何樹斌,郭理想,李菁,王燚,劉澤民,程宇陽,呼天明,龍明秀

(西北農(nóng)林科技大學(xué)動物科技學(xué)院, 陜西 楊凌 712100)

叢枝菌根真菌與豆科植物共生體研究進(jìn)展

何樹斌,郭理想,李菁,王燚,劉澤民,程宇陽,呼天明,龍明秀*

(西北農(nóng)林科技大學(xué)動物科技學(xué)院, 陜西 楊凌 712100)

叢枝菌根真菌(arbuscular mycorrhizal fungi，AMF)是一類廣泛分布在土壤中與植物根系共生的真菌，幾乎所有的農(nóng)業(yè)生態(tài)系統(tǒng)和自然界的土壤中都有AMF的分布。在AMF與植物的共生體中，AMF消耗植物光合有機(jī)產(chǎn)物的同時，將土壤中更多的磷和氮等營養(yǎng)物質(zhì)轉(zhuǎn)運(yùn)給寄主植物。豆科植物作為一種重要的農(nóng)業(yè)種質(zhì)資源，能與AMF形成共生體系。研究表明，AMF能夠促進(jìn)豆科植物生長、提高其對礦質(zhì)營養(yǎng)元素和水分的吸收能力、增強(qiáng)其生物固氮能力和抗逆能力等。為了更好地利用AMF促進(jìn)豆科植物的生產(chǎn)，本研究分析了共生體建立過程中可能存在的信號轉(zhuǎn)導(dǎo)機(jī)制，論述了AMF提高豆科植物產(chǎn)量及營養(yǎng)價值的研究成果，闡明了AMF提高豆科植物抗逆能力的內(nèi)在機(jī)制，探討了AMF與根瘤菌的互作的潛在機(jī)制，并對今后AMF與豆科植物共生在農(nóng)業(yè)領(lǐng)域的研究方向進(jìn)行了展望。

叢枝菌根真菌；豆科植物；根瘤菌；共生體；抗逆；協(xié)同增效

叢枝菌根真菌(arbuscular mycorrhizal fungi, AMF)是土壤微生物群落的重要組成部分，超過80%的陸生植物根系中都有AMF的存在[1]。在這個共生體系內(nèi)，AMF的根外菌絲增強(qiáng)了根系的吸收能力，為植物提供了更多生長所需的營養(yǎng)物質(zhì)(如磷和氮等)，與此同時，AMF通過根內(nèi)菌絲從寄主植物體內(nèi)攝取菌根繁殖和生長所必須的碳水化合物等[2-3]。

過去半個多世紀(jì)以來，使用氮肥和磷肥已經(jīng)成為發(fā)展中國家提高作物產(chǎn)量的重要手段，但只有30%～50%的氮肥和10%～45%的磷肥被作物吸收[4]?；实拇罅渴褂貌坏觿×谁h(huán)境污染，而且推高了農(nóng)產(chǎn)品價格，降低了農(nóng)產(chǎn)品品質(zhì)等[5]。由于AMF能給共生植物提供氮磷等營養(yǎng)物質(zhì)，它對植物的促生作用被認(rèn)為是一項(xiàng)可以降低化肥使用，具有廣泛應(yīng)用前景的技術(shù)措施，對保障全球糧食安全與農(nóng)業(yè)可持續(xù)發(fā)展具有深遠(yuǎn)意義[5]。

豆科植物不但是人類和動物蛋白的重要來源之一，而且由于其固氮培肥的原因在草地農(nóng)業(yè)生態(tài)系統(tǒng)中發(fā)揮著重要作用[6]。絕大多數(shù)豆科植物如紫花苜蓿(Medicagosativa)[7]、蒺藜苜蓿(M.truncatula)[8]、百脈根(Lotuscorniculatus)[9]和菜豆(Phaseolusvulgaris)[10]等都能與AMF建立起共生體系。由于根瘤菌(Rhizobium)是豆科植物的天然共生菌，所以，AMF能夠與豆科植物形成AMF-豆科植物-根瘤菌三者共生體系。為了更好的利用AMF促進(jìn)豆科植物生長和提高其資源利用效率，闡明共生體諸多機(jī)理性的問題，筆者分析了這個共生體建立過程中可能存在的信號轉(zhuǎn)導(dǎo)機(jī)制，論述了AMF提高豆科植物產(chǎn)量及氮磷含量的研究成果，闡明了AMF提高豆科植物抗逆能力的生理學(xué)機(jī)制，探討了AMF與根瘤菌互作的潛在機(jī)制，并對今后AMF與豆科植物共生在農(nóng)業(yè)領(lǐng)域的研究方向進(jìn)行了展望。

1 AMF與豆科植物共生關(guān)系建立的信號傳遞機(jī)制

在根瘤菌與豆科植物的結(jié)瘤過程中，豆科植物分泌的多酚類化合物黃酮、異黃酮等，在微生物與共生植物之間起到了一定的“信息交流”作用，調(diào)節(jié)了相關(guān)結(jié)瘤基因的表達(dá)和轉(zhuǎn)錄[11-12]。類似的研究也表明，AMF侵染后植物根系中類黃酮物質(zhì)的含量有所增加[13]，增加的類黃酮類物質(zhì)能夠刺激AMF的侵染[14]，增加孢子的萌發(fā)、菌絲的生長及分支等[11]。同時，AMF還可以在其共生體系形成過程中分泌一種擴(kuò)散性因子——菌根因子(Myc factor)，來調(diào)控植物對類黃酮物質(zhì)的分泌，對宿主植物產(chǎn)生共生誘導(dǎo)性反應(yīng)[11]，誘發(fā)宿主植物共生信號的釋放[15]。因此，類黃酮物質(zhì)在AMF與植物共生關(guān)系的建立過程中也起到重要的信號傳遞作用[11,16]。但是，目前對于菌根因子信號傳遞尚缺乏直接的證據(jù)[17]。最新的研究已證明，過氧化氫(H2O2)和一氧化氮(NO)在AMF與豆科植物共生體建立及互作關(guān)系上發(fā)揮重要的信號作用，但還不明確這些活性物質(zhì)是在什么時間和位置上被產(chǎn)生的[18]。此外，通過基因組序列分析，生長素(auxin)、乙烯(ethylene)、獨(dú)角金內(nèi)酯(strigolactone)和疏水蛋白(hydrophobins)等信號物質(zhì)在分子水平上均參與AMF共生體建立[19]，但在寄主植物與微生物之間的信息交流方面還缺乏關(guān)鍵證據(jù)?？傊嘘P(guān)AMF與豆科植物共生關(guān)系建立過程中的信息交流途徑還不明確，深入闡釋AMF與豆科植物之間的信號識別與傳遞機(jī)制，對于建立高效的共生系統(tǒng)將是至關(guān)重要的。

2 AMF對豆科植物碳同化和產(chǎn)量的影響

AMF和根瘤菌與植物的共生系統(tǒng)，是以微生物消耗光合有機(jī)產(chǎn)物為前提的。因此，AMF和根瘤菌的侵染刺激了共生植物對碳的需求，繼而提高了共生植物的光合速率[20-22]，以此彌補(bǔ)微生物對碳的額外消耗[21,23]。研究表明，豆科植物完全有能力補(bǔ)償微生物對光合碳的消耗[20,22,24]。微生物可能通過以下機(jī)制影響了共生植物碳同化能力。第一，AMF菌絲體內(nèi)脂類的合成分解驅(qū)動了碳的代謝，增加了AMF對碳的需要[25]，提高了地下部分的碳匯強(qiáng)度[26]。第二，由于碳匯強(qiáng)度的增加加速了磷酸丙糖合成蔗糖并運(yùn)輸?shù)巾g皮部的能力，當(dāng)磷再次回到葉綠體內(nèi)時促進(jìn)了磷的循環(huán)速率[27]，進(jìn)一步激活了卡爾文循環(huán)中RuBP(1, 5-二磷酸核酮糖)的再生[28]。第三，植物氮磷營養(yǎng)水平和光合營養(yǎng)元素同化及利用效率的增加促使微生物提高共生植物碳匯能力[21-22,26]。盡管有證據(jù)表明AMF能刺激共生植物的光合碳同化，但對產(chǎn)量的影響卻一直備受爭議。有研究認(rèn)為，AMF共生體呼吸速率的提高消耗了部分光合產(chǎn)物[21]，同化生產(chǎn)與呼吸消耗相抵消，作物產(chǎn)量并沒有顯著變化[23,29]。盡管也有研究利用穩(wěn)定性同位素從共生系統(tǒng)的角度，從碳分配與營養(yǎng)物質(zhì)的輸出的角度估算AMF在共生體內(nèi)碳的消耗比例[30]，但顯然這項(xiàng)研究還不充分，仍需深入探討。

3 AMF促進(jìn)對豆科植物磷氮等營養(yǎng)物質(zhì)的吸收

AMF的菌絲數(shù)量較大，不但能夠增加根系吸收營養(yǎng)的面積，改變根圍的微生物組成[31]，而且能增強(qiáng)植物根際土壤中磷酸酶的活性[32]，吸收植物不能主動吸收的磷[33]，進(jìn)而提高了植物對土壤中磷元素的吸收能力[34]。尤其是在磷缺乏的土壤中，AMF從土壤中轉(zhuǎn)運(yùn)磷元素供共生植物的能力非常顯著[22]。在磷缺乏的土壤中氮的含量往往也相對較低[35]，AMF不但能提高豆科植物磷的含量，而且也能提高其對氮的吸收[36]。AMF能夠通過谷氨酰胺合成酶和谷氨酸合成(GS-GOGAT)途徑吸收銨態(tài)氮(NH4+)和硝態(tài)氮(NO3-)，并儲存在它們的外生菌根里(ERM)，然后再將其整合成氨基酸并以精氨酸的形式轉(zhuǎn)運(yùn)到內(nèi)生菌根(IRM)，再在IRM里將精氨酸分解、轉(zhuǎn)運(yùn)給共生植物[37]。但是，也有研究表明，AMF在植物吸收氮的過程中并沒有發(fā)揮明顯的作用，其機(jī)制仍備受爭議，需深入研究[38]。除氮磷外，AMF在促進(jìn)豆科植物在微量元素吸收方面也發(fā)揮著積極作用[39]。研究表明，AMF的侵染能夠提高鷹嘴豆(Cicerarietinum)獲取鋅[40]和大豆(Glycinemax)獲取銅和鋅[41]等的能力。此外，AMF的菌絲還能增加共生植物對鈣、鎂、錳、鐵、硅等穩(wěn)定元素或者微量元素的吸收[42]。最新研究結(jié)果表明，AMF能夠提高蒺藜苜蓿在硫稀缺環(huán)境下的生長能力和植物內(nèi)硫元素的含量[43]。由于硫可用于植物的光合作用及其生長發(fā)育，因此，這對豆科植物抵御生物和非生物脅迫的響應(yīng)是非常重要的。但是，關(guān)于AMF促進(jìn)豆科植物有關(guān)礦質(zhì)營養(yǎng)吸收的深層次的機(jī)制還需要更深入的研究[39]。

此外，AMF提高豆科植物磷和其他營養(yǎng)物質(zhì)的能力取決于特定的共生體系[42]，對紅蕓豆(Phaseolusvulgaris)和鷹嘴豆等研究已經(jīng)證明了上述觀點(diǎn)，即不同微生物組合促進(jìn)共生植物磷和氮吸收的能力是不同的[44-45]。因此，研究和篩選適合不同豆科植物促進(jìn)其營養(yǎng)物質(zhì)吸收的高效兼容的AMF菌株，將有助于進(jìn)一步推動開發(fā)利用菌根資源，提高資源的利用效率，實(shí)現(xiàn)可持續(xù)的農(nóng)業(yè)發(fā)展模式。

4 AMF對豆科植物抗逆能力的影響

植物在生長發(fā)育過程中會遇到各種生物與非生物脅迫，如何提高植物的抗逆性是科學(xué)家們研究的熱點(diǎn)。大量的研究證實(shí)AMF能夠提高共生植物抵御干旱、鹽堿、重金屬、高溫等脅迫的能力。

4.1 AMF提高豆科植物的抗旱能力

研究表明，AMF能夠有效緩解干旱對豆科植物的傷害。首先，AMF共生對植物水勢產(chǎn)生了積極的影響[46]，提高了植物葉片的相對含水量，使得豆科植物形成干旱逃避機(jī)制[47]；其次，AMF提高了共生植物體內(nèi)營養(yǎng)元素的含量[48]和碳水化合物的百分比[49]，高濃度的磷元素能夠增加根系中磷元素的分配[50]，而碳水化合物能夠穩(wěn)定脫氫酶和細(xì)胞膜，保護(hù)生物結(jié)構(gòu)免于干旱脫水[49]，進(jìn)而提高了植株抵御干旱的能力；此外，AMF還可以通過提高共生植物的滲透調(diào)節(jié)[51]和植物體內(nèi)脫落酸水平[52]，使得植株在干旱環(huán)境中能保持更好的葉片蒸騰作用和根系間的水分運(yùn)輸平衡[53]。但是，AMF提高寄主植物抗旱性的準(zhǔn)確機(jī)制仍需做進(jìn)一步的研究[54]，尤其需要進(jìn)一步闡明AMF提高豆科植物抗逆性在分子水平上的應(yīng)答機(jī)制。

4.2 AMF提高豆科植物的抗鹽堿能力

AMF除了提高植物的抗旱性，還能提高其抗鹽堿的能力[55]，因此被譽(yù)為是良好的鹽堿土生物改良者[56]。分析其內(nèi)在機(jī)制，一方面，AMF增強(qiáng)了植物的滲透勢，氣體交換能力和水分利用效率等生理學(xué)過程[49,56-57]；另一方面，AMF誘導(dǎo)植株產(chǎn)生了抗生素和植物激素等次生代謝產(chǎn)物，并引起一系列生理過程，最終緩解了鹽脅迫對植物的傷害[58-59]。此外，共生植物體內(nèi)氮磷元素水平發(fā)生變化[57,60-61]，幫助植株降低了對鈉離子的吸收，緩解了鈉離子的毒害作用，間接地維持了葉綠素的濃度[49]，促進(jìn)其正常生長。但這與Ruiz-Lozano等[62]的研究結(jié)論是相反的，即AMF提高植物抗鹽能力并非是由于植物體內(nèi)營養(yǎng)物質(zhì)的變化所導(dǎo)致的。因此，有關(guān)AMF提高豆科植物抗鹽性的研究還需要深入闡明其內(nèi)在機(jī)制。

4.3 AMF提高豆科植物的抗重金屬毒害和高溫脅迫的能力

隨著工業(yè)化和城市化進(jìn)程的推進(jìn)，重金屬污染成為亟待解決的重要生態(tài)問題之一。大量的研究表明，AMF不僅能夠減輕干旱和鹽脅迫對植物的損傷，還能夠顯著降低大豆等豆科植物對重金屬的攝入量，緩解重金屬的毒害作用，增強(qiáng)了其抵抗重金屬毒害的能力[63-64]。這可能是因?yàn)锳MF大量的菌絲起到了屏障作用，阻止了金屬離子由地下到地上部分的轉(zhuǎn)移[65]，而且AMF較強(qiáng)的絡(luò)合重金屬元素的能力，增強(qiáng)了寄主植物對這些重金屬離子的耐性，從而減輕植物遭受重金屬污染的程度[66]。由此可見，重金屬污染區(qū)域的治理可以利用豆科植物和AMF共生體系達(dá)到最佳治理效應(yīng)[64]。近些年來，全球氣候變化一直是人們關(guān)注的熱點(diǎn)，溫度升高對植物生長的影響也是科學(xué)家們研究的重點(diǎn)。Hu等[67]的研究證實(shí)，AMF能緩解夜間高溫對蒺藜苜蓿的不良影響。這可能是由于AMF改善了共生植物光合作用的能力[68]、增加了對水分和礦質(zhì)營養(yǎng)的吸收[69]、提高了各種抗氧化類物質(zhì)的含量[70]，進(jìn)而提高了共生植物抵御溫度脅迫的能力。關(guān)于AMF提高豆科植物對高溫適應(yīng)性的研究還很少，其深層次的作用機(jī)理仍是未來研究的方向。

AMF提高豆科植物抗逆性的研究范圍很廣。除能提高共生植物抗干旱、鹽堿、重金屬和高溫外，AMF還能夠提高豆科植物的抗病性等[71]。筆者認(rèn)為，由于AMF與豆科植物的共生具有普遍性和廉價性，提高共生植物抗逆性也是經(jīng)濟(jì)的、生態(tài)的、環(huán)保的。因此，有關(guān)AMF提高豆科植物抗性的研究具有重要意義，需要進(jìn)一步掌握其潛在的機(jī)制并拓展其應(yīng)用范圍。

5 AMF與根瘤菌的互作機(jī)制

5.1 AMF對豆科植物生物固氮的影響

豆科植物是根瘤菌的天然寄主，根瘤菌能夠固定大氣中的氮?dú)鉃橹参锼肹72]。對紫花苜蓿[73]、大豆[41]和金合歡(Acaciafarnesiana)[74]的研究表明，AMF的侵染顯著增加了共生植物的結(jié)瘤數(shù)、鮮瘤重、固氮酶的活力、豆血紅蛋白的含量等，即AMF的侵染能夠促進(jìn)根瘤的生長，提高生物固氮能力[5,21,39]。這可能是因?yàn)椋紫?，AMF的侵染提高了豆科植物吸收磷元素和固氮所需其他營養(yǎng)物質(zhì)能力；其次，由于AMF侵染后的豆科植物具有更高的光合作用和呼吸速率[21]，提高了碳向根瘤和菌根的流動，使根瘤能夠?yàn)楣采参锕潭ǜ嗟牡?/p>

圖1 叢枝菌根真菌與豆科植物共生機(jī)制Fig.1 Simplified model for the mechanism of arbuscular mycorrhizal fungi and legumes symbiosis虛線框表示不確定過程Dotted square mean some uncertain processes.

5.2 AMF與根瘤菌的協(xié)同增效機(jī)制

AMF和根瘤菌是相互緊密聯(lián)系的[75]，它們的相互作用直接影響了豆科植物的生長、產(chǎn)量[44]及豆科植物-根瘤菌-AMF三者共生體系的效率[29]。對山黧豆(Lathyrussativus)[57]、紫花苜蓿[76]和豌豆(Pisumsativum)[77]等的研究表明，AMF與根瘤菌同時接種對共生植物的促進(jìn)作用要超過單一接種。這被認(rèn)為是AMF和根瘤菌之間相互兼容所發(fā)揮的協(xié)同增效作用[78-79]。但也有研究表明，它們之間存在相互不兼容的競爭[80]。這可能是由于AMF需要較高的光合速率和呼吸速率，抑制了根瘤的生長[21]。目前關(guān)于共生體中影響雙重接種協(xié)同效應(yīng)的機(jī)制還沒有較為統(tǒng)一的結(jié)果，需要進(jìn)一步的闡明[42,81]。

6 展望

AMF對植物最大的益處是AMF消耗植物光合作用產(chǎn)物的同時供給植物氮和磷等營養(yǎng)元素(圖 1)。目前，通過穩(wěn)定性同位素示蹤技術(shù)已經(jīng)估算了碳的流向，但這種方法不能夠區(qū)分根系和微生物的呼吸作用[82]。為了進(jìn)一步闡明碳的轉(zhuǎn)移量及在植物體內(nèi)的儲藏機(jī)制，利用微生物攜帶的對碳有響應(yīng)的標(biāo)記基因，可以在時間和空間上動態(tài)定量植物與微生物之間的碳轉(zhuǎn)移與消耗[82-83]，但這項(xiàng)技術(shù)的應(yīng)用還是空白，應(yīng)該利用分子生物學(xué)和生物信息學(xué)技術(shù)進(jìn)一步完善相關(guān)研究。此外，在逆境情況下簡單的用植物獲得的磷和氮等營養(yǎng)物質(zhì)來定量分析AMF對植物的有益作用顯然是不完整的[82]，因此，有必要通過穩(wěn)定性同位素技術(shù)深入研究豆科植物-根瘤菌-AMF三者共生體系在逆境脅迫下碳的分配、消耗及收益規(guī)律。

全球氣候變化背景下，全球CO2濃度升高備受人們的關(guān)注。隨著CO2濃度的升高，植物可利用的碳、對營養(yǎng)元素的需要能力及AMF的侵染率均增加[84]。因此，AMF與豆科植物在CO2升高的環(huán)境下是最佳生長環(huán)境[75]。但是，在氣候變化背景下，AMF對豆科植物個體及在生態(tài)系統(tǒng)水平上的研究還很少。此外，AMF在植物-土壤系統(tǒng)中碳轉(zhuǎn)移和陸地生態(tài)系統(tǒng)碳氮循環(huán)過程中發(fā)揮著重要的作用[85-86]。但有關(guān)AMF對豆科植物土壤物理化學(xué)屬性、土壤碳匯和土壤碳氮循環(huán)能力的研究還比較少，尤其是在全球氣候變化背景下，闡明AMF與豆科植物土壤碳固存和碳氮循環(huán)之間的耦聯(lián)關(guān)系是很必要的。

References：

[1] Nanjareddy K, Blanco L, Arthikala M K,etal. Nitrate regulates rhizobial and mycorrhizal symbiosis in common bean (PhaseolusvulgarisL.). Journal of Integrative Plant Biology, 2014, 56(3): 281-298.

[2] Smith S E, Read D J. Mycorrhizal Symbiosis[M]. 2nd Edition. London: Academic Press, 1997.

[3] Smith S E, Read D J. Mycorrhizal Symbiosis[M]. 3rd Edition. London: Academic Press, 2008.

[4] Adesemoye A O, Kloeppe J W. Plant-microbes interactions in enhanced fertilizer-use efficiency. Applied Microbiology and Biotechnology, 2009, 85(1): 1-12.

[5] Abd-Alla M H, El-Enany A W E, Nafady N A,etal. Synergistic interaction ofRhizobiumleguminosarumbv.viciaeand arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (ViciafabaL.) in alkaline soil. Microbiological Research, 2014, 169(1): 49-58.

[6] Graham P H, Vance C P. Legumes: importance and constraints to greater use. Plant Physiology, 2003, 131(3): 872-877.

[7] Duan T, Facelli E, Smith S E,etal. Differential effects of soil disturbance and plant residue retention on function of arbuscular mycorrhizal (AM) symbiosis are not reflected in colonization of roots or hyphal development in soil. Soil Biology and Biochemistry, 2011, 43(3): 571-578.

[8] Krajinski F, Frenzel A. Towards the elucidation of AM-specific transcription inMedicagotruncatula. Phytochemistry, 2007, 68(1): 75-81.

[9] Meghvansi M K, Prasad K, Harwani D,etal. Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi andBradyrhizobiumjaponicumin the alluvial soil. European Journal of Soil Biology, 2008, 44(3): 316-323.

[10] De Mita S, Streng A, Bisseling T,etal. Evolution of a symbiotic receptor through gene duplications in the legume-rhizobium mutualism. New Phytologist, 2014, 201(3): 961-972.

[11] Song F Q, Wang L, Ma F. Research on the Symbiotic System between Arbuscular Mycorrhiza Fungi andAmorphafruticosa[M]. Beijing: Science Press, 2013. 宋福強(qiáng), 王立, 馬放. 叢枝菌根真菌-紫穗槐共生體系的研究[M]. 北京: 科學(xué)出版社, 2013.

[12] Cooper J E. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. Journal of Applied Microbiology, 2007, 103(5): 1355-1365.

[13] Schliemann W, Ammer C, Strack D. Metabolite profiling of mycorrhizal roots ofMedicagotruncatula. Phytochemistry, 2008, 69(1): 112-146.

[14] Larose G, Chênevert R, Moutoglis P,etal. Flavonoid levels in roots ofMedicagosativaare modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. Journal of Plant Physiology, 2002, 159(12): 1329-1339.

[15] Kosuta S, Chabaud M, Lougnon G,etal. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots ofMedicagotruncatula. Plant Physiology, 2003, 131(3): 952-962.

[16] Morandi D, Branzanti B, Gianinazzi-Pearson V. Effect of some plant flavonoids oninvitrobehaviour of an arbuscular mycorrhizal fungus. Agronomie, 1992, 12: 811-816.

[17] Catoira R, Galera C, De Billy F,etal. Four genes ofMedicagotruncatulacontrolling components of a nod factor transduction pathway. The Plant Cell, 2000, 12(9): 1647-1665.

[18] Puppo A, Pauly N, Boscari A,etal. Hydrogen peroxide and nitric oxide: key regulators of the legume—rhizobium and mycorrhizal symbioses. Antioxidants & Redox Signaling, 2013, 18(16): 2202-2219.

[19] Raudaskoski M, Kothe E. Novel findings on the role of signal exchange in arbuscular and ectomycorrhizal symbioses. Mycorrhiza, 2015, 25(4): 243-252.

[20] Jia Y, Gray V M, Straker C J. The influence ofRhizobiumand arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation byViciafaba. Annals of Botany, 2004, 94(2): 251-258.

[21] Mortimer P E, Pérez-Fernández M A, Valentine A J. The role of arbuscular mycorrhizal colonization in the carbon and nutrient economy of the tripartite symbiosis with nodulatedPhaseolusvulgaris. Soil Biology and Biochemistry, 2008, 40(5): 1019-1027.

[22] Kaschuk G, Kuyper T W, Leffelaar P A,etal. Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses. Soil Biology and Biochemistry, 2009, 41(6): 1233-1244.

[23] Wright D P, Read D J, Scholes J D. Mycorrhizal sink strength influences whole plant carbon balance ofTrifoliumrepensL. Plant, Cell & Environment, 1998, 21(9): 881-891.

[24] Gray V M. The role of the C∶N∶P stoichiometry in the carbon balance dynamics of the Legume-AMF-Rhizobiumtripartite symbiotic association[M]. Plant Growth and Health Promoting Bacteria. Berlin: Springer-Verlag Berlin Heidelberg, 2010.

[25] Bago B, Pfeffer P E, Abubaker J,etal. Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiology, 2003, 131(3): 1496-1507.

[26] Mortimer P E, Le Roux M R, Pérez-Fernández M A,etal. The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legumeAcaciacyclopsunder nutrient limiting conditions. Plant and Soil, 2013, 366(1/2): 229-241.

[27] Paul M J, Foyer C H. Sink regulation of photosynthesis. Journal of Experimental Botany, 2001, 52: 1383-1400.

[28] Black K G, Mitchell D T, Osborne B A. Effect of mycorrhizal-enhanced leaf phosphate status on carbon partitioning, translocation and photosynthesis in cucumber. Plant, Cell & Environment, 2000, 23(8): 797-809.

[29] Xavier L J C, Germida J J. Selective interactions between arbuscular mycorrhizal fungi andRhizobiumleguminosarumbv.viceaeenhance pea yield and nutrition. Biology and Fertility of Soils, 2003, 37(5): 261-267.

[30] Harris D, Pacovsky R S, Paul E A. Carbon economy of Soybean-Rhizobium-Glomusassociations. New Phytologist, 1985, 101(3): 427-440.

[31] Hodge A, Campbell C D, Fitter A H. An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature, 2001, 413: 297-299.

[32] Goicoechea N, Antolin M C, Strnad M,etal. Root cytokinins, acid phosphatase and nodule activity in drought-stressed mycorrhizal or nitrogen-fixing alfalfa plants. Journal of Experimental Botany, 1996, 47(5): 683-686.

[33] Rausch C, Daram P, Brunner S,etal. A phosphate transporter expressed in arbuscule-containing cells in potato. Nature, 2001, 414: 462-470.

[34] Sanginga N, Lyasse O, Singh B B. Phosphorus use efficiency and nitrogen balance of cowpea breeding lines in a low P soil of the derived savanna zone in West Africa. Plant and Soil, 2000, 220(1/2): 119-128.

[35] Hayman D S. Mycorrhizae of nitrogen-fixing legumes. Journal of Applied Microbiology and Biotechnology, 1986, 2(1): 121-145.

[36] Wang S, Feng Z, Wang X,etal. Arbuscular mycorrhizal fungi alter the response of growth and nutrient uptake of snap bean (PhaseolusvulgarisL.) to O3. Journal of Environmental Sciences, 2011, 23(6): 968-974.

[37] Govindarajulu M, Pfeffer P E, Jin H,etal. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature, 2005, 435: 819-823.

[38] Johnson N C. Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist, 2010, 185(3): 631-647.

[39] Chalk P M, Souza R F, Urquiaga S,etal. The role of arbuscular mycorrhiza in legume symbiotic performance. Soil Biology and Biochemistry, 2006, 38(9): 2944-2951.

[40] Thompson J P. Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops and its expression in phosphorus deficiency of sunflower. Crop and Pasture Science, 1987, 38(5): 847-867.

[41] Antunes P M, Rajcan I, Goss M J. Specific flavonoids as interconnecting signals in the tripartite symbiosis formed by arbuscular mycorrhizal fungi,Bradyrhizobiumjaponicum(Kirchner) Jordan and soybean (Glycinemax(L.) Merr.). Soil Biology and Biochemistry, 2006, 38(3): 533-543.

[42] Clark R B, Zeto S K. Mineral acquisition by arbuscular mycorrhizal plants. Journal of Plant Nutrition, 2000, 23(7): 867-902.

[43] Wipf D, Mongelard G, van Tuinen D,etal. Transcriptional responses ofMedicagotruncatulaupon sulfur deficiency stress and arbuscular mycorrhizal symbiosis. Frontiers in Plant Science, 2014, 5: 1-17.

[44] Ahmad M H. Compatibility and co-selection of vesicular-arbuscular mycorrhizal fungi and rhizobia for tropical legumes. Critical Reviews in Biotechnology, 1995, 15(3/4): 229-239.

[45] Tavasolee A, Aliasgharzad N, SalehiJouzani G,etal. Interactive effects of arbuscular mycorrhizal fungi and rhizobial strains on chickpea growth and nutrient content in plant. African Journal of Biotechnology, 2011, 10(39): 7585-7591.

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

[47] Aliasgharzad N, Neyshabouri M R, Salimi G. Effects of arbuscular mycorrhizal fungi andBradyrhizobiumjaponicumon drought stress of soybean. Biologia, 2006, 61(19): 324-328.

[48] Kong J, Pei Z, Du M,etal. Effects of arbuscular mycorrhizal fungi on the drought resistance of the mining area repair plant Sainfoin. International Journal of Mining Science and Technology, 2014, 24(4): 485-489.

[49] Soliman A S H, Shanan N T, Massoud O N,etal. Improving salinity tolerance ofAcaciasaligna(Labill.) plant by arbuscular mycorrhizal fungi andRhizobiuminoculation. African Journal of Biotechnology, 2012, 11(5): 1259-1266.

[50] Augé R M, Toler H D, Saxton A M. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza, 2015, 25(1): 13-24.

[51] Porcel R, Ruiz-Lozano J M. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. Journal of Experimental Botany, 2004, 55: 1743-1750.

[52] Martín-Rodríguez J, León-Morcillo R, Vierheilig H,etal. Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytologist, 2011, 190(1): 193-205.

[53] Aroca R, Vernieri P, Ruiz-Lozano J M. Mycorrhizal and non-mycorrhizalLactucasativaplants exhibit contrasting responses to exogenous ABA during drought stress and recovery. Journal of Experimental Botany, 2008, 59(8): 2029-2041.

[54] Wu Q S, Xia R X. Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. Journal of Plant Physiology, 2006, 163(4): 417-425.

[55] Al-Karaki G N, Hammad R. Mycorrhizal influence on fruit yield and mineral content of tomato grown under salt stress. Journal of Plant Nutrition, 2001, 24(8): 1311-1323.

[56] 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.

[57] Jin L, Sun X W, Wang X J,etal. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth ofLathyrussativusunder sulphate salt stress. Symbiosis, 2010, 50(3): 157-164.

[58] De Varennes A, Goss M J. The tripartite symbiosis between legumes, rhizobia and indigenous mycorrhizal fungi is more efficient in undisturbed soil. Soil Biology and Biochemistry, 2007, 39(10): 2603-2607.

[59] Kaschuk G, Leffelaar P A, Giller K E,etal. Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biology and Biochemistry, 2010, 42(1): 125-127.

[60] Al-Karaki G N. Growth of mycorrhizal tomato and mineral acquisition under salt stress. Mycorrhiza, 2000, 10(2): 51-54.

[61] Labidi S, Jeddi F B, Tisserant B,etal. Field application of mycorrhizal bio-inoculants affects the mineral uptake of a forage legume (HedysarumcoronariumL.) on a highly calcareous soil. Mycorrhiza, 2015, 25(4): 297-309.

[62] Ruiz-Lozano J M, Azcon R, Gomez M. Alleviation of salt stress by arbuscular-mycorrhizalGlomusspecies inLactucasativaplants. Physiologia Plantarum, 1996, 98(4): 767-772.

[63] Andrade S A L, Abreu C A, De Abreu M F,etal. Influence of lead additions on arbuscular mycorrhiza andRhizobiumsymbioses under soybean plants. Applied Soil Ecology, 2004, 26(2): 123-131.

[64] Al-Garni S M S. Increased heavy metal tolerance of cowpea plants by dual inoculation of an arbuscular mycorrhizal fungi and nitrogen-fixerRhizobiumbacterium. African Journal of Biotechnology, 2006, 5(2): 133-142.

[65] Joner E J, Briones R, Leyval C. Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant and Soil, 2000, 226(2): 227-234.

[66] Yang X M, Chen B D, Zhu Y G,etal. Effect of arbuscular mycorrhizal fungi (Glomusintraradices) on growth and mineral nutrition of maize plants in copper contaminated soils. Acta Ecologica Sinica, 2008, 28(3): 1052-1057. 楊秀梅, 陳保冬, 朱永官, 等. 叢枝菌根真菌對銅污染土壤上玉米生長的影響. 生態(tài)學(xué)報(bào), 2008, 28(3): 1052-1057.

[67] Hu Y, Wu S, Sun Y,etal. Arbuscular mycorrhizal symbiosis can mitigate the negative effects of night warming on physiological traits ofMedicagotruncatulaL. Mycorrhiza, 2015, 25(2): 131-142.

[68] Martin C A, Stutz J C. Interactive effects of temperature and arbuscular mycorrhizal fungi on growth, P uptake and root respiration ofCapsicumannuumL. Mycorrhiza, 2004, 14(4): 241-244.

[69] Ruotsalainen A L, Kyt?viita M M. Mycorrhiza does not alter low temperature impact onGnaphaliumnorvegicum. Oecologia, 2004, 140(2): 226-233.

[70] Yang X H, Sun Z H, Zeng B. Research of mycorrhizal in citrus orchards of Sanxia Reservoir Area[C]. China Association for Science and Technology in 2005 Academic Essays, 2005. 楊曉紅, 孫中海, 曾斌. 三峽庫區(qū)橘園叢枝菌根真菌無梗囊霉屬調(diào)查研究[C]. 中國科協(xié)2005年學(xué)術(shù)年會論文集, 2005.

[71] Thiagarajan T R, Ahmad M H. Phosphatase activity and cytokinin content in cowpeas (Vignaunguiculata) inoculated with a vesicular-arbuscular mycorrhizal fungus. Biology and Fertility of Soils, 1994, 17(1): 51-56.

[72] Lodwig E M, Hosie A H F, Bourdès A,etal. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobiumsymbiosis. Nature, 2003, 422: 722-726.

[73] Toro M, Azcón R, Barea J M. The use of isotopic dilution techniques to evaluate the interactive effects ofRhizobiumgenotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition byMedicagosativa. New Phytologist, 1998, 138(2): 265-273.

[74] Benbrahim K F, Ismaili M. Interactions in the symbiosis ofAcaciasalignawithGlomusmosseaeandRhizobiumin a fumigated and unfumigated soil. Arid Land Research and Management, 2002, 16(4): 365-376.

[75] Gavito M E, Curtis P S, Mikkelsen T N,etal. Atmospheric CO2and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (PisumsativumL.) plants. Journal of Experimental Botany, 2000, 51: 1931-1938.

[76] Wu F Y, Bi Y L, Wong M H. Dual inoculation with an arbuscular mycorrhizal fungus andRhizobiumto facilitate the growth of alfalfa on coal mine substrates. Journal of Plant Nutrition, 2009, 32(5): 755-771.

[77] Geneva M, Zehirov G, Djonova E,etal. The effect of inoculation of pea plants with mycorrhizal fungi andRhizobiumon nitrogen and phosphorus assimilation. Plant Soil and Environment, 2006, 52(10): 435-539.

[78] Stancheva I, Geneva M, Djonova E,etal. Response of alfalfa (MedicagosativaL.) growth at low accessible phosphorus source to the dual inoculation with mycorrhizal fungi and nitrogen fixing bacteria. General and Applied Plant Physiology, 2008, (34): 319-326.

[79] Teng Y, Luo Y, Sun X,etal. Influence of arbuscular mycorrhiza and rhizobium on phytoremediation by alfalfa of an agricultural soil contaminated with weathered PCBs: a field study. International Journal of Phytoremediation, 2010, 12(5): 516-533.

[80] Behlenfalvay G J, Brown M S, Stafford A E.Glycine-Glomus-Rhizobiumsymbiosis II. Antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiology, 1985, 79: 1054-1058.

[81] Zarei M, Saleh-Rastin N, Alikhani H A,etal. Responses of lentil to co-inoculation with phosphate-solubilizing rhizobial strains and arbuscular mycorrhizal fungi. Journal of Plant Nutrition, 2006, 29(8): 1509-1522.

[82] Morgan J A W, Bending G D, White P J. Biological costs and benefits to plant-microbe interactions in the rhizosphere. Journal of Experimental Botany, 2005, 56: 1729-1739.

[83] Killham K, Yeomans C. Rhizosphere carbon flow measurement and implications: from isotopes to reporter genes. Plant and Soil, 2001, 232: 91-96.

[84] Hartwig U A, Wittmann P, Braun R,etal. Arbuscular mycorrhiza infection enhances the growth response ofLoliumperenneto elevated atmospheric pCO2. Journal of Experimental Botany, 2002, 53: 1207-1213.

[85] Zhu Y G, Miller R M. Carbon cycling by arbuscular mycorrhizal fungi in soil-plant systems. Trends in Plant Science, 2003, 8(9): 407-409.

[86] Wilson G W T, Rice C W, Rillig M C,etal. Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecology Letters, 2009, 12(5): 452-461.

Advances in arbuscular mycorrhizal fungi and legumes symbiosis research

HE Shu-Bin, GUO Li-Xiang, LI Jing, WANG Yi, LIU Ze-Min, CHENG Yu-Yang, HU Tian-Ming,LONG Ming-Xiu*

CollegeofAnimalScienceandTechnology,NorthwestA&FUniversity,Yangling712100,China

Arbuscular mycorrhizal fungi (AMF), are widely distributed in the soil and plant roots of almost all agricultural ecosystems. In this symbiosis, AMF consumes carbohydrates produced by the host plant using the hyphae associated with the roots for growth and reproduction; at the same time arbuscular mycorrhizal hyphae enhance the capacity for root absorption, which provides nutrients needed for growth (such as phosphorus and nitrogen). Legumes can form symbiosis with arbuscular mycorrhizal fungi. Numerous studies indicate that arbuscular mycorrhizal fungi can improve legume growth, promote the absorption of mineral nutrients and water, and enhance biological nitrogen fixation capacity and stress resistance. The aim of this study was to enable better use of mycorrhizal fungi to promote legume production; the signal transduction mechanisms that may exist during the establishment of symbiosis were analyzed and the responses of legume yield and nutritional value to arbuscular mycorrhizal are discussed. The internal mechanisms of increased stress resistance due to arbuscular mycorrhizal are clarified, potential mechanisms of the interactions between arbuscular mycorrhizal and rhizobia are explored and the prospects for arbuscular mycorrhizal and legumes symbiosis studies in the future are addressed.

arbuscular mycorrhizal fungi; legume; rhizobium; symbiont; stress resistance; synergistic

10.11686/cyxb2016228

http://cyxb.lzu.edu.cn

2016-05-30；改回日期：2016-09-20

國家自然科學(xué)基金項(xiàng)目(31402128)和西北農(nóng)林科技大學(xué)基本科研業(yè)務(wù)專項(xiàng)(2014YB007)資助。

何樹斌(1983-)，男，甘肅武威人，講師，博士。E-mail:heshubin@nwsuaf.edu.cn*通信作者Corresponding author. E-mail: longmingxiu@nwsuaf.edu.cn

何樹斌, 郭理想, 李菁, 王燚, 劉澤民, 程宇陽, 呼天明, 龍明秀. 叢枝菌根真菌與豆科植物共生體研究進(jìn)展. 草業(yè)學(xué)報(bào), 2017, 26(1): 187-194.

HE Shu-Bin, GUO Li-Xiang, LI Jing, WANG Yi, LIU Ze-Min, CHENG Yu-Yang, HU Tian-Ming, LONG Ming-Xiu. Advances in arbuscular mycorrhizal fungi and legumes symbiosis research. Acta Prataculturae Sinica, 2017, 26(1): 187-194.