活性氧調(diào)控豆科植物早期結(jié)瘤的研究進(jìn)展*

汪 錦, 陳 平, 杜 青, 張曉娜, 周 穎, 任建銳, 王 甜, 雍太文

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活性氧調(diào)控豆科植物早期結(jié)瘤的研究進(jìn)展*

汪 錦, 陳 平, 杜 青, 張曉娜, 周 穎, 任建銳, 王 甜, 雍太文**

(四川農(nóng)業(yè)大學(xué)農(nóng)學(xué)院/四川省作物帶狀復(fù)合種植工程技術(shù)研究中心/農(nóng)業(yè)部西南作物生理生態(tài)與耕作重點(diǎn)實(shí)驗(yàn)室 成都 611130)

活性氧(reactive oxygen species, ROS)是一類(lèi)具有高反應(yīng)活性的氧衍生物, 包括超氧陰離子(?O2—)、羥自由基(?OH)、過(guò)氧羥自由基(?HO2)以及過(guò)氧化氫(H2O2)等。植物在進(jìn)行有氧代謝或遭遇生物與非生物脅迫時(shí)會(huì)產(chǎn)生ROS, 它不僅僅是有氧代謝的有毒副產(chǎn)物, 同時(shí)能作為信號(hào)分子調(diào)節(jié)體內(nèi)代謝過(guò)程, 對(duì)抗外界環(huán)境。豆科植物形成根瘤時(shí)同樣會(huì)產(chǎn)生ROS, 這種ROS的變化區(qū)別于病原體入侵, 而是作為一種信號(hào)物質(zhì)參與結(jié)瘤過(guò)程。結(jié)瘤因子(nod factor, NF)誘導(dǎo)下ROS的產(chǎn)生參與了浸染線形成時(shí)細(xì)胞壁的重建、植物基質(zhì)糖蛋白(matrix glycoprotein, MGP)的交聯(lián)和肌動(dòng)蛋白微絲的成核和延長(zhǎng)過(guò)程。細(xì)胞質(zhì)膜NADPH氧化酶(respiratory burst oxidase homologue, RBOHs)是共生過(guò)程中ROS產(chǎn)生的主要途徑,基因的過(guò)表達(dá)會(huì)促進(jìn)根瘤菌浸染和根瘤形成, 同時(shí)根瘤中的共生微粒體數(shù)量增加, 固氮效率提高, 而表達(dá)受抑制后會(huì)減少ROS的產(chǎn)生, 同時(shí)下調(diào)結(jié)瘤相關(guān)基因、、的表達(dá), 抑制固氮酶活性。此外, ROS時(shí)空上的變化與Ca2+相關(guān)聯(lián), 協(xié)同調(diào)控根系結(jié)瘤。ROS的產(chǎn)生是植物與微生物早期的識(shí)別信號(hào), 通過(guò)認(rèn)識(shí)ROS在早期結(jié)瘤過(guò)程中的作用有助于我們進(jìn)一步理解共生關(guān)系建立的特異性。本文就ROS在早期結(jié)瘤過(guò)程中的產(chǎn)生及其發(fā)揮的作用做了綜述, 指出ROS通過(guò)直接或間接作用誘導(dǎo)結(jié)瘤基因的表達(dá), 是豆科植物根瘤形成以及功能固氮的重要信號(hào)分子。

活性氧; 結(jié)瘤信號(hào); 根瘤形成; 固氮; 豆科作物

自然環(huán)境中的含氮化合物約1/2來(lái)自生物固氮, 1/2來(lái)自人類(lèi)活動(dòng), 主要是肥料的生產(chǎn)和石油的消耗[1]。大量微生物能將空氣中的N2還原成銨態(tài)氮, 并與植物[主要是豆科(Leguminosae)植物]建立共生關(guān)系, 其中, 根瘤菌能與一百多種農(nóng)業(yè)作物共生固氮[1]。據(jù)統(tǒng)計(jì), 在全球范圍內(nèi), 根瘤菌與豆科作物共生固定的氮素每年大約有2億t[2]。豆科作物是重要的糧食作物和經(jīng)濟(jì)作物, 占世界主要作物產(chǎn)量的25%[1]。豆科作物根瘤固定的氮素會(huì)殘留在土壤中為非豆科作物提供氮源[3], 因此被廣泛應(yīng)用于輪作和間套作系統(tǒng), 具有明顯的生態(tài)效益和經(jīng)濟(jì)效益。

共生關(guān)系的建立始于豆科作物與根瘤菌的分子信號(hào)交流。豆科植物缺氮時(shí)植株根系會(huì)分泌一類(lèi)特殊的類(lèi)黃酮物質(zhì), 它是一大類(lèi)具有C6-C3-C6結(jié)構(gòu)基本骨架的低分子量多酚類(lèi)物質(zhì)的總稱。根瘤菌感知類(lèi)黃酮信號(hào)后會(huì)生成結(jié)瘤因子(nod factor, NF), 結(jié)瘤因子是一類(lèi)專(zhuān)一性脂殼寡糖信號(hào)(lipochitooligosacc-harides, LCOs)[4], 它能使根毛變形卷曲并產(chǎn)生持續(xù)的胞內(nèi)Ca2+振蕩, 引發(fā)一系列信號(hào)級(jí)聯(lián)放大反應(yīng), 激活下游轉(zhuǎn)錄調(diào)節(jié)子的轉(zhuǎn)錄, 其中包括鈣離子/鈣調(diào)素蛋白激酶CCaMK (calcium and calmodulin-dependent protein kinase)[5-6]、NSP1 (nodulation signaling pathway 1)[7]、NSP2 (nodulation signaling pathway 2)[8]、ERN (Ets2 repressor factor required for nodulation)[9]和NIN (nodule inception)[10-11]。而這些轉(zhuǎn)錄調(diào)節(jié)子能激活早期結(jié)瘤基因(early nodulation genes, ENODs)的表達(dá)[12], 誘發(fā)根瘤形成。根瘤中的固氮根瘤菌能與宿主植株進(jìn)行有效的代謝物交換, 根瘤菌將空氣中的氮?dú)廪D(zhuǎn)換為氨為宿主提供氮源, 而宿主保護(hù)共生根瘤菌不受環(huán)境威脅的同時(shí)為其提供有機(jī)碳[2]。

活性氧(reactive oxygen species, ROS)是氧分子(O2)逐步還原所產(chǎn)生的一類(lèi)具有高反應(yīng)活性的代謝產(chǎn)物。氧分子單電子還原形成超氧陰離子(?O2-)和過(guò)氧羥自由基(?HO2), 第2次單電子還原會(huì)形成過(guò)氧化氫(H2O2), 第3次單電子還原則產(chǎn)生羥自由基(?OH), 而?OH的再次還原形成水分子(H2O)(圖1)。在植物體內(nèi), ROS主要在葉綠體、線粒體和過(guò)氧化物酶體中產(chǎn)生, 是植株有氧代謝的副產(chǎn)物。正常生理狀態(tài)下, 植物細(xì)胞體內(nèi)產(chǎn)生的ROS水平較低。ROS的化學(xué)不穩(wěn)定性使其在生物體中發(fā)揮多方面功能, 特別是植物與微生物的互作過(guò)程中[13-14]。早年研究發(fā)現(xiàn)植株在受到病原體感染時(shí)會(huì)使宿主產(chǎn)生一種特殊的信號(hào)——氧化爆發(fā), 即短時(shí)間內(nèi)大量的ROS產(chǎn)生以抵御病原體入侵。這些ROS不僅具有直接的抗菌作用, 而且能影響防御基因的表達(dá)、過(guò)敏反應(yīng)的激活、細(xì)胞壁蛋白的交聯(lián)和植保素的產(chǎn)生等[15]。同時(shí), 植物能維持適當(dāng)?shù)腞OS濃度使其作為第二信使介導(dǎo)植株生長(zhǎng)和對(duì)外界環(huán)境的響應(yīng), 如細(xì)胞伸長(zhǎng)與分裂[16-18]、氣孔關(guān)閉、種子萌發(fā)、細(xì)胞程序性死亡[19-20]以及側(cè)根的生長(zhǎng)與花的發(fā)育[21]。研究發(fā)現(xiàn)根瘤菌在浸染豆科作物時(shí)同樣會(huì)伴隨ROS水平的變化。這種變化區(qū)別于病原體入侵, 而是作為一種重要的信號(hào)物質(zhì)促使結(jié)瘤發(fā)生。

圖1 活性氧的產(chǎn)生和信號(hào)調(diào)控

1 結(jié)瘤因子誘導(dǎo)ROS的產(chǎn)生

豆科植物感知NFs信號(hào)后會(huì)使根毛卷曲, 包裹根瘤菌, 根瘤菌穿過(guò)根毛形成浸染線逐步進(jìn)入根皮層,最終形成根瘤。該過(guò)程包含了一系列復(fù)雜的信號(hào)轉(zhuǎn)導(dǎo)機(jī)制: Ca2+內(nèi)流與Ca2+振蕩、ROS的產(chǎn)生、細(xì)胞質(zhì)的烷基化以及結(jié)瘤基因的表達(dá)[22]。NF處理數(shù)秒后的菜豆()根毛細(xì)胞尖端能檢測(cè)到短暫升高的ROS, 且不同于真菌誘導(dǎo)子、ATP、H2O2以及UV處理下的ROS水平。因此, NF能誘導(dǎo)ROS的產(chǎn)生, 且該ROS具有NF誘導(dǎo)的特異性[23]。突變菌不能產(chǎn)生NF, 當(dāng)它與蒺藜苜蓿()接種時(shí), 檢測(cè)不到ROS的變化, 說(shuō)明ROS的產(chǎn)生可能發(fā)生在NF信號(hào)感知的下游[24]。Breakspear等[25]發(fā)現(xiàn)NF能激活結(jié)瘤誘導(dǎo)的過(guò)氧化物酶基因(rhizobially induced peroxidases,), 這些基因的表達(dá)可能與ROS的產(chǎn)生有關(guān)。

細(xì)胞質(zhì)膜NADPH氧化酶(respiratory burst oxidase homologue, RBOHs)是植物與病原體互作過(guò)程中氧化爆發(fā)的主要來(lái)源[26], 也是共生過(guò)程中ROS產(chǎn)生的重要途徑[27]。NF受體突變的苜蓿()植株在NF處理下不能抑制過(guò)氧化氫的外流率, 而將野生型苜蓿用NF預(yù)處理1 h后, 添加DPI(NADPH氧化酶活性抑制劑)會(huì)使過(guò)氧化氫外流率較對(duì)照減少20%, 可以推測(cè)NADPH氧化酶可能參與NF誘導(dǎo)下的ROS的產(chǎn)生[28]。無(wú)活性的NF處理后的苜蓿檢測(cè)不到ROS的變化, 說(shuō)明根毛中RBOHs依賴的ROS水平變化需要特殊的NF的激活[29]。然而, 這種NF的誘導(dǎo)并非持續(xù)的, 一段時(shí)間后NF會(huì)抑制H2O2的產(chǎn)生[30-31]。NF的這種雙重作用可能在根瘤菌與豆科作物的共生信號(hào)中扮演著重要角色。

2 ROS參與浸染線的形成和根瘤發(fā)育

植株受到病原侵害時(shí)會(huì)迅速做出過(guò)敏反應(yīng)(hypersensitive response, HR)。HR主要表現(xiàn)為浸染點(diǎn)的局部細(xì)胞死亡, 以阻礙細(xì)菌的進(jìn)一步侵入, 同時(shí)會(huì)誘導(dǎo)系統(tǒng)防御抵抗烈性病原體。其早期特征是在短時(shí)間內(nèi)產(chǎn)生大量的ROS[32]。研究發(fā)現(xiàn)根瘤菌浸染豆科植物時(shí)會(huì)發(fā)生過(guò)敏反應(yīng), 利用NBT著色法觀察到苜蓿浸染線和年幼根瘤及成熟根瘤的浸染細(xì)胞中均有大量的ROS產(chǎn)生, 并使浸染點(diǎn)附近的根毛細(xì)胞迅速死亡[33-34]。而ROS的產(chǎn)生以及特定細(xì)胞的死亡與浸染口的形成密切相關(guān)[35]。根毛生長(zhǎng)與浸染線的伸長(zhǎng)具有相似性, 諸如浸染口絲狀激動(dòng)蛋白的累積和浸染線生長(zhǎng)頂端分泌小泡的沉淀[36], 而ROS參與了浸染線延伸過(guò)程中細(xì)胞壁的重建[37]。H2O2能通過(guò)聚合細(xì)胞壁中的酚類(lèi)物質(zhì)來(lái)增加細(xì)胞壁硬度, 而氫氧自由基則通過(guò)裂解細(xì)胞壁聚合物增加細(xì)胞壁松弛程度[38]。Rubio等[39]在浸染線基質(zhì)、外壁周?chē)约捌蛹?xì)胞間隙中檢測(cè)到大量H2O2, 可能與浸染線和細(xì)胞壁的形成有關(guān)。浸染線的形成是通過(guò)一種植物基質(zhì)糖蛋白(plant matrix glycoprotein, MGP)的交聯(lián)作用, 它主要存在于植物組織的胞外基質(zhì)和浸染線的內(nèi)腔, 而MGP的不溶性會(huì)受到H2O2的調(diào)節(jié)[40]。能編碼一種ABL類(lèi)似蛋白, 這種蛋白參與了肌動(dòng)蛋白微絲的成核和延長(zhǎng)過(guò)程, 與根瘤菌的浸染密切相關(guān), 而H2O2能調(diào)節(jié)的表達(dá)[41]。

NADPH氧化酶是產(chǎn)生ROS的主要酶類(lèi)。NADPH氧化酶抑制劑DPI處理蒺藜苜蓿根系會(huì)抑制根毛的卷曲和浸染線的形成[42]。NADPH氧化酶基因近年來(lái)被發(fā)現(xiàn)存在于豆科植物的基因庫(kù)中, 利用RNAi敲除菜豆中的NADPH氧化酶基因后, ROS產(chǎn)生明顯減少且結(jié)瘤受到抑制[43]。而過(guò)表達(dá)的菜豆根系能促進(jìn)根瘤菌的浸染, 增加根瘤數(shù)量[44]。Jamet等[45]利用H2O2穩(wěn)態(tài)缺陷菌接種苜蓿時(shí), 根瘤菌過(guò)氧化物酶的過(guò)量表達(dá)會(huì)減少浸染線中的H2O2濃度, 浸染線的形成受到影響。在擬南芥()中發(fā)現(xiàn)了一種膜聯(lián)蛋白(AtAnn1), 它能調(diào)節(jié)RBOH來(lái)源的ROS刺激下Ca2+的內(nèi)流[46-47]。Carrasco- Castilla等[48]發(fā)現(xiàn)菜豆-RNAi轉(zhuǎn)基因根系中, 根瘤原基中ROS的產(chǎn)生受阻,、和的轉(zhuǎn)錄水平均下調(diào), 導(dǎo)致浸染線的形成和延伸受到影響, 根瘤發(fā)育受到限制。因此, 植株可能利用調(diào)節(jié)ROS水平來(lái)控制浸染線的延伸及結(jié)瘤信號(hào)。根瘤中的一種特異性NCR多肽能控制類(lèi)菌體的分裂過(guò)程[49]。研究發(fā)現(xiàn), 花生()根瘤中H2O2的增加會(huì)提高類(lèi)菌體的密度, ROS可能通過(guò)調(diào)節(jié)NCR的氧化還原狀態(tài)來(lái)控制類(lèi)菌體的分裂[50]。TOR蛋白參與了ROS信號(hào)的感知和信號(hào)傳遞[51], 菜豆的-RNAi突變根系中,基因的轉(zhuǎn)錄水平下調(diào), 且ROS水平下降, ROS相關(guān)結(jié)瘤基因轉(zhuǎn)錄顯著下降, 浸染線數(shù)量明顯降低, 且浸染受阻, 根瘤中共生體和類(lèi)菌體數(shù)量減少, 固氮有效性下降[52]。ROS能控制根系細(xì)胞的增殖和分化[16], 根瘤生長(zhǎng)發(fā)育過(guò)程中, ROS可能參與了根瘤原基的分化, 但具體機(jī)制有待進(jìn)一步研究。

ROS不僅在早期根瘤形成中發(fā)揮了重要作用, 而且在后期根瘤的固氮功能中至關(guān)重要[44]。侵染后生長(zhǎng)6周左右的根瘤細(xì)胞中有H2O2的存在[34], 而NADPH氧化酶基因主要在不定型根瘤的分生區(qū)尖端進(jìn)行表達(dá), 且該基因的表達(dá)與固氮能力密切相關(guān),基因表達(dá)量的下降會(huì)顯著抑制固氮酶活性[27]。過(guò)表達(dá)突變株的ROS含量增加, 根瘤中有更豐富的共生微粒體, 每個(gè)浸染細(xì)胞中的類(lèi)菌體數(shù)量更多, 聚-β-羥基丁酸鹽的含量更高, 有效提高了固氮效率[44]。根瘤固氮需要植株為類(lèi)菌體提供碳源, 蔗糖合成酶在碳代謝中發(fā)揮了重要作用, 而根瘤中的氧化還原環(huán)境會(huì)影響蔗糖合成酶在根瘤中的功能。此外, ROS可能還參與了根瘤后期的衰老。不定型根瘤的衰老區(qū)及侵染后生長(zhǎng)10周左右的定型根瘤的共生微粒體周?chē)軝z測(cè)到大量H2O2的存在, 這些H2O2可能與根瘤衰老時(shí)引發(fā)的氧化脅迫有關(guān)[53]。

3 Ca2+與ROS協(xié)同調(diào)控根系結(jié)瘤

Ca2+信號(hào)是植物對(duì)外界環(huán)境作出生理和細(xì)胞反應(yīng)的核心調(diào)節(jié)子。Ca2+流信息的編碼和傳遞主要通過(guò)Ca2+結(jié)合蛋白上的Ca2+響應(yīng)啟動(dòng)元件來(lái)調(diào)節(jié)轉(zhuǎn)錄和磷酸化, 從而影響基因的表達(dá)和細(xì)胞生理[54]。Ca2+信號(hào)流是結(jié)瘤過(guò)程中一條重要的信號(hào)通路[37]。

Ca2+和ROS是植物頂端生長(zhǎng)的重要因素, 例如花粉管的生長(zhǎng)以及根毛的伸長(zhǎng)[55-57]。同時(shí), 纖維細(xì)胞的生長(zhǎng)也受到Ca2+和ROS的調(diào)控[58-59]。NADPH氧化酶產(chǎn)生的ROS對(duì)Ca2+通道的激活可能是ROS介導(dǎo)信號(hào)途徑的重要步驟, 是植物常見(jiàn)的信號(hào)鏈路[37,60-61], 而擬南芥可能參與了ROS和細(xì)胞質(zhì)Ca2+濃度驅(qū)動(dòng)的信號(hào)以及ROS激活的Ca2+流[62]。ROS可以激活細(xì)胞質(zhì)膜Ca2+通道, Ca2+內(nèi)流通過(guò)正反饋調(diào)節(jié)激活NADPH氧化酶相關(guān)的RBOH蛋白[37,63-64], 主要依賴RBOH蛋白的EF-手型結(jié)構(gòu)域和N端區(qū)上游區(qū)域[65]?？梢酝茰y(cè), Ca2+流能同時(shí)作用于ROS的上游和下游[60]。

高等植物在受到病菌侵害時(shí)會(huì)發(fā)生氧化迸發(fā), 該反應(yīng)主要是由致病誘導(dǎo)子與特異受體的相互作用所致。誘導(dǎo)子與受體的結(jié)合會(huì)激活Ca2+通道產(chǎn)生Ca2+流從而調(diào)節(jié)NADPH氧化酶活性[28,66]。豆科作物結(jié)瘤時(shí), NF會(huì)引起豆科植物根毛細(xì)胞兩種典型的離子情況變化, 一是Ca2+流, 二是Ca2+振蕩[67]。研究發(fā)現(xiàn), 影響Ca2+振蕩的苜蓿突變體(、、、、和)在受到NF處理時(shí), ROS的產(chǎn)生會(huì)減少[28]?？梢圆聹y(cè)Ca2可能與ROS存在某種聯(lián)系。進(jìn)一步研究發(fā)現(xiàn), Ca2+變化的同時(shí)伴有ROS的產(chǎn)生。Ca2+與ROS在早期共生互作過(guò)程中可能發(fā)揮協(xié)同作用[23]。Morieri等[29]認(rèn)為NF會(huì)激活NF受體誘導(dǎo)根瘤形成的兩條途徑, 第一條是Ca2+振蕩, 其次是RBOH活性和Ca2+流, 后者與根瘤菌的浸染有關(guān)。盡管RBOH在這一過(guò)程中的激活機(jī)制尚不清楚, 但已有研究發(fā)現(xiàn)RBOH的N端能與Ca2+結(jié)合誘導(dǎo)ROS的產(chǎn)生[65,68]。由于RBOH產(chǎn)生的ROS能促進(jìn)Ca2+通道的打開(kāi)[56], 可以猜測(cè)結(jié)瘤早期信號(hào)傳遞中, 二者可能存在某種反饋調(diào)節(jié)。Glyan’ko等[69]發(fā)現(xiàn)NADPH氧化酶的激活依賴Ca2+通道的打開(kāi), 而過(guò)多的Ca2+會(huì)抑制NADPH氧化酶的活性。在根毛細(xì)胞尖端, ROS在時(shí)空上的變化與Ca2+流相關(guān)聯(lián), NF信號(hào)感知后, 短暫的ROS響應(yīng)可能會(huì)激活根毛尖端的Ca2+通道, Ca2+內(nèi)流, 而Ca2+反過(guò)來(lái)會(huì)活化NAD(P)H氧化酶產(chǎn)生更多的ROS, 引發(fā)一系列信號(hào)傳遞[23](圖2)。

4 根瘤形成依賴ROS的合理控制

ROS對(duì)根毛浸染有著重要作用, 但是持續(xù)升高的ROS水平對(duì)結(jié)瘤有不利影響[70]。在紫花苜蓿結(jié)瘤時(shí)不是所有的浸染線都會(huì)成功延伸至根瘤原基, 許多浸染線的形成會(huì)由于根皮層的過(guò)敏反應(yīng)而中止[23]。外源施用ROS會(huì)阻礙NF誘導(dǎo)的根毛膨大和分枝[30]。因此, 有假設(shè)認(rèn)為NF會(huì)激活第一次ROS的產(chǎn)生幫助結(jié)瘤, 而會(huì)抑制與防御反應(yīng)相關(guān)的第二次ROS的產(chǎn)生[71]。NF通過(guò)調(diào)節(jié)植物的抗氧化機(jī)制和ROS生產(chǎn)系統(tǒng)[31], 抑制或清除ROS的產(chǎn)生來(lái)維持ROS在體內(nèi)的穩(wěn)態(tài)[23], 使根瘤菌能進(jìn)入宿主而不會(huì)激發(fā)植株的防御反應(yīng)[23]。

flg22是一種細(xì)菌鞭毛蛋白, 它能引發(fā)一系列防御反應(yīng), 如Ca2+內(nèi)流、ROS的產(chǎn)生、絲裂原激活蛋白的活化以及基因的表達(dá)等。而將NF作用于非豆科作物擬南芥時(shí), 它會(huì)抑制flg22誘導(dǎo)的ROS的產(chǎn)生[72]。NF處理菜豆根毛細(xì)胞時(shí), ROS含量在1 min左右會(huì)達(dá)到最大值, 3 min后開(kāi)始逐漸降低, 而H2O2和UV處理后其ROS的含量在3 min后仍然持續(xù)升高, 殼聚糖處理后在5min后急劇上升, 9 min達(dá)到最大值[30]。NF作用于蒺藜苜蓿根部時(shí), 20~30 min后H2O2的流出會(huì)受到抑制[28], 且NADPH氧化酶同源物的轉(zhuǎn)錄表達(dá)減少。不難想象, ROS只有在適宜的時(shí)間與位置產(chǎn)生才能使根瘤菌順利進(jìn)入宿主而不引發(fā)過(guò)敏反應(yīng)[23]。而蒺藜苜蓿對(duì)NF的初始響應(yīng)是區(qū)別于防御反應(yīng)下的氧化爆發(fā)。PGA是一類(lèi)防御相關(guān)的氧化爆發(fā)誘導(dǎo)子, 研究發(fā)現(xiàn), 同PGA處理比較, NF處理下的苜蓿略微加速了H2O2的外流, 且在20 min內(nèi)發(fā)生逆轉(zhuǎn)?？梢哉J(rèn)為, NF使植物過(guò)氧化氫外流率的減緩有助于根毛的卷曲和浸染所需的細(xì)胞壁生長(zhǎng)的變化, 同時(shí)抑制了防御反應(yīng)相關(guān)基因的表達(dá)[28]。植株也能通過(guò)調(diào)節(jié)體內(nèi)抗氧化酶的代謝來(lái)控制氧化環(huán)境, 為共生發(fā)育提供合適的條件。Mu?oz等[31]發(fā)現(xiàn)在花生接種后15~30 min, 其根系的過(guò)氧化氫酶(CAT)活性增加, 60 min后活性開(kāi)始下降, 而過(guò)氧化酶(PX)在接種后30~60 min后增加, 240 min后開(kāi)始下降。百脈根()根瘤中發(fā)現(xiàn)了兩種谷胱甘肽過(guò)氧化酶(glutathione peroxidases, Gpxs)[73], 且在浸染區(qū)大量表達(dá), NF通過(guò)激活和抑制相關(guān)的抗氧化物酶來(lái)合理控制氧化環(huán)境。

圖2 活性氧(ROS)與Ca2+在豆科作物結(jié)瘤信號(hào)傳遞中扮演的角色

LysM RLKs: 受體激酶; RBOH: 細(xì)胞質(zhì)膜NADPH氧化酶。LysM RLKs: receptor kinases; RBOH: respiratory burst oxidase homologue.

紫花苜蓿在結(jié)瘤共生時(shí), 其浸染線中能檢測(cè)到O2-和H2O2, 而在類(lèi)菌體和根瘤菌中未能檢測(cè)到ROS的存在, 表明根瘤菌存在一種高效的ROS清除機(jī)制。研究發(fā)現(xiàn)兩種過(guò)氧化氫酶katB和katC在浸染過(guò)程中具有重要的作用,和突變菌不能正常結(jié)瘤[74], 根瘤菌從浸染線中釋放后, 形成的類(lèi)菌體迅速衰老。而過(guò)氧化氫酶編碼基因及其轉(zhuǎn)錄激活子編碼基因的突變菌也表現(xiàn)出根瘤數(shù)目的減少及固氮效率的降低[73]。細(xì)胞質(zhì)超氧化物歧化酶(superoxide dismutase, SOD)的編碼基因的突變菌接種苜蓿后, 能被宿主正常識(shí)別, 且5 d后浸染線的數(shù)量與野生型植株無(wú)差異, 然而10 d后, 浸染線生長(zhǎng)終止, 根瘤形成受阻。SOD的缺失使根瘤菌遭受氧化脅迫, 從而抑制了浸染線的形成[75]。花生與根瘤菌早期互作過(guò)程中, 根瘤菌中的過(guò)氧化酶(peroxidase, PX)參與調(diào)節(jié)宿主的氧化爆發(fā)免疫反應(yīng)[50], 清除有害的ROS。

豆科作物通過(guò)控制ROS來(lái)調(diào)節(jié)早期結(jié)瘤相關(guān)的信號(hào)通路, 根瘤菌利用自身的抗氧化物酶改變氧化環(huán)境, 二者協(xié)調(diào)作用使浸染線正常形成, 最終誘導(dǎo)根瘤發(fā)生。

5 結(jié)論與展望

豆科作物從根瘤菌浸染再到根瘤形成發(fā)育伴隨著一系列復(fù)雜的信號(hào)傳遞。ROS同Ca2+一樣在細(xì)胞信號(hào)轉(zhuǎn)導(dǎo)中的作用不可小覷。它能作為一種信號(hào)物質(zhì)間接調(diào)節(jié)早期結(jié)瘤過(guò)程, 通過(guò)ROS受體或Ca2+信號(hào)來(lái)激活相關(guān)基因的表達(dá)[41], 同時(shí)參與后期發(fā)育以及功能固氮(圖2)。根瘤菌與宿主的兼容性取決于防御反應(yīng)的抑制程度[76], 而ROS的產(chǎn)生是植物常見(jiàn)的防御反應(yīng), 可能與結(jié)瘤特異性有重要聯(lián)系。

除ROS外, 活性氮(RNS)是另一種參與植物生長(zhǎng)發(fā)育及生物與非生物脅迫的活性物質(zhì)[77-78]。共生結(jié)瘤過(guò)程中, NO在根瘤形成發(fā)育及功能固氮中同樣發(fā)揮重要作用[79], 它能調(diào)節(jié)線粒體呼吸和碳氮代謝, 同時(shí)與ROS存在密切的聯(lián)系[14,71,80], NO能通過(guò)調(diào)節(jié)NADPH氧化酶的活性來(lái)控制ROS的產(chǎn)生[81]。過(guò)氧化亞硝酸鹽(ONOO-)是NO與O2-發(fā)生作用時(shí)的信號(hào)分子, 可能參與共生結(jié)瘤時(shí)二者的交互作用[82]。同時(shí), Blanquet等[83]的研究證明了NO與O2-在根瘤中的直接聯(lián)系。然而, 共生結(jié)瘤過(guò)程中ROS/NO交互作用類(lèi)型還有待于繼續(xù)挖掘。

非豆科作物由于不能正確識(shí)別結(jié)瘤因子而不能形成根瘤[84]。ROS的產(chǎn)生是植物與微生物早期的識(shí)別信號(hào), 而在豆科結(jié)瘤過(guò)程中, ROS作用的靶基因和靶蛋白, ROS與NO的時(shí)空關(guān)系以及與防御反應(yīng)的聯(lián)系等尚不清楚。通過(guò)認(rèn)識(shí)ROS在早期結(jié)瘤過(guò)程中的信號(hào)傳遞有助于進(jìn)一步理解共生關(guān)系建立的特異性, 利用分子手段來(lái)控制共生關(guān)系, 擴(kuò)大共生范圍, 從而提高根瘤固氮的農(nóng)業(yè)潛力。

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The role of reactive oxygen in regulating early nodulation of legumes*

WANG Jin, CHEN Ping, DU Qing, ZHANG Xiaona, ZHOU Ying, REN Jianrui, WANG Tian, YONG Taiwen**

(College of Agronomy, Sichuan Agricultural University / Sichuan Engineering Research Center for Crop Strip Intercropping System / Key Laboratory of Crop Ecophysiology and Farming System in Southwest, Ministry of Agriculture, Chengdu 611130, China)

Research on the production and function of reactive oxygen species (ROS) formed during early nodulation in legumes was reviewed. The ROS are highly reactive oxygen derivatives, including superoxide anion (?O2-), hydroxyl radical (?OH), hydroperoxyl radical (?HO2), and hydrogen peroxide (H2O2). These radicals were produced during aerobic metabolism and when plants were under biotic and abiotic stresses. While toxic, these compounds serve as signalers that can trigger metabolism regulations to combat adverse environments. The ROS are produced during nodulation in legumes, induced by the nod factor (NF), to participate in infection formation, contributing to cell wall reconstruction, cross-linking of matrix glycoprotein (MGP), and actin microfilament nucleation and branching. Symbiotic production of ROS is primarily through cytoplasmic membrane NADPH respiratory burst oxidase homologue (RBOHs). Overexpression ofstimulates rhizobia infection and nodule formation, resulting in increased number of symbiotic microsomes and nitrogen fixation efficiencies. Conversely, inhibition ofdecreases the production of ROS and down-regulates the expression of related,and. The ROS regulate nodulation also in conjunction with Ca2+through spatial and temporal alterations. In conclusion, ROS in legumes are a group of signaler molecules that function to regulate nodulation through genes expression.

ROS; Nodulation signal; Nodulation; Nitrogen fixation; Legume

, E-mail: yongtaiwen@sicau.edu.cn

Sep. 14, 2018;

Nov. 1, 2018

Q945

A

2096-6237(2019)03-0405-08

10.13930/j.cnki.cjea.180839

汪錦, 陳平, 杜青, 張曉娜, 周穎, 任建銳, 王甜, 雍太文. 活性氧調(diào)控豆科植物早期結(jié)瘤的研究進(jìn)展[J]. 中國(guó)生態(tài)農(nóng)業(yè)學(xué)報(bào)(中英文), 2019, 27(3): 405-412

WANG J, CHEN P, DU Q, ZHANG X N, ZHOU Y, REN J R, WANG T, YONG T W. The role of reactive oxygen in regulating early nodulation of legumes[J]. Chinese Journal of Eco-Agriculture, 2019, 27(3): 405-412

* 國(guó)家自然科學(xué)基金面上項(xiàng)目(31671625)和國(guó)家重點(diǎn)研發(fā)計(jì)劃項(xiàng)目(2016YFD0300202)資助

雍太文, 主要從事作物生理生態(tài)研究。E-mail: yongtaiwen@sicau.edu.cn

汪錦, 主要從事根瘤形成及根系分泌物方面的研究。E-mail: Wjinida@163.com

2018-09-14

2018-11-01

* This study was supported by the National Natural Science Foundation of China (31671625) and the National Key Research and Development Project of China (2016YFD0300202).