān)鍵酶基因(gibberellin 20-oxidase 2)表達(dá)量在花芽分化期顯著增加，他們認(rèn)為基因表達(dá)的積累與FT蛋白的激活有關(guān)，F(xiàn)T蛋白通過下調(diào)成花抑制因子SVP (short vegetative phase)的表達(dá)水平來增加GA20ox2的表達(dá)量。因此，在長日照下FT信號(hào)運(yùn)輸至SAM后，可促進(jìn)GA積累，促進(jìn)花芽分化。Li等[55]發(fā)現(xiàn)高GA含量又可反饋抑制基因表達(dá)，他們認(rèn)為SVP是SAM中GA生物合成相關(guān)基因的關(guān)鍵調(diào)控者。FLC/SVP復(fù)合物可上調(diào)(gib-berellin 2-oxidase)的表達(dá)促進(jìn)GA的降解，還可促進(jìn)GA合成關(guān)鍵酶GA3ox (gibberellin 3-oxidase)的抑制因子(tempranillo 1)和的表達(dá)[47,54]。因此，SVP/FLC復(fù)合物可以影響GA合成和代謝相關(guān)酶來調(diào)控GA在SAM中的動(dòng)態(tài)平衡。除了調(diào)控GA生物合成和分解代謝的方式外，DELLA可將GA信號(hào)傳遞到多種調(diào)控途徑。DELLA可激活miR159的轉(zhuǎn)錄表達(dá)，抑制MYB33 (MYB domain protein 33)的活性，從而完成對花分生組織特異性基因(leafy)的抑制，延緩成花進(jìn)程[56~59]。也有研究指出，GA信號(hào)可直接上調(diào)的激活因子(suppressor of overexpression of constans)的表達(dá)，實(shí)現(xiàn)對LFY的激活，該過程不依賴于DELLA和miR159/MYB33調(diào)控途徑[56,60]。但是，Yu等[27]發(fā)現(xiàn)DELLA可抑制SPLs的轉(zhuǎn)錄來下調(diào)SOC1的表達(dá)水平；也有研究指出在長日照條件下，在花芽分化期SOC1可引起SAM中部分表達(dá)量的上調(diào)，從而實(shí)現(xiàn)自我調(diào)節(jié)的反饋回路[23,61]?？梢?，GA對LFY的調(diào)控存在多種復(fù)雜的調(diào)控機(jī)制。

GA也參與SAM中由miR156及其靶基因調(diào)控的年齡途徑[62]。miR156-SPLs調(diào)控模式在進(jìn)化上較為保守，隨著植物生長發(fā)育逐漸下調(diào)miR156的水平導(dǎo)致SPLs的積累增加；SPLs擁有眾多參與SAM成花調(diào)控的靶基因，如miR172、、(apetala 1)和(fruitful)等成花基因[62~64]。外源噴灑GA僅能輕微緩解過表達(dá)miR156植株的晚花表型[27,65]，可見在SPLs積累過少時(shí)，GA對DELLA蛋白的降解并不能激活成花。所以，GA參與年齡途徑的調(diào)控發(fā)生在mi156表達(dá)量降低后，參與增加SPLs的積累調(diào)控。DELLA蛋白對的調(diào)控可分為轉(zhuǎn)錄和轉(zhuǎn)錄后兩個(gè)水平。DELLA蛋白抑制莖尖不同基因的轉(zhuǎn)錄激活[23,24]。Park等[66]和Zhang等[67]均發(fā)現(xiàn)DELLA與染色質(zhì)重塑因子PKL(pickle)的拮抗結(jié)合可抑制基因的轉(zhuǎn)錄。而轉(zhuǎn)錄后的調(diào)控是DELLA蛋白直接與SPLs結(jié)合，降低SPLs結(jié)合靶基因的活性[27,65]。越來越多的研究已經(jīng)證實(shí)GA通過DELLA-SPLs互作機(jī)制調(diào)控成花，在短日照條件下這種互作機(jī)制尤為顯著[27,65,68,69]，但GA的具體作用與的種類密切相關(guān)。在短日照下突變體與GA缺陷型突變體均呈現(xiàn)為極晚花表型，因此Hyun等[65]認(rèn)為是DELLA在短日照下調(diào)控的關(guān)鍵性靶基因，只有當(dāng)GA充足并消除DELLA對SPL15的抑制作用，SPL15與SOC1才能協(xié)同誘導(dǎo)FUL的表達(dá)，影響SAM其他成花基因的表達(dá)。但Xu等[69]的研究結(jié)果指出短日照下的成花調(diào)控作用不是唯一的，原因是序列存在高度的冗余。相反，在花分生組織中當(dāng)DELLA與SPL9結(jié)合后，有助于激活A(yù)P1啟動(dòng)子的轉(zhuǎn)錄表達(dá)[70]。因此，DELLA與SPLs的互作需要根據(jù)SPL的種類及其調(diào)控的DNA序列具體分析。

2 其他激素途徑

2.1 JA

JA及其衍生物屬于脂質(zhì)類植物激素，JA類衍生物的信號(hào)途徑及應(yīng)對逆境脅迫的反應(yīng)機(jī)制被研究的較為透徹[71,72]，但在花期調(diào)控中的作用研究較少。擬南芥中參與JA應(yīng)答的HDA6 (histone deacetylase 6)參與染色質(zhì)的去乙?；^程，抑制基因表達(dá)，這表明HDA6是JA參與成花調(diào)控的關(guān)鍵因子[73~75]。有研究顯示，擬南芥JA合成缺陷型突變體表現(xiàn)為雄性不育，同時(shí)發(fā)現(xiàn)突變體的花絲延伸能力、花粉成熟和花藥開裂程度均受到影響[76,77]。同時(shí)，雙基因突變體也呈現(xiàn)短花瓣、短雄蕊花絲和花藥不開裂等現(xiàn)象[78]。而外源噴灑JA后，隨著JA含量增多調(diào)節(jié)花絲成熟的(auxin respo-nse factor 6)和基因在花藥開裂期大量表達(dá)，可見JA可促進(jìn)雄蕊和雌蕊成熟[78]。研究表明，和分別是miR167和miR160的靶基因[78,79]，因此JA與miR167和miR160共同控制和參與成花調(diào)控[80]。Zhai等[81]還發(fā)現(xiàn)JA可借助JAZ (jasmonate ZIM-domain protein)蛋白將信號(hào)傳遞給轉(zhuǎn)錄因子MYCs (myelocytomatosis proteins)，來抑制的表達(dá)并延遲成花。雖然以上結(jié)果顯示JA參與花器官發(fā)育或抑制的表達(dá)，但其在成花途徑中的作用還缺乏研究，與其他激素是否存在串聯(lián)調(diào)控機(jī)制也未被證實(shí)。

2.2 ABA

ABA是一類倍半萜類植物激素，參與植物蛋白質(zhì)和脂質(zhì)合成、種子脫水耐受、種子休眠和成花等生長發(fā)育過程[82]，同時(shí)ABA還參與多種非生物脅迫應(yīng)答[83,84]。目前，ABA信號(hào)是否參與花芽分化仍存在爭議，很多報(bào)道相互對立[85,86]。生理研究發(fā)現(xiàn)，ABA積累被認(rèn)可有利于木本植物溫州蜜柑()的花芽孕育[87]；但是在溫州蜜柑花芽誘導(dǎo)期，ABA處于較低水平，在花原基形成時(shí)才上升到較高水平，故ABA對花芽分化的作用因所處階段而異[88]。ABA在陸地棉()[89]、蘋果()[90]的花芽分化期含量逐漸增高，可見高濃度ABA有利于花芽分化；但高含量的ABA不利于龍眼()的花芽形成[91]。在草本植物中，內(nèi)源ABA是打破百合花()鱗莖休眠促進(jìn)花芽分化的關(guān)鍵物質(zhì)[92]，ABA在菊花()花芽分化期呈現(xiàn)為逐漸升高的現(xiàn)象[93]?；虻难芯堪l(fā)現(xiàn)，ABA可激活和基因表達(dá)，有利于擬南芥的花芽分化[94,95]。在長日照下，和突變體呈現(xiàn)晚花現(xiàn)象，而在短日照條件下表現(xiàn)正常[94,95]。

ABA信號(hào)可能參與激活轉(zhuǎn)錄或增強(qiáng)CO蛋白功能。ABA可磷酸化激活A(yù)BA反應(yīng)元件結(jié)合蛋白(ABA responsive element binding protein, AREB)來促進(jìn)的轉(zhuǎn)錄[96~99]。突變體中轉(zhuǎn)錄處于低水平并呈現(xiàn)晚花表型[100,101]；但在ABA缺陷型的突變體中，表達(dá)量雖然呈現(xiàn)下調(diào)趨勢，卻呈現(xiàn)極早花表型[100,102]。因此，ABA是否通過調(diào)控轉(zhuǎn)錄有待進(jìn)一步研究。ABA還影響CO蛋白功能和信號(hào)傳遞[95]。ABA可泛素化降解ABI3 (abscisic acid-insensitive 3)，釋放與ABI3結(jié)合的CO蛋白來促進(jìn)成花[35,103,104]。ABA還調(diào)控MYCs轉(zhuǎn)錄因子抑制FT蛋白表達(dá)，GA也存在MYC3-FT調(diào)控模式，JA調(diào)控也存在類似機(jī)制，因此ABA、GA和JA存在串聯(lián)調(diào)節(jié)CO、FT蛋白功能的現(xiàn)象[11,81,105]。ABA還可負(fù)調(diào)控下游基因延遲成花。ABA可上調(diào)bZIP轉(zhuǎn)錄因子ABI5 (abscisic acid-insensitive 5)和AP2結(jié)構(gòu)域轉(zhuǎn)錄因子ABI4 (abscisic acid-insensi-tive 4)的表達(dá)來激活轉(zhuǎn)錄[106,107]，降低表達(dá)量，延遲擬南芥成花。而的表達(dá)可被GA上調(diào)[56,60]，可見SOC1可能是GA和ABA信號(hào)進(jìn)行串聯(lián)調(diào)控的關(guān)鍵點(diǎn)之一。

2.3 ET

植物催熟激素ET與果實(shí)成熟、葉片衰老、脅迫應(yīng)答和成花過程都密切相關(guān)[108]。ET在植物組織內(nèi)分布具有廣泛性，但只有當(dāng)葉片損傷、成熟或被切除才會(huì)造成ET的合成增加。有研究發(fā)現(xiàn)ET合成受抑制的擬南芥突變體呈現(xiàn)出早花表型[109]，而ET組成型表達(dá)的突變體在短日照條件下呈晚花表型，可見ET可抑制擬南芥成花。Achard等[110]認(rèn)為ET可促進(jìn)DELLE蛋白的積累，抑制GA信號(hào)并延遲成花。低溫環(huán)境下的成花延遲現(xiàn)象被認(rèn)為屬于ET調(diào)控，Alonso等[111]認(rèn)為由于ET的抑制作用，雖然春化途徑后擬南芥體內(nèi)促進(jìn)成花的miRNA被激活，但不呈現(xiàn)開花現(xiàn)象。ET可上調(diào)甘藍(lán)型油菜()中的表達(dá)表達(dá)量，在增強(qiáng)植物抗病性同時(shí)可促進(jìn)的表達(dá)來延遲成花[112]。雖然ET可調(diào)控DELLA和HAD19蛋白實(shí)現(xiàn)對花期的調(diào)控，但ET與其他激素在成花途徑中的串聯(lián)作用機(jī)制還需要深入研究。

2.4 IAA

IAA是最早被鑒定的植物激素，影響植物細(xì)胞的伸長、分化，參與種子發(fā)育、側(cè)根形成、根和葉片的生長發(fā)育等多種生理過程[19]。同時(shí)IAA也參與植物成花調(diào)控。Mai等[113]發(fā)現(xiàn)與IAA缺陷型突變體(auxin resistant 2)在短日照下延遲成花。外源施加不同濃度IAA溶液會(huì)影響花朵的正常發(fā)育[114]。IAA是局部合成，經(jīng)過極性運(yùn)輸至作用部位，在植物體內(nèi)呈現(xiàn)梯度分布，這種動(dòng)態(tài)分布與成花進(jìn)程密切相關(guān)[115]。PIN (pin-formed)蛋白家族與IAA的極性運(yùn)輸密切相關(guān)[25]，擬南芥突變體缺失IAA的極性運(yùn)輸能力，出現(xiàn)針狀花序，花、維管組織發(fā)育缺陷[26]，外源噴灑IAA可以逆轉(zhuǎn)這種情況誘導(dǎo)成花[116]。Przemeck等[117]發(fā)現(xiàn)突變體僅能形成裸花序柄，因此IAA響應(yīng)因子ARF5 (auxin response factor 5)活性被認(rèn)為與花原基的啟動(dòng)密切相關(guān)。與花器官發(fā)育相關(guān)基因、(aintegumenta)和(aintegumenta-like 6)均屬于ARF5的靶基因[118]。ARFs和IAA還可以通過促進(jìn)和的表達(dá)[119,120]、抑制DELLA蛋白表達(dá)[121]的形式參與到GA生物合成和信號(hào)傳導(dǎo)的過程?？梢姡琁AA可以通過調(diào)節(jié)GA含量和促進(jìn)DELLA降解的方式促進(jìn)成花。

2.5 CTK

CTK是一類N6-取代的嘌呤衍生物，參與細(xì)胞的增殖和分化，與植物生長發(fā)育密切相關(guān)，在開花植物中CTK具有延緩衰老的作用[122]。盡管CTK是否參與成花轉(zhuǎn)變目前還存在爭議，但CTK調(diào)控花分生組織細(xì)胞的分裂和分化已被證實(shí)[123]。CKX (cyto-kinin oxidase/dehydrogenase enzymes)是催化降解CTK的關(guān)鍵酶，雙突變體呈現(xiàn)異常膨大的花序和花分生長組織，因此CTK參與花芽分化中細(xì)胞分化的調(diào)控[124]。Corbesier等[125]發(fā)現(xiàn)成花刺激后葉片和韌皮部中內(nèi)源CTK含量迅速增加；在短日照下，外源施加CTK可誘導(dǎo)營養(yǎng)生長期植物在細(xì)胞層面進(jìn)行成花轉(zhuǎn)變[126]?？梢?，CTK含量增加與成花轉(zhuǎn)變的存在密切聯(lián)系。此外，CTK可下調(diào)的表達(dá)水平，促進(jìn)AP2蛋白表達(dá)，使植物呈現(xiàn)花瓣增加、雄蕊和心皮增殖等缺陷型花型[31]?？梢奀TK與GA信號(hào)在miR172和AP2途徑實(shí)現(xiàn)串聯(lián)調(diào)控，但CTK參與成花調(diào)控的機(jī)制尚未被完全解析[127]。

2.6 SA

SA可促進(jìn)成花、調(diào)節(jié)種子發(fā)芽、抑制頂端優(yōu)勢、促進(jìn)測生生長、調(diào)節(jié)膜透性等多種植物生長發(fā)育[22]。目前，有關(guān)SA調(diào)控成花的研究報(bào)道越來越多。如4 μmol/L濃度的SA可促進(jìn)煙草()愈傷組織形成花蕾[128]。蒼耳屬植物韌皮部的SA含量僅在開花期能檢測到[129]。外源噴灑濃度為3~ 10 μmol/L的SA溶液，可刺激對光周期不敏感的檸檬屬植物成花[130]。這些發(fā)現(xiàn)均顯示出SA含量增加在誘導(dǎo)成花或促進(jìn)花器官發(fā)育中的作用。但是外源施加SA又可緩解由營養(yǎng)不良脅迫引起的牽牛()的早花現(xiàn)象[131]，因此SA對成花的調(diào)控與植物所處狀態(tài)密切相關(guān)[131,132]。外源施加SA溶液或紫外照射可誘導(dǎo)SA的積累，來抑制野生型擬南芥FLC轉(zhuǎn)錄因子的表達(dá)，從而促進(jìn)成花[130]。但在SA缺陷型突變體中SA是否存在抑制轉(zhuǎn)錄并促進(jìn)成花的機(jī)制仍有爭議，這是由于和的表達(dá)在短日照和長日照條件下是不同的。在長日照條件下，SA缺乏植物的和的表達(dá)水平與野生型相比下降約50%；在短日照條件下，SA缺乏植物的表達(dá)量與野生型相比增加2~3倍，但的表達(dá)兩者間無顯著差異[130]。同時(shí)，外源施加SA可逆轉(zhuǎn)突變株的晚花表型，但在長日照下對突變株無顯著改善現(xiàn)象[133]?？梢?，SA參與成花調(diào)控網(wǎng)絡(luò)的串聯(lián)點(diǎn)可能位于CO下游和SOC1上游區(qū)域，但具體機(jī)制以及SA是否參與成花調(diào)控還有待進(jìn)行深入研究。

3 結(jié)語與展望

植物成花調(diào)控不僅受外界環(huán)境因子影響，而且植物體內(nèi)的各種激素存在互相協(xié)同和拮抗作用，是一個(gè)復(fù)雜的調(diào)控過程。植物激素調(diào)控是植物感受外部環(huán)境變化信號(hào)，利用多種激素的協(xié)同或拮抗的作用調(diào)整自身的生長和分化進(jìn)程，增強(qiáng)對環(huán)境適應(yīng)能力的調(diào)控方式。最新的研究表明，以DELLA介導(dǎo)的GA信號(hào)調(diào)節(jié)中樞及其調(diào)控的多種成花因子(如CO、FT、LFY和SOC1等)，在GA和其他成花途徑或激素信號(hào)途徑關(guān)鍵調(diào)控因子的互相作用中發(fā)揮著重要作用。目前，對于激素調(diào)節(jié)植物成花的機(jī)制還未被深入解析，在不同植物的成花進(jìn)程和花器官發(fā)育中激素調(diào)控機(jī)制、激素的動(dòng)態(tài)變化以及在不同組織或細(xì)胞的精準(zhǔn)分布都尚待進(jìn)一步闡明。隨著高通量測序技術(shù)的發(fā)展以及轉(zhuǎn)錄組、蛋白質(zhì)組和代謝組等手段在成花調(diào)控研究中的應(yīng)用，必將會(huì)全面解析激素調(diào)控植物成花的網(wǎng)絡(luò)途徑。

今后對激素調(diào)控成花機(jī)理的研究可能主要集中在以下幾個(gè)方面：(1)進(jìn)一步闡明激素在不同環(huán)境下與各種成花途徑互作的分子機(jī)制，以及多種激素在時(shí)間和空間上協(xié)同或拮抗的串聯(lián)互作機(jī)制。(2)表觀遺傳機(jī)制及其對植物成花的生理、代謝和分子調(diào)控影響，解析激素調(diào)控成花的表觀遺傳規(guī)律。隨著氣候變化的加劇，表觀遺傳對成花誘導(dǎo)的影響越來越顯著，而植物激素信號(hào)在表觀遺傳調(diào)控營養(yǎng)期到生殖期的轉(zhuǎn)變過程中不可或缺。DNA甲基化、組蛋白翻譯后修飾和miRNAs剪切等表觀遺傳調(diào)控將指導(dǎo)人們更好地開發(fā)適應(yīng)新環(huán)境挑戰(zhàn)的植物。(3)應(yīng)用外源激素調(diào)控花芽分化或花器官發(fā)育的可行性。不同物種、品種等激素調(diào)控的差異性較大，對開花植物特別是附加值較高的花卉植物的調(diào)控可借助溫室大棚調(diào)控光周期或溫度等手段來實(shí)現(xiàn)。但是對于大田種植或附加值較低的植物，此方法成本較高。因此研究開發(fā)和應(yīng)用外源激素控制成花對指導(dǎo)農(nóng)業(yè)生產(chǎn)具有重要意義。

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Progress on the mechanism of hormones regulating plant flower formation

Liping Zou, Cheng Pan, Mengxin Wang, Lin Cui, Baoyu Han

Flowering is the adaptability of plants in response to the environment, which is regulated by the complex flowering control network formed by a variety of exogenous and endogenous signals. Plant hormones, the most important endogenous signal participants, play important roles in the process of plant flowering. Recent reports reveal the pivotal roles of hormones in the epigenetic regulation and flowering promotion pathway. In addition, synergistic or antagonistic interaction has been observed among many hormones. Numerous hormones have been found to be involved in the regulation of the multiple flowering development regulation and signaling pathways mediated by DELLA protein in the gibberellin (GA) pathway. In this review, we summarize the recent advances ofthe flowering mechanisms related to GA pathway and discuss the effects of abscisic acid (ABA), auxin (IAA), cytokinin (CTK), salicylic acid (SA), jasmonic acid (JA), and ethylene (ET) on flowering, including their cross-regulation with DELLA, miRNAs, and transcription factor (TFs). This review provides a reference for further comprehensive analysis of the hormone-regulated network of plant flower formation.

plant hormone; flower bud differentiation; floral regulation; signal transduction

2020-01-13;

2020-03-11

國家重點(diǎn)研發(fā)計(jì)劃項(xiàng)目(編號(hào)：2018YFC1604402)，浙江省重點(diǎn)研發(fā)計(jì)劃項(xiàng)目(編號(hào)：2020C02026)和浙江省基礎(chǔ)公益研究計(jì)劃項(xiàng)目(編號(hào)：LGN18C160006，LGN20C140005)資助[Supported by the National Key Research and Development Program of China (No. 2018YFC1604402), the Zhejiang Provincial Key Research and Development Program of China (No.2020C02026), and the Zhejiang Provincial Fundamental and Public Welfare of China (Nos. LGN18C160006, LGN20C140005)]

鄒禮平，在讀碩士研究生，專業(yè)方向：生物化學(xué)與分子生物學(xué)。E-mail: 1223760931@qq.com

韓寶瑜，博士，教授，研究方向：化學(xué)生態(tài)與分子生物學(xué)。E-mail: hanby15@163.com

10.16288/j.yczz.20-014

2020/4/16 9:17:22

URI: http://kns.cnki.net/kcms/detail/11.1913.R.20200416.0846.002.html

(責(zé)任編委: 李傳友)