丛枝菌根真菌与豆科植物共生体研究进展

何树斌,郭理想,李菁,王燚,刘泽民,程宇阳,呼天明,龙明秀

(西北农林科技大学动物科技学院, 陕西 杨凌 712100)

丛枝菌根真菌与豆科植物共生体研究进展

何树斌,郭理想,李菁,王燚,刘泽民,程宇阳,呼天明,龙明秀*

(西北农林科技大学动物科技学院, 陕西 杨凌 712100)

丛枝菌根真菌(arbuscular mycorrhizal fungi，AMF)是一类广泛分布在土壤中与植物根系共生的真菌，几乎所有的农业生态系统和自然界的土壤中都有AMF的分布。在AMF与植物的共生体中，AMF消耗植物光合有机产物的同时，将土壤中更多的磷和氮等营养物质转运给寄主植物。豆科植物作为一种重要的农业种质资源，能与AMF形成共生体系。研究表明，AMF能够促进豆科植物生长、提高其对矿质营养元素和水分的吸收能力、增强其生物固氮能力和抗逆能力等。为了更好地利用AMF促进豆科植物的生产，本研究分析了共生体建立过程中可能存在的信号转导机制，论述了AMF提高豆科植物产量及营养价值的研究成果，阐明了AMF提高豆科植物抗逆能力的内在机制，探讨了AMF与根瘤菌的互作的潜在机制，并对今后AMF与豆科植物共生在农业领域的研究方向进行了展望。

丛枝菌根真菌；豆科植物；根瘤菌；共生体；抗逆；协同增效

丛枝菌根真菌(arbuscular mycorrhizal fungi, AMF)是土壤微生物群落的重要组成部分，超过80%的陆生植物根系中都有AMF的存在[1]。在这个共生体系内，AMF的根外菌丝增强了根系的吸收能力，为植物提供了更多生长所需的营养物质(如磷和氮等)，与此同时，AMF通过根内菌丝从寄主植物体内摄取菌根繁殖和生长所必须的碳水化合物等[2-3]。

过去半个多世纪以来，使用氮肥和磷肥已经成为发展中国家提高作物产量的重要手段，但只有30%～50%的氮肥和10%～45%的磷肥被作物吸收[4]。化肥的大量使用不但加剧了环境污染，而且推高了农产品价格，降低了农产品品质等[5]。由于AMF能给共生植物提供氮磷等营养物质，它对植物的促生作用被认为是一项可以降低化肥使用，具有广泛应用前景的技术措施，对保障全球粮食安全与农业可持续发展具有深远意义[5]。

豆科植物不但是人类和动物蛋白的重要来源之一，而且由于其固氮培肥的原因在草地农业生态系统中发挥着重要作用[6]。绝大多数豆科植物如紫花苜蓿(Medicagosativa)[7]、蒺藜苜蓿(M.truncatula)[8]、百脉根(Lotuscorniculatus)[9]和菜豆(Phaseolusvulgaris)[10]等都能与AMF建立起共生体系。由于根瘤菌(Rhizobium)是豆科植物的天然共生菌，所以，AMF能够与豆科植物形成AMF-豆科植物-根瘤菌三者共生体系。为了更好的利用AMF促进豆科植物生长和提高其资源利用效率，阐明共生体诸多机理性的问题，笔者分析了这个共生体建立过程中可能存在的信号转导机制，论述了AMF提高豆科植物产量及氮磷含量的研究成果，阐明了AMF提高豆科植物抗逆能力的生理学机制，探讨了AMF与根瘤菌互作的潜在机制，并对今后AMF与豆科植物共生在农业领域的研究方向进行了展望。

1 AMF与豆科植物共生关系建立的信号传递机制

在根瘤菌与豆科植物的结瘤过程中，豆科植物分泌的多酚类化合物黄酮、异黄酮等，在微生物与共生植物之间起到了一定的“信息交流”作用，调节了相关结瘤基因的表达和转录[11-12]。类似的研究也表明，AMF侵染后植物根系中类黄酮物质的含量有所增加[13]，增加的类黄酮类物质能够刺激AMF的侵染[14]，增加孢子的萌发、菌丝的生长及分支等[11]。同时，AMF还可以在其共生体系形成过程中分泌一种扩散性因子——菌根因子(Myc factor)，来调控植物对类黄酮物质的分泌，对宿主植物产生共生诱导性反应[11]，诱发宿主植物共生信号的释放[15]。因此，类黄酮物质在AMF与植物共生关系的建立过程中也起到重要的信号传递作用[11,16]。但是，目前对于菌根因子信号传递尚缺乏直接的证据[17]。最新的研究已证明，过氧化氢(H2O2)和一氧化氮(NO)在AMF与豆科植物共生体建立及互作关系上发挥重要的信号作用，但还不明确这些活性物质是在什么时间和位置上被产生的[18]。此外，通过基因组序列分析，生长素(auxin)、乙烯(ethylene)、独角金内酯(strigolactone)和疏水蛋白(hydrophobins)等信号物质在分子水平上均参与AMF共生体建立[19]，但在寄主植物与微生物之间的信息交流方面还缺乏关键证据。总之，有关AMF与豆科植物共生关系建立过程中的信息交流途径还不明确，深入阐释AMF与豆科植物之间的信号识别与传递机制，对于建立高效的共生系统将是至关重要的。

2 AMF对豆科植物碳同化和产量的影响

AMF和根瘤菌与植物的共生系统，是以微生物消耗光合有机产物为前提的。因此，AMF和根瘤菌的侵染刺激了共生植物对碳的需求，继而提高了共生植物的光合速率[20-22]，以此弥补微生物对碳的额外消耗[21,23]。研究表明，豆科植物完全有能力补偿微生物对光合碳的消耗[20,22,24]。微生物可能通过以下机制影响了共生植物碳同化能力。第一，AMF菌丝体内脂类的合成分解驱动了碳的代谢，增加了AMF对碳的需要[25]，提高了地下部分的碳汇强度[26]。第二，由于碳汇强度的增加加速了磷酸丙糖合成蔗糖并运输到韧皮部的能力，当磷再次回到叶绿体内时促进了磷的循环速率[27]，进一步激活了卡尔文循环中RuBP(1, 5-二磷酸核酮糖)的再生[28]。第三，植物氮磷营养水平和光合营养元素同化及利用效率的增加促使微生物提高共生植物碳汇能力[21-22,26]。尽管有证据表明AMF能刺激共生植物的光合碳同化，但对产量的影响却一直备受争议。有研究认为，AMF共生体呼吸速率的提高消耗了部分光合产物[21]，同化生产与呼吸消耗相抵消，作物产量并没有显著变化[23,29]。尽管也有研究利用稳定性同位素从共生系统的角度，从碳分配与营养物质的输出的角度估算AMF在共生体内碳的消耗比例[30]，但显然这项研究还不充分，仍需深入探讨。

3 AMF促进对豆科植物磷氮等营养物质的吸收

AMF的菌丝数量较大，不但能够增加根系吸收营养的面积，改变根围的微生物组成[31]，而且能增强植物根际土壤中磷酸酶的活性[32]，吸收植物不能主动吸收的磷[33]，进而提高了植物对土壤中磷元素的吸收能力[34]。尤其是在磷缺乏的土壤中，AMF从土壤中转运磷元素供共生植物的能力非常显著[22]。在磷缺乏的土壤中氮的含量往往也相对较低[35]，AMF不但能提高豆科植物磷的含量，而且也能提高其对氮的吸收[36]。AMF能够通过谷氨酰胺合成酶和谷氨酸合成(GS-GOGAT)途径吸收铵态氮(NH4+)和硝态氮(NO3-)，并储存在它们的外生菌根里(ERM)，然后再将其整合成氨基酸并以精氨酸的形式转运到内生菌根(IRM)，再在IRM里将精氨酸分解、转运给共生植物[37]。但是，也有研究表明，AMF在植物吸收氮的过程中并没有发挥明显的作用，其机制仍备受争议，需深入研究[38]。除氮磷外，AMF在促进豆科植物在微量元素吸收方面也发挥着积极作用[39]。研究表明，AMF的侵染能够提高鹰嘴豆(Cicerarietinum)获取锌[40]和大豆(Glycinemax)获取铜和锌[41]等的能力。此外，AMF的菌丝还能增加共生植物对钙、镁、锰、铁、硅等稳定元素或者微量元素的吸收[42]。最新研究结果表明，AMF能够提高蒺藜苜蓿在硫稀缺环境下的生长能力和植物内硫元素的含量[43]。由于硫可用于植物的光合作用及其生长发育，因此，这对豆科植物抵御生物和非生物胁迫的响应是非常重要的。但是，关于AMF促进豆科植物有关矿质营养吸收的深层次的机制还需要更深入的研究[39]。

此外，AMF提高豆科植物磷和其他营养物质的能力取决于特定的共生体系[42]，对红芸豆(Phaseolusvulgaris)和鹰嘴豆等研究已经证明了上述观点，即不同微生物组合促进共生植物磷和氮吸收的能力是不同的[44-45]。因此，研究和筛选适合不同豆科植物促进其营养物质吸收的高效兼容的AMF菌株，将有助于进一步推动开发利用菌根资源，提高资源的利用效率，实现可持续的农业发展模式。

4 AMF对豆科植物抗逆能力的影响

植物在生长发育过程中会遇到各种生物与非生物胁迫，如何提高植物的抗逆性是科学家们研究的热点。大量的研究证实AMF能够提高共生植物抵御干旱、盐碱、重金属、高温等胁迫的能力。

4.1 AMF提高豆科植物的抗旱能力

研究表明，AMF能够有效缓解干旱对豆科植物的伤害。首先，AMF共生对植物水势产生了积极的影响[46]，提高了植物叶片的相对含水量，使得豆科植物形成干旱逃避机制[47]；其次，AMF提高了共生植物体内营养元素的含量[48]和碳水化合物的百分比[49]，高浓度的磷元素能够增加根系中磷元素的分配[50]，而碳水化合物能够稳定脱氢酶和细胞膜，保护生物结构免于干旱脱水[49]，进而提高了植株抵御干旱的能力；此外，AMF还可以通过提高共生植物的渗透调节[51]和植物体内脱落酸水平[52]，使得植株在干旱环境中能保持更好的叶片蒸腾作用和根系间的水分运输平衡[53]。但是，AMF提高寄主植物抗旱性的准确机制仍需做进一步的研究[54]，尤其需要进一步阐明AMF提高豆科植物抗逆性在分子水平上的应答机制。

4.2 AMF提高豆科植物的抗盐碱能力

AMF除了提高植物的抗旱性，还能提高其抗盐碱的能力[55]，因此被誉为是良好的盐碱土生物改良者[56]。分析其内在机制，一方面，AMF增强了植物的渗透势，气体交换能力和水分利用效率等生理学过程[49,56-57]；另一方面，AMF诱导植株产生了抗生素和植物激素等次生代谢产物，并引起一系列生理过程，最终缓解了盐胁迫对植物的伤害[58-59]。此外，共生植物体内氮磷元素水平发生变化[57,60-61]，帮助植株降低了对钠离子的吸收，缓解了钠离子的毒害作用，间接地维持了叶绿素的浓度[49]，促进其正常生长。但这与Ruiz-Lozano等[62]的研究结论是相反的，即AMF提高植物抗盐能力并非是由于植物体内营养物质的变化所导致的。因此，有关AMF提高豆科植物抗盐性的研究还需要深入阐明其内在机制。

4.3 AMF提高豆科植物的抗重金属毒害和高温胁迫的能力

随着工业化和城市化进程的推进，重金属污染成为亟待解决的重要生态问题之一。大量的研究表明，AMF不仅能够减轻干旱和盐胁迫对植物的损伤，还能够显著降低大豆等豆科植物对重金属的摄入量，缓解重金属的毒害作用，增强了其抵抗重金属毒害的能力[63-64]。这可能是因为AMF大量的菌丝起到了屏障作用，阻止了金属离子由地下到地上部分的转移[65]，而且AMF较强的络合重金属元素的能力，增强了寄主植物对这些重金属离子的耐性，从而减轻植物遭受重金属污染的程度[66]。由此可见，重金属污染区域的治理可以利用豆科植物和AMF共生体系达到最佳治理效应[64]。近些年来，全球气候变化一直是人们关注的热点，温度升高对植物生长的影响也是科学家们研究的重点。Hu等[67]的研究证实，AMF能缓解夜间高温对蒺藜苜蓿的不良影响。这可能是由于AMF改善了共生植物光合作用的能力[68]、增加了对水分和矿质营养的吸收[69]、提高了各种抗氧化类物质的含量[70]，进而提高了共生植物抵御温度胁迫的能力。关于AMF提高豆科植物对高温适应性的研究还很少，其深层次的作用机理仍是未来研究的方向。

AMF提高豆科植物抗逆性的研究范围很广。除能提高共生植物抗干旱、盐碱、重金属和高温外，AMF还能够提高豆科植物的抗病性等[71]。笔者认为，由于AMF与豆科植物的共生具有普遍性和廉价性，提高共生植物抗逆性也是经济的、生态的、环保的。因此，有关AMF提高豆科植物抗性的研究具有重要意义，需要进一步掌握其潜在的机制并拓展其应用范围。

5 AMF与根瘤菌的互作机制

5.1 AMF对豆科植物生物固氮的影响

豆科植物是根瘤菌的天然寄主，根瘤菌能够固定大气中的氮气为植物所利用[72]。对紫花苜蓿[73]、大豆[41]和金合欢(Acaciafarnesiana)[74]的研究表明，AMF的侵染显著增加了共生植物的结瘤数、鲜瘤重、固氮酶的活力、豆血红蛋白的含量等，即AMF的侵染能够促进根瘤的生长，提高生物固氮能力[5,21,39]。这可能是因为，首先，AMF的侵染提高了豆科植物吸收磷元素和固氮所需其他营养物质能力；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动，使根瘤能够为共生植物固定更多的氮。

图1 丛枝菌根真菌与豆科植物共生机制Fig.1 Simplified model for the mechanism of arbuscular mycorrhizal fungi and legumes symbiosis虚线框表示不确定过程Dotted square mean some uncertain processes.

5.2 AMF与根瘤菌的协同增效机制

AMF和根瘤菌是相互紧密联系的[75]，它们的相互作用直接影响了豆科植物的生长、产量[44]及豆科植物-根瘤菌-AMF三者共生体系的效率[29]。对山黧豆(Lathyrussativus)[57]、紫花苜蓿[76]和豌豆(Pisumsativum)[77]等的研究表明，AMF与根瘤菌同时接种对共生植物的促进作用要超过单一接种。这被认为是AMF和根瘤菌之间相互兼容所发挥的协同增效作用[78-79]。但也有研究表明，它们之间存在相互不兼容的竞争[80]。这可能是由于AMF需要较高的光合速率和呼吸速率，抑制了根瘤的生长[21]。目前关于共生体中影响双重接种协同效应的机制还没有较为统一的结果，需要进一步的阐明[42,81]。

6 展望

AMF对植物最大的益处是AMF消耗植物光合作用产物的同时供给植物氮和磷等营养元素(图 1)。目前，通过稳定性同位素示踪技术已经估算了碳的流向，但这种方法不能够区分根系和微生物的呼吸作用[82]。为了进一步阐明碳的转移量及在植物体内的储藏机制，利用微生物携带的对碳有响应的标记基因，可以在时间和空间上动态定量植物与微生物之间的碳转移与消耗[82-83]，但这项技术的应用还是空白，应该利用分子生物学和生物信息学技术进一步完善相关研究。此外，在逆境情况下简单的用植物获得的磷和氮等营养物质来定量分析AMF对植物的有益作用显然是不完整的[82]，因此，有必要通过稳定性同位素技术深入研究豆科植物-根瘤菌-AMF三者共生体系在逆境胁迫下碳的分配、消耗及收益规律。

全球气候变化背景下，全球CO2浓度升高备受人们的关注。随着CO2浓度的升高，植物可利用的碳、对营养元素的需要能力及AMF的侵染率均增加[84]。因此，AMF与豆科植物在CO2升高的环境下是最佳生长环境[75]。但是，在气候变化背景下，AMF对豆科植物个体及在生态系统水平上的研究还很少。此外，AMF在植物-土壤系统中碳转移和陆地生态系统碳氮循环过程中发挥着重要的作用[85-86]。但有关AMF对豆科植物土壤物理化学属性、土壤碳汇和土壤碳氮循环能力的研究还比较少，尤其是在全球气候变化背景下，阐明AMF与豆科植物土壤碳固存和碳氮循环之间的耦联关系是很必要的。

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. 宋福强, 王立, 马放. 丛枝菌根真菌-紫穗槐共生体系的研究[M]. 北京: 科学出版社, 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. 杨秀梅, 陈保冬, 朱永官, 等. 丛枝菌根真菌对铜污染土壤上玉米生长的影响. 生态学报, 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, Kytöviita 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. 杨晓红, 孙中海, 曾斌. 三峡库区橘园丛枝菌根真菌无梗囊霉属调查研究[C]. 中国科协2005年学术年会论文集, 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

国家自然科学基金项目(31402128)和西北农林科技大学基本科研业务专项(2014YB007)资助。

何树斌(1983-)，男，甘肃武威人，讲师，博士。E-mail:heshubin@nwsuaf.edu.cn*通信作者Corresponding author. E-mail: longmingxiu@nwsuaf.edu.cn

何树斌, 郭理想, 李菁, 王燚, 刘泽民, 程宇阳, 呼天明, 龙明秀. 丛枝菌根真菌与豆科植物共生体研究进展. 草业学报, 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.