62. Gomez-Sagasti MT, Marino D (2015) PGPRs and nitrogen-fixing legumes: a perfect team
for efficient Cd phytoremediation? Front Plant Sci 6:1–9. https://doi.org/10.3389/
fpls.2015.00081
63. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546. https://doi.org/10.1146/annurev.
arplant.59.032607.092839
64. Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in
the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9. https://doi.org/10.1111/
j.1574-6968.2008.01254.x
65. Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the
legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. https://doi.org/10.1146/annurevgenet-110410-132549
66. Gresshoff PM, Lohar D, Chan PK, Biswas B, Jiang Q, Reid D, Ferguson B, Stacey G (2009)
Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav
4:818–823
67. Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D,
Chaintreuil C, Prin Y, Nouwen N, Giraud E (2010) Large-scale transposon mutagenesis of
photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant-Microbe Interact
23:760–770. https://doi.org/10.1094/MPMI-23-6-0760
68. Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho K, Hashiguchi M,
Akashi R, Hirsch AM, Arima S, Suzuki A (2009) Enhanced nodulation and nitrogen fixation
in the abscisic acid low-sensitive mutant enhanced nitrogen fixation of Lotus japonicas. Plant
Physiol 151:1965–1976. https://doi.org/10.1104/pp.109.142638
69. Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume – rhizobial
mutualism. Cell Microbiol 14:334–342. https://doi.org/10.1111/j.1462-5822.2011.01736.x
70. Karunakaran R, Ramachandran VK, Seaman JC, East AK, Mouhsine B, Mauchline TH,
Prell J, Skeffington A, Poole PS (2009) Transcriptomic analysis of Rhizobium leguminosarum
biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol
191:4002–4014. https://doi.org/10.1128/JB.00165-09
71. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. https://doi.org/10.1007/s11104-0089833-8
72. Giles ED, Oldroyd GE, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to
long-term harmony in legume-microbe symbioses. Plant Physiol 137:1205–1220. https://doi.
org/10.1104/pp.104.057661
73. Kiss E, Oláh B, Kaló P, Morales M, Heckmann AB, Borbola A, Lózsa A, Kontár K,
Middleton P, Downie JA, Oldroyd GE, Endre G (2009) LIN, a novel type of U-box/WD40
protein, controls early infection by rhizobia in legumes. Plant Physiol 151:1239–1249. https://
doi.org/10.1104/pp.109.143933
74. Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts.
Nat Rev Microbiol 16:291–303. https://doi.org/10.1038/nrmicro.2017.171
75. Reddy P, Rendón-Anaya M, Soto del Río M, Khandual S (2007) Flavonoids as signaling
molecules and regulators of root nodule development. Dyn Soil Dyn Plant 1:83–94
76. Wheatley RM, Poole PS (2018) Mechanisms of bacterial attachment to roots. FEMS Microbiol
Rev 42:448–461. https://doi.org/10.1093/femsre/fuy014
77. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A,
Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in
the rhizosphere microbiome of plants. ISME J7:2248–2258. https://doi.org/10.1038/
ismej.2013.119
78. Van Egeraat AWSM (1975) The possible role of homoserine in the development of Rhizobium
leguminosarumin the rhizosphere of pea seedlings. Plant Soil 42:381–386. https://doi.org/
10.1007/BF00010013
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
317
for efficient Cd phytoremediation? Front Plant Sci 6:1–9. https://doi.org/10.3389/
fpls.2015.00081
63. Oldroyd GED, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59:519–546. https://doi.org/10.1146/annurev.
arplant.59.032607.092839
64. Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in
the rhizobium-legume symbiosis. FEMS Microbiol Lett 285:1–9. https://doi.org/10.1111/
j.1574-6968.2008.01254.x
65. Oldroyd GED, Murray JD, Poole PS, Downie JA (2011) The rules of engagement in the
legume-rhizobial symbiosis. Annu Rev Genet 45:119–144. https://doi.org/10.1146/annurevgenet-110410-132549
66. Gresshoff PM, Lohar D, Chan PK, Biswas B, Jiang Q, Reid D, Ferguson B, Stacey G (2009)
Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav
4:818–823
67. Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F, Boursot M, Vallenet D,
Chaintreuil C, Prin Y, Nouwen N, Giraud E (2010) Large-scale transposon mutagenesis of
photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for nod-independent symbiosis with Aeschynomene indica. Mol Plant-Microbe Interact
23:760–770. https://doi.org/10.1094/MPMI-23-6-0760
68. Tominaga A, Nagata M, Futsuki K, Abe H, Uchiumi T, Abe M, Kucho K, Hashiguchi M,
Akashi R, Hirsch AM, Arima S, Suzuki A (2009) Enhanced nodulation and nitrogen fixation
in the abscisic acid low-sensitive mutant enhanced nitrogen fixation of Lotus japonicas. Plant
Physiol 151:1965–1976. https://doi.org/10.1104/pp.109.142638
69. Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume – rhizobial
mutualism. Cell Microbiol 14:334–342. https://doi.org/10.1111/j.1462-5822.2011.01736.x
70. Karunakaran R, Ramachandran VK, Seaman JC, East AK, Mouhsine B, Mauchline TH,
Prell J, Skeffington A, Poole PS (2009) Transcriptomic analysis of Rhizobium leguminosarum
biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol
191:4002–4014. https://doi.org/10.1128/JB.00165-09
71. Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. https://doi.org/10.1007/s11104-0089833-8
72. Giles ED, Oldroyd GE, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to
long-term harmony in legume-microbe symbioses. Plant Physiol 137:1205–1220. https://doi.
org/10.1104/pp.104.057661
73. Kiss E, Oláh B, Kaló P, Morales M, Heckmann AB, Borbola A, Lózsa A, Kontár K,
Middleton P, Downie JA, Oldroyd GE, Endre G (2009) LIN, a novel type of U-box/WD40
protein, controls early infection by rhizobia in legumes. Plant Physiol 151:1239–1249. https://
doi.org/10.1104/pp.109.143933
74. Poole P, Ramachandran V, Terpolilli J (2018) Rhizobia: from saprophytes to endosymbionts.
Nat Rev Microbiol 16:291–303. https://doi.org/10.1038/nrmicro.2017.171
75. Reddy P, Rendón-Anaya M, Soto del Río M, Khandual S (2007) Flavonoids as signaling
molecules and regulators of root nodule development. Dyn Soil Dyn Plant 1:83–94
76. Wheatley RM, Poole PS (2018) Mechanisms of bacterial attachment to roots. FEMS Microbiol
Rev 42:448–461. https://doi.org/10.1093/femsre/fuy014
77. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, Osbourn A,
Grant A, Poole PS (2013) Comparative metatranscriptomics reveals kingdom level changes in
the rhizosphere microbiome of plants. ISME J7:2248–2258. https://doi.org/10.1038/
ismej.2013.119
78. Van Egeraat AWSM (1975) The possible role of homoserine in the development of Rhizobium
leguminosarumin the rhizosphere of pea seedlings. Plant Soil 42:381–386. https://doi.org/
10.1007/BF00010013
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
317