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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Interactions between soybean, Bradyrhizobium japonicum and Soybean mosaic virus: the effects depend on the interaction sequence

Sofía Andreola https://orcid.org/0000-0002-5544-0228 A B , Marianela Rodriguez A B , Rodrigo Parola A B , Sergio Alemano https://orcid.org/0000-0003-2701-1052 C and Ramiro Lascano https://orcid.org/0000-0002-9576-9941 A D E
+ Author Affiliations
- Author Affiliations

A Instituto de Fisiología y Recursos Genéticos Vegetales, Centro de Investigaciones Agropecuarias-INTA, Camino 60 Cuadras Km 5 y ½, X5020ICA, Córdoba, Argentina.

B Unidad de Estudios Agropecuarios (UDEA- CONICET), Camino 60 cuadras km, 5.5 X5020ICA, Córdoba, Argentina.

C Departamento de Ciencias Naturales, Facultad de Ciencias Exactas, Físico-Químicas y Naturales, Universidad Nacional de Río Cuarto, Río Cuarto, Córdoba, Argentina.

D Cátedra de Fisiología Vegetal, Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, Av. Vélez Sarsfield 299, Córdoba, Argentina.

E Corresponding author. Email: lascano.ramiro@conicet.gov.ar

Functional Plant Biology 46(11) 1036-1048 https://doi.org/10.1071/FP17361
Submitted: 27 April 2017  Accepted: 25 June 2019   Published: 2 October 2019

Abstract

The symbiotic interaction between soybean and nitrogen-fixing rhizobia can lead to plant growth promotion and induced systemic responses. Symbiotic interactions may increase tolerance/resistance to abiotic/biotic stress conditions, but are also sensitive to environmental conditions. Soybean mosaic virus (SMV), which is transmitted by seed and aphids, severely affects crop yields in many areas of the world, consequently virus infection may precede rhizobium infection or vice versa in the field. With the hypothesis that sequence of interaction is a key determinant of the resulting responses; growth, primary metabolism and defence responses were evaluated in different interaction sequences. Results showed that vegetative growth was promoted by Bradyrhizobium japonicum (Bj) inoculation and drastically impaired by SMV infection. The negative effect of SMV single infection on soybean growth parameters was correlated with photosynthesis decrease, sugar accumulation, oxidative damage, and increases in salicylic acid levels. Bj inoculation partially reversed virus-induced symptoms, mainly at Bj-SMV sequence. However, this symptom attenuation did not correlate with less virus accumulation. Nodulation was negatively affected by SMV, particularly when virus infection was previous to Bj inoculation (SMV-Bj). Defence related hormones (salicylic acid (SA)/jasmonic acid (JA)) and the expression of defence-related genes were dependent on the sequence of tripartite interaction. The present study showed that the sequence of the tripartite interaction among soybean, Bj and SMV determinates the tolerance/susceptibility to SMV infection, through changes in the defence mechanism and metabolic alteration.

Additional keywords: defence, rhizobia systemic response, soybean primary metabolism, symbiotic interaction, tripartite interaction.


References

Arif M, Hassan S (2002) Evaluation of resistance in soybean germplasm to soybean mosaic Potyvirus under field conditions. Journal of Biological Sciences 2, 601–604.
Evaluation of resistance in soybean germplasm to soybean mosaic Potyvirus under field conditions.Crossref | GoogleScholarGoogle Scholar |

Babu M, Gagarinova AG, Brandle JE, Wang A (2008) Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection. Journal of General Virology 89, 1069–1080.
Association of the transcriptional response of soybean plants with soybean mosaic virus systemic infection.Crossref | GoogleScholarGoogle Scholar | 18343851PubMed |

Balachandran S, Hurry VM, Kelley SE, Osmond CB, Robinson SA, Rohozinski J, Seaton GGR, Sims DA (1997) Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis. Physiologia Plantarum 100, 203–213.
Concepts of plant biotic stress. Some insights into the stress physiology of virus-infected plants, from the perspective of photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Ballhorn DJ, Kay J, Kautz S (2014) Quantitative effects of leaf area removal on indirect defense of lima bean (Phaseolus lunatus) in nature. Journal of Chemical Ecology 40, 294–296.
Quantitative effects of leaf area removal on indirect defense of lima bean (Phaseolus lunatus) in nature.Crossref | GoogleScholarGoogle Scholar | 24573494PubMed |

Bao D, Ganbaatar O, Cui X, Yu R, Bao W, Falk B, Wuriyanghan H (2018) Down-regulation of genes coding for core RNAi components and disease resistance proteins via corresponding microRNAs might be correlated with successful Soybean mosaic virus infection in soybean. Molecular Plant Pathology 19, 948–960.
Down-regulation of genes coding for core RNAi components and disease resistance proteins via corresponding microRNAs might be correlated with successful Soybean mosaic virus infection in soybean.Crossref | GoogleScholarGoogle Scholar | 28695996PubMed |

Bashar T (2015) ‘Characterization of seed transmission of soybean mosaic virus in soybean.’ (University of Western Ontario, London, ON, Canada)

Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genetics and Molecular Biology 35, 1044–1051.
Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents.Crossref | GoogleScholarGoogle Scholar | 23411488PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |

Broughton WJ, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. The Biochemical Journal 125, 1075–1080.
Control of leghaemoglobin synthesis in snake beans.Crossref | GoogleScholarGoogle Scholar | 5144223PubMed |

Clark MF, Adams AN (1977) Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. Journal of General Virology 34, 475–483.
Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses.Crossref | GoogleScholarGoogle Scholar | 323416PubMed |

Conrath U (2009) ‘Priming of induced plant defense responses. Advances in botanical research’, 1st edn. (Elsevier: Amsterdam)

Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman M-A, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for Battle. Molecular Plant-Microbe Interactions 19, 1062–1071.
Priming: getting ready for Battle.Crossref | GoogleScholarGoogle Scholar | 17022170PubMed |

Cui X, Chen X, Wang A (2011) Detection, understanding and control of soybean mosaic virus. Molecular aspects of breeding. (Ed. A Sudaric) (IntechOpen). Available at https://www.intechopen.com/books/soybean-molecular-aspects-of-breeding/detection-understanding-and-controlof-soybean-mosaic-virus [Verified 2 July 2019].

de Román M, Fernández I, Wyatt T, Sahrawy M, Heil M, Pozo MJ (2011) Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi. Journal of Ecology 99, 36–45.
Elicitation of foliar resistance mechanisms transiently impairs root association with arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

de Souza EM, Granada CE, Sperotto RA (2016) Plant pathogens affecting the establishment of plant–symbiont interaction. Frontiers in Plant Science 7,
Plant pathogens affecting the establishment of plant–symbiont interaction.Crossref | GoogleScholarGoogle Scholar | 26834779PubMed |

De Vleesschauwer D, Höfte M (2009) Rhizobacteria-induced systemic tesistance. Advances in Botanical Research 51, 223–281.
Rhizobacteria-induced systemic tesistance.Crossref | GoogleScholarGoogle Scholar |

Di Rienzo JA, Casanoves F, Balzarini MG, González L, Tablada M, Robledo CW (2016) InfoStat version 2016. Available at https://www.infostat.com.ar/ [Verified 2 July 2019].

Díaz-Cruz GA, Cassone BJ (2018) A tale of survival : molecular defense mechanisms of soybean to overcome Soybean mosaic virus infection. Physiological and Molecular Plant Pathology 102, 79–87.
A tale of survival : molecular defense mechanisms of soybean to overcome Soybean mosaic virus infection.Crossref | GoogleScholarGoogle Scholar |

Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. Journal of Agricultural and Food Chemistry 53, 8437–8442.
Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 16248534PubMed |

Elbadry M, Taha RM, Eldougdoug KA, Gamal-Eldin H (2006) Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria. Journal of Plant Diseases and Protection 113, 247–251.
Induction of systemic resistance in faba bean (Vicia faba L.) to bean yellow mosaic potyvirus (BYMV) via seed bacterization with plant growth promoting rhizobacteria.Crossref | GoogleScholarGoogle Scholar |

Fales FW (1951) The assimilation and degradation of carbohydrates by yeast cells. The Journal of Biological Chemistry 193, 113–124.

Ferguson BJ, Mathesius U (2014) Phytohormone regulation of legume–rhizobia interactions. Journal of Chemical Ecology 40, 770–790.
Phytohormone regulation of legume–rhizobia interactions.Crossref | GoogleScholarGoogle Scholar | 25052910PubMed |

Gil-Quintana E, Larrainzar E, Seminario A, Díaz-Leal JL, Alamillo JM, Pineda M, Arrese-Igor C, Wienkoop S, González EM (2013) Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean. Journal of Experimental Botany 64, 2171–2182.
Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.Crossref | GoogleScholarGoogle Scholar | 23580751PubMed |

Golem S, Culver JN (2003) Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana. Molecular Plant-Microbe Interactions 16, 681–688.
Tobacco mosaic virus induced alterations in the gene expression profile of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12906112PubMed |

Guan HP, Janes HW (1991) Light regulation of sink metabolism in tomato fruit: II. Carbohydrate metabolizing enzymes. Plant Physiology 96, 922–927.
Light regulation of sink metabolism in tomato fruit: II. Carbohydrate metabolizing enzymes.Crossref | GoogleScholarGoogle Scholar | 16668276PubMed |

Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Archives of Biochemistry and Biophysics 125, 189–198.
Photoperoxidation in isolated chloroplasts.Crossref | GoogleScholarGoogle Scholar | 5655425PubMed |

Huot B, Yao J, Montgomery BL, He SY (2014) Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant 7, 1267–1287.
Growth-defense tradeoffs in plants: a balancing act to optimize fitness.Crossref | GoogleScholarGoogle Scholar | 24777989PubMed |

Johnson RA, Wichern DW (2002) Principal components. In ‘Applied multivariate statistical analysis’. pp. 430–480. (Pearson Education, Prentice Hall, Upper Saddle River, NJ, USA)

Kang HG, Singh KB (2000) Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. The Plant Journal 21, 329–339.
Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects.Crossref | GoogleScholarGoogle Scholar | 10758484PubMed |

Khadhair AH, Sinha RC, Peterson JF (1984) Effect of white clover mosaic virus infection on various processes relevant to symbiotic Nz fixation in red clover’. Canadian Journal of Botany 62, 38–43.
Effect of white clover mosaic virus infection on various processes relevant to symbiotic Nz fixation in red clover’.Crossref | GoogleScholarGoogle Scholar |

Laguna IG, Rodriguez Pardina P, Truol G, Fiorona M, Nome CF, DiFeo L, Alemandri V (2008) ‘Enfermedades causadas por virus en cultivos de soja en Argentina.’ (Ediciones INTA: Buenos Aires, Argentina)

Lehto K, Tikkanen M, Hiriart J-B, Paakkarinen V, Aro E-M (2003) Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus. Molecular Plant-Microbe Interactions 16, 1135–1144.
Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus.Crossref | GoogleScholarGoogle Scholar | 14651347PubMed |

Liao L, Chen P, Buss GR, Yang Q, Tolin SA (2002) Inheritance and allelism of resistance to soybean mosaic virus in Zao18 soybean from China. The Journal of Heredity 93, 447–452.
Inheritance and allelism of resistance to soybean mosaic virus in Zao18 soybean from China.Crossref | GoogleScholarGoogle Scholar | 12642647PubMed |

Lilly ST, Drummond RSM, Pearson MN, MacDiarmid RM (2011) Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana. Molecular Plant-Microbe Interactions 24, 294–304.
Identification and validation of reference genes for normalization of transcripts from virus-infected Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21091160PubMed |

Loebenstain G, Carr JP (2006) ‘Natural resistance mechanisms of plants to viruses.’ (Springer: Berlin)

López M, Muñoz N, Lascano HR, Izaguirre-Mayoral ML (2017) The seed-borne Southern bean mosaic virus hinders the early events of nodulation and growth in Rhizobium-inoculated Phaseolus vulgaris L. Functional Plant Biology 44, 208–218.
The seed-borne Southern bean mosaic virus hinders the early events of nodulation and growth in Rhizobium-inoculated Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar |

López-Baena FJ, Monreal JA, Pérez-Montaño F, Guasch-Vidal B, Bellogín RA, Vinardell JM, Ollero FJ (2009) The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean. Molecular Plant-Microbe Interactions 22, 1445–1454.
The absence of Nops secretion in Sinorhizobium fredii HH103 increases GmPR1 expression in Williams soybean.Crossref | GoogleScholarGoogle Scholar | 19810813PubMed |

Louie R (1995) Vascular puncture of maize kernels for the mechanical transmission of maize white line mosaic virus and other viruses of maize. Phytopathology 85, 139–143.
Vascular puncture of maize kernels for the mechanical transmission of maize white line mosaic virus and other viruses of maize.Crossref | GoogleScholarGoogle Scholar |

Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63, 541–556.
Plant-growth-promoting rhizobacteria.Crossref | GoogleScholarGoogle Scholar | 19575558PubMed |

Marquez N, María M, Giachero L, Gallou A, Debat HJ, Cranenbrouck S, Di Rienzo JA, Pozo MJ, Ducasse DA, Declerck S (2018) Transcriptional changes in mycorrhizal and nonmycorrhizal soybean plants upon infection with the fungal pathogen Macrophomina phaseolina. Molecular Plant-Microbe Interactions 31, 842–855.
Transcriptional changes in mycorrhizal and nonmycorrhizal soybean plants upon infection with the fungal pathogen Macrophomina phaseolina.Crossref | GoogleScholarGoogle Scholar | 29498566PubMed |

Mazarei M, Elling AA, Maier TR, Puthoff DP, Baum TJ (2007) GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis. Molecular Plant-Microbe Interactions 20, 107–119.
GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17313162PubMed |

Moy P, Qutob D, Chapman BP, Atkinson I, Gijzen M (2004) Patterns of gene expression upon infection of soybean plants by Phytophthora sojae. Molecular Plant-Microbe Interactions 17, 1051–1062.
Patterns of gene expression upon infection of soybean plants by Phytophthora sojae.Crossref | GoogleScholarGoogle Scholar | 15497398PubMed |

Muñoz N, Rodriguez M, Robert G, Lascano R (2014) Negative short-term salt effects on the soybean-Bradyrhizobium japonicum interaction and partial reversion by calcium addition. Functional Plant Biology 41, 96–105.
Negative short-term salt effects on the soybean-Bradyrhizobium japonicum interaction and partial reversion by calcium addition.Crossref | GoogleScholarGoogle Scholar |

Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology 140, 249–262.
The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death.Crossref | GoogleScholarGoogle Scholar |

Orellana RG, Weber DF, Cregan PB (1980) Nitrogen-fixing competence of Rhizobium japonicum strains in soybean infected with tobacco ringspot virus. Physiological Plant Pathology 17, 381–388.
Nitrogen-fixing competence of Rhizobium japonicum strains in soybean infected with tobacco ringspot virus.Crossref | GoogleScholarGoogle Scholar |

Orellana RG, Reynolds SL, Sloger C, van Berkum P (1983) Specific effects of Soybean mosaic virus on total N, ureide-N, and symbiotc N2-fixation activity in Glycine max and G. soja. Physiology and Biochemistry 73, 1156–1160.

Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar | 11972351PubMed |

Pieterse CMJ, Van Pelt JA, Van Wees SCM, Ton J, León-Kloosterziel KM, Keurentjes JJB, Verhagen BWM, Knoester M, Van der Sluis I, Bakker PAHM, Van Loon LC (2001) Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression. European Journal of Plant Pathology 107, 51–61.
Rhizobacteria-mediated induced systemic resistance: triggering, signaling and expression.Crossref | GoogleScholarGoogle Scholar |

Pieterse CMJ, Leon-Reyes A, Van Der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308–316.
Networking by small-molecule hormones in plant immunity.Crossref | GoogleScholarGoogle Scholar |

Pinheiro GL, Marques CS, Costa MDBL, Reis PAB, Alves MS, Carvalho CM, Fietto LG, Fontes EPB (2009) Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response. Gene 444, 10–23.
Complete inventory of soybean NAC transcription factors: sequence conservation and expression analysis uncover their distinct roles in stress response.Crossref | GoogleScholarGoogle Scholar | 19497355PubMed |

Pompe-Novak M, Gruden K, Baebler Š, Krečič-Stres H, Kovač M, Jongsma M, Ravnikar M (2006) Potato virus Y induced changes in the gene expression of potato (Solanum tuberosum L.). Physiological and Molecular Plant Pathology 67, 237–247.
Potato virus Y induced changes in the gene expression of potato (Solanum tuberosum L.).Crossref | GoogleScholarGoogle Scholar |

Rodríguez M, Taleisnik E, Lenardon S, Lascano R (2010) Are Sunflower chlorotic mottle virus infection symptoms modulated by early increases in leaf sugar concentration? Journal of Plant Physiology 167, 1137–1144.
Are Sunflower chlorotic mottle virus infection symptoms modulated by early increases in leaf sugar concentration?Crossref | GoogleScholarGoogle Scholar | 20413182PubMed |

Rodríguez M, Muñoz N, Lenardon S, Lascano R (2012) The chlorotic symptom induced by Sunflower chlorotic mottle virus is associated with changes in redox-related gene expression and metabolites. Plant Science 196, 107–116.
The chlorotic symptom induced by Sunflower chlorotic mottle virus is associated with changes in redox-related gene expression and metabolites.Crossref | GoogleScholarGoogle Scholar | 23017905PubMed |

Rodríguez M, Munoz N, Lenardon S, Lascano R (2013) Redox-related metabolites and gene expression modulated by sugar in sunflower leaves: similarities with Sunflower chlorotic mottle virus-induced symptom. Redox Report 18, 27–35.
Redox-related metabolites and gene expression modulated by sugar in sunflower leaves: similarities with Sunflower chlorotic mottle virus-induced symptom.Crossref | GoogleScholarGoogle Scholar | 23321504PubMed |

Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45
Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data.Crossref | GoogleScholarGoogle Scholar | 19237396PubMed |

Sheen J (1990) Metabolic repression of transcription in higher plants. The Plant Cell 2, 1027–1038.
Metabolic repression of transcription in higher plants.Crossref | GoogleScholarGoogle Scholar | 2136626PubMed |

Soltabayeva A, Srivastava S, Kurmanbayeva A, Bekturova A, Fluhr R, Sagi M (2018) Early senescence in older leaves of low nitrate-grown Atxdh1 uncovers a role for purine catabolism in N supply. Plant Physiology 178, 1027–1044.
Early senescence in older leaves of low nitrate-grown Atxdh1 uncovers a role for purine catabolism in N supply.Crossref | GoogleScholarGoogle Scholar | 30190419PubMed |

Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant, Cell & Environment 14, 741–762.
Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells.Crossref | GoogleScholarGoogle Scholar |

Tachi H, Fukuda-Yamada K, Kojima T, Shiraiwa M, Takahara H (2009) Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress. Plant Physiology and Biochemistry 47, 73–79.
Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress.Crossref | GoogleScholarGoogle Scholar | 19010689PubMed |

Tecsi LI, Smith AM, Maule AJ, Leegood RC (1996) A spatial analysis of physiological changes associated with infection of cotyledons of marrow plants with cucumber mosaic virus. Plant Physiology 111, 975–985.
A spatial analysis of physiological changes associated with infection of cotyledons of marrow plants with cucumber mosaic virus.Crossref | GoogleScholarGoogle Scholar | 12226342PubMed |

Tu JC, Ford RE, Grau C (1970a) Some factors affecting the nodulation and nodule efficiency in soybeans infected by soybean mosaic virus. Phytopathology 60, 1653–1656.
Some factors affecting the nodulation and nodule efficiency in soybeans infected by soybean mosaic virus.Crossref | GoogleScholarGoogle Scholar |

Tu JC, Ford RE, Quiniones SS (1970b) Effects of soybean mosaic virus and/or bean pod mottle virus infection on soybean nodulation. Phytopathology 60, 518–523.
Effects of soybean mosaic virus and/or bean pod mottle virus infection on soybean nodulation.Crossref | GoogleScholarGoogle Scholar |

Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annual Review of Plant Biology 64, 781–805.
Transport and metabolism in legume-rhizobia symbioses.Crossref | GoogleScholarGoogle Scholar | 23451778PubMed |

Vadez V, Sinclair TR (2001) Leaf ureide degradation and N2 fixation tolerance to water deficit in soybean. Journal of Experimental Botany 52, 153–159.
Leaf ureide degradation and N2 fixation tolerance to water deficit in soybean.Crossref | GoogleScholarGoogle Scholar | 11181724PubMed |

Vincent J (1970) ‘A manual for the practical study of the root-nodule bacteria.’ (Blackwell Scientific Publications: Oxford)

Vogels GD, Van Der Drift C (1970) Differential analyses of glyoxylate derivatives. Analytical Biochemistry 33, 143–157.
Differential analyses of glyoxylate derivatives.Crossref | GoogleScholarGoogle Scholar | 5413235PubMed |

Wang A (2009) Soybean mosaic virus: research progress and future perspectives. In ‘World Soybean Research Conference VIII, Beijing, China’. Available at Www.Wsrc2009.Cn [Verified 2 July 2019]

Wasik BR, Turner PE (2013) On the biological success of viruses. Annual Review of Microbiology 67, 519–541.
On the biological success of viruses.Crossref | GoogleScholarGoogle Scholar | 23808330PubMed |

Watanabe S, Kounosu Y, Shimada H, Sakamoto A (2014) Arabidopsis xanthine dehydrogenase mutants defective in purine degradation show a compromised protective response to drought and oxidative stress. Plant Biotechnology (Sheffield, England) 31, 173–178.
Arabidopsis xanthine dehydrogenase mutants defective in purine degradation show a compromised protective response to drought and oxidative stress.Crossref | GoogleScholarGoogle Scholar |

Wu X, Valli A, García JA, Zhou X, Cheng X (2019) The tug-of-war between plants and viruses: great progress and many remaining questions. Viruses 11, 203
The tug-of-war between plants and viruses: great progress and many remaining questions.Crossref | GoogleScholarGoogle Scholar |

Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Molecular Plant-Microbe Interactions 25, 139–150.
Modulation of host immunity by beneficial microbes.Crossref | GoogleScholarGoogle Scholar | 21995763PubMed |