Genomic Research Favoring Higher Soybean Production

Author(s): Marcela C. Pagano*, Mohammad Miransari*, Eduardo J.A. Corrêa, Neimar F. Duarte, Bakhytzhan K. Yelikbayev

Journal Name: Current Genomics

Volume 21 , Issue 7 , 2020


DOI : 10.2174/1389202921999200824125710

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Graphical Abstract:


Abstract:

Interest in the efficient production of soybean, as one of the most important crop plants, is significantly increasing worldwide. Soybean symbioses, the most important biological process affecting soybean yield and protein content, were revitalized due to the need for sustainable agricultural practices. Similar to many crop species, soybean can establish symbiotic associations with the soil bacteria rhizobia, and with the soil fungi, arbuscular mycorrhizal fungi, and other beneficial rhizospheric microorganisms are often applied as biofertilizers. Microbial interactions may importantly affect soybean production and plant health by activating different genomic pathways in soybean. Genomic research is an important tool, which may be used to elucidate and enhance the mechanisms controlling such actions and interactions. This review presents the available details on the genomic research favoring higher soybean production. Accordingly, new technologies applied to plant rhizosphere and symbiotic microbiota, root-plant endophytes, and details about the genetic composition of soybean inoculant strains are highlighted. Such details may be effectively used to enhance soybean growth and yield, under different conditions, including stress, resulting in a more sustainable production.

Keywords: Gene editing, germplasms, mutants, soybean genome, symbiotic microbes, microbial associations.

[1]
Wall, D.H.; Nielsen, U.N. Biodiversity and ecosystem services: is it the same below ground? Nat. Edu. Knowledge, 2012, 3(12), 8.
[2]
Pagano, M.C.; Schalamuk, S.; Cabello, M.N. Arbuscular mycorrhizal parameters and indicators of soil health and functioning: applications for agricultural and agroforestal systems. In: Soil Microbes and Environmental Health; Miransari, M., Ed.; Nova Science Publishers: New York, USA, 2011, pp. 267-276.
[3]
Pagano, M.C.; Covacevich, F. Arbuscular Mycorrhizas in Agroecosystems. Mycorrhizal Fungi: Soil, Agriculture and Environmental Implications; Fulton, S.M., Ed.; Nova Science Publishers: New York, 2011, pp. 35-65.
[4]
Pagano, M.C. Mycorrhiza: Occurrence in Natural and Restored Environments; Nova Science Publishers: New York, 2012.
[5]
Simard, S.; Austin, M.E. The role of mycorrhizas in forest soil stability with climate change.Climate change and variability. ; Simard, S., Austin, M. E., Ed; . , 2010, pp. 275-302.
[http://dx.doi.org/10.5772/9813]
[6]
Miransari, M.; Riahi, H.; Eftekhar, F.; Minaie, A.; Smith, D.L. Improving soybean (Glycine max L.) N2 fixation under stress. J. Plant Growth Regul., 2013, 32(4), 909-921.
[http://dx.doi.org/10.1007/s00344-013-9335-7]
[7]
FAO (Food and Agriculture Organization). 2003.http://apps.fao.org
[8]
López-López, A.; Rosenblueth, M.; Martínez, J.; Martínez-Romero, E. Rhizobial symbioses in tropical legumes and non-legumes.Soil Biology and Agriculture in the tropics, Soil Biology; ; P. Dion, Ed; . , 2010, 21, pp. 163-184.
[http://dx.doi.org/10.1007/978-3-642-05076-3_8]
[9]
Rodríguez-Navarro, D.N.; Oliver, I.M.; Contreras, M.A.; Ruiz-Sainz, J.E. Soybean interactions with soil microbes, agronomical and molecular aspects. Agron. Sustain. Dev., 2011, 31(1), 173-190.
[http://dx.doi.org/10.1051/agro/2010023]
[10]
Cattelan, A.J.; Dall’Agnol, A. The rapid soybean growth in Brazil. OCL, 2018, 25(1), 1-12.
[11]
Sugiyama, A.; Ueda, Y.; Takase, H.; Yazaki, K. Cotton-groundnut intercropping system: a pragmatic approach for increasing edible oilseeds production in India. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci., 2015, 87(3), 761-767.
[12]
Singh, R.J.; Alam, N.M.; Kumar, S. Bt Cotton-groundnut intercropping system: a pragmatic approach for increasing edible oilseeds production in India. Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci., 2017, 87(3), 761-767.
[http://dx.doi.org/10.1007/s40011-015-0643-5]
[13]
Masuda, T.; Goldsmith, P.D. World soybean production: area harvested, yield, and long-term projections. Int. Food Agribus. Manag. Rev., 2009, 12(4), 143-161.
[14]
Agyei, D.; Potumarthi, R.; Danquah, M.K. Food-derived multifunctional bioactive proteins and peptides: Applications and recent advances. Biotechnology of Bioactive Compounds: Sources and Applications; Gupta, V.K.; Tuohy, M.G.; O’Donovan, A; Lohani, M., Ed.; Wiley-Blackwell: Chichester, 2015, pp. 507-524.
[http://dx.doi.org/10.1002/9781118733103.ch20]
[15]
The Economist. The miracle of the cerrado: Brazil has revolutionised its own farms. Can it do the same for others? , 2010.Available from: . http://www.economist.com/node/16886442
[16]
Chianu, J.N.; Huising, J.; Danso, S.; Okoth, P.; Chianu, J.N.; Sanginga, N. Financial value of nitrogen fixation in soybean in Africa: increasing benefits for smallholder farmers. J. Life Sci., 2010, 4(6), 50-59.
[17]
Mpepereki, S.; Javaheri, F.; Davis, P.; Giller, K.E. Soybeans and sustainable agriculture: ‘Promiscuous’ soybeans in southern Africa. Field Crops Res., 2000, 65(2-3), 137-149.
[http://dx.doi.org/10.1016/S0378-4290(99)00083-0]
[18]
Tilman, D.; Balzer, C.; Hill, J.; Befort, B.L. Global food demand and the sustainable intensification of agriculture. Proc. Natl. Acad. Sci. USA, 2011, 108(50), 20260-20264.
[http://dx.doi.org/10.1073/pnas.1116437108] [PMID: 22106295]
[19]
Foley, J.A.; Ramankutty, N.; Brauman, K.A.; Cassidy, E.S.; Gerber, J.S.; Johnston, M.; Mueller, N.D.; O’Connell, C.; Ray, D.K.; West, P.C.; Balzer, C.; Bennett, E.M.; Carpenter, S.R.; Hill, J.; Monfreda, C.; Polasky, S.; Rockström, J.; Sheehan, J.; Siebert, S.; Tilman, D.; Zaks, D.P.M. Solutions for a cultivated planet. Nature, 2011, 478(7369), 337-342.
[http://dx.doi.org/10.1038/nature10452] [PMID: 21993620]
[20]
Foyer, C.H.; Nguyen, H.T.; Lam, H-M.A. A seed change in our understanding of legume biology from genomics to the efficient cooperation between nodulation and arbuscular mycorrhizal fungi. Plant Cell Environ., 2018, 41(9), 1949-1954.
[PMID: 30520104]
[21]
Wingeyer, A.B.; Amado, T.J.C.; Pérez-Bidegain, M.; Studdert, G.A.; Varela, C.H.P.; Garcia, F.O.; Karlen, D.L. Soil quality impacts of current south American agricultural practices. Sustainability, 2015, 7(2), 2212-2242.
[http://dx.doi.org/10.3390/su7022213]
[22]
Vanhie, M.; Deen, W.; Lauzon, J.D.; Hooker, D.C. Effect of increasing levels of maize (Zea mays L.) residue on no-tillsoybean (Glycine max Merr.) in Northern production regions: a review. Soil Tillage Res., 2015, 150, 201-210.
[http://dx.doi.org/10.1016/j.still.2015.01.011]
[23]
Higo, M.; Isobe, K.; Yamaguchi, M.; Drijber, R.A.; Jeske, E.S.; Ishii, R. Diversity and vertical distribution of indigenous arbuscular mycorrhizal fungi under two soybean rotational systems. Biol. Fertil. Soils, 2013, 49(8), 1085-1096.
[http://dx.doi.org/10.1007/s00374-013-0807-5]
[24]
Salvagiotti, F.; Cassman, K.G.; Specht, J.E.; Walters, D.T.; Weiss, A.; Dobermann, A. Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crops Res., 2008, 108, 1-13.
[http://dx.doi.org/10.1016/j.fcr.2008.03.001]
[25]
MAPA . Ministério da Agricultura, Pecuária e Abastecimento , 2015.http://www.agricultura.gov.br/
[26]
Sobolevsky, A.; Moschini, G.; Lapan, H. Genetically modified crops and product differentiation: trade and welfare effects in the soybean complex. Am. J. Agric. Econ., 2005, 87(3), 621-644.
[http://dx.doi.org/10.1111/j.1467-8276.2005.00752.x]
[27]
Castro, G.S.A.; Crusciol, C.A.C. Yield and mineral nutrition of soybean, maize, and Congo signal grass as affected by limestone and slag. Pesqui. Agropecu. Bras., 2013, 48(6), 673-681.
[http://dx.doi.org/10.1590/S0100-204X2013000600013]
[28]
Ho, Y. Plant-microbe ecology: interactions of plants and symbiotic microbial communities; Plant Ecology-Traditional Approaches To Recent Trends, IntechOpen, 2017, pp. 93-119.
[29]
Li, M.W.; Wang, Z.; Jiang, B.; Kaga, A.; Wong, F.L.; Zhang, G.; Han, T.; Chung, G.; Nguyen, H.; Lam, H.M. Impacts of genomic research on soybean improvement in East Asia. Theor. Appl. Genet., 2020, 133(5), 1655-1678.
[http://dx.doi.org/10.1007/s00122-019-03462-6] [PMID: 31646364]
[30]
Fang, C.; Ma, Y.; Wu, S.; Liu, Z.; Wang, Z.; Yang, R.; Hu, G.; Zhou, Z.; Yu, H.; Zhang, M.; Pan, Y.; Zhou, G.; Ren, H.; Du, W.; Yan, H.; Wang, Y.; Han, D.; Shen, Y.; Liu, S.; Liu, T.; Zhang, J.; Qin, H.; Yuan, J.; Yuan, X.; Kong, F.; Liu, B.; Li, J.; Zhang, Z.; Wang, G.; Zhu, B.; Tian, Z. Genome-wide association studies dissect the genetic networks underlying agronomical traits in soybean. Genome Biol., 2017, 18(1), 161.
[http://dx.doi.org/10.1186/s13059-017-1289-9] [PMID: 28838319]
[31]
Zhang, J.; Wang, X.; Lu, Y.; Bhusal, S.J.; Song, Q.; Cregan, P.B.; Yen, Y.; Brown, M.; Jiang, G.L. Genome-wide scan for seed composition provides insights into soybean quality improvement and the impacts of domestication and breeding. Mol. Plant, 2018, 11(3), 460-472.
[http://dx.doi.org/10.1016/j.molp.2017.12.016] [PMID: 29305230]
[32]
Frank, B. Uber die Pilzsymbiose der Leguminosen. Ber. Dtsch. Bot. Ges., 1889, 7, 332-346.
[33]
Fred, E.B.; Baldwin, I.L.; McCoy, E. Root nodule bacteria and leguminous plants. University of Wisconsin Studies in Science No.5; University of Wisconsin: Madison, 1932.
[34]
Holt, J.G.; Krieg, N.R.; Sneath, P.H.A.; Staley, J.T.; Williams, S.T. Bergey’s manual of Determinative Bacteriology; Williams and Wilkins Press: Baltimore, 1994.
[35]
Elkan, G.H. Taxonomy of the rhizobia. Can. J. Microbiol., 1992, 38(6), 446-450.
[http://dx.doi.org/10.1139/m92-075]
[36]
Allen, O.N.; Allen, E.K. The Leguminosae; University of Wisconsin Press: Madison, Wis., 1981.
[http://dx.doi.org/10.1007/978-1-349-06142-6]
[37]
Jordan, D.C. Transfer of Rhizobium japonicum Buchanan 1980 to Bradyrhizobiumgen. nov. a genus of slow growing root nodule bacteria from leguminous plants. Int. J. Sys. Bact., 1982, 32(1), 136-139.
[http://dx.doi.org/10.1099/00207713-32-1-136]
[38]
Young, J.A.W.; Haukka, K. Diversity and phylogeny of rhizobia. New Phytol., 1996, 133(1), 87-94.
[http://dx.doi.org/10.1111/j.1469-8137.1996.tb04344.x]
[39]
Delamuta, J.R.M.; Ribeiro, R.A.; Ormeño-Orrillo, E.; Melo, I.S.; Martínez-Romero, E.; Hungria, M. Polyphasic evidence supporting the reclassification of Bradyrhizobium japonicum group Ia strains as Bradyrhizobium diazoefficiens sp. nov. Int. J. Syst. Evol. Microbiol., 2013, 63(Pt 9), 3342-3351.
[http://dx.doi.org/10.1099/ijs.0.049130-0] [PMID: 23504968]
[40]
Sprent, J.I.; Ardley, J.; James, E.K. Biogeography of nodulated legumes and their nitrogen-fixing symbionts. New Phytol., 2017, 215(1), 40-56.
[http://dx.doi.org/10.1111/nph.14474] [PMID: 28211601]
[41]
Kuykendall, L.D.; Saxena, B.; Devine, T.E.; Udell, S.E. Genetic diversity in Bradyrhizobium japonicum Jordan. 1982 and a proposal for Bradyrhizobium elkani sp. nov. Can. J. Microbiol., 1992, 38(6), 501-505.
[http://dx.doi.org/10.1139/m92-082]
[42]
Xu, L.M.; Ge, C.; Cui, Z.; Li, J.; Fan, H. Bradyrhizobium liaoningense sp. nov., isolated from the root nodules of soybeans. Int. J. Syst. Bacteriol., 1995, 45(4), 706-711.
[http://dx.doi.org/10.1099/00207713-45-4-706] [PMID: 7547289]
[43]
Young, J.P.W. Phylogenetic classification of nitrogen-fixing organisms.Biological Nitrogen Fixation ; Stacey, G. Burris and Evans H.J, Eds. . Chapman and Hall, New York, USA. , 1991, pp. 43-86.
[44]
Willems, A. The taxonomy of rhizobia: An overview. Plant Soil, 2006, 287(1-2), 3-14.
[http://dx.doi.org/10.1007/s11104-006-9058-7]
[45]
Cooper, J.E. Early interactions between legumes and rhizobia: disclosing complexity in a molecular dialogue. J. Appl. Microbiol., 2007, 103(5), 1355-1365.
[http://dx.doi.org/10.1111/j.1365-2672.2007.03366.x] [PMID: 17953546]
[46]
Denison, R.F.; Toby Kiers, E. Why are most rhizobia beneficial to their plant hosts, rather than parasitic? Microbes Infect., 2004, 6(13), 1235-1239.
[http://dx.doi.org/10.1016/j.micinf.2004.08.005] [PMID: 15488744]
[47]
Laranjo, M.; Alexandre, A.; Oliveira, S. Legume growth-promoting rhizobia: an overview on the Mesorhizobium genus. Microbiol. Res., 2014, 169(1), 2-17.
[http://dx.doi.org/10.1016/j.micres.2013.09.012] [PMID: 24157054]
[48]
Sprent, J.I. Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol., 2007, 174(1), 11-25.
[http://dx.doi.org/10.1111/j.1469-8137.2007.02015.x] [PMID: 17335493]
[49]
Parniske, M. Uptake of bacteria into living plant cells, the unifying and distinct feature of the nitrogen-fixing root nodule symbiosis. Curr. Opin. Plant Biol., 2018, 44, 164-174.
[http://dx.doi.org/10.1016/j.pbi.2018.05.016] [PMID: 30071473]
[50]
Dwivedi, S.L.; Sahrawat, K.L.; Upadhyaya, H.D.; Mengoni, A.; Galardini, M.; Bazzicalupo, M.; Biondi, E.G.; Hungria, M.; Kaschuk, G.; Blair, M.W.; Ortiz, R. Advances in host plant and rhizobium genomics to enhance symbiotic nitrogen fixation in grain legumes. Adv. Agron., 2015, 129, 1-116.
[http://dx.doi.org/10.1016/bs.agron.2014.09.001]
[51]
Uchida, Y.; Akiyama, H. Mitigation of postharvest nitrous oxide emissions from soybean ecosystems: A review. Soil Sci. Plant Nutr., 2013, 59(4), 477-487.
[http://dx.doi.org/10.1080/00380768.2013.805433]
[52]
Hungria, M.; Loureiro, M.F.; Mendes, I.C.; Campo, R.J.; Graham, P.H. Inoculant preparation, production and application.Nitrogen fixation in agriculture, forestry, ecology, and the environment ; Werner, D.; Newton, W.E., Eds.; Kluwer: Dordrecht, . , 2005, pp. 223-253. a.
[http://dx.doi.org/10.1007/1-4020-3544-6_11]
[53]
Hungria, M.; Franchini, J.C.; Campo, R.J.; Graham, P.H. The importance of nitrogen fixation to soybean cropping in South America.Newton, W. E. (Org.). Nitrogen fixation in agriculture: forestry ecology and environment; ; Werner, D., Ed.;. Kluwer Academic Publishers: Dordrecht, , 2005, pp. 25 -42. b.
[http://dx.doi.org/10.1007/1-4020-3544-6_3]
[54]
Keyser, H.H.; Li, F. Potential for increasing biological nitrogen fixation in soybean. Plant Soil, 1992, 141, 119-135.
[http://dx.doi.org/10.1007/BF00011313]
[55]
Hungria, M.; Mendes, I.C. Nitrogen fixation with soybean: the perfect symbiosis? Biological Nitrogen Fixation ; de Bruijn, F.J., Ed.; Wiley: Hoboken, . , 2015.
[http://dx.doi.org/10.1002/9781119053095.ch99]
[56]
Campo, R.J. Silva, Araujo R.; Hungria, M. Molybdenum-enriched soybean seeds enhance N accumulation, seed yield, and seed protein content in Brazil. Field Crops Res., 2009, 110(3), 219-224.
[http://dx.doi.org/10.1016/j.fcr.2008.09.001]
[57]
Diaz, D.A.R.; Pedersen, P.; Sawyer, J.E. Soybean response to inoculation and nitrogen application following long-term grass pasture. Crop Sci., 2009, 49(3), 1058-1062.
[http://dx.doi.org/10.2135/cropsci2008.08.0510]
[58]
Barcellos, F.G.; Menna, P.; da Silva Batista, J.S.; Hungria, M. Evidence of horizontal transfer of symbiotic genes from a Bradyrhizobium japonicum inoculant strain to indigenous diazotrophs Sinorhizobium (Ensifer) fredii and Bradyrhizobium elkanii in a Brazilian Savannah soil. Appl. Environ. Microbiol., 2007, 73(8), 2635-2643.
[http://dx.doi.org/10.1128/AEM.01823-06] [PMID: 17308185]
[59]
Nandasena, K.G.; O’Hara, G.W.; Tiwari, R.P.; Sezmiş, E.; Howieson, J.G. In situ lateral transfer of symbiosis islands results in rapid evolution of diverse competitive strains of mesorhizobia suboptimal in symbiotic nitrogen fixation on the pasture legume Biserrula pelecinus L. Environ. Microbiol., 2007, 9(10), 2496-2511.
[http://dx.doi.org/10.1111/j.1462-2920.2007.01368.x] [PMID: 17803775]
[60]
Miranda, J.C.C. Cerrado, Micorriza Arbuscular ocorrência e manejo. Embrapa; Planaltina, 2008.
[61]
Miranda, J.C.C.; Vilela, L.; Miranda, L.N. Dynamics and contribution of arbuscular mycorrhiza in culture systems with crop rotation. Pesqui. Agropecu. Bras., 2005, 40(10), 1005-1014.
[http://dx.doi.org/10.1590/S0100-204X2005001000009]
[62]
Grümberg, B.C.; Urcelay, C.; Shroeder, M.A.; Vargas-Gil, S.; Luna, C.M. The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol. Fertil. Soils, 2015, 51(1), 1-1.
[http://dx.doi.org/10.1007/s00374-014-0942-7]
[63]
Palleroni, N.J. Present situation of the taxonomy of aerobic pseudomonads. Pseudomonas: Molecular Biology and Biotechnology; Galli, E.; Silver, S; Witholt, B., Ed.; American Society for Microbiology: Washington, DC, 1992, pp. 105-115.
[64]
Rhamani, H.A.; Saleh-Rastin, N.; Khavazi, K.; Asgharzadeh, A.; Fewer, D.; Kiani, S.; Lindstrom, K. Selection of thermotolerant bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi-arid regions of Iran. World J. Microbiol. Biotechnol., 2009, 25, 591-600.
[http://dx.doi.org/10.1007/s11274-008-9927-8]
[65]
Raaijmakers, J.M.; Paulitz, T.C.; Steinberg, C.; Alabouvette, C.; Moënne-Loccoz, Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil, 2009, 321(1-2), 341-361.
[http://dx.doi.org/10.1007/s11104-008-9568-6]
[66]
Minhoni, M.T.A.; Cardoso, E.J.B.N.; Eira, A.F. Efeitos da adição de fosfato de rocha, bagaço de cana-de-açúcar, fosfato solúvel e fungo micorrízico no crescimento e na absorção de nutrientes por plantas de soja. Rev. Bras. Ciênc. Solo, 1993, 17, 173-178.
[67]
Porcel, R.; Barea, J.M.; Ruiz-Lozano, J.M. Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol., 2003, 157(1), 135-143.
[http://dx.doi.org/10.1046/j.1469-8137.2003.00658.x]
[68]
Aysan, E.; Demir, S. Using arbuscular mycorrhizal fungi and Rhizobium leguminosarum, biovar Phaseoli against Sclerotinia sclerotiorum (Lib.) de bary in the common bean Phaseolus vulgaris L. Plant Pathol. J., 2009, 8, 74-78.
[http://dx.doi.org/10.3923/ppj.2009.74.78]
[69]
Barea, J.M.; Azcón, R.; Azcón-Aguilar, C. Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek, 2002, 81(1-4), 343-351.
[http://dx.doi.org/10.1023/A:1020588701325] [PMID: 12448732]
[70]
Contreras-Cornejo, H.A.; Macías-Rodríguez, L.; del-Val, E.; Larsen, J. Ecological functions of Trichoderma spp. and their secondary metabolites in the rhizosphere: interactions with plants. FEMS Microbiol. Ecol., 2016, 92(4), fiw036
[http://dx.doi.org/10.1093/femsec/fiw036] [PMID: 26906097]
[71]
Cao, Y.; Halane, M.K.; Gassmann, W.; Stacey, G. The role of plant innate immunity in the legume-rhizobium symbiosis. Annu. Rev. Plant Biol., 2017, 68, 535-561.
[http://dx.doi.org/10.1146/annurev-arplant-042916-041030] [PMID: 28142283]
[72]
Miransari, M.; Abrishamchi, A.; Khoshbakht, K.; Niknam, V. Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit. Rev. Biotechnol., 2014, 34(2), 123-133.
[http://dx.doi.org/10.3109/07388551.2012.731684] [PMID: 23113535]
[73]
Miransari, M. Plant growth promoting rhizobacteria. J. Plant Nutr., 2014, 37(14), 2227-2235.
[http://dx.doi.org/10.1080/01904167.2014.920384]
[74]
Strauss, S.L.; Kluepfel, D.A. Anaerobic soil disinfestation: a chemical-independent approach to pre-plant control of plant pathogens. J. Integr. Agric., 2015, 14(11), 2309-2318.
[http://dx.doi.org/10.1016/S2095-3119(15)61118-2]
[75]
Dashti, N.; Zhang, F.; Hynes, R.; Smith, D.L. Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean (Glycine max (L.) Merr.) under short season conditions. Plant Soil, 1998, 200, 205-213.
[http://dx.doi.org/10.1023/A:1004358100856]
[76]
Xie, Z.P.; Staehelin, C.; Vierheilig, H.; Wiemken, A.; Jabbouri, S.; Broughton, W.J.; Vogeli-Lange, R.; Boller, T.; Xie, Z.P. Rhizobial nodulation factors stimulate mycorrhizal colonization of undulating and non-nodulating soybeans. Plant Physiol., 1995, 108(4), 1519-1525.
[http://dx.doi.org/10.1104/pp.108.4.1519] [PMID: 12228558]
[77]
Ramesh, A.; Sharma, S.K.; Yadav, N.; Joshi, O.P. Phosphorus mobilization from native soil P-pool upon inoculation with phytate-mineralizing and phosphate-solubilizing Bacillus aryabhattai isolates for improved P-acquisition and growth of soybean and wheat crops in microcosm conditions. Agric. Res., 2014, 3(2), 118-127.
[http://dx.doi.org/10.1007/s40003-014-0105-y]
[78]
Kwak, Y.; Jung, B.K.; Shin, J.H. Complete genome sequence of Pseudomonas rhizosphaerae IH5T (=DSM 16299T), a phosphate-solubilizing rhizobacterium for bacterial biofertilizer. J. Biotechnol., 2015, 193, 137-138.
[http://dx.doi.org/10.1016/j.jbiotec.2014.11.031] [PMID: 25483321]
[79]
Abd-Alla, M.H.; El-Enany, A.W.E.; Nafady, N.A.; Khalaf, D.M.; Morsy, F.M. 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. Microbiol. Res., 2014, 169(1), 49-58.
[http://dx.doi.org/10.1016/j.micres.2013.07.007] [PMID: 23920230]
[80]
Li, S.M.; Li, L.; Zhang, F.S. Enhancing phosphorus and nitrogen uptake of faba bean by inoculating arbuscular mycorrhizal fungus and Rhizobium leguminosarum. J. China. Agric. Uni, 2004, 9, 11-15.
[81]
Afkhami, M.E.; Almeida, B.K.; Hernandez, D.J.; Kiesewetter, K.N.; Revillini, D.P. Tripartite mutualisms as models for understanding plant-microbial interactions. Curr. Opin. Plant Biol., 2020, 56, 28-36.
[http://dx.doi.org/10.1016/j.pbi.2020.02.003] [PMID: 32247158]
[82]
Wang, X.; Pan, Q.; Chen, F.; Yan, X.; Liao, H. Effects of co-inoculation with arbuscular mycorrhizal fungi and rhizobia on soybean growth as related to root architecture and availability of N and P. Mycorrhiza, 2011, 21(3), 173-181.
[http://dx.doi.org/10.1007/s00572-010-0319-1] [PMID: 20544230]
[83]
Yan, J.; Chen, W.; Han, X.; Wang, E.; Zou, W.; Zhang, Z. Genetic diversity of indigenous soybean-nodulating rhizobia in response to locally-based long term fertilization in a Mollisol of Northeast China. World J. Microbiol. Biotechnol., 2017, 33(1), 6.
[http://dx.doi.org/10.1007/s11274-016-2170-9] [PMID: 27848139]
[84]
Kalita, M.; Małek, W. Root nodules of Genista germanica harbor Bradyrhizobium and Rhizobium bacteria exchanging nodC and nodZ genes. Syst. Appl. Microbiol., 2020, 43(1), 126026
[http://dx.doi.org/10.1016/j.syapm.2019.126026] [PMID: 31706562]
[85]
Kanehara, K.; Minamisawa, K. Complete genome sequence of Bradyrhizobium japonicum J5, isolated from a soybean nodule in Hokkaido, Japan. Genome Announc., 2017, 5(6), e01619-e16.
[http://dx.doi.org/10.1128/genomeA.01619-16] [PMID: 28183772]
[86]
Htwe, A.Z.; Yamakawa, T. Enhanced plant growth and/or nitrogen fixation by leguminous and non-leguminous crops after single or dual inoculation of Streptomyces griseoflavus P4 with Bradyhizobium strains. Afr. J. Microbiol. Res., 2015, 9, 2337-2344.
[http://dx.doi.org/10.5897/AJMR2015.7796]
[87]
Sakamoto, K.; Ogiwara, N.; Kaji, T.; Sugimoto, Y.; Ueno, M.; Sonoda, M.; Matsui, A.; Ishida, J.; Tanaka, M.; Totoki, Y.; Shinozaki, K.; Seki, M. Transcriptome analysis of soybean (Glycine max) root genes differentially expressed in rhizobial, arbuscular mycorrhizal, and dual symbiosis. J. Plant Res., 2019, 132(4), 541-568.
[http://dx.doi.org/10.1007/s10265-019-01117-7] [PMID: 31165947]
[88]
Saïdi, S.; Ramírez-Bahena, M.H.; Santillana, N.; Zúñiga, D.; Álvarez-Martínez, E.; Peix, A.; Mhamdi, R.; Velázquez, E. Rhizobium laguerreae sp. nov. nodulates Vicia faba on several continents. Int. J. Syst. Evol. Microbiol., 2014, 64(Pt 1), 242-247.
[http://dx.doi.org/10.1099/ijs.0.052191-0] [PMID: 24067731]
[89]
Shi, Y.; Li, J.; Wang, J.; Zhu, R.; Li, S.; Li, Q.; Chen, L.; Zhu, J.; Zou, J.; Wang, J.; Chang, H. Nodulation and genomic capacity of a novel high-latitude Bradyrhizobium japonicum HLNEAU001. J. Soil Sci. Plant Nutr., 2019, 19(2), 277-289.
[http://dx.doi.org/10.1007/s42729-019-00027-w]


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VOLUME: 21
ISSUE: 7
Year: 2020
Published on: 21 October, 2020
Page: [481 - 490]
Pages: 10
DOI: 10.2174/1389202921999200824125710
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