張偉珍，古麗君，段廷玉(草地農(nóng)業(yè)生態(tài)系統(tǒng)國家重點實驗室 農(nóng)業(yè)部草牧業(yè)創(chuàng)新重點實驗室 蘭州大學(xué)草地農(nóng)業(yè)科技學(xué)院，甘肅 蘭州 730020)

叢枝菌根(arbuscular mycorrhizae，AM)是由球囊菌門真菌(Glomeromycota)與陸生植物的根形成的一種共生體，在世界范圍內(nèi)分布十分廣泛。90%的維管植物都能形成AM真菌，120余種AM真菌可以和超過200 000種植物共生[1]。AM真菌可以活化土壤中的無機營養(yǎng)元素，促進(jìn)宿主植物對養(yǎng)分(如N、P、K、Zn等)的吸收[2-6]，改善宿主的營養(yǎng)狀況[7]；促進(jìn)水分代謝，增強植物抗旱性[8]；提高宿主植物對低溫、高溫的耐受性[9-10]；同時AM真菌亦可增強植物耐鹽堿的能力[11]，減輕土壤重金屬污染對植物造成的危害[12]；提高植物抗病性[13]、抗蟲性[14]，提高植物品質(zhì)及其產(chǎn)量，對于植物適應(yīng)各種逆境脅迫具有重要意義。

AM真菌在植物不同物種間的競爭中也有重要作用，可以引起群落的演替，促進(jìn)物種多樣性變化，影響生態(tài)系統(tǒng)的群落結(jié)構(gòu)變化，促進(jìn)系統(tǒng)中的碳循環(huán)及氮循環(huán)，從而在一定程度上影響全球氣候的變化[15-17]。菌根生物技術(shù)的應(yīng)用十分廣泛，它在牧場草地修復(fù)、干旱地區(qū)土壤的改良、開墾荒山、植樹造林以及保護自然生態(tài)資源、維持生態(tài)系統(tǒng)的穩(wěn)定等方面均有重要作用[18]。AM真菌可以促進(jìn)地表垃圾分解，抑制土壤微生物群落的生長，因此菌根生物技術(shù)也可廣泛應(yīng)用于環(huán)境修復(fù)，且這類技術(shù)具有適應(yīng)性強的優(yōu)點，即使在各種不利生態(tài)環(huán)境條件下，也能很好地應(yīng)用，從而能更好地維持生態(tài)系統(tǒng)平衡[19-21]。因此加大對AM真菌的研究，尤其是利用AM真菌與植物共生對植物抗逆性的影響，對于實現(xiàn)農(nóng)業(yè)可持續(xù)發(fā)展、促進(jìn)生物多樣性保護具有重要意義。

1 AM真菌對植物抗非生物逆境的抗性機制

1.1 抗旱

自然界諸多環(huán)境因子都會限制或影響植物進(jìn)行正常生理生化代謝，水分是最普遍的脅迫因子之一[22-23]。水分缺失會導(dǎo)致植物葉面積減小，氣孔關(guān)閉，根系呼吸作用加強，植株葉片光合速率和光合能力下降，嚴(yán)重時甚至造成植被大面積死亡；干旱地區(qū)土壤貧瘠，植被退化，生物多樣性較少，生態(tài)系統(tǒng)穩(wěn)定性降低，生態(tài)環(huán)境持續(xù)惡化，易遭受破壞且難以修復(fù)[24]。所以，提高植物體對干旱脅迫的耐受性可以促進(jìn)植物群落多樣性變化、維持生態(tài)系統(tǒng)結(jié)構(gòu)和功能的穩(wěn)定。

大量研究表明，AM真菌與植物體共生可以促進(jìn)宿主植物對水分的吸收與利用，提高植物對干旱脅迫的抵抗能力[25]。近年來，國內(nèi)外學(xué)者已對此進(jìn)行了大量的試驗驗證。對紫花苜蓿(Medicagosativa)、三葉草(Trifoliumalexandrium)等多種植物[26-33]的研究結(jié)果表明，在干旱脅迫條件下，摩西球囊霉(Glomusmosseae)、根內(nèi)球囊霉(G.intraradices)等AM真菌可以促進(jìn)植物生長，提高植物抗旱能力。在對紫花苜蓿的研究中發(fā)現(xiàn)，當(dāng)土壤相對含水量下降到20%時，接種摩西球囊霉的植株相比未接菌植株，其地上及地下部分的干物質(zhì)產(chǎn)量平均可增加57.93和16.47 g，可溶性糖含量增加0.018%，可溶性蛋白含量增加0.004%，丙二醛含量降低0.007 μmol·g-1[26]。有關(guān)接種AM真菌對植物體內(nèi)脯氨酸含量的影響仍存在很多爭議，對民勤絹蒿(Seriphidiumminchünense)的研究發(fā)現(xiàn)，在水分脅迫下接種AM真菌的植株葉片脯氨酸含量低于未接菌植株[28]，但在對連翹(Forsythiasuspensa)的研究中則發(fā)現(xiàn)，接種AM真菌顯著增加了植株葉片脯氨酸含量[29]。AM真菌也可提高抗氧化酶類，包括超氧化物歧化酶(SOD)、過氧化物酶(POD)和過氧化氫酶(CAT)等的活性，在土壤相對含水量為30%的干旱脅迫條件下，以摩西球囊霉和縮球囊霉(G.constrictum)接種紫穗槐(Amorphafruticosa)，其SOD活性較未接種AM真菌植株最高可增加6.61 U·(g·h)-1，POD活性最高增加189.61 μg·(g·min)-1，CAT活性最高增加49.38 U·(g·min)-1，而植株根系活力相應(yīng)提高0.17 mg·(g·h)-1[33]。另外，AM真菌對植物的作用還包括促進(jìn)土壤團聚體的形成，改善土壤理化性質(zhì)；促進(jìn)生長素合成，抑制脅迫響應(yīng)因子脫落酸的合成等(表1)。

AM真菌提高植物抗旱性的作用機制可以歸納為生理生化機制和分子機制。AM真菌影響植物抗旱性主要表現(xiàn)在植物體自身產(chǎn)生的生理生化反應(yīng)，包括提高可溶性糖、可溶性蛋白等滲透調(diào)節(jié)物質(zhì)的積累，從而提高細(xì)胞液濃度，降低細(xì)胞滲透勢，防止細(xì)胞脫水，細(xì)胞水勢降低，與外界形成較高的水勢差，提高細(xì)胞吸水或保水能力，從而適應(yīng)水分脅迫環(huán)境[26]；改變根系及葉片形態(tài)，降低葉片電解質(zhì)透出率，增加氣孔導(dǎo)度，提高根系導(dǎo)水性，增加葉綠素積累，促進(jìn)植物光合作用[27]；提高抗氧化酶類活性，增強宿主的活性氧(ROS)清除能力，降低H2O2的積累，減輕對原生質(zhì)膜的傷害，保護生物膜的完整性，有效減輕干旱脅迫對植物的傷害[23,31]；AM真菌可以分泌具有良好膠水性能的球囊霉素，有效增加土壤的滲透性及穩(wěn)定性，而AM真菌菌絲則可以與土壤微粒結(jié)合，構(gòu)建土壤團聚體的結(jié)構(gòu)骨架，促進(jìn)穩(wěn)定性較高的土壤團聚體的形成，改善土壤理化性質(zhì)，從而實現(xiàn)植物耐旱性能的提升[40]；AM真菌菌絲網(wǎng)絡(luò)構(gòu)成了高效的營養(yǎng)物質(zhì)吸收和轉(zhuǎn)運系統(tǒng)，可以提高植物養(yǎng)分吸收效率，增強宿主植物的資源獲取能力，促進(jìn)植物營養(yǎng)代謝，從而促進(jìn)水分吸收與利用，提高宿主抗旱性[41]。而究其本質(zhì)，AM真菌提高植物抗旱性主要是通過上調(diào)或者下調(diào)脅迫應(yīng)答基因表達(dá)，以及誘導(dǎo)新的抗逆基因表達(dá)等來實現(xiàn)的，如特異性調(diào)節(jié)水孔蛋白基因、編碼脫水素的基因gmPIP2、gmlea8和gmlea10等相關(guān)基因的表達(dá)，其中水孔蛋白基因控制著水孔蛋白的合成，這種蛋白可以形成一個具有高度選擇性的獨立水通道，從而促進(jìn)植物體水分的吸收與運輸；而基因gmPIP2、gmlea8和gmlea10均可編碼脫水素，這是植物體內(nèi)的一種晚期胚胎富集蛋白(late embryogenesis-abundant proteins，LEA)，具有很強的親水性，可以維持細(xì)胞膜結(jié)構(gòu)及功能的穩(wěn)定，保護蛋白質(zhì)和螯合金屬離子，因此與植物響應(yīng)干旱脅迫密切相關(guān)[30-32]。目前，有關(guān)AM真菌對植物干旱脅迫的影響及其抗性機制的研究主要集中于植物個體水平的生理生化層面，而對于菌根植物適應(yīng)干旱脅迫的分子機制還缺乏系統(tǒng)深入的研究。

表1 AM真菌對干旱脅迫的響應(yīng)及其機制Table 1 Response and mechanism of AM fungi to drought stress

續(xù)表1

宿主植物HostplantAM真菌AMfungi試驗條件Experimentalcondition水分處理WatertreatmentAM作用AMfunction參考文獻(xiàn)Reference小葉錦雞兒Caraganamicrophylla蒙古扁桃Prunusmongolica摩西球囊霉G．mosseae根內(nèi)球囊霉G．intraradices盆栽Pots55%；35%提高植株生物量與根系活力，降低葉片水分飽和虧(WSD)含量Increasedplantbiomassandrootactivi?ty，reducedleafWSDcontent．[36]腎臟紫云英Anthylliscytisoides土壤AM真菌SoilAMfungi水培Hydroponics50%～70%提高抗氧化酶類活性Increasedantioxidantenzymaticactivity．[37]馬鈴薯Solanumtuberosum根內(nèi)球囊霉G．intraradices大田Field正常供水Well?watered；干旱脅迫Droughtstress提高硝酸還原酶活性Increasednitratereductaseenzymaticactivity．[38]菜豆Phaseolusvulgaris土壤AM真菌SoilAMfungi盆栽Pots正常供水Well?watered；干旱脅迫Droughtstress增加9-順式-環(huán)氧類胡蘿卜雙加氧酶(NCED)的mRNA豐度IncreasedNCEDenzymemRNAabundance．[39]

1.2 溫度

溫度是影響植物生長發(fā)育的一個重要因素，溫度過高或過低都會影響植物正常的生理過程甚至引起植物體死亡，因此研究如何提高植物對溫度脅迫的抗性極其重要。近年來，國內(nèi)外專家學(xué)者對水稻(Oryzasativa)、君遷子(Diospyroslotus)[9-10,42-51]等多種植物進(jìn)行了研究，發(fā)現(xiàn)AM真菌可以有效增加宿主植物對高溫、低溫脅迫的抗性(表2)。以地表球囊霉(G.versiforme)接種君遷子，發(fā)現(xiàn)地表球囊霉可以促進(jìn)宿主苗木的生長，增強枝干的營養(yǎng)貯藏水平，并顯著提高了君遷子一年生苗的抗凍性[10]。與未接種植株相比，接種處理后君遷子苗高增加50.7%，地上部干重為未接種植株的4.4倍；苗木木質(zhì)部的淀粉含量增加4.56%，韌皮部的全氮含量增加0.15%，韌皮部的可溶性糖含量增加1.76%；凍害指數(shù)下降21.7%。摩西球囊霉和根內(nèi)球囊霉也具有同樣的作用，只是處理效果較地表球囊霉稍差，這可能與植物對不同菌種的依賴性有關(guān)。在對玉米的接種試驗中發(fā)現(xiàn)，15 ℃的低溫脅迫條件下，扭形球囊霉(G.tortuosum)可以提高葉片中碳水化合物的含量，其中可溶性糖增加44%，還原性糖含量增加95%；另外，植物氮代謝也會受到一定影響，接種后玉米葉片及根部的總氮和硝態(tài)氮含量均增加，硝酸還原酶(NR)、谷氨酰胺合成酶(GS)等氮代謝酶的活性也顯著提高[45]。40 ℃高溫脅迫下，幼套球囊霉(G.etunicatum)可增強根系活力，減緩葉綠素分解速度，提高水分的利用效率，提高植物細(xì)胞質(zhì)膜的穩(wěn)定性，從而減緩高溫對細(xì)胞膜的傷害程度[44](表2)。

表2 AM真菌對溫度脅迫的響應(yīng)及其機制Table 2 Response and mechanism of AM fungi to temperature stress

續(xù)表2

宿主植物HostplantAM真菌AMfungi試驗條件ExperimentalconditionAM作用AMfunction參考文獻(xiàn)Reference黃瓜Cucumissativus摩西球囊霉G．mosseae盆栽Pots晝/夜Day/night：25℃/15℃；15℃/10℃增加酚類物質(zhì)、類黃酮積累，促進(jìn)抗逆相關(guān)基因表達(dá)Improvedphenolcontent，flavonoidcontent，promotedstress?relatedgeneexpression．[49]牡丹Paeoniasuffruticosa摩西球囊霉G．mosseae地表球囊霉G．versiforme盆栽Pots25℃；30℃；35℃；40℃增強細(xì)胞膜穩(wěn)定性，降低葉綠素分解Increasedcellmembranestability，re?ducedchlorophylldecomposition．[50]切花月季Rosahybrida切花菊花Chrysanthemummorifolium透光球囊霉G．diuphauam地表球囊霉G．versiforme盆栽Pots晝/夜Day/night：25℃/18℃；35℃/28℃；10℃/5℃增強SOD、POD、CAT、GR、APX等酶活性，提高清除過氧化物的能力ReinfoceSOD，POD，CAT，GR，APXenzymaticactivity，improvedclearper?oxideability．[51]

AM真菌提高植物對溫度脅迫的抗性其機制主要包括：調(diào)節(jié)碳氮代謝，促進(jìn)植物體內(nèi)碳水化合物的積累，促進(jìn)氮素吸收，增加植物體內(nèi)蛋白質(zhì)氨基酸的合成，從而緩和低溫對玉米生長的抑制作用[45]；增強SOD、POD、CAT、谷胱甘肽還原酶(GR)、抗壞血酸專一性過氧化物酶(APX)等抗氧化酶類活性，降低膜脂過氧化水平，維持植物細(xì)胞質(zhì)膜的穩(wěn)定性，提高宿主植物清除O2-·和H2O2等過氧化物的能力，減緩對細(xì)胞膜的傷害[42,48,51]；減緩葉綠素分解，提高葉綠素含量及葉綠素?zé)晒猓龠M(jìn)光合作用，提高氣孔導(dǎo)度，加快蒸騰速率，促進(jìn)植物體內(nèi)水分循環(huán)，增強植物抗逆性[43-44]；另外，在受到溫度脅迫時，AM真菌可刺激多種脅迫誘導(dǎo)基因(如多胺合成代謝相關(guān)基因和植株根系中的Os01g0701500D27、D17、D10等基因)的表達(dá)，這些基因均與植物對溫度脅迫的應(yīng)答有關(guān)，特異性誘導(dǎo)此類基因表達(dá)可有效提高宿主植物對溫度脅迫的抵抗能力[9,49]。

1.3 鹽堿、重金屬

中國鹽漬土的分布范圍廣、面積大、類型多，總面積約1億hm2[52]。土壤鹽堿化不僅可限制植物體的正常生長發(fā)育，還會造成嚴(yán)重的生態(tài)環(huán)境問題[53]。土壤重金屬污染不僅對植物生長造成很大危害，還會造成生態(tài)環(huán)境質(zhì)量惡化[54]。所以土地鹽堿化治理以及消除土壤重金屬污染是全球面臨亟待解決的資源與生態(tài)環(huán)境難題。高羊茅(Festucaarundinacea)、羊草(Leymuschinensis)等10種植物與AM真菌共生的研究結(jié)果[55-64]表明(表3)，鹽堿條件下接種摩西球囊霉可顯著提高高羊茅葉片抗氧化酶活性，在1.6%的鹽脅迫時，接種植株的SOD、POD和CAT活性分別比未接種植株提高了11.2%、8.3%和10.9%；接種摩西球囊霉還可提高抗壞血酸含量，在0.8%、1.2%和1.6%的鹽脅迫時，接種植株的抗壞血酸含量分別比未接種植株提高了9.1%、12.4%和19.5%；在1.2% NaCl脅迫下，接種摩西球囊霉的高羊茅葉片與未接種處理相比，丙二醛含量和膜透性分別降低35.4%和25.6%；在0.8%、1.2%和1.6%的鹽脅迫時，接種植株的可溶性糖含量分別比未接種處理提高24.2%、16.7%和8.8%，脯氨酸含量分別比未接種處理降低31.3%、30.5%和28.9%[58]。鎘脅迫條件下，接種摩西球囊霉可增加水稻植株生物量，促進(jìn)生長，經(jīng)測定接種處理的植株地上干重與未接種對照相比，增加幅度為10.76%～59.48%；接種AM真菌能顯著提高光能利用率，促進(jìn)植物光合作用；接種摩西球囊霉后，保證水稻安全生產(chǎn)的土壤鎘含量閾值擴增至0.21 mg·kg-1[57]。

在鹽堿脅迫下，AM真菌可以提高植物對鹽堿的耐受性，緩解對植物體造成的傷害。其抗性機制主要包括提高植物生物量，促進(jìn)植物生長，增加氣孔導(dǎo)度，提高光合色素的積累，促進(jìn)植物光合作用，加快宿主體內(nèi)的物質(zhì)循環(huán)與能量轉(zhuǎn)運[64]；改變宿主植物體內(nèi)的滲透調(diào)節(jié)物質(zhì)，如增加可溶性糖、可溶性蛋白、氨基酸等的含量及組成，降低丙二醛含量，有效調(diào)節(jié)植物組織內(nèi)的滲透平衡，從而提高植物體耐鹽堿能力[61,65]；提高抗氧化酶類(包括SOD、POD和CAT等)活性和抗氧化劑(抗壞血酸)含量，增強植物抗氧化防御系統(tǒng)，降低氧化脅迫對植物造成的傷害，保證細(xì)胞內(nèi)正常生理生化反應(yīng)及代謝得以順利進(jìn)行；擴大植物根系的吸收范圍，提高礦質(zhì)養(yǎng)分的吸收速率、強化滲透調(diào)節(jié)作用并維持植物內(nèi)源激素平衡，減緩離子毒害[58]；AM真菌也可以通過調(diào)節(jié)與耐鹽堿相關(guān)的基因表達(dá)，如獨腳金內(nèi)酯(strigolactone, SL)合成相關(guān)基因、根部編碼PIP和TIP的基因等，增強植物對鹽堿脅迫的抗性效應(yīng)[55-56]。

在重金屬脅迫下，AM真菌可以提高脯氨酸含量，激活超氧化物歧化酶活性，減少氧化脅迫對機體造成的生理傷害，保障細(xì)胞代謝及生理生化反應(yīng)，進(jìn)而提高對重金屬脅迫的抵御能力[57]；增強植物根系及菌絲本身對重金屬元素的固持作用，抑制其轉(zhuǎn)運，減輕對地上部造成的損傷[66]；增加根系細(xì)胞中金屬螯合物質(zhì)的含量，促進(jìn)重金屬元素在植物根系的固持，抑制轉(zhuǎn)運，減少地上部植物組織內(nèi)的重金屬含量，提高植物耐重金屬性[59]；誘導(dǎo)相關(guān)抗性基因或蛋白(如PEPC蛋白合成相關(guān)基因)的表達(dá)，提高植物對重金屬污染的耐受性[63]。

2 AM真菌對植物抗生物逆境的抗性機制

2.1 病害

病害是草地生產(chǎn)的重要限制因子之一，病原菌入侵可引致草地植物病害，使草地退化、衰敗，不僅造成牧草嚴(yán)重減產(chǎn)，還會影響草地生態(tài)系統(tǒng)的持久力和穩(wěn)定性[67]。 AM真菌可通過與病原菌互作，減輕病害發(fā)生，提高植物抗病性[68]。表4中總結(jié)了包括黃瓜(Cucumissativus)、西瓜(Citrulluslanatus)在內(nèi)的多種植物與病原菌、AM真菌形成共生體系，從而影響宿主植物抗病性的研究結(jié)果[69-79]。尖孢鐮刀菌 (Fusariumoxysporum)可引起黃瓜枯萎病，在黃瓜育苗時接種地表球囊霉可有效減輕尖孢鐮刀菌的侵染，經(jīng)試驗測定，雙接種地表球囊霉和尖孢鐮刀菌可使植株的病情指數(shù)較單接種尖孢鐮刀菌處理降低37.5%；另對4周齡的黃瓜幼苗雙接種尖孢鐮刀菌和地表球囊霉，兩周后測得植株根系丙二醛含量較相應(yīng)單接種尖孢鐮刀菌處理降低了35%[69]。地表球囊霉同樣對尖孢鐮刀菌引起的西瓜枯萎病有較好的抑制作用，研究表明在西瓜苗床播種時接種地表球囊霉可以降低根內(nèi)鐮刀菌繁殖體數(shù)量，平均比未接種對照減少約59.7%[70]。AM真菌除了可以減輕鐮刀菌屬(Fusarium)、疫霉菌屬(Phytophthora)等根部病原真菌引起的植物病害，還可以抵抗病原線蟲的入侵，對線蟲病害也有一定防治效果。采用分根培養(yǎng)系統(tǒng)對番茄進(jìn)行試驗，接種摩西球囊霉與南方根結(jié)線蟲(Meloidogyneincognit)于同一根室，AM 真菌的侵染率受到抑制，病情指數(shù)下降34；接種摩西球囊霉與南方根結(jié)線蟲于不同根室，病情指數(shù)下降14[76]。另有研究發(fā)現(xiàn)，聚生球囊霉(G.fasciculatu)可以抑制大豆胞囊線蟲(Heteroderaglycines)卵囊增長，減少產(chǎn)卵數(shù)及幼蟲數(shù)量，顯著降低其病情指數(shù)，減輕病害發(fā)生程度[77]。AM真菌與病原菌及病原線蟲的互作可以有效抑制病原物對植株的侵染、減輕發(fā)病率、減少植株死亡率，保證植物正常生長。

AM真菌與病原菌的互作機理是復(fù)雜的、多種機制協(xié)同作用的結(jié)果，主要包括：降低病原菌繁殖體數(shù)量，且AM真菌與病原菌存在競爭關(guān)系，可以減少病原菌侵染位點，顯著降低死株率、發(fā)病率和病情指數(shù)，降低病害發(fā)生程度[70]；促進(jìn)植物細(xì)胞皮層加厚，并構(gòu)建菌絲網(wǎng)絡(luò)，形成對根部入侵病原真菌的機械屏障，AM真菌的泡囊和叢枝結(jié)構(gòu)也能阻止病原菌菌絲穿過，增強病原真菌侵入根系的難度，減低病原真菌對根系的侵染率[80-81]；增強SOD、POD、苯丙氨酸解氨酶(PAL)等多種酶的活性，合成抗細(xì)菌和抗真菌的次生代謝產(chǎn)物(主要包括植保素、酶類、酚類化合物和氨基酸類化合物等)，保護植物體不受病原菌侵染[82-83]；促進(jìn)植物體對養(yǎng)分元素的吸收與利用，減少病原菌入侵對植物體造成的傷害，增強植物抗性效應(yīng)[84-85]。

其他機理還包括介導(dǎo)植物抗逆信號轉(zhuǎn)導(dǎo)，如Pozo等[86]研究發(fā)現(xiàn),G.mosseae和G.intraradices可通過誘導(dǎo)植物產(chǎn)生水解酶，減輕植物病害癥狀。進(jìn)一步研究發(fā)現(xiàn)，植物根系分泌獨腳金內(nèi)酯，誘導(dǎo)AM真菌菌絲伸展及侵染植物，AM真菌侵染初期，誘導(dǎo)植物水楊酸(SA)含量增加，增強植物系統(tǒng)獲得抗病性(SAR)，當(dāng)AM真菌進(jìn)入植物皮層細(xì)胞內(nèi)后，水楊酸含量降低，而叢枝形成階段，植物茉莉酸(JA)含量提高，同時促進(jìn)植物脫落酸(ABA)含量增加，增強植物細(xì)胞壁抗性。SA、JA等信號傳導(dǎo)物質(zhì)還可誘導(dǎo)防御性基因表達(dá)，增強植物抗病能力。另外，AM真菌可改變植物根系分泌物的化學(xué)組分，影響根際細(xì)菌群落組成，進(jìn)而誘導(dǎo)植物茉莉酸、乙烯相關(guān)系統(tǒng)性抗性[87-88]。AM真菌亦可誘導(dǎo)抗病相關(guān)基因的表達(dá)，增強效應(yīng)蛋白如SP7的積累，提高植物抗病性[89-92]。AM真菌對線蟲的生長發(fā)育及其繁殖同樣具有抑制作用，能夠抑制線蟲卵囊的增長，提高相關(guān)酶活性，降低病情指數(shù)，有效減輕病原線蟲的侵染，降低線蟲病害發(fā)生[76-79]。

表4 AM真菌對植物抗病性的影響及其機制Table 4 Effects of AM fungi on plant disease resistance and its mechanism

2.2 蟲害

昆蟲是生物群落中十分重要的組成部分，在植物的生長發(fā)育過程中扮演了必不可少的角色。一方面，一些植食性昆蟲取食植物葉片，并將植物體作為生長場所，植物正常生長發(fā)育受阻，產(chǎn)量及品質(zhì)降低，嚴(yán)重時甚至可導(dǎo)致植被大面積死亡，危害農(nóng)林牧業(yè)發(fā)展，造成嚴(yán)重經(jīng)濟損失。另一方面，一些天敵昆蟲可以捕食害蟲，減少其對植物的取食及為害，傳粉昆蟲有助于植物花粉的傳播，而有的昆蟲還可以攜帶并傳播植物種子。研究AM真菌-植物-昆蟲這三者之間的相互作用，對于植物害蟲的防治和有益昆蟲的保護具有重要指導(dǎo)意義。大量研究表明，AM真菌具有調(diào)控植物與昆蟲互作的效應(yīng)[93]。在對垂穗披堿草(Elymusnutans)、長葉車前(Plantagolanceolata)等植物與昆蟲相互作用的研究[94-101]表明(表5)，幼套球囊霉可以誘導(dǎo)植物產(chǎn)生含量與組分更多的揮發(fā)性化合物，主要是萜烯類、醇類、酯類和少量烷烴類物質(zhì)，通常這類物質(zhì)是作為植物-昆蟲營養(yǎng)關(guān)系中信息傳遞的媒介[94]。Hempel等[98]用摩西球囊霉和根內(nèi)球囊霉接種梯牧草(Phleumpratense)，研究植物、蚜蟲(Rhopalosiphumpadi) 與寄生蜂(Aphidiusrhopalosiphi)的相互關(guān)系，發(fā)現(xiàn)接種AM 真菌可增加植物生物量5.2%，降低蚜蟲的蟲口數(shù)量47%。對矢車菊(Centaureacyanus)的研究[14]則發(fā)現(xiàn)AM真菌也可以吸引授粉昆蟲，增加其在植株上的訪問頻率，促進(jìn)植物傳粉。

表5 AM真菌對植物抗蟲性的影響及其機制Table 5 Effects of AM fungi on plant insect resistance and its mechanism

AM真菌與昆蟲的作用機制包括兩個方面。一是直接毒殺作用，AM真菌侵染植物后產(chǎn)生的毒性代謝物，對害蟲具有抑制或毒殺效果[102]；二是間接影響，AM真菌侵染植物后，通過影響植物的營養(yǎng)代謝來影響昆蟲的發(fā)育及繁殖，也可通過調(diào)節(jié)害蟲天敵間接影響害蟲，控制害蟲的種群數(shù)量[99]；誘導(dǎo)植物產(chǎn)生揮發(fā)性化合物，如E-2-己烯-1-醇、芳樟醇、苯甲醛、香芹酚等，這類物質(zhì)對害蟲具有趨避作用，可以保護植物，減少昆蟲取食，提高植物抗蟲性[94,97]；另外，一旦害蟲取食植物，AM真菌可以通過強大的菌絲網(wǎng)絡(luò)在鄰近植株間傳遞抗蟲防御信號，使鄰近植株及時進(jìn)入防御狀態(tài)，減少害蟲取食[97]。AM真菌菌絲網(wǎng)絡(luò)傳遞信號的功能極為穩(wěn)定可靠，因此在害蟲防治以及有益昆蟲保護等方面應(yīng)用前景十分廣泛。

3 展望

隨著國家“糧改飼”及種植業(yè)結(jié)構(gòu)調(diào)整政策的進(jìn)一步深入，草地農(nóng)業(yè)在食物安全及生態(tài)環(huán)境建設(shè)中的重要性日益突出。草地多分布在干旱、高寒、土壤貧瘠地區(qū)，逆境脅迫嚴(yán)重影響植物的生長發(fā)育，造成牧草減產(chǎn)和草地退化。因此，提高草類植物對逆境的抗性，對于提高牧草產(chǎn)量，促進(jìn)系統(tǒng)種群多樣性以及維持草地生態(tài)系統(tǒng)穩(wěn)定極其重要。目前有關(guān)于AM真菌與植物互作的研究主要集中于少數(shù)幾個AM真菌屬，如病害多限于球囊霉屬的研究，鑒于不同AM真菌對植物抗逆性影響不同，應(yīng)加強對菌根真菌多樣性及豐富度對草地植物抗逆的影響及機理的研究；同時，目前的研究多為人工模擬單一逆境，應(yīng)加強AM真菌-草地植物對多種逆境因子響應(yīng)的研究[103-105]。機理方面，AM真菌提高植物抗逆機理包括促進(jìn)植物養(yǎng)分吸收、生長，調(diào)節(jié)植物生理、生化代謝，誘導(dǎo)信號介導(dǎo)，基因及蛋白表達(dá)等諸多方面，應(yīng)關(guān)注不同抗性機理的相關(guān)性，強化現(xiàn)代分子生物學(xué)技術(shù)和細(xì)胞學(xué)技術(shù)應(yīng)用，推動AM真菌在促進(jìn)植物抗逆機理方面的研究。

References:

[1] Smith S E,Read D J.Mycorrhizal Symbiosis.New York:Academic Press,2010.

[2] Sawers R J H,Svane S F,Quan C,Gr?nlund M,Wozniak B,Gebreselassie M N,González-Muoz E,Chávez Montes R A,Baxter I,Goudet J,Jakobsen I,Paszkowski U.Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters.New Phytologist,2017,214(2):632-643.

[3] 郭艷娥,李芳,李應(yīng)德,段廷玉.AM真菌促進(jìn)植物吸收利用磷元素的機制.草業(yè)科學(xué),2016,33(12):2379-2390.

Guo Y E,Li F,Li Y D,Duan T Y.Progress in the elucidation of the mechanisms of arbuscular mycorrhizal fungi in promotion of phosphorus uptake and utilization by plants.Pratacultural Science,2016,33(12):2379-2390.(in Chinese)

[4] Zhang W,Chen X X,Liu Y M,Liu D Y,Chen X P,Zou C Q.Zinc uptake by roots and accumulation in maize plants as affected by phosphorus application and arbuscular mycorrhizal colonization.Plant and Soil,2017,413(1/2):59-71.

[5] Tian H,Yuan X L, Duan J F,Li W H,Zhai B N,Gao Y J.Influence of nutrient signals and carbon allocation on the expression of phosphate and nitrogen transporter genes in winter wheat (Triticumaestivum L.) roots colonized by arbuscular mycorrhizal fungi.PLoS One,2017,12(2):e0172154.

[6] Zhang H Q,Wei S Z,Hu W T,Xiao L M,Tang M.Arbuscular mycorrhizal fungus Rhizophagus irregularis increased potassium content and expression of genes encoding potassium channels inLyciumbarbarum.Frontiers in Plant Science,2017,8:440.

[7] Leyval C,Turnau K,Haselwandter K.Effect of heavy metal pollution on mycorrhizal colonization and function:Physiological,ecological and applied aspects.Mycorrhiza,1997,7(3):139-153.

[8] Augé R M.Water relations,drought and vesicular-arbuscular mycorrhizal symbiosis.Mycorrhiza,2001,11(1):3-42.

[9] 齊國輝,楊文利,張林平,李憲濤,高素娜.叢枝菌根真菌對君遷子貯藏營養(yǎng)及抗凍性的影響.河北農(nóng)業(yè)大學(xué)學(xué)報，2005,28(1):62-64.

Qi G H,Yang W L,Zhang L P,Li X T,Gao S N.Effects of arbuscular mycorrhizal fungi on storage nutrient and cold resistance ofDiospyroslotusL.Journal of Agricultural University of Hebei,2005,28(1):62-64.(in Chinese)

[10] Liu Z,Li Y,Wang J,He X,Tian C.Different respiration metabolism between mycorrhizal and non-mycorrhizal rice under low-temperature stress:A cry for help from the host.The Journal of Agricultural Science,2015,153(4):602-614.

[11] Garg N,Pandey R.Effectiveness of native and exotic arbuscular mycorrhizal fungi on nutrient uptake and ion homeostasis in salt-stressedCajanuscajanL.(Millsp.) genotypes.Mycorrhiza,2015,25(3):165-180.

[12] Galli U,Schüepp H,Brunold C.Heavy metal binding by mycorrhizal fungi.Physiologia Plantarum,1994,92(2):364-368.

[13] Morandi D,Gollotte A,Camporota P.Influence of an arbuscular mycorrhizal fungus on the interaction of a binucleate Rhizoctonia species with Myc+and Myc-pea roots.Mycorrhiza,2002,12(2):97-102.

[14] Gange A C,Smith A K.Arbuscular mycorrhizal fungi influence visitation rates of pollinating insects.Ecological Entomology,2005,30(5):600-606.

[15] Van der Heijden M G A,Boller T W,Sanders R.Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure.Ecology,1998,79(6):2082-2091.

[16] Ehrenfeld J G,Ravit B,Elgersma K.Feedback in the plant-soil system.Annual Review of Environment and Resources,2005,30(1):75-115.

[17] Lin G,McCormack M L,Ma C,Guo D.Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests.New Phytologist,2017,213(3):1440-1451.

[18] 王賢波.叢枝菌根(AM)的研究進(jìn)展及展望.杭州農(nóng)業(yè)科技,2007(2):19-21.

Wang X B.Research progress and prospects of arbuscular mycorrhizae(AM).Hangzhou Agricultural Technology,2007(2):19-21.(in Chinese)

[19] Gui H,Hyde K,Xu J C,Mortimer P.Arbuscular mycorrhiza enhance the rate of litter decomposition while inhibiting soil microbial community development.Scientific Reports,2017,7(7):42184.

[20] 王立,賈文奇,馬放,李世陽,張淑娟.菌根技術(shù)在環(huán)境修復(fù)領(lǐng)域中的應(yīng)用及展望.生態(tài)環(huán)境學(xué)報,2010,19(2):487-493.

Wang L,Jia W Q,Ma F,Li S Y,Zhang S J.Mycorrhizal technology application and prospects in the field of environmental remediation.Journal of Ecological Environment,2010,19(2):487-493.(in Chinese)

[21] Zhang T,Sun Y,Shi Z Y,Feng G.Arbuscular mycorrhizal fungi can accelerate the restoration of degraded spring grassland in Central Asia.Journal of Rangeland Ecology and Management,2012,65(4):426-432.

[22] Boyer J S.Plant productivity and environment.Science,1982,218:443-448.

[23] Ciais P H,Reichstein M,Viovy N,Granier A,Ogée J,Allard V,Aubinet M,Buchmann N,Bernhofer C,Carrara A,Chevallier F,de Noblet N,Friend A D,Friedllingstein P,Grünwald T,Heinesch B,Keronen P,Knohl A,Krinner G,Loustau D,Manca G,Matteucci G,Miglietta F,Ourcival J M,Papale D,Pilegaard K,Rambal S,Seufert G,Soussana J F,Sanz M J,Schulze E D,Vesala T,Valentini R.Europe-wide reduction in primary productivity caused by the heat and drought in 2003.Nature,2005,437:529-533.

[24] Qian Y B,Jiang J,Wu Z N.Soil heterogeneity and its impact on ecological distribution of plant community in the aiby lake area.Arid Land Geography,2003,26(3):217-222.

[25] 李芳,高萍,段廷玉.AM菌根真菌對非生物逆境的響應(yīng)及其機制.草地學(xué)報,2016,24(3):491-500.

Li F,Gao P,Duan T Y.Response and mechanism of arbuscular mycorrhizal fungi to abiotic stress.Journal of Grassland,2016,24(3):491-500.(in Chinese)

[26] 任愛天,魯為華,馬春暉,楊潔晶.接種AM真菌對紫花苜?？购敌缘挠绊?新疆農(nóng)業(yè)科學(xué),2014,51(9):1677-1685.

Ren A T,Lu W H,Ma C H,Yang J J.Effect of arbuscular mycorrhiza fungi on drought tolerance ofMedicagosativaL.Xinjiang Agricultural Science,2014,51(9):1677-1685.(in Chinese)

[27] 張海涵.黃土高原枸杞根際微生態(tài)特征及其共生真菌調(diào)控寄主生長與耐旱響應(yīng)機制.楊凌:西北農(nóng)林科技大學(xué)博士學(xué)位論文,2011.

Zhang H H.Micro-ecosystem associated with the rhizosphere ofLyciumbarbarumfrom the loess plateau and the mechanism of symbiotic fungal inoculation on the host plant growth and drought resistance.PhD Thesis.Yangling:North West Agriculture and Forestry University,2011.(in Chinese)

[28] 賀學(xué)禮,高露,趙麗莉.水分脅迫下叢枝菌根AM真菌對民勤絹蒿生長與抗旱性的影響.生態(tài)學(xué)報,2011,31(4):1029-1037.

He X L,Gao L,Zhao L L.Effects of AM fungi on the growth and drought resistance ofSeriphidiumminchünenseunder water stress.Ecology,2011,31(4):1029-1037.(in Chinese)

[29] 趙平娟,安鋒,唐明.叢枝菌根真菌對連翹幼苗抗旱性的影響.西北植物學(xué)報,2007,27(2):396-399.

Zhao P J,An F,Tang M.Effects of arbuscular mycorrhiza fungi on drought resistance ofForsythiasuspensa.Journal of Northwest Botany,2007,27(2):396-399.(in Chinese)

[30] Zézé A,Brou Y C,Meddich A,Marty F.Molecular identification of MIP genes expressed in the roots of an arbuscular mycorrhizalTrifoliumalexandriumL. under water stress.African Journal of Agricultural Research,2008,3(1):78-83.

[31] Aroca R,del Mar Alguacil M,Vernieri P,Ruiz-Lozano J M.Plant responses to drought stress and exogenous ABA application are modulated differently by mycorrhization in tomato and an ABA-deficient mutant (sitiens).Microbial Ecology,2008,56(4):704-719.

[32] Ruiz-Lozano J M,Porcel R,Aroca R.Does the enhanced tolerance of arbuscular mycorrhizal plants to water deficit involve modulation of droughtinduced plant genes?New Phytologist,2006,171(4):693-698.

[33] 陳婕,謝靖,唐明.水分脅迫下叢枝菌根真菌對紫穗槐生長和抗旱性的影響.北京林業(yè)大學(xué)報,2014,36(6):142-148.

Chen J,Xie J,Tang M.Effects of arbuscular mycorrhizal fungi on the growth and drought resistance ofAmorphafruticosaunder water stress.Journal of Beijing Forestry University,2014,36(6):142-148.(in Chinese)

[34] 黃志.叢枝菌根真菌對甜瓜抗旱性的生理效應(yīng)及分子機制的研究.楊凌:西北農(nóng)林科技大學(xué)博士學(xué)位論文,2010.

Huang Z.Studies on the physiological effect and mechanisms of arbuscular mycorrhizal fungi (AMF) in drought resistance of Melon.PhD Thesis.Yangling:North West Agriculture and Forestry University,2010.(in Chinese)

[35] Ruiz-Lozano J M,del Mar Alguacil M,Bárzana G,Vernieri P,Aroca R.Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins.Plant Molecular Biology,2009,70(5):565-579.

[36] 張華.AM真菌對小葉錦雞兒和蒙古扁桃生長、抗旱性及總黃酮含量的影響.呼和浩特:內(nèi)蒙古大學(xué)碩士學(xué)位論文,2013.

Zhang H.The effects of AM fungi on growth,drought resistance and total flavonoids content ofCaraganamicrophyllaLam. andAmygdalusmongolicaMaxim.Master Thesis.Hohhot:University of Inner Mongolia,2013.(in Chinese)

[37] Goicoechea N,Merino S,Sánchez-Díaz M.Arbuscular mycorrhizal fungi can contribute to maintain antioxidant and carbon metabolism in nodules ofAnthylliscytisoidesL. subjected to drought.Journal of Plant Physiology,2005,162(1):27-35.

[38] Subramanian K S,Santhanakrishnan P,Balasubramanian P.Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress.Scientia Horticulturae,2006,107(3):245-253.

[39] Qin X,Zeevaart J A D.The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean.Proceedings of the National Academy of Sciences,1999,96(26):15354-15361.

[40] Rillig M C,Wright S F,Eviner V T.The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation:Comparing effects of five plant species.Plant and Soil,2002,238(2):325-333.

[41] Jiang W,Gou G,Ding Y.Influences of arbuscular mycorrhizal fungi on growth and mineral element absorption of chenglu hybrid bamboo seedlings.Pakistan Journal of Botany,2013,45(1):303-310.

[42] 潘傳威,劉小芳,屈鵬飛,吳強盛.叢枝菌根真菌提高溫度脅迫下枳根系抗氧化能力.長江大學(xué)學(xué)報(自然科學(xué)版),2011,8(9):245-247.

Pan C W,Liu X F,Qu P F,Wu Q S.Arbuscular mycorrhizal fungi increased antioxidant capacity ofPoncirustrifoliataroots under temperature stress.Journal of Yangtze University(Natural Science Edition),2011,8(9):245-247.(in Chinese)

[43] 陳笑瑩,宋鳳斌,朱先燦,劉勝群,柏會子.高溫脅迫下叢枝菌根真菌對玉米光合特性的影響.華北農(nóng)學(xué)報,2013,28(2):108-113.

Chen X Y,Song F B,Zhu X C,Liu S Q,Bai H Z.Effects of arbuscular mycorrhizal fungi on photosynthetic characteristics in maize plants under high temperature stress.Agriculture in North China,2013,28(2):108-113.(in Chinese)

[44] Zhu X C,Song F B,Liu S Q,Liu T D.Effects of arbuscular mycorrhizal fungus on photosynthesis and water status of maize under high temperature stress.Plant and Soil,2011,346(1/2):189-199.

[45] 陳笑瑩.低溫脅迫下叢枝菌根真菌對玉米碳氮代謝的影響.長春:中國科學(xué)院研究生院(東北地理與農(nóng)業(yè)生態(tài)研究所)博士學(xué)位論文,2014.

Chen X Y.Effects of arbuscular mycorrhizal fungi on carbon and nitrogen metabolism of maize under low temperature stress.PhD Thesis.Changchun:Graduate School of Chinese Academy of Sciences(Northeast Institute of Geography and Agricultural Ecology),2014.(in Chinese)

[46] Zhu X C,Song F B,Liu F L,Liu S Q,Tian C J.Carbon and nitrogen metabolism in arbuscular mycorrhizal maize plants under low-temperature stress.Crop and Pasture Science,2015,66(1):62-70.

[47] 韓冰,賀超興,閆妍,郭世榮,于賢昌.AMF對低溫脅迫下黃瓜幼苗生長和葉片氧化系統(tǒng)的影響.中國農(nóng)業(yè)科學(xué),2011,44(8):1646-1653.

Han B,He C X,Yan Y,Guo S R,Yu X C.Effects of arbuscular mycorrhiza fungi on seedlings growth and antioxidant systems of leaves in cucumber under low temperature stress.Chinese Academy of Agricultural Sciences,2011,44(8):1646-1653.(in Chinese)

[48] Liu A,Chen S,Chang R,Liu D,Chen H,Ahammed G J,Lin X,He C.Arbuscular mycorrhizae improve low temperature tolerance in cucumber via alterations in H2O2accumulation and ATPase activity.Journal of Plant Research,2014,127(6):775-785.

[49] Chen S,Jin W,Liu A,Zhang S,Liu D,Wang F,Lin X,He C.Arbuscular mycorrhizal fungi (AMF) increase growth and secondary metabolism in cucumber subjected to low temperature stress.Scientia Horticulturae,2013,160:222-229.

[50] 李思龍,張玉剛,陳丹明,馬健,郭紹霞.叢枝菌根對高溫脅迫下牡丹生理生化的影響.中國農(nóng)學(xué)通報,2009,25(7):154-157.

Li S L,Zhang Y G,Chen D M,Ma J,Guo S X.Effect of arbuscular mycorrhizal fungi on physiology and biochemistry of tree peony under high temperature stress.Chinese Agricultural Science Bulletin,2009,25(7):154-157.(in Chinese)

[51] 孔佩佩.叢枝菌根真菌對切花月季和切花菊生長及溫度脅迫耐受性的影響.北京:中國農(nóng)業(yè)科學(xué)院碩士學(xué)位論文,2011.

Kong P P.Effects of arbuscular mycorrhizal fungi on growth and temperature tolerance ofRosanybridandChrysanthemummorifolium.Master Thesis.Beijing:Chinese Academy of Agricultural Sciences,2011.(in Chinese)

[52] 楊勁松.中國鹽漬土研究的發(fā)展歷程與展望.土壤學(xué)報,2008,45(5):837-845.

Yang J S.Development history and prospect of research on saline soil in China.Journal of Soil,2008,45(5):837-845.(in Chinese)

[53] Porcel R,Aroca R,Ruiz-Lozano J.Salinity stress alleviation using arbuscular mycorrhizal fungi：A review.Agronomy for Sustainable Development,2012,32(1):181-200.

[54] 王紅新.叢枝菌根真菌在植物修復(fù)重金屬污染土壤中的作用.中國土壤與肥料,2010(5):1-5.

Wang H X.Arbuscular mycorrhizal fungi’s role in the phytoremediation of soils contaminated by heavy metals.Soils and Fertilizers in China,2010(5):1-5.(in Chinese)

[55] Ouziad F,Wilde P,Schmelzer E,Hildebrandt U,Bothe H.Analysis of expression of aquaporins and Na+/H+transporters in tomato colonized by arbuscular mycorrhizal fungi and affected by salt stress.Environmental and Experimental Botany,2006,57(1/2):177-186．

[56] 張瑞萍.水稻質(zhì)膜質(zhì)子泵基因?qū)Φ土酌{迫的響應(yīng)和叢枝菌根的影響.南京:南京農(nóng)業(yè)大學(xué)博士學(xué)位論文,2011.

Zhang R P.Adaptation to Pi deficiency and effects to mycorrhiza of the rice plasma membrane H+-ATPasegenes.PhD Thesis.Nanjing:Nanjing Agricultural University,2011.(in Chinese)

[57] 劉雙洋.叢枝菌根真菌對水稻鎘脅迫響應(yīng)及其轉(zhuǎn)運過程的影響研究.哈爾濱:哈爾濱工業(yè)大學(xué)碩士學(xué)位論文,2015.

Liu S Y.The research on response to cadmium stress and transport process of rice under infection of arbuscular mycorrhizal fungi.Master Thesis.Harbin:Harbin Institute of Technology,2015.(in Chinese)

[58] 楊海霞,劉潤進(jìn),郭紹霞.AM真菌摩西球囊霉對鹽脅迫條件下高羊茅生長特性的影響.草業(yè)學(xué)報,2014,23(4):195-203.

Yang H X,Liu R J,Guo S X.Effects of arbuscular mycorrhizal fungi Glomus mosseae on growth characteristics ofFestucaarundinaceaunder salt stress.Acta Prataculturae Sinica,2014,23(4):195-203.(in Chinese)

[59] 李霞,彭霞薇,伍松林,李志茹,馮紅梅,江澤平.叢枝菌根對翅莢木生長及吸收累積重金屬的影響.環(huán)境科學(xué),2014,35 (8):3142-3148.

Li X,Peng X W,Wu S L,Li Z R,Feng H M,Jiang Z P.Effect of arbuscular mycorrhizae on growth,heavy metal uptake and accumulation ofZeniainsignischun seedlings.Environmental Science,2014,35(8):3142-3148.(in Chinese)

[60] 黃晶,凌婉婷,孫艷娣,劉娟.叢枝菌根真菌對紫花苜蓿吸收土壤中鎘和鋅的影響.農(nóng)業(yè)環(huán)境科學(xué)學(xué)報,2012,31(1):99-105.

Huang J,Ling W T,Sun Y D,Liu J.Impacts of arbuscular mycorrhizal fungi inoculation on the uptake of cadmium and zinc by alfalfa in contaminated soil.Journal of Agro-environmental Science,2012,31(1):99-105.(in Chinese)

[61] Moradi A,Younesi O.Influence of arbuscular mycorrhiza on membrane lipid peroxidation and soluble sugar content of soybean under salt stress.Agriculturae Conspectus Scientificus,2015,79(4):227-232.

[62] He Z Q,Huang Z.Expression analysis ofLeNHX1 gene in mycorrhizal tomato under salt stress.Journal of Microbiology, 2013,51(1):100-104.

[63] 周權(quán)男,楊禮富,王真輝.砷脅迫對叢枝菌根接種玉米葉片蛋白表達(dá)譜的影響.西南農(nóng)業(yè)學(xué)報,2014,27(6):2370-2373.

Zhou Q N,Yang L F,Wang Z H.Effect of arsenic stress on protein expression profiles from maize leaves of abuscular mycorrhizal fungi (AMF) inoculation.Southwest Journal of Agriculture Science,2014,27(6):2370-2373.(in Chinese)

[64] Lin J X,Wang Y N,Sun S N,Mu C S,Yan X F.Effects of arbuscular mycorrhizal fungi on the growth,photosynthesis and photosynthetic pigments ofLeymuschinensisseedlings under salt-alkali stress and nitrogen deposition.Science of the Total Environment,2017,576:234-241.

[65] Evelin H,Kapoor R,Giri B.Arbuscular mycorrhizal fungi in alleviation of salt stress:A review.Annals of Botany,2009, 104(7):1263-1280.

[66] 林雙雙,孫向偉,王曉娟,李媛媛,羅巧玉,孫莉,金樑.AM真菌提高寄主植物耐受重金屬脅迫的生理機制.草業(yè)科學(xué),2013,30(3):365-374.

Lin S S,Sun X W,Wang X J,Li Y Y,Luo Q Y,Sun L,Jin L.Mechanisms of AM fungi to increase physiological tolerance to heavy metal of host plant.Pratacultural Science,2013,30(3):365-374.(in Chinese)

[67] 南志標(biāo),李春杰,白原生.我國草類作物病害及其防治對策.北京:海洋出版社,2003.

Nan Z B,Li C J,Bai Y S.Grass Plant Diseases and Their Control Countermeasures in China.Beijing:China Ocean Press,2003.(in Chinese)

[68] 張峰,段廷玉,閆飛揚,李芳.叢枝菌根真菌與根際微生物的互作.草業(yè)科學(xué),2014,31(9):1673-1685.

Zhang F,Duan T Y,Yan F Y,Li F.Advances in the interactions of arbuscular mycorrhizal fungi and rhizosphere microorganism.Pratacultural Science,2014,31(9):1673-1685.(in Chinese)

[69] 王倡憲.AM真菌對設(shè)施黃瓜幼苗生長及抗枯萎病能力研究.北京:中國農(nóng)業(yè)大學(xué)博士學(xué)位論文,2005.

Wang C X.Studies on effects of AMF on growth and resistance of cucumber seedlings to wilt disease under protected conditions.PhD Thesis.Beijing:China Agricultural University,2005.(in Chinese)

[70] 李敏.AM真菌對西瓜抗枯萎病的效應(yīng)及其機制.北京:中國農(nóng)業(yè)大學(xué)博士學(xué)位論文,2005.

Lin M.Effects of AM fungi on resistance to Fusarium wilt in watermelon (Citrulluslanatus) and related mechanism.PhD Thesis.Beijing:China Agricultural University,2005.(in Chinese)

[71] Safir G R.The Influence of vesicular-arbuscular mycorrhiza on the resistance on onion toPyrenochaetaterrestris.Master Thesis.Urbana:University of Illinois,1968.

[72] Maya M A,Matsubara Y.Tolerance toFusariumwiltand anthracnose diseases and changes of antioxidative activity in mycorrhizal cyclamen.Crop Protection,2013,47:41-48.

[73] Martínez-Medina A,Roldán A,Pascual J A.Interaction between arbuscular mycorrhizal fungi andTrichodermaharzianumunder conventional and low input fertilization field condition in melon crops:Growth response andFusariumwiltbiocontrol.Applied Soil Ecology,2011,47(2):98-105.

[74] Kloppholz S,Kuhn H,Requena N.A secreted fungal effector ofGlomusintraradicespromotes symbiotic biotrophy.Current Biology,2011,21(14):1204-1209.

[75] 朱紅惠,姚青,羊宋貞.AM真菌與拮抗細(xì)菌的互作及對番茄根系酚類物質(zhì)的影響.華南農(nóng)業(yè)大學(xué)學(xué)報,2003,24(3):20-23.

Zhu H H,Yao Q,Yang S Z.Interaction between AM fungus and antagonistic bacterium and its effect on tomato root phenolic compounds.Journal of South China Agricultural University,2003,24(3):20-23.(in Chinese)

[76] 盛萍萍,王彬,苑學(xué)霞,王小坤,劉潤進(jìn).AM真菌誘導(dǎo)的番茄信號物質(zhì)及其對根結(jié)線蟲的抑制效應(yīng).植物病理學(xué)報,2012,42(3):323-327.

Sheng P P,Wang B,Yuan X X,Wang X K,Liu R J.Physiological effect of signal substances in tomato plants induced by arbuscular mycorrhizal fungi.Plant Pathology Journal,2012,42(3):323-327.(in Chinese)

[77] 李海燕,劉潤進(jìn),束懷瑞.叢枝菌根真菌與大豆胞囊線蟲相互作用研究初報.植物病理學(xué)報,2002,32(4):356-360.

Li H Y,Liu R J,Shu H R.A preliminary report on interactions between arbuscular mycorrhizal fungi and soybean cyst nematode.Plant Pathology Journal,2002,32(4):356-360.(in Chinese)

[78] 陳書霞,姜永華,劉宏久,程智慧.AM真菌和根結(jié)線蟲互作對黃瓜生長及生理特征的影響.植物保護學(xué)報,2012,39(3):253-259.

Chen S X,Jiang Y H,Liu H J,Chen Z H.Interaction between AM fungi and root-knot nematodes cucumber growth and the effect for physiological characteristics.Journal of Plant Protection,2012,39(3):253-259.(in Chinese)

[79] Banuelos J,Trejo D,Alarcon A,Lara L,Moreira C,Cruz S.The reduction in proline buildup in mycorrhizal plants affected by nematodes.Journal of Soil Science and Plant Nutrition,2012,12(2):263-270.

[80] Merrild M P,Ambus P,Rosendahl S,Jakobsen L.Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants.New Phytologist,2013,200(1):229-240.

[81] Hardham A R,Mitchell H J.Use of molecular cytology to study the structure and biology of phytopathogenic and mycorrhizal fungi.Fungal Genetics and Biology,1998,24(1):252-284.

[82] Ortu G,Balestrini R,Pereira P A,Becker J D,Küster H,Bonfante P.Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions.Molecular Plant,2012,5(4):951-954.

[83] Fiorilli V,Catoni M,Francia D,Cardinale F,Lanfranco L.The arbuscular mycorrhizal symbiosis reduces disease severity in tomato plants infected byBotrytiscinerea.Journal of Plant Pathology,2011,93(1):237-242.

[84] Abbott L K,Robson A D.The role of vesicular arbuscular mycorrhizal fungi in agriculture and the selection of fungi for inoculation.Crop and Pasture Science,1982,33(2):389-408.

[85] Thompson J P,Wildermuth G B.Colonization of crop and pasture species with vesicular-arbuscular mycorrhizal fungi and a negative correlation with root infection byBipolarissorokiniana.Canadian Journal of Botany,1989,67(3):687-693.

[86] Pozo M J,Cordier C,Dumas-Gaudot E,Gianinazzi S,Barea J M,Azcon-Aguilar C.Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses toPhytophthorainfectionin tomato plants.Journal of Experimental Botany,2002,53:525-534.

[87] Cameron D D,Neal A L,van Wees S C M,Ton J.Mycorrhiza-induced resistance:more than the sum of its parts?Trends in Plant Science,2013,18(10):539-545.

[88] Pozo M J,Azcon-Aguilar C.Unraveling mycorrhiza-induced resistance.Current Opinion in Plant Biology,2007,10(4):393-398.

[89] Ruiz-Lozano J M,Roussel H,Gianinazzi S,Gianinazzi-Pearson V.Defense genes are differentially induced by a mycorrhizal fungus andRhizobiumsp. in wild-type and symbiosis-defective pea genotypes.Molecular Plant-Microbe Interactions,1999,12(11):976-984.

[90] Pozo M J,Azcón-Aguilar C,Dumas-Gaudot E,Barea J M.β-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or phytophthora parasitica and their possible involvement in bioprotection.Plant Science,1999,141(2):149-157.

[91] Gao L L,Smith F A,Smith S E.The rmc locus does not affect plant interactions or defence-related gene expression when tomato (Solanumlycopersicum) is infected with the root fungal parasite,Rhizoctonia.Functional Plant Biology,2006,33(3):289-296.

[92] Gao L L,Knogge W,Delp G,Smith F A,Smith S E.Expression patterns of defense-related genes in different types of arbuscular mycorrhizal development in wild-type and mycorrhiza-defective mutant tomato.Molecular Plant-Microbe Interactions,2004,17(10):1103-1113.

[93] Vannette R L,Rasmann S.Arbuscular mycorrhizal fungi mediate below-ground plant-herbivore interactions:A phylogenetic study.Functional Ecology,2012,26(5):1033-1042.

[94] 劉月華,鐘夢瑩,武瑞鑫,位曉婷,潘多,邵新慶.AM真菌介導(dǎo)垂穗披堿草抗蟲作用研究.草地學(xué)報,2016,24(3):604-609.

Liu Y H,Zhong M Y,Wu R X,Wei X T,Pan D,Shao X X.Study of the inductive effect of arbuscular mycorrhizal fungi onElymusnutanspest-resistant information.Journal of Grassland,2016,24(3):604-609.(in Chinese)

[95] Gange A C,West H M.Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects inPlantagolanceolataL.New Phytologist,1994,128(1):79-87.

[96] Barber N A.Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores byCucumissativus. Journal of Plant Ecology,2013,6(2):171-176.

[97] Xie L J,Song Y Y,Zeng R S,Wang R L,Wei X C,Ye M,Hu L,Zhang H.Disease resistance signal transfer between roots of different tomato plants through common arbuscular mycorrhiza networks.Chinese Journal of Applied Ecology,2012,23(5):1145-1152.

[98] Hempel S,Stein C,Unsicker S,Renker C,Auge H,Weisser W,Buscot F.Specific bottom-up effects of arbuscular mycorrhizal fungi across a plant-herbivore-parasitoid system.Oecologia,2009,160(2):267-277.

[99] Moon D C,Barnouti J,Younginger B.Context-dependent effects of mycorrhizae on herbivore density and parasitism in a tritrophic coastal study system.Ecological Entomology,2013,38(1):31-39.

[100] Nishida T,Izumi N,Katayama N,Ohgushi T.Short-term response of arbuscular mycorrhizal association to spider mite herbivory.Population Ecology,2009,51(2):329-334.

[101] Cosme M,Stout M J,Wurst S.Effect of arbuscular mycorrhizal fungi (Glomusintraradices) on the oviposition of rice water weevil (Lissorhoptrusoryzophilus).Mycorrhiza,2011,21(7):651.

[102] Song Y Y,Zeng R S,Xu J F,Li J,Shen X,Yihdego W G.Interplant communication of tomato plants through underground common mycorrhizal networks.PLoS One,2010,5(10):e13324.

[103] 弓明欽,陳應(yīng)龍,仲崇祿.菌根研究及應(yīng)用.北京:中國林業(yè)出版社,1997.

Gong M Q,Chen Y L,Zhong C L.Research and Applications of Mycorrhizae.Beijing:China Forestry Publishing House,1997.(in Chinese)

[104] Zhao P J,An F,Ding M M.Advances in the researches of the methanism of disease resistance promotion of mycorrhiza.Journal of Northwest Forestry University,2004,19(1):93-97.

[105] Tang M,Chen H,Shang H S H.Effects of arbuscular mycorrhizal fungi (AMF) onHippophaerhamnoidesdrought resistance.Scientia Silvae Sinicae,1999,35(3):48-52.