丛枝菌根真菌与豆科植物共生体研究进展

doi:10.11686/cyxb2016228

摘要/Abstract

摘要： 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。

Abstract: 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.

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[J]. 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[J]. Acta Prataculturae Sinica, 2017, 26(1): 187-194.

参考文献

[1]　Nanjareddy K, Blanco L, Arthikala M K, et al. Nitrate regulates rhizobial and mycorrhizal symbiosis in common bean (Phaseolus vulgaris L.). 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, et al. Synergistic interaction of Rhizobium leguminosarum bv. viciae and arbuscular mycorrhizal fungi as a plant growth promoting biofertilizers for faba bean (Vicia faba L.) 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, et al. 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 in Medicago truncatula. Phytochemistry, 2007, 68(1): 75-81.
[9]　Meghvansi M K, Prasad K, Harwani D, et al. Response of soybean cultivars toward inoculation with three arbuscular mycorrhizal fungi and Bradyrhizobium japonicum in the alluvial soil. European Journal of Soil Biology, 2008, 44(3): 316-323.
[10]　De Mita S, Streng A, Bisseling T, et al. 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 and Amorpha fruticosa[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 of Medicago truncatula. Phytochemistry, 2008, 69(1): 112-146.
[14]　Larose G, Chênevert R, Moutoglis P, et al. Flavonoid levels in roots of Medicago sativa are 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, et al. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology, 2003, 131(3): 952-962.
[16]　Morandi D, Branzanti B, Gianinazzi-Pearson V. Effect of some plant flavonoids on in vitro behaviour of an arbuscular mycorrhizal fungus. Agronomie, 1992, 12: 811-816.
[17]　Catoira R, Galera C, De Billy F, et al. Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. The Plant Cell, 2000, 12(9): 1647-1665.
[18]　Puppo A, Pauly N, Boscari A, et al. 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 of Rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. 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 nodulated Phaseolus vulgaris. Soil Biology and Biochemistry, 2008, 40(5): 1019-1027.
[22]　Kaschuk G, Kuyper T W, Leffelaar P A, et al. 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 of Trifolium repens L. 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-Rhizobium tripartite symbiotic association[M]. Plant Growth and Health Promoting Bacteria. Berlin: Springer-Verlag Berlin Heidelberg, 2010.
[25]　Bago B, Pfeffer P E, Abubaker J, et al. 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, et al. The dual symbiosis between arbuscular mycorrhiza and nitrogen fixing bacteria benefits the growth and nutrition of the woody invasive legume Acacia cyclops under 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 and Rhizobium leguminosarum bv. viceae enhance 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-Glomus associations. 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, et al. 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, et al. 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, et al. Arbuscular mycorrhizal fungi alter the response of growth and nutrient uptake of snap bean (Phaseolus vulgaris L.) to O3. Journal of Environmental Sciences, 2011, 23(6): 968-974.
[37]　Govindarajulu M, Pfeffer P E, Jin H, et al. 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, et al. 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, Bradyrhizobium japonicum (Kirchner) Jordan and soybean (Glycine max (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, et al. Transcriptional responses of Medicago truncatula upon 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, et al. 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 and Bradyrhizobium japonicum on drought stress of soybean. Biologia, 2006, 61(19): 324-328.
[48]　Kong J, Pei Z, Du M, et al. 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, et al. Improving salinity tolerance of Acacia saligna (Labill.) plant by arbuscular mycorrhizal fungi and Rhizobium inoculation. 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 á, León-Morcillo R, Vierheilig H, et al. 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-mycorrhizal Lactuca sativa plants 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-stressed Cajanus cajan L.(Millsp.) genotypes. Mycorrhiza, 2015, 25(3): 165-180.
[57]　Jin L, Sun X W, Wang X J, et al. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth of Lathyrus sativus under 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, et al. 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, et al. Field application of mycorrhizal bio-inoculants affects the mineral uptake of a forage legume (Hedysarum coronarium L.) 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-mycorrhizal Glomus species in Lactuca sativa plants. Physiologia Plantarum, 1996, 98(4): 767-772.
[63]　Andrade S A L, Abreu C A, De Abreu M F, et al. Influence of lead additions on arbuscular mycorrhiza and Rhizobium symbioses 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-fixer Rhizobium bacterium. 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, et al. Effect of arbuscular mycorrhizal fungi (Glomus intraradices) 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, et al. Arbuscular mycorrhizal symbiosis can mitigate the negative effects of night warming on physiological traits of Medicago truncatula L. 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 of Capsicum annuum L. Mycorrhiza, 2004, 14(4): 241-244.
[69]　Ruotsalainen A L, Kyt?viita M M. Mycorrhiza does not alter low temperature impact on Gnaphalium norvegicum. 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 (Vigna unguiculata) 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, et al. Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature, 2003, 422: 722-726.
[73]　Toro M, Azcón R, Barea J M. The use of isotopic dilution techniques to evaluate the interactive effects of Rhizobium genotype, mycorrhizal fungi, phosphate-solubilizing rhizobacteria and rock phosphate on nitrogen and phosphorus acquisition by Medicago sativa. New Phytologist, 1998, 138(2): 265-273.
[74]　Benbrahim K F, Ismaili M. Interactions in the symbiosis of Acacia saligna with Glomus mosseae and Rhizobium in 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, et al. Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) 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 and Rhizobium to 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, et al. The effect of inoculation of pea plants with mycorrhizal fungi and Rhizobium on nitrogen and phosphorus assimilation. Plant Soil and Environment, 2006, 52(10): 435-539.
[78]　Stancheva I, Geneva M, Djonova E, et al. Response of alfalfa (Medicago sativa L.) 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, et al. 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-Rhizobium symbiosis II. Antagonistic effects between mycorrhizal colonization and nodulation. Plant Physiology, 1985, 79: 1054-1058.
[81]　Zarei M, Saleh-Rastin N, Alikhani H A, et al. 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, et al. Arbuscular mycorrhiza infection enhances the growth response of Lolium perenne to 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, et al. 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.