植物對鹽堿脅迫的響應(yīng)機(jī)制研究進(jìn)展

王佺珍,劉 倩,高婭妮, 柳 旭

西北農(nóng)林科技大學(xué), 動(dòng)物科技學(xué)院草業(yè)科學(xué)系, 楊凌 712100

植物對鹽堿脅迫的響應(yīng)機(jī)制研究進(jìn)展

王佺珍,劉 倩*,高婭妮, 柳 旭

西北農(nóng)林科技大學(xué), 動(dòng)物科技學(xué)院草業(yè)科學(xué)系, 楊凌 712100

鹽堿脅迫是制約植物生長發(fā)育的主要非生物脅迫之一,也是制約農(nóng)作物生產(chǎn)和生態(tài)環(huán)境建設(shè)的嚴(yán)峻問題。研究作物的耐鹽堿機(jī)理,對開發(fā)和有效利用鹽堿地有重要的現(xiàn)實(shí)意義。許多研究將鹽堿脅迫籠統(tǒng)稱為鹽脅迫,實(shí)際上這是兩種不同的非生物脅迫,且堿脅迫對植物的傷害要大于鹽脅迫?？偨Y(jié)性闡述了鹽堿脅迫對植物的危害。從生物量、光合作用、離子平衡和膜透性等方面分析了植物對鹽堿脅迫的響應(yīng)機(jī)制,并結(jié)合最新研究從多角度綜述了植物的抗鹽堿機(jī)理,包括合成滲透調(diào)節(jié)物質(zhì)、提高抗氧化酶活性、對離子的選擇性吸收及pH平衡和誘導(dǎo)抗鹽堿相關(guān)基因表達(dá)。提出了抗鹽堿性的途徑,即外源物質(zhì)的加入、與真菌的協(xié)同效應(yīng)、利用生物技術(shù)手段、培育耐鹽堿品種和抗性鍛煉。最后針對植物適應(yīng)鹽堿逆境方面的研究進(jìn)行了展望,提出了當(dāng)前研究需要解決的問題和突破口,旨在為提高植物耐鹽堿能力、增加作物產(chǎn)量提供一定的理論依據(jù)。

鹽堿脅迫；響應(yīng)；緩解；研究進(jìn)展

Abstract： Salinity-alkalinity stress (SAS) is one of the major abiotic stresses affecting the growth and development of plants and has been a severe problem that restricts crop production and even the development of the ecological environment. It is vital to understand the mechanisms behind the response to SAS in plants for effective reclamation and utilization of saline-alkali soil. Plants vary in response to salt and alkali stresses, but salt stress has generally been the focus of numerous SAS studies. In addition, alkali stress is more severe than salt stress because of the accompanying high pH stress, which can inhibit uptake of ions and disrupt the ionic balance of cells. This article briefly describes the damage caused by these stresses and interprets the mechanisms in terms of the influences on biomass, photosynthesis, ion balance, and membrane permeability using a comprehensive summary of the advances in research on the physiological and biochemical responses to SAS. We focused on the alleviating mechanisms of plants under SAS with regard to selective ion absorption and pH balance, the synthesis of osmotic regulation substances, improvement of enzymatic antioxidant capacity, and the expression of genes relevant to SAS tolerance. Furthermore, this article proposes five ways to cope with SAS, including the addition of exogenous substances, synergistic effects of fungi, use of biotechnological tools, SAS acclimation, and breeding cultivars for SAS tolerance. Significant progress has been made using traditional methods to improve SAS tolerance, although genetic tools play a major role and comprise the direction of our further research as well. There is an urgent need to select SAS-tolerant varieties through biotechnological methods. The prospects for developing SAS tolerance are also discussed, with the aim of providing a reference for improving plant resistance to stresses and increasing crop yield. 1) Although SAS limits crop growth and reduces agricultural productivity, it may also improve the quality of some fruits. It is, therefore, important to determine a balance between the yield and quality of plants. It is also necessary to determine the dominant factors in salt-alkali tolerance. Some indices have been frequently used in past studies, and a breakthrough in new indices is required. 2) The differentially expressed proteins detected in plants have not been completely understood. The revelation of useful information related to SAS tolerance will lead to some unexpected discoveries. In the near future, it is important to increase the tolerance of plants to SAS by using genetic engineering technologies. The importance of genes in negative regulation needs to be considered. High throughput analysis of the differences in SAS tolerance between salt-tolerant plants and salt-sensitive plants may aid in determining the root causes of the differences. More economic and ecological benefits can be achieved by cultivating additional SAS-tolerant plants and exploring the beneficial effect of saline-alkali tolerant plants on saline-alkali land that requires restoration and amelioration. These analyses also provided new insights into understanding the potential tolerance systems within plants.

KeyWords: salinity-alkalinity stress; response; alleviation; research progress

世界上大約有20%的灌溉土壤受到鹽度的影響,且呈不斷惡化的趨勢[1- 2]。預(yù)計(jì)到2050年,50%以上的耕地會(huì)發(fā)生鹽堿化[3],嚴(yán)重威脅著土地利用率和作物產(chǎn)量[4]。中國鹽堿地尤其是內(nèi)陸鹽堿地多是鹽化和堿化混合,成分復(fù)雜且程度各異,使人們很容易將鹽堿混為一談,統(tǒng)稱其為鹽堿地[5]。實(shí)際上,土壤鹽化與堿化分別以鹽度、pH值升高為主要特點(diǎn),并非兩種相同的非生物脅迫[6]。鹽化和堿化常常同時(shí)發(fā)生,這種現(xiàn)象在很多地區(qū)普遍存在。最近數(shù)據(jù)統(tǒng)計(jì)顯示,中國東北鹽堿侵害的草地面積已達(dá)70%[7], 且仍在擴(kuò)大。鹽、堿對植物的危害程度從大到小依次是鹽堿脅迫、堿脅迫、鹽脅迫[8- 9]。鹽堿脅迫會(huì)降低土壤滲透勢、使離子失衡、打亂生理過程、抑制植物生長、降低作物的質(zhì)量和產(chǎn)量。嚴(yán)重地區(qū)甚至?xí)?dǎo)致植物死亡。隨著科學(xué)技術(shù)的進(jìn)步,鹽堿地在技術(shù)改良方面已經(jīng)取得了很多成果,也是應(yīng)該繼續(xù)努力的方向。但是,還存在著很多地域、資源、成本等限制,因而,培育耐鹽堿品種的植物,提高植物的耐鹽堿能力是緩解鹽堿地對植物影響的一個(gè)有效生物措施,同時(shí)還可以產(chǎn)生較好的生態(tài)和經(jīng)濟(jì)效益,促進(jìn)農(nóng)業(yè)的可持續(xù)發(fā)展。因此,關(guān)于植物適應(yīng)鹽堿逆境的研究已成為國內(nèi)外專家學(xué)者們當(dāng)前研究中的一個(gè)熱點(diǎn)。之前關(guān)于植物對鹽脅迫或堿脅迫的響應(yīng)及緩解機(jī)制的研究很多,但是對混合鹽堿脅迫下所涉及的植物的生理生化反應(yīng)、基因組學(xué)、分子生物學(xué)等多角度的響應(yīng)及緩解機(jī)制的綜述研究卻鮮有報(bào)道。因此,本文綜合分析了植物對鹽堿響應(yīng)及緩解機(jī)制的不同觀點(diǎn),提出了提高植物抗鹽堿性的有效措施,最后針對植物適應(yīng)鹽堿逆境方面的研究進(jìn)行了展望,以期為提高植物耐鹽堿能力、增加作物產(chǎn)量提供科學(xué)參考和理論依據(jù)。

1 鹽堿對植物的傷害

類似于其他非生物脅迫,植物響應(yīng)鹽堿逆境過程中涉及了復(fù)雜的生理生化反應(yīng)[10]。鹽堿脅迫會(huì)對植物產(chǎn)生很多不利的影響,包括鹽脅迫造成的滲透脅迫、離子毒害、氧化應(yīng)激等,除此之外,還會(huì)由于堿脅迫下pH的升高對植物造成進(jìn)一步的傷害。根系周圍土壤pH值升高時(shí),一些金屬離子如Fe2+、Mg2+、Ca2+等沉積,伴隨著無機(jī)陰離子減少,植物對礦質(zhì)營養(yǎng)的吸收受阻,造成嚴(yán)重營養(yǎng)脅迫[11- 12](圖1),進(jìn)而干擾植物的各種代謝活動(dòng)。這些結(jié)論大部分是在短期脅迫下研究得出的,而Munns等[10- 13]證明了在長期鹽堿脅迫下,隨著脅迫時(shí)間的延長,植物呈兩個(gè)生長階段,第一階段是其對短期脅迫的響應(yīng)(由水或滲透脅迫造成的),第二階段是對長期脅迫的調(diào)整[14](由植物體內(nèi)離子毒害作用造成的)。植物在鹽堿化土壤上生存,既要通過滲透調(diào)節(jié)和離子均衡來躲避滲透脅迫和離子毒害,又要維持體內(nèi)的pH平衡。那么鹽堿脅迫具體是通過怎樣的生理生化過程來影響植物生長的？又可以通過什么樣的機(jī)制來緩解這種傷害的呢？ 越來越多的學(xué)者開始深入地研究這些問題。

圖1 鹽堿脅迫對植物的傷害Fig.1 The harmness of salinity-alkalinity stress to plants

2 植物對鹽堿的響應(yīng)

2.1 對種子萌發(fā)和生物量的影響

外部形態(tài)和生長狀況是反映植物受鹽堿傷害程度大小的最直觀表現(xiàn)。早期種子萌發(fā)時(shí)就會(huì)受到環(huán)境脅迫的影響。Vu等[15]研究發(fā)現(xiàn)草木樨(Melilotusofficinalis)種子在未發(fā)芽階段可以通過某種機(jī)制來抵抗脅迫,在萌發(fā)階段,鹽度是影響其萌發(fā)的主導(dǎo)因素,pH是次要因素。低濃度的鹽可以促進(jìn)種子萌發(fā),高濃度則會(huì)明顯抑制其萌發(fā),且隨著鹽濃度的升高,抑制作用增強(qiáng)。類似結(jié)果在栓皮櫟(Quercusvariabilis)[16]、苜蓿(MedicagosativaL.)[17]、紅堅(jiān)木(Dysoxylumspp.)[18]、非洲菊(GerberajamesoniiBolus)[19]種子等研究中均有報(bào)道,同時(shí),渠曉霞等[20]解釋了休眠是種子抵抗鹽堿脅迫的主要策略。二型性種子在各種鹽度下的萌發(fā)策略不同。鹽脅迫下,鹽地堿蓬(SuaedasalsL.)[21-23]、藜(ChenopodiumalbumL.)[24]的棕色種子比黑色種子離子含量和萌發(fā)率更高,表現(xiàn)出更強(qiáng)的耐鹽性。外源ACC與KNO3的協(xié)同作用可以顯著提高藜黑色種子的萌發(fā)率,低濃度的CaCl2則對棕色種子有更好的緩解作用[24- 25]。GA、硫脲和硝酸鹽能緩解鹽度對蕎麥(HalopyrummucronatumL.)夏季種子的影響,GA、CTK和甜菜堿能夠減弱鹽度對冬季種子發(fā)芽的抑制[26]。此外,一些物理方法如低溫層積、松土、去除種皮通過打破休眠也可以降低鹽度對種子的傷害程度[27]。

植物對鹽堿脅迫的形態(tài)響應(yīng)主要是通過地上、地下生物量的分配體現(xiàn)的,且地上部形態(tài)和生物量表現(xiàn)更顯著。混合鹽堿脅迫下,植物株高、葉片數(shù)、莖長及地上部分干物質(zhì)重等均有所下降,地下部含水量和幼苗根長下降幅度相對較小,根莖莖節(jié)長度和比根長增加[28],對于一些耐鹽堿植物,低濃度鹽堿脅迫還可以促進(jìn)其生長,各耐鹽指數(shù)呈正態(tài)分布,表現(xiàn)出低促高抑的效應(yīng)[29],植株地上部分/地下部分干鮮重顯著下降[30]?；旌消}堿脅迫主要是通過影響植物對水分的吸收利用[31]、光合作用、酶代謝、氣孔因素[32]等來影響其重量的。

2.2 光合作用減弱

光合作用是植物物質(zhì)能量來源的關(guān)鍵代謝過程,鹽堿脅迫下,葉片細(xì)胞結(jié)構(gòu)發(fā)生顯著變化[33],光合受阻,光合速率下降。許多研究從各個(gè)角度對此做出了全面解釋。Yang等[6]實(shí)驗(yàn)證明了隨著鹽度和pH的增大,苜蓿葉片中凈光合速率、氣孔導(dǎo)度和胞間CO2濃度下降。鹽堿脅迫中產(chǎn)生的離子毒害和高pH值對植物的光系統(tǒng)II 反應(yīng)中心會(huì)造成損傷,使光合電子傳遞和PSII的光合作用活力被抑制[34]。同時(shí),葉綠體結(jié)構(gòu)損傷[35],參與光反應(yīng)和卡爾文循環(huán)的酶和蛋白下調(diào)[36]。而葉片色素的含量還與植物抗鹽堿性和鹽堿的種類、濃度有關(guān)。也有研究者認(rèn)為,光合作用產(chǎn)生的干物質(zhì)主要在葉片中積累,鹽堿脅迫下葉原基的發(fā)生受到抑制,單株植物的光合面積減少,因而間接造成植物碳同化量減少使得植物生長受到影響[37]。此外,Mg2+是葉綠素合成的必要元素,而堿脅迫還會(huì)導(dǎo)致Mg2+沉淀,使得葉綠素合成受阻[38],含量減少,光合作用減弱。實(shí)際上,凡是涉及到能量供應(yīng)的碳水化合物代謝、光合作用、TCA循環(huán)都會(huì)受到鹽堿脅迫的抑制,且堿脅迫的抑制程度大于鹽脅迫,高豐度的單糖和TCA循環(huán)中間體的積累提供了更多的能量來源[39]。

2.3 擾亂離子動(dòng)態(tài)平衡

離子在植物正常生長過程中起著重要的作用,土壤鹽堿化會(huì)打破植物體內(nèi)的離子的動(dòng)態(tài)平衡[40]。特別是堿脅迫下pH的升高會(huì)破壞根系離子的吸收運(yùn)輸。Shaheen[41]等研究發(fā)現(xiàn)羊草的根莖和葉片中,Na+含量隨著土壤鹽堿程度的增大顯著增加,而K+含量則明顯減少。在禾本科鹽生互米花草(Spartinaalterniflora)[42]、甜高粱(Sorghumbicolor)[43]、玉米(ZeamaizeL.)[44]中也得到了相似的結(jié)論。同時(shí),H+-ATP酶活性增強(qiáng),Na+/ K+交換活動(dòng)顯著上調(diào),而H+-PPase活性則有所下降。這也說明了H+-ATP酶和Na+/K+的平衡在植物抗鹽堿脅迫中發(fā)揮著重要作用。根部K+外流引起的K+-Na+不平衡還會(huì)使氣孔導(dǎo)度變小,氣孔的長度、寬度和氣孔孔徑寬度均隨鹽堿濃度的增加而降低[45]。Wang等[9]發(fā)現(xiàn)限制向日葵離子運(yùn)輸?shù)闹饕课皇亲尤~節(jié)區(qū)。不同濃度的鹽堿脅迫對抗逆性不同的植物影響有所差異,但高濃度的鹽堿脅迫會(huì)普遍對離子平衡產(chǎn)生不利影響。

2.4 膜透性增大

細(xì)胞膜是使細(xì)胞維持穩(wěn)定胞內(nèi)代謝環(huán)境的必要屏障,其具有的選擇透過性可以調(diào)節(jié)和選擇物質(zhì)進(jìn)出。在鹽堿脅迫中,植物首先受到傷害的是細(xì)胞膜的結(jié)構(gòu)和功能,引起質(zhì)膜透性增大。一方面植物體內(nèi)滲透勢升高,使植物的各種膜系統(tǒng)產(chǎn)生滲透脅迫。另一方面,由于帶電單價(jià)離子濃度的升高對細(xì)胞產(chǎn)生專性毒害作用,使一些生物大分子如酶、蛋白質(zhì)以及膜結(jié)構(gòu)的穩(wěn)定性被破壞[46]。植物葉片質(zhì)膜受傷害程度隨鹽堿濃度的增大而增加,高鹽濃度下,膜的選擇透過性被破壞,大量電解質(zhì)外滲。

生物膜的破壞主要是由膜質(zhì)過氧化造成的,質(zhì)膜的破壞程度可以用細(xì)胞質(zhì)膜透性的變化和丙二醛(malondialdehyde,MDA) 的含量來反映[47]。具有細(xì)胞毒性的膜脂過氧化產(chǎn)物丙二醛,會(huì)引起生物大分子如蛋白質(zhì)、核酸等的交聯(lián)聚合。它與質(zhì)膜透性的變化規(guī)律相同[48],兩者顯著正相關(guān),Li等[49]發(fā)現(xiàn)在輕度和中度鹽堿脅迫下,歐李(Cerasushumilis(Bge.) Sok.)葉片中MDA含量的變化趨勢與CK類似,而在重度脅迫下MDA在葉片中的含量從一開始就急劇增加。這在白刺[50]、水稻(Oryzasativa)[51]中都得到了驗(yàn)證。因此,細(xì)胞膜透性的變化反應(yīng)了外部不良環(huán)境對植物細(xì)胞的傷害程度,同時(shí)細(xì)胞膜在逆境下的穩(wěn)定性也反映了植物抗逆性的高低。

3 植物對鹽堿脅迫的緩解機(jī)制

鹽堿逆境下,植物主要通過合成滲透調(diào)節(jié)物質(zhì)、提高酶的抗氧化能力、對離子選擇性吸收、營養(yǎng)平衡、改變代謝類型、調(diào)整生物量的分配等方法來減輕不良環(huán)境對其生長發(fā)育造成的傷害。其中,植物體根的代謝調(diào)控發(fā)揮著重要作用[52-53],是植物應(yīng)對鹽堿脅迫的第一道屏障,積累溶質(zhì)來進(jìn)行滲透調(diào)節(jié)是緩解鹽堿脅迫的主要途徑。

3.1 合成滲透調(diào)節(jié)物質(zhì)

參與植物抗鹽堿過程的滲透調(diào)節(jié)物質(zhì)主要包括兩大類：(1) 從外界環(huán)境進(jìn)入植物細(xì)胞的無機(jī)離子,如K+、NO-3、Cl-和無機(jī)酸鹽等。(2) 細(xì)胞內(nèi)合成的有機(jī)溶質(zhì),如脯氨酸、甜菜堿、膽堿、有機(jī)酸等,還包括一些代謝中間產(chǎn)物如糖類及其衍生物等。這兩類滲透調(diào)節(jié)物質(zhì)在植物抵抗鹽堿脅迫中都發(fā)揮著重要作用。

Ranganayakulu等[54]發(fā)現(xiàn)高濃度鹽、堿脅迫下,花生(ArachishypogaeaL.)莖葉中甜菜堿大量積累。外源甜菜堿可以明顯提高萵苣(LactucasativaL.)[55]的生長。甜菜堿不僅參與細(xì)胞的滲透調(diào)節(jié)還在植物氣孔運(yùn)動(dòng)、穩(wěn)定生物大分子、呼吸作用等過程中發(fā)揮著重要作用。噴施外源甜菜堿,可以提高作物的滲透調(diào)節(jié)能力,減輕逆境對其的傷害[56]。

游離狀態(tài)的脯氨酸在植物體內(nèi)廣泛分布,是主要的有機(jī)滲透調(diào)節(jié)物質(zhì)。在穩(wěn)定生物大分子結(jié)構(gòu)、解除氨毒及作為能量庫調(diào)節(jié)細(xì)胞氧化還原勢等方面也起著重要作用。脯氨酸的積累是植物在鹽堿脅迫下自身出現(xiàn)的一種防御性行為,也是其遭受逆境脅迫的一種信號(hào)[57]。葉面噴施脯氨酸可以刺激莖葉和根部的生長,對提高植物干鮮重、光合速率、抗氧化酶活性等都有貢獻(xiàn)[58]。

可溶性糖不僅可以為有機(jī)物的合成提供物質(zhì)和能量,還作為一種滲透調(diào)節(jié)物質(zhì)在植物的生長發(fā)育起著重要作用,隨著鹽堿濃度的增大,植物可溶性糖含量呈先增多后減少的趨勢[59],耐鹽性強(qiáng)的在較高鹽堿濃度下可溶性糖含量仍顯著增加。在鷹嘴豆生殖生長期輸入蔗糖,可以增加不同組織中的總糖和緩解鹽誘導(dǎo)的繁殖障礙,增強(qiáng)其耐鹽性[60]。

有機(jī)酸可以清除單態(tài)氧和包含OH-的自由基,在離子平衡和酸堿調(diào)節(jié)中發(fā)揮作用。燕麥幼苗在鹽脅迫和堿脅迫下的生理響應(yīng)機(jī)制是不同的,鹽脅迫下以積累Cl-為主,堿脅迫下以積累有機(jī)酸為主[31]。Guo等[61]發(fā)現(xiàn)星星草(Puccinelliatenuiflora)在響應(yīng)堿脅迫中起關(guān)鍵作用的是根際有機(jī)酸(主要是檸檬酸)的積累,同時(shí)還發(fā)現(xiàn)甜菜堿、膽堿在鹽脅迫和堿脅迫下都對滲透調(diào)節(jié)的影響是微不足道的。這與大多數(shù)研究者的結(jié)論略有差異,其中特殊的機(jī)理還有待進(jìn)一步探討。此外,在鹽堿脅迫下,羊草中主要積累檸檬酸,蓼科中主要積累草酸[62-63],說明不同植物在緩解鹽堿對其造成的傷害中有機(jī)酸代謝調(diào)節(jié)不同。隨著脅迫時(shí)間的延長,有機(jī)酸含量下降[64],但是尚不明確這是由于其中的鹽離子及pH引起的還是合成代謝被抑制導(dǎo)致的。

3.2 提高酶的抗氧化能力

植物體內(nèi)的抗氧化酶包括超氧化物歧化酶(SOD)、過氧化物酶(POD)、過氧化氫酶(CAT)和抗壞血酸過氧化物酶(APX)等。它們主要通過清除體內(nèi)的活性氧來保護(hù)酶系統(tǒng),還參與細(xì)胞的光合、呼吸、木質(zhì)素的形成等,在葉綠體、線粒體、細(xì)胞質(zhì)中發(fā)揮作用。這些酶的活性可以反應(yīng)植物體內(nèi)代謝和抗逆性的變化。滲透調(diào)節(jié)能力越強(qiáng),保護(hù)酶活性越高的植物,對鹽堿逆境能表現(xiàn)出更好的適應(yīng)性[65-66]。

3.3 對離子的選擇性吸收及pH平衡

圖2 鹽脅迫信號(hào)轉(zhuǎn)導(dǎo)過程(參考郭文芳(2015)[80]改匯) Fig.2 Signal Transduction Pathways in Response to Salt Stress in Plants

在鹽堿脅迫下,Na+的積累會(huì)使細(xì)胞的膜系統(tǒng)受損,而K+作為一種重要的無機(jī)溶質(zhì),對降低植物細(xì)胞滲透勢和維持水分平衡至關(guān)重要。植物通過限制Na+進(jìn)入細(xì)胞,并選擇性吸收K+來維持組織細(xì)胞的高K+/Na+值以保證的正常生理代謝[72]。在植物抗鹽堿中,這種離子選擇性吸收和離子平衡比滲透調(diào)節(jié)物脯氨酸發(fā)揮著更大的作用[73]。

植物鹽脅迫信號(hào)轉(zhuǎn)導(dǎo)途徑主要有蛋白激酶途徑、ABA途徑(依賴ABA途徑、不依賴ABA途徑)、SOS途徑(圖2)。Ca2+作為第二信使與堿脅迫顯著正相關(guān),高濃度的鈣會(huì)立即觸發(fā)SOS[74]鈉排除系統(tǒng)來減輕鈉的傷害[75-76],還可以誘導(dǎo)合成新的脅迫蛋白。研究發(fā)現(xiàn),在鹽堿脅迫下鈣離子含量的增加有利于提高大米[77]、小麥[78]、番茄(LycopersiconesculentumMill.)[79]等的耐鹽堿能力。因此,植物可以通過增強(qiáng)對鈣的吸收來緩解鹽堿脅迫。最新研究還發(fā)現(xiàn),高鹽脅迫下,胡楊釋放的胞內(nèi)Ca2+和H2O2會(huì)介導(dǎo)產(chǎn)生胞外ATP (eATP)信號(hào)[69],該物質(zhì)不僅可以調(diào)節(jié)植物的生長和抗氧化防御,還能間接調(diào)節(jié)其耐鹽性。

Mg2+是葉綠素形成必不可少的元素,在光合和呼吸作用中的某些酶也需要有Mg2+的激活才能發(fā)揮作用,此外,它還可以調(diào)節(jié)氣孔關(guān)閉,影響離子平衡。Rubio 等[81]報(bào)道提高鹽堿處理液中Ca2+的含量后,胡椒(PipernigrumL.)的蒴果產(chǎn)量增加。鹽堿脅迫下植物會(huì)吸收這些對自身有利的離子,排出有害離子。同時(shí),植物還可以通過提高對微量元素的吸收及分配能力來保持體內(nèi)營養(yǎng)均衡[82],更好地適應(yīng)鹽堿脅迫。

在調(diào)節(jié)植物體pH平衡中,起主導(dǎo)作用的是有機(jī)酸和無機(jī)陰離子,鹽脅迫下細(xì)胞內(nèi)有機(jī)酸變化幅度較小,而在堿脅迫下會(huì)顯著增加來補(bǔ)充體內(nèi)的陰離子保證細(xì)胞pH穩(wěn)定。

3.4 誘導(dǎo)抗鹽堿相關(guān)基因表達(dá)

鹽堿脅迫會(huì)抑制一些正常基因的表達(dá),而加強(qiáng)與抗脅迫相關(guān)基因的表達(dá)。植物的耐鹽堿性不是由單個(gè)基因決定的,是多個(gè)抗逆基因共同表達(dá)調(diào)控的。 擬南芥中PutAPX超表達(dá)提高葉綠素含量、降低膜脂過氧化程度[83]；GmST1增加對ABA的敏感性,減少活性氧的產(chǎn)生[84]；AtHD2D[85]增加根冠比、減少M(fèi)AD含量。不同的基因通過調(diào)控不同的代謝途徑都可以提高其耐鹽堿性,這些耐鹽堿基因主要包括四大類：(1)合成滲透保護(hù)物質(zhì)的相關(guān)基因(2)離子轉(zhuǎn)運(yùn)蛋白基因(3)抗氧化相關(guān)基因(4)信號(hào)轉(zhuǎn)導(dǎo)相關(guān)基因。PEAMT基因催化產(chǎn)生磷酸膽堿提高遼寧堿蓬抗鹽性[86]、McNHX2表達(dá)產(chǎn)物NHX逆向轉(zhuǎn)運(yùn)蛋白作為離子轉(zhuǎn)運(yùn)體通過調(diào)節(jié)Na+濃度維持冰花(Mesembryanthemumcrystallinum)細(xì)胞內(nèi)離子穩(wěn)態(tài)提高其耐鹽性[87]。SlSAMS1在番茄中過表達(dá)可促進(jìn)多胺的積累,而多胺可以提高H2O2酶的活性,從而減緩細(xì)胞氧化損傷增強(qiáng)其抗鹽堿性[8]。煙草中NtABF及RrANR對ROS的清除和ABA信號(hào)途徑的正調(diào)控可使植物免受高鹽堿危害[88]。這些不同類型的基因共同協(xié)作幫助植物度過鹽堿逆境。

隨著鹽堿脅迫的增加,總糖含量和可溶性蛋白質(zhì)也會(huì)增加。張建秋等[89]在鹽堿脅迫下用雙向電泳技術(shù)分析白刺中蛋白表達(dá)情況時(shí)發(fā)現(xiàn),其葉片中蛋白總量無顯著變化,但對鹽堿脅迫有正貢獻(xiàn)的特異蛋白表達(dá)如66, 28kD蛋白明顯增多。近年來,越來越多的研究發(fā)現(xiàn),鐵蛋白的mRNA和蛋白質(zhì)也會(huì)在逆境脅迫下顯著增加,鐵蛋白通過貯藏鐵離子來幫助植物抵御氧化脅迫[90]。有報(bào)道顯示,轉(zhuǎn)基因煙草(NicotianatabacumL.)過表達(dá)鐵蛋白后,植株對活性氧的脅迫耐受性顯著提高[91]。野大豆(Glycinegracilis)的根系可以依賴特定的轉(zhuǎn)錄因子和氧化還原相關(guān)基因來響應(yīng)鹽堿脅迫[92],越來越多的耐鹽堿相關(guān)蛋白如SGF14c蛋白[93]、GsSKP21蛋白[94]、GmbZIP110[95]等在大豆中被發(fā)現(xiàn)。此外,SAM合成酶[96]、 MdSOS2L1蛋白激酶[97]等通過多胺代謝也能提高番茄的抗鹽堿能力。半胱氨酸蛋白酶抑制劑GsCPI14與鈣/鈣調(diào)素結(jié)合的受體樣蛋白激酶GsCBRLK相互作用幫助大豆抵御鹽堿脅迫[98]。由此可見,植物通過抗逆基因的選擇性表達(dá),產(chǎn)生一些抗鹽堿相關(guān)蛋白也是植物抵抗鹽脅迫的一種有效方式,而這些蛋白究竟是通過怎樣的機(jī)理來幫助植物抵抗鹽堿脅迫的還有待進(jìn)一步研究。

4 提高植物抗鹽堿性的途徑

4.1 外源物質(zhì)的加入

施加外源物質(zhì)是緩解鹽堿脅迫的一種有效抗鹽方式,現(xiàn)在已經(jīng)有越來越多對鹽堿脅迫下幼苗生長有緩解作用的外源物質(zhì)被發(fā)現(xiàn)。較常用的外源添加物主要包括四大類,一是滲透調(diào)節(jié)物質(zhì)如甜菜堿、糖類[99]、有機(jī)酸等；二是與降低膜透性有關(guān)的物質(zhì)如水楊酸、腐殖酸、Ca2+等；三是可以提高植物抗氧化能力的物質(zhì)如硒、硅[100-101]、NO[102]、γ-氨基丁酸[103]等,四是植物生長調(diào)節(jié)劑如茉莉酸[104]、CTK[105]、IAA等,此外還有一些其他物質(zhì)如鑭[106]、降黑素[107]等也可以提高植物的抗鹽堿性。當(dāng)然,還有很多外源物質(zhì)尚未發(fā)現(xiàn),需要我們深入研究發(fā)現(xiàn)更多可以提高植物抗鹽堿性的外源物質(zhì)。張毅等[108-109]研究發(fā)現(xiàn)葉面噴施亞精胺(Spd)會(huì)明顯促進(jìn)番茄生長,提高其耐鹽堿性,并證實(shí)了這與Spd對光合機(jī)構(gòu)的保護(hù)效應(yīng)和參與氮代謝提高營養(yǎng)平衡密切相關(guān)。此外該物質(zhì)還可以減輕對番茄根系線粒體的傷害[110]。Chunthaburee等[111]補(bǔ)充Spd還可以通過增強(qiáng)花青素,酚類物質(zhì)含量和抗氧化能力提高水稻的耐鹽堿性。因此,作為一種低成本的抗鹽堿方式,外源物質(zhì)緩解逆境脅迫成為研究中的熱點(diǎn)。

4.2 與真菌的協(xié)同效應(yīng)

內(nèi)生菌可以通過參與滲透調(diào)節(jié)[112]、光合作用、提高植物營養(yǎng)[113]、增強(qiáng)抗氧化系統(tǒng)等方面來緩解鹽堿脅迫對植物的傷害。Herriel等[114]報(bào)道,在NaCl脅迫下接2 種AMF對辣椒(Capsicumannuum)和洋蔥(Alliumcepa)的生長都有促進(jìn)作用,能明顯提高這兩種作物的抗鹽堿性。Zarea等[115]研究發(fā)現(xiàn)在小麥上接種內(nèi)生菌可以通過提高葉綠素含量,促進(jìn)光合作用來提高植物的抗鹽堿性。用菌根真菌既可以提高植物的抗鹽堿性又可以減少化學(xué)制劑的使用,減輕環(huán)境壓力。在這方面的研究也可以挖掘更多的思路。

4.3 利用生物技術(shù)手段

轉(zhuǎn)基因技術(shù)一直是學(xué)術(shù)研究中的熱點(diǎn),其安全性也是一個(gè)備受爭議的話題。轉(zhuǎn)OsCYP2基因水稻在苗期的抗鹽堿能力要高于對照[116]。野生大豆中分離出的基因GsJAZ2[117]、新型混合富含脯氨酸型基因GsEARLI17[118]；甜高粱中的SbCIPKs基因[119]；苜蓿中的MtWRKY76[120]、GsGSTU13[121]等都對植物耐鹽堿脅迫起著正調(diào)控作用。用攜帶小麥TaNHX2基因的根癌農(nóng)桿菌LBA4404侵染辣椒(CapsicumannuumL.),發(fā)現(xiàn)轉(zhuǎn)基因辣椒的脯氨酸、葉綠素、SOD、APX、相對含水量水平都增強(qiáng)、并減少H2O2、丙二醛含量[122]。此外,有研究報(bào)道相同條件下種植轉(zhuǎn)SOS基因高羊茅會(huì)減低土壤pH和鹽堿度。但是還沒有探明到底是哪種差異引起的。雖然現(xiàn)在在轉(zhuǎn)基因技術(shù)方面的研究越來越熱,但是相比于其他方法,這方面的研究成果相對較少,還有很大的提升的空間。

4.4 培育耐鹽堿品種

與生物技術(shù)手段相結(jié)合,對植物基因進(jìn)行修飾改造實(shí)現(xiàn)抗鹽堿基因的轉(zhuǎn)移；品種間雜交；對現(xiàn)有植物進(jìn)行耐鹽堿篩選等都是培育耐鹽堿品種的有效途徑。如擬南芥中多胺氧化酶5的功能缺失突變[123]、二倍體野生西方白三葉和普通白三葉回交[124]都可以選育出耐鹽堿品種。還要大量培育像沙棘、甜高粱、結(jié)縷草等這樣本身有較強(qiáng)耐鹽堿性的植物。此外,抗鹽堿性差異較大的兩種植物還可以通過嫁接[125]提高抗性。

4.5 抗性鍛煉

抗鹽堿鍛煉可以提高植物的抗鹽堿性。高等植物會(huì)有一些“脅迫記憶”或“脅迫印記”,植物首次受到的脅迫可以通過適應(yīng)性響應(yīng)的誘導(dǎo)增強(qiáng)植物的抗逆性[126]。一般植物在幼苗時(shí)期對鹽堿最為敏感,播種前用不同梯度的鹽堿溶液浸泡種子一段時(shí)間,吸水膨脹后再進(jìn)行萌發(fā),可以提高植物的耐鹽堿性。擬南芥種子用甲萘醌亞硫酸氫鈉(MSB)浸種后發(fā)現(xiàn)對種子萌發(fā)并沒有影響,但是卻會(huì)使擬南芥生長更快,積累更多的脯氨酸,表現(xiàn)出更高的耐鹽堿性[127]。

5 展望

在鹽堿脅迫方面,關(guān)于植物對鹽脅迫的響應(yīng)機(jī)制是研究最多的,在堿脅迫和混合鹽堿脅迫方面的研究的相對較少,而且很多研究中將鹽堿脅迫籠統(tǒng)的稱為鹽脅迫,缺乏科學(xué)性。鹽化與堿化常常同時(shí)發(fā)生,存在相互影響的交互作用。因此,研究混合鹽堿脅迫對提高作物產(chǎn)量和環(huán)境建設(shè)的影響有重要的現(xiàn)實(shí)意義。

(1) 找到平衡點(diǎn),確定主導(dǎo)影響因子 鹽堿脅迫雖會(huì)降低植物產(chǎn)量,但也會(huì)提高一些植物果實(shí)的質(zhì)量,如小麥[1]、番茄[128]、燕麥[129]等,因此,確定能使植物產(chǎn)量和質(zhì)量達(dá)到最優(yōu)的鹽濃度平衡閾值,是今后研究的一個(gè)新的突破口。目前,大多數(shù)研究多集中在種子萌發(fā)過程和植物幼苗時(shí)期,對植物整個(gè)生命過程的系統(tǒng)綜合研究較少,從植物生長的不同時(shí)期不同部位進(jìn)行探討比較各指標(biāo)的動(dòng)態(tài)變化和具體的信號(hào)轉(zhuǎn)導(dǎo)過程或許會(huì)有新的發(fā)現(xiàn)。此外,各生理過程受到不同離子、蛋白、次級(jí)代謝產(chǎn)物等交互作用的影響,發(fā)現(xiàn)新指標(biāo)、確定不同時(shí)期影響植物不同部位的主導(dǎo)因素以及植物耐鹽堿主導(dǎo)因子也是必要的。

(2) 篩選抗性基因,全面解釋機(jī)制 目前,植物對鹽堿脅迫響應(yīng)的分子機(jī)制研究還處于初級(jí)階段,篩選耐鹽堿相關(guān)基因、對基因家族進(jìn)行轉(zhuǎn)錄組測序、系統(tǒng)發(fā)育分析、亞細(xì)胞定位及利用蛋白質(zhì)互作和表達(dá)譜信息對基因功能深層預(yù)測是當(dāng)前研究的重中之重。同時(shí),也不能忽視對植物抗性有負(fù)調(diào)控作用的基因改造研究,如擬南芥中的AtRNP1[130]。植物抗鹽堿性是由多個(gè)基因共同調(diào)控的一個(gè)復(fù)雜過程,從耐鹽植物和敏鹽植物之間在抗鹽堿方面差異的角度開展高通量差異數(shù)據(jù)分析,進(jìn)而找出造成差異的根本原因,發(fā)揮蛋白質(zhì)和基因組學(xué)的優(yōu)勢,利用cDNA芯片、雙向電泳技術(shù)、農(nóng)桿菌介導(dǎo)法等對植物耐鹽堿基因進(jìn)行生物學(xué)鑒定,實(shí)現(xiàn)抗鹽堿基因的轉(zhuǎn)移,從植物生理學(xué)、基因組學(xué)、分子生物學(xué)、蛋白組學(xué)等不同學(xué)科綜合系統(tǒng)地挖掘和解釋植物的抗鹽堿機(jī)制對于改良作物具有重要的意義,也將是今后研究的熱門課題。此外,很多植物中檢測到差異表達(dá)蛋白中超過一半的蛋白質(zhì)信息是未知信息,這些未知信息里必定蘊(yùn)藏著與抗鹽堿相關(guān)的有用信息,這些信息的揭示必將在植物抗鹽堿研究中有重大突破。改造并篩選得到越來越多耐鹽堿的修復(fù)植物必將帶來更大的生態(tài)和經(jīng)濟(jì)效益,這種環(huán)境友好型的生物手段無疑具有很大的潛在優(yōu)勢和發(fā)展前景。

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Reviewonthemechanismsoftheresponsetosalinity-alkalinitystressinplants

WANG Quanzhen,LIU Qian*, GAO Yani, LIU Xu

DepartmentofGrasslandScience,CollegeofAnimalsScienceandTechnology,NorthwestAgricultureandForestryUniversity,Yangling712100,China

國家自然科學(xué)基金項(xiàng)目(31472138)

2016- 05- 16; < class="emphasis_bold">網(wǎng)絡(luò)出版日期

日期:2017- 03- 25

*通訊作者Corresponding author.E-mail: 1033820376@qq.com

10.5846/stxb201605160941

王佺珍，劉倩,高婭妮, 柳旭.植物對鹽堿脅迫的響應(yīng)機(jī)制研究進(jìn)展.生態(tài)學(xué)報(bào),2017,37(16):5565- 5577.

Wang Q Z， Liu Q, Gao Y N, Liu X.Review on the mechanisms of the response to salinity-alkalinity stress in plants.Acta Ecologica Sinica,2017,37(16):5565- 5577.