molecules by direct binding. Proc Natl Acad Sci U S A 109:13859–13864. https://doi.org/
10.1073/pnas.1205171109
97. Vedam V, Haynes JG, Kannenberg EL, Carlson RW, Sherrier DJ (2004) A Rhizobium
leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with
delayed and defective bacteroid formation. Mol Plant-Microbe Interact 17:283–291
98. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC (2008)
Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti
or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci U S A 105:704–709. https://doi.
org/10.1073/pnas.0709338105
99. Jones KM (2012) Increased production of the exopolysaccharide succinoglycan enhances
Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. J Bacteriol
194:4322–4331. https://doi.org/10.1128/JB.00751-12
100. D’Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant
immunity. Trends Microbiol 12:555–561
101. de Vasconcelos MA, Cunha CO, Arruda FVS, Carneiro VA, Bastos RM, Mercante FM, do
Nascimento KS, Cavada BS, dos Santos RP, Teixeira EH (2013) Effect of leguminous lectins
on the growth of Rhizobium tropici CIAT899. Molecules 18:5792–5803. https://doi.org/
10.3390/molecules18055792
102. Wang LX, Wang Y, Pellock B, Walker GC (1999) Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J Bacteriol
181:6788–6796
103. Kelly SJ, Muszynski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N, Carlson RW,
Stougaard J, Ronson CW (2013) Conditional requirement for exopolysaccharide in the
Mesorhizobium-Lotus symbiosis. Mol Plant-Microbe Interact 26:319–329. https://doi.org/
10.1094/MPMI-09-12-0227-R
104. Reuhs BL, Geller DP, Kim JS, Fox JE, Kolli VS, Pueppke SG (1998) Sinorhizobium fredii and
Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific
K antigens. Appl Environ Microbiol 64:4930–4938
105. Raetz CRH, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in
gram-negative bacteria. Annu Rev Biochem 76:295–329. https://doi.org/10.1146/annurev.
biochem.76.010307.145803
106. Gore RS, Miller KJ (1993) Cyclic [beta]-1,6 -1,3 Glucans are synthesized by Bradyrhizobium
japonicum bacteroids within soybean (Glycine max) root nodules. Plant Physiol 102:191–194
107. Koronakis V, Eswaran J, Hughes C (2004) Structure and function of TolC: the bacterial exit
duct for proteins and drugs. Annu Rev Biochem 73:467–489
108. Mongiardini EJ, Ausmees N, Pérez-Giménez J, Julia Althabegoiti M, Ignacio Quelas J,
López-García SL, Lodeiro AR (2008) The rhizobial adhesion protein RapA1 is involved in
adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol Ecol 65:279–288.
https://doi.org/10.1111/j.1574-6941.2008.00467.x
109. Krishnan HB, Lorio J, Kim WS, Jiang G, Kim KY, DeBoer M, Pueppke SG (2003) Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like
surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii
USDA257. Mol Plant-Microbe Interact 16:617–625
110. Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein
secretion systems. Nat Rev Microbiol 7:312–320. https://doi.org/10.1038/nrmicro2091
111. Liu H, Zhang C, Yang J, Yu N, Wang E (2018) Hormone modulation of legume-rhizobial
symbiosis. J Integr Plant Biol 60:632–648. https://doi.org/10.1111/jipb.12653
112. Maheshwari DK (2012) Bacteria in agrobiology: plant probiotics. Springer Science & Business Media, pp 201–211. https://doi.org/10.1007/978-3-642-27515-9_11
113. Imada EL, Rolla Dos Santos AADP, de Oliveira ALM, Hungria M, Rodrigues EP (2017)
Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter
Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Res Microbiol 168:283–292.
https://doi.org/10.1016/j.resmic.2016.10.010
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
319
10.1073/pnas.1205171109
97. Vedam V, Haynes JG, Kannenberg EL, Carlson RW, Sherrier DJ (2004) A Rhizobium
leguminosarum lipopolysaccharide lipid-A mutant induces nitrogen-fixing nodules with
delayed and defective bacteroid formation. Mol Plant-Microbe Interact 17:283–291
98. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC (2008)
Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti
or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci U S A 105:704–709. https://doi.
org/10.1073/pnas.0709338105
99. Jones KM (2012) Increased production of the exopolysaccharide succinoglycan enhances
Sinorhizobium meliloti 1021 symbiosis with the host plant Medicago truncatula. J Bacteriol
194:4322–4331. https://doi.org/10.1128/JB.00751-12
100. D’Haeze W, Holsters M (2004) Surface polysaccharides enable bacteria to evade plant
immunity. Trends Microbiol 12:555–561
101. de Vasconcelos MA, Cunha CO, Arruda FVS, Carneiro VA, Bastos RM, Mercante FM, do
Nascimento KS, Cavada BS, dos Santos RP, Teixeira EH (2013) Effect of leguminous lectins
on the growth of Rhizobium tropici CIAT899. Molecules 18:5792–5803. https://doi.org/
10.3390/molecules18055792
102. Wang LX, Wang Y, Pellock B, Walker GC (1999) Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti. J Bacteriol
181:6788–6796
103. Kelly SJ, Muszynski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N, Carlson RW,
Stougaard J, Ronson CW (2013) Conditional requirement for exopolysaccharide in the
Mesorhizobium-Lotus symbiosis. Mol Plant-Microbe Interact 26:319–329. https://doi.org/
10.1094/MPMI-09-12-0227-R
104. Reuhs BL, Geller DP, Kim JS, Fox JE, Kolli VS, Pueppke SG (1998) Sinorhizobium fredii and
Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific
K antigens. Appl Environ Microbiol 64:4930–4938
105. Raetz CRH, Reynolds CM, Trent MS, Bishop RE (2007) Lipid A modification systems in
gram-negative bacteria. Annu Rev Biochem 76:295–329. https://doi.org/10.1146/annurev.
biochem.76.010307.145803
106. Gore RS, Miller KJ (1993) Cyclic [beta]-1,6 -1,3 Glucans are synthesized by Bradyrhizobium
japonicum bacteroids within soybean (Glycine max) root nodules. Plant Physiol 102:191–194
107. Koronakis V, Eswaran J, Hughes C (2004) Structure and function of TolC: the bacterial exit
duct for proteins and drugs. Annu Rev Biochem 73:467–489
108. Mongiardini EJ, Ausmees N, Pérez-Giménez J, Julia Althabegoiti M, Ignacio Quelas J,
López-García SL, Lodeiro AR (2008) The rhizobial adhesion protein RapA1 is involved in
adsorption of rhizobia to plant roots but not in nodulation. FEMS Microbiol Ecol 65:279–288.
https://doi.org/10.1111/j.1574-6941.2008.00467.x
109. Krishnan HB, Lorio J, Kim WS, Jiang G, Kim KY, DeBoer M, Pueppke SG (2003) Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like
surface appendages and exported by a type III protein secretion system in Sinorhizobium fredii
USDA257. Mol Plant-Microbe Interact 16:617–625
110. Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein
secretion systems. Nat Rev Microbiol 7:312–320. https://doi.org/10.1038/nrmicro2091
111. Liu H, Zhang C, Yang J, Yu N, Wang E (2018) Hormone modulation of legume-rhizobial
symbiosis. J Integr Plant Biol 60:632–648. https://doi.org/10.1111/jipb.12653
112. Maheshwari DK (2012) Bacteria in agrobiology: plant probiotics. Springer Science & Business Media, pp 201–211. https://doi.org/10.1007/978-3-642-27515-9_11
113. Imada EL, Rolla Dos Santos AADP, de Oliveira ALM, Hungria M, Rodrigues EP (2017)
Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter
Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Res Microbiol 168:283–292.
https://doi.org/10.1016/j.resmic.2016.10.010
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
319