26. Foo E, McAdam EL, Weller JL, Reid JB (2016) Interactions between ethylene, gibberellins,
and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea. J Exp
Bot 67:2413–2424. https://doi.org/10.1093/jxb/erw047
27. Kohlen W, Ng JLP, Deinum EE, Mathesius U (2018) Auxin transport, metabolism, and
signalling during nodule initiation: indeterminate and determinate nodules. J Exp Bot
69:229–244. https://doi.org/10.1093/jxb/erx308
28. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Factories 5:1–19.
https://doi.org/10.1186/1475-2859-5-7
29. Rinaudi LV, Gonzalez JE (2009) The low-molecular-weight fraction of exopolysaccharide II
from Sinorhizobium meliloti is a crucial determinant of biofilm formation. J Bacteriol
191:7216–7224. https://doi.org/10.1128/JB.01063-09
30. Carlson RW, Forsberg LS, Kannenberg EL (2010) Lipopolysaccharides in rhizobium-legume
symbioses. In: Wang X, Quinn PJ (eds) Endotoxins: structure, function and recognition.
Springer, Dordrecht, pp 339–386
31. Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A (2017) Synthesis of rhizobial
exopolysaccharides and their importance for symbiosis with legume plants. Genes (Basel)
8:10–12. https://doi.org/10.3390/genes8120360
32. Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive
oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New
Phytol 173:39–49. https://doi.org/10.1111/j.1469-8137.2006.01901.x
33. Glian’ko AK, Akimova GP, Makarova LE, Sokolova MG, Vasil’eva GG (2007) Oxidation
processes at initial stages of interaction of root nodule bacteria (Rhizobium leguminosarum)
and pea (Pisum sativum L.): a review. Prikl Biokhim Mikrobiol 43:576–582
34. Glian’ko AK, Vasil’eva GG (2010) Reactive oxygen and nitrogen species in legume-rhizobial
symbiosis: a review. Prikl Biokhim Mikrobiol 46:21–28
35. Cardenas L, Martinez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular
ROS changes in living root hair cells responding to Nod factors (NFs). Plant J 56:802–813.
https://doi.org/10.1111/j.1365-313X.2008.03644.x
36. Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume-rhizobium
symbiosis. Mol Plant 2:370–377. https://doi.org/10.1093/mp/ssn090
37. Munoz V, Ibanez F, Tordable M, Megias M, Fabra A (2015) Role of reactive oxygen species
generation and Nod factors during the early symbiotic interaction between bradyrhizobia and
peanut, a legume infected by crack entry. J Appl Microbiol 118:182–192. https://doi.org/
10.1111/jam.12669
38. Santos R, Hérouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol 38:750–759. https://doi.org/
10.1046/j.1365-2958.2000.02178.x
39. Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Update on
plant antioxidants biochemistry and molecular biology of antioxidants in the rhizobia-legume
symbiosis 1, 2. Society 133:499–509. https://doi.org/10.1104/pp.103.025619.for
40. Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N,
Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in
legume root nodules. J Exp Bot 66:2979–2990. https://doi.org/10.1093/jxb/erv066
41. Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D,
Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key
players in the legume-Rhizobium symbiosis. J Exp Bot 57:1769–1776. https://doi.org/
10.1093/jxb/erj184
42. Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000)
Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381
43. Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I, Genre A, Huguet S, Frendo P,
Puppo A, Pauly N (2013) Hydrogen peroxide-regulated genes in the Medicago truncatulaSinorhizobium meliloti symbiosis. New Phytol 198:179–189. https://doi.org/10.1111/
nph.12120
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
315
and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea. J Exp
Bot 67:2413–2424. https://doi.org/10.1093/jxb/erw047
27. Kohlen W, Ng JLP, Deinum EE, Mathesius U (2018) Auxin transport, metabolism, and
signalling during nodule initiation: indeterminate and determinate nodules. J Exp Bot
69:229–244. https://doi.org/10.1093/jxb/erx308
28. Skorupska A, Janczarek M, Marczak M, Mazur A, Król J (2006) Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Factories 5:1–19.
https://doi.org/10.1186/1475-2859-5-7
29. Rinaudi LV, Gonzalez JE (2009) The low-molecular-weight fraction of exopolysaccharide II
from Sinorhizobium meliloti is a crucial determinant of biofilm formation. J Bacteriol
191:7216–7224. https://doi.org/10.1128/JB.01063-09
30. Carlson RW, Forsberg LS, Kannenberg EL (2010) Lipopolysaccharides in rhizobium-legume
symbioses. In: Wang X, Quinn PJ (eds) Endotoxins: structure, function and recognition.
Springer, Dordrecht, pp 339–386
31. Marczak M, Mazur A, Koper P, Żebracki K, Skorupska A (2017) Synthesis of rhizobial
exopolysaccharides and their importance for symbiosis with legume plants. Genes (Basel)
8:10–12. https://doi.org/10.3390/genes8120360
32. Lohar DP, Haridas S, Gantt JS, VandenBosch KA (2007) A transient decrease in reactive
oxygen species in roots leads to root hair deformation in the legume-rhizobia symbiosis. New
Phytol 173:39–49. https://doi.org/10.1111/j.1469-8137.2006.01901.x
33. Glian’ko AK, Akimova GP, Makarova LE, Sokolova MG, Vasil’eva GG (2007) Oxidation
processes at initial stages of interaction of root nodule bacteria (Rhizobium leguminosarum)
and pea (Pisum sativum L.): a review. Prikl Biokhim Mikrobiol 43:576–582
34. Glian’ko AK, Vasil’eva GG (2010) Reactive oxygen and nitrogen species in legume-rhizobial
symbiosis: a review. Prikl Biokhim Mikrobiol 46:21–28
35. Cardenas L, Martinez A, Sanchez F, Quinto C (2008) Fast, transient and specific intracellular
ROS changes in living root hair cells responding to Nod factors (NFs). Plant J 56:802–813.
https://doi.org/10.1111/j.1365-313X.2008.03644.x
36. Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume-rhizobium
symbiosis. Mol Plant 2:370–377. https://doi.org/10.1093/mp/ssn090
37. Munoz V, Ibanez F, Tordable M, Megias M, Fabra A (2015) Role of reactive oxygen species
generation and Nod factors during the early symbiotic interaction between bradyrhizobia and
peanut, a legume infected by crack entry. J Appl Microbiol 118:182–192. https://doi.org/
10.1111/jam.12669
38. Santos R, Hérouart D, Puppo A, Touati D (2000) Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Mol Microbiol 38:750–759. https://doi.org/
10.1046/j.1365-2958.2000.02178.x
39. Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Update on
plant antioxidants biochemistry and molecular biology of antioxidants in the rhizobia-legume
symbiosis 1, 2. Society 133:499–509. https://doi.org/10.1104/pp.103.025619.for
40. Matamoros MA, Saiz A, Peñuelas M, Bustos-Sanmamed P, Mulet JM, Barja MV, Rouhier N,
Moore M, James EK, Dietz KJ, Becana M (2015) Function of glutathione peroxidases in
legume root nodules. J Exp Bot 66:2979–2990. https://doi.org/10.1093/jxb/erv066
41. Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Hérouart D,
Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key
players in the legume-Rhizobium symbiosis. J Exp Bot 57:1769–1776. https://doi.org/
10.1093/jxb/erj184
42. Becana M, Dalton DA, Moran JF, Iturbe-Ormaetxe I, Matamoros MA, Rubio MC (2000)
Reactive oxygen species and antioxidants in legume nodules. Physiol Plant 109:372–381
43. Andrio E, Marino D, Marmeys A, de Segonzac MD, Damiani I, Genre A, Huguet S, Frendo P,
Puppo A, Pauly N (2013) Hydrogen peroxide-regulated genes in the Medicago truncatulaSinorhizobium meliloti symbiosis. New Phytol 198:179–189. https://doi.org/10.1111/
nph.12120
13 Legume-Rhizobium Symbiosis: Secondary Metabolites, Free Radical Processes. . .
315