Abstract
Polyamines (PAs) are ubiquitous low molecular weight, molecules found in all living cells with participation in a variety of processes. The establishment of symbiotic interactions between soil nitrogen fixing bacteria (rhizobia) and leguminous plants, as well as the formation of the root nodules where the rhizobia are hosted, depends on the production of PAs by both partners. In the bacteria, PAs provide certain traits that facilitate the recognition between the symbionts, while in the plant, PAs participate in the production of signaling molecules like hydrogen peroxide (H2O2) and nitric oxide (NO), detected during the initial stages of the symbiosis. Once the symbiosis is established, the high amount and variety of PAs in the root nodules together to their participation in the metabolic reactions supporting nitrogen fixation, suggest their involvement in the nodule functioning. In addition, PAs are key players in the response to abiotic stresses contributing to the adaptation of the symbiosis to salinity, specially, by an increment in the production of PAs in the bacteroids and their interactions with other anti-stress plant hormones. Considering the importance of biological nitrogen fixation in soil fertility and agriculture productivity in a context of climate change, in this review we describe the participation of PAs to the rhizobia-legume interaction and the nitrogen fixation process, as well as its involvement in the response to salinity in the symbiosis.
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References
Alcázar R, Marco F, Cuevas JC et al (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3
Alcázar R, Altabella T, Marco F et al (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249. https://doi.org/10.1007/s00425-010-1130-0
Andrio E, Marino D, Marmeys A et al (2013) Hydrogen peroxide-regulated genes in the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 198:179–189. https://doi.org/10.1111/nph.12120
Angelini R, Cona A, Federico R et al (2010) Plant amine oxidases “on the move”: an update. Plant Physiol Biochem 48:560–564. https://doi.org/10.1016/j.plaphy.2010.02.001
Aranjuelo I, Arrese-Igor C, Molero G (2014) Nodule performance within a changing environmental context. J Plant Physiol 171:1076–1090. https://doi.org/10.1016/j.jplph.2014.04.002
Bachrach U (2010) The early history of polyamine research. Plant Physiol Biochem 48:490–495. https://doi.org/10.1016/j.plaphy.2010.02.003
Becerra-Rivera VA, Dunn MF (2019) Polyamine biosynthesis and biological roles in rhizobia. FEMS Microbiol Lett. https://doi.org/10.1093/femsle/fnz084
Becerra-Rivera VA, Bergström E, Thomas-Oates J, Dunn MF (2018) Polyamines are required for normal growth in Sinorhizobium meliloti. Microbiol UK 164:600–613. https://doi.org/10.1099/mic.0.000615
Becerra-Rivera VA, Arteaga A, Leija A et al (2020) Polyamines produced by Sinorhizobium meliloti Rm8530 contribute to symbiotically relevant phenotypes ex planta and to nodulation efficiency on alfalfa. Microbiol Read Engl 166:278–287. https://doi.org/10.1099/mic.0.000886
Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plant. Annu Rev Cell Dev Biol 16:1–18. https://doi.org/10.1146/annurev.cellbio.16.1.1
Borucki W, Sujkowska M (2008) The effects of sodium chloride-salinity upon growth, nodulation, and root nodule structure of pea (Pisum sativum L.) plants. Acta Physiol Plant 30:293–301. https://doi.org/10.1007/s11738-007-0120-8
Boscari A, del Giudice J, Ferrarini A et al (2013a) Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with sinorhizobiummeliloti: Which role for nitric oxide? Plant Physiol 161:425–439. https://doi.org/10.1104/pp.112.208538
Boscari A, Meilhoc E, Castella C et al (2013b) Which role for nitric oxide in symbiotic N2-fixing nodules: toxic by-product or useful signaling/metabolic intermediate? Front Plant Sci. https://doi.org/10.3389/fpls.2013.00384
Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125
Braeken K, Daniels R, Vos K et al (2008) Genetic determinants of swarming in Rhizobium etli. Microb Ecol 55:54–64. https://doi.org/10.1007/s00248-007-9250-1
Bunsupa S, Katayama K, Ikeura E et al (2012) Lysine decarboxylase catalyzes the first step of quinolizidine alkaloid biosynthesis and coevolved with alkaloid production in leguminosae. Plant Cell 24:1202. https://doi.org/10.1105/tpc.112.095885
Cam Y, Pierre O, Boncompagni E et al (2012) Nitric oxide (NO): a key player in the senescence of Medicago truncatula root nodules. New Phytol 196:548–560. https://doi.org/10.1111/j.1469-8137.2012.04282.x
Chatterjee S, Choudhuri MM, Ghosh B (1983) Changes in polyamine contents during root and nodule growth of Phaseolus mungo. Phytochemistry 22(7):1553–1556
Chen D, Shao Q, Yin L et al (2019) Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2018.01945
Choudhary SP, Oral HV, Bhardwaj R et al (2012) Interaction of brassinosteroids and polyamines enhances copper stress tolerance in Raphanus sativus. J Exp Bot 63:5659–5675. https://doi.org/10.1093/jxb/ers219
Cona A, Rea G, Angelini R et al (2006) Functions of amine oxidases in plant development and defence. Trends Plant Sci 11:80–88. https://doi.org/10.1016/j.tplants.2005.12.009
Damiani I, Pauly N, Puppo A et al (2016) Reactive oxygen species and nitric oxide control early steps of the legume—Rhizobium symbiotic interaction. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00454
del Giudice J, Cam Y, Damiani I et al (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405–417. https://doi.org/10.1111/j.1469-8137.2011.03693.x
Del Pilar CM, Ligero F, Lluch C (1999) Effects of NaCl on growth and nitrogen fixation and assimilation of inoculated and KNO3 fertilized Vicia faba L. and Pisum sativum L. plants. Plant Sci 140:127–136. https://doi.org/10.1016/S0168-9452(98)00201-5
Diao Q, Song Y, Shi D, Qi H (2017) Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum mill) seedlings. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00203
Dunn M (2017) Rhizobial amino acid metabolism: polyamine biosynthesis and functions. In: The handbook of microbial metabolism of amino acids, JPF D’Mello. CABI International, pp 352–370.
Efrose RC, Flemetakis E, Sfichi L et al (2008) Characterization of spermidine and spermine synthases in Lotus japonicus: induction and spatial organization of polyamine biosynthesis in nitrogen fixing nodules. Planta 228:37–49. https://doi.org/10.1007/s00425-008-0717-1
Erisman JW, Galloway J, Seitzinger S et al (2011) Reactive nitrogen in the environment and its effect on climate change. Carbon Nitrogen Cycles 3:281–290. https://doi.org/10.1016/j.cosust.2011.08.012
Fitzgerald JS (1964) Alkaloids of the australian leguminosae. Ii. The occurrence of sparteine in templetonia egena. Aust J Chem 17:159–159. https://doi.org/10.1071/CH9640159
Flores-Tinoco CE, Tschan F, Fuhrer T et al (2020) Co-catabolism of arginine and succinate drives symbiotic nitrogen fixation. Mol Syst Biol 16:9419. https://doi.org/10.15252/msb.20199419
Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319. https://doi.org/10.1093/jxb/erh003
Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875. https://doi.org/10.1105/tpc.105.033589
Fujihara S (2009) Biogenic amines in rhizobia and legume root nodules. Microbes Environ 24:1–13. https://doi.org/10.1264/jsme2.ME08557
Fujihara S, Harada Y (1989) Fast-growing root nodule bacteria produce a novel polyamine, aminobutylhomospermidine. Biochem Biophys Res Commun 165:659–666. https://doi.org/10.1016/S0006-291X(89)80016-6
Fujihara S, Yoneyama T (1999) Polyamine metabolism of root nodule bacteria. In: Recent research developments in microbiology, SG Pandalai. Research Signpost, Trivandrum, pp 55–80
Fujihara S, Nakashima T, Kurogochi Y, Yamaguchi M (1986) Distribution and metabolism of Sym-homospermidine and canavalmine in the sword bean Canavalia-gladiata cv shironata. Plant Physiol 82:795–800
Fujihara S, Abe H, Yoneyama T (1995) A new polyamine 4-aminobutylcadaverine. Occurrence and its biosynthesis in root nodules of adzuki ben plant Vigna angularis. J Biol Chem 270:9932–9938. https://doi.org/10.1074/jbc.270.17.9932
Fujihara S, Terakado J, Nishibori N (2006) Accumulation of an aromatic amine, β-phenethylamine, in root nodules of adzuki bean Vigna angularis. Plant Soil 280:229–237. https://doi.org/10.1007/s11104-005-3096-4
Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110:197–207. https://doi.org/10.1111/j.1438-8677.1997.tb00629.x
Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45. https://doi.org/10.1007/s00726-007-0501-8
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168. https://doi.org/10.1016/j.tplants.2010.11.007
Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036. https://doi.org/10.1007/s11738-013-1239-4
Gupta K, Sengupta A, Chakraborty M, Gupta B (2016) Hydrogen peroxide and polyamines act as double edged swords in plant abiotic stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01343
Hamana K, Matsuzaki S (1992) Polyamines as a chemotaxonomic marker in bacterial systematics. Crit Rev Microbiol 18:261–283. https://doi.org/10.3109/10408419209113518
Hamana K, Minamisawa K, Matsuzaki S (1990) Polyamines in rhizobium, bradyrhizobium, azorhizobium and argobacterium. FEMS Microbiol Lett 71:71–76. https://doi.org/10.1016/0378-1097(90)90034-N
Handa AK, Fatima T, Mattoo AK (2018) Polyamines: bio-molecules with diverse functions in plant and human health and disease. Front Chem. https://doi.org/10.3389/fchem.2018.00010
Hanfrey CC, Pearson BM, Hazeldine S et al (2011) Alternative spermidine biosynthetic route is critical for growth of Campylobacter jejuni and is the dominant polyamine pathway in human gut microbiota. J Biol Chem 286:43301–43312. https://doi.org/10.1074/jbc.M111.307835
Herbst EJ, Snell EE (1949) Putrescine and related compounds as growth factors for Hemophilus parainfluenzae 7991. J Biol Chem 181:47–54
Hidalgo-Castellanos J, Duque AS, Burgueño A et al (2019a) Overexpression of the arginine decarboxylase gene promotes the symbiotic interaction Medicago truncatula-Sinorhizobium meliloti and induces the accumulation of proline and spermine in nodules under salt stress conditions. J Plant Physiol 241:153034. https://doi.org/10.1016/j.jplph.2019.153034
Hidalgo-Castellanos J, Marín-Peña A, Jiménez-Jiménez S et al (2019b) Polyamines oxidation is required in the symbiotic interaction Medicago truncatula–Sinorhizobium meliloti but does not participate in the regulation of polyamines level under salinity. Plant Growth Regul 88:297–307. https://doi.org/10.1007/s10725-019-00508-z
Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311. https://doi.org/10.1016/j.biotechadv.2011.01.003
Jamet A, Mandon K, Puppo A, Hérouart D (2007) H2O2 is required for optimal establishment of the Medicago sativa/Sinorhizobium meliloti symbiosis. J Bacteriol 189:8741–8745. https://doi.org/10.1128/JB.01130-07
Jancewicz AL, Gibbs NM, Masson PH (2016) Cadaverine’s Functional Role in Plant Development and Environmental Response. Front Plant Sci 7:870. https://doi.org/10.3389/fpls.2016.00870
Jensen ES, Peoples MB, Boddey RM et al (2012) Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review Agron Sustain Dev 32:329–364. https://doi.org/10.1007/s13593-011-0056-7
Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821. https://doi.org/10.1016/j.plaphy.2007.08.001
Jiménez-Bremont JF, Marina M, Guerrero-González ML et al (2014) Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00095
Kato K, Kanahama K, Kanayama Y (2010) Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules. J Plant Physiol 167:238–241. https://doi.org/10.1016/j.jplph.2009.08.006
Khadri M, Tejera NA, Lluch C (2006) Alleviation of salt stress in common bean (Phaseolus vulgaris) by exogenous abscisic acid supply. J Plant Growth Regul 25:110–119. https://doi.org/10.1007/s00344-005-0004-3
Kusano T, Kim DW, Liu T, Berberich T (2015) Polyamine catabolism in plants. In: Polyamines: A Universal Molecular Nexus for Growth, Survival, and Specialized Metabolism. pp 77–88
Kuznetsov V, Shorina M, Aronova E et al (2007) NaCl- and ethylene-dependent cadaverine accumulation and its possible protective role in the adaptation of the common ice plant to salt stress. Plant Sci 172:363–370. https://doi.org/10.1016/j.plantsci.2006.09.012
Lahiri K, Chattopadhyay S, Ghosh B (2004) Correlation of endogenous free polyamine levels with root nodule senescence in different genotypes in Vigna mungo L. J Plant Physiol 161:563–571. https://doi.org/10.1078/0176-1617-01057
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Biol 48:251–275
Leach J, Keyster M, Du Plessis M, Ludidi N (2010) Nitric oxide synthase activity is required for development of functional nodules in soybean. J Plant Physiol 167:1584–1591. https://doi.org/10.1016/j.jplph.2010.06.019
Lee J, Sperandio V, Frantz DE et al (2009) An alternative polyamine biosynthetic pathway is widespread in bacteria and essential for biofilm formation in Vibrio cholerae. J Biol Chem 284:9899–9907. https://doi.org/10.1074/jbc.M900110200
Lin S-Y, Hameed A, Huang H-I, Young C-C (2020) Allorhizobium terrae sp. Nov., isolated from paddy soil, and reclassification of rhizobium oryziradicis (Zhao et al. 2017) as allorhizobium oryziradicis comb nov. Int J Syst Evol Microbiol 70:397–405. https://doi.org/10.1099/ijsem.0.003770
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
López M, Herrera-Cervera JA, Iribarne C et al (2008) Growth and nitrogen fixation in Lotus japonicus and Medicago truncatula under NaCl stress: nodule carbon metabolism. J Plant Physiol 165:641–650. https://doi.org/10.1016/j.jplph.2007.05.009
Lopez-Gomez M, Sandal N, Stougaard J, Boller T (2012) Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J Exp Bot 63:393–401. https://doi.org/10.1093/jxb/err291
Lopez-Gomez M, Palma F, Lluch C (2013) Strategies of salt tolerance in the rhizobia-legume symbiosis. In: Beneficial plant-microbial interactions. ecology and applications. CRC Press, pp 99–121
Lopez-Gomez M, Cobos-Porras L, Hidalgo-Castellanos J, Lluch C (2014a) Occurrence of polyamines in root nodules of Phaseolus vulgaris in symbiosis with Rhizobium tropici in response to salt stress. Phytochemistry 107:32–41. https://doi.org/10.1016/j.phytochem.2014.08.017
Lopez-Gomez M, Hidalgo-Castellanos J, Iribarne C, Lluch C (2014b) Proline accumulation has prevalence over polyamines in nodules of Medicago sativa in symbiosis with Sinorhizobium meliloti during the initial response to salinity. Plant Soil 374:149–159. https://doi.org/10.1007/s11104-013-1871-1
Lopez-Gomez M, Cobos-Porras L, Prell J, Lluch C (2016a) Homospermidine synthase contributes to salt tolerance in free-living Rhizobium tropici and in symbiosis with Phaseolus vulgaris. Plant Soil 404:413–425. https://doi.org/10.1007/s11104-016-2848-7
Lopez-Gomez M, Hidalgo-Castellanos J, Lluch C, Herrera-Cervera JA (2016b) 24-Epibrassinolide ameliorates salt stress effects in the symbiosis Medicago truncatula-Sinorhizobium meliloti and regulates the nodulation in cross-talk with polyamines. Plant Physiol Biochem 108:212–221. https://doi.org/10.1016/j.plaphy.2016.07.017
Lopez-Gomez M, Hidalgo-Castellanos J, Ruben Munoz-Sanchez J et al (2017) Polyamines contribute to salinity tolerance in the symbiosis Medicago truncatula-Sinorhizobium meliloti by preventing oxidative damage. Plant Physiol Biochem 116:9–17. https://doi.org/10.1016/j.plaphy.2017.04.024
Matamores MA, Dalton DA, Ramos J et al (2003) Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:499–509. https://doi.org/10.1104/pp.103.025619
Michael AJ (2016a) Polyamines in eukaryotes, bacteria, and archaea. J Biol Chem 291:14896–14903. https://doi.org/10.1074/jbc.R116.734780
Michael AJ (2016b) Biosynthesis of polyamines and polyamine-containing molecules. Biochem J 473:2315–2329. https://doi.org/10.1042/BCJ20160185
Michael AJ (2018) Polyamine function in archaea and bacteria. J Biol Chem 293:18693–18701. https://doi.org/10.1074/jbc.TM118.005670
Miller KJ, Wood JM (1996) Osmoadaptacion by rhizosphere bacteria. Annu Rev Microbiol 50:101–136. https://doi.org/10.1146/annurev.micro.50.1.101
Montiel J, Nava N, Cárdenas L et al (2012) A Phaseolus vulgaris NADPH oxidase gene is required for root infection by rhizobia. Plant Cell Physiol 53:1751–1767. https://doi.org/10.1093/pcp/pcs120
Moro GA, Graziano MN, Coussio JD (1975) Alkaloids of Prosopis nigra. Phytochemistry 14:827. https://doi.org/10.1016/0031-9422(75)83054-8
Moschou PN, Wu J, Cona A et al (2012) The polyamines and their catabolic products are significant players in the turnover of nitrogenous molecules in plants. J Exp Bot 63:5003–5015. https://doi.org/10.1093/jxb/ers202
Nagata M, Murakami E-I, Shimoda Y et al (2008) Expression of a class 1 hemoglobin gene and production of nitric oxide in response to symbiotic and pathogenic bacteria in Lotus japonicus. Mol Plant Microbe Interact 21:1175–1183. https://doi.org/10.1094/MPMI-21-9-1175
Nagata M, Hashimoto M, Murakami E-I et al (2009) A possible role of class 1 plant hemoglobin at the early stage of legume-rhizobium symbiosis. Plant Signal Behav 4:202–204. https://doi.org/10.4161/psb.4.3.7796
Nguyen S, Leija C, Kinch L et al (2015) Deoxyhypusine modification of eukaryotic translation initiation factor 5A (eIF5A) is essential for Trypanosoma brucei growth and for expression of polyprolyl-containing proteins. J Biol Chem 290:19987–19998. https://doi.org/10.1074/jbc.M115.656785
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
Oshima T (2010) Enigmas of biosyntheses of unusual polyamines in an extreme thermophile, Thermus thermophilus. Plant Physiol Biochem 48:521–526. https://doi.org/10.1016/j.plaphy.2010.03.011
Palma F, López-Gómez M, Tejera NA, Lluch C (2013) Salicylic acid improves the salinity tolerance of Medicago sativa in symbiosis with Sinorhizobium meliloti by preventing nitrogen fixation inhibition. Plant Sci 208:75–82. https://doi.org/10.1016/j.plantsci.2013.03.015
Palma F, López-Gómez M, Tejera NA, Lluch C (2014) Involvement of abscisic acid in the response of Medicago sativa plants in symbiosis with Sinorhizobium meliloti to salinity. Plant Sci 223:16–24. https://doi.org/10.1016/j.plantsci.2014.02.005
Patel CN, Wortham BW, Lines JL et al (2006) Polyamines are essential for the formation of plague biofilm. J Bacteriol 188:2355–2363. https://doi.org/10.1128/JB.188.7.2355-2363.2006
Peoples MB, Brockwell J, Herridge DF et al (2009) The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17. https://doi.org/10.1007/BF03179980
Podlešáková K, Ugena L, Spíchal L et al (2019) Phytohormones and polyamines regulate plant stress responses by altering GABA pathway. New Biotechnol 48:53–65. https://doi.org/10.1016/j.nbt.2018.07.003
Puppo A, Pauly N, Boscari A et al (2013) Hydrogen peroxide and nitric oxide: key regulators of the legume—rhizobium and mycorrhizal symbioses. Antioxid Redox Signal 18:2202–2219. https://doi.org/10.1089/ars.2012.5136
Radhakrishnan R, Lee I-J (2013) Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiol Plant 35:263–269. https://doi.org/10.1007/s11738-012-1072-1
Schuber F (1989) Influence of polyamines on membrane functions. Biochem J 260:1–10. https://doi.org/10.1042/bj2600001
Serraj R, Roy G, Drevon J (1994) Salt stress induces a decrease in the oxygen-uptake of soybean nodules and in their permeability to oxygen diffusion. Physiol Plant 91:161–168
Shaw FL, Elliott KA, Kinch LN et al (2010) Evolution and multifarious horizontal transfer of an alternative biosynthetic pathway for the alternative polyamine sym-homospermidine. J Biol Chem 285:14711–14723. https://doi.org/10.1074/jbc.M110.107219
Shevyakova NI, Musatenko LI, Stetsenko LA et al (2013) Effects of abscisic acid on the contents of polyamines and proline in common bean plants under salt stress. Russ J Plant Physiol 60:200–211. https://doi.org/10.1134/S102144371301007X
Signorelli S, Sainz M, Tabares-da Rosa S, Monza J (2020) The role of nitric oxide in nitrogen fixation by legumes. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00521
Smith TA (1977) Homospermidine in rhizobium and legume root nodules. Phytochemistry 16:278–279. https://doi.org/10.1016/S0031-9422(00)86803-X
Soussi M, Ocana A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J Exp Bot 49:1329–1337. https://doi.org/10.1093/jexbot/49.325.1329
Stagnari F, Maggio A, Galieni A, Pisante M (2017) Multiple benefits of legumes for agriculture sustainability: an overview. Chem Biol Technol Agric 4:2. https://doi.org/10.1186/s40538-016-0085-1
Streeter JG (1991) Transport and metabolism of carbon and nitrogen in legume nodules. In: Callow JA (ed) Advances in botanical research. Academic Press, New York, pp 129–187
Tabor CW, Tabor H (1985) Polyamines in microorganisms. Microbiol Rev 49:81–99
Takano A, Kakehi J-I, Takahashi T (2012) Thermospermine is not a minor polyamine in the plant kingdom. Plant Cell Physiol 53:606–616. https://doi.org/10.1093/pcp/pcs019
Terakado J, Yoneyama T, Fujihara S (2006) Shoot-applied polyamines suppress nodule formation in soybean (Glycine max). J Plant Physiol 163:497–505. https://doi.org/10.1016/j.jplph.2005.05.007
Tiburcio AF, Altabella T, Bitrián M, Alcázar R (2014) The roles of polyamines during the lifespan of plants: from development to stress. Planta 240:1–18. https://doi.org/10.1007/s00425-014-2055-9
Torrigiani P (1996) Polyamines as regulators of plant growth and development. G Bot Ital 130:15–21. https://doi.org/10.1080/11263509609439489
Tun NN, Santa-Catarina C, Begum T et al (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354. https://doi.org/10.1093/pcp/pci252
Urano K, Maruyama K, Ogata Y et al (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078. https://doi.org/10.1111/j.1365-313X.2008.03748.x
Vassileva V, Ignatov G (1999) Polyamine-induced changes in symbiotic parameters of the Galega orientalis-Rhizobium galegae nitrogen-fixing system. Plant Soil 210:83–91. https://doi.org/10.1023/A:1004636800869
Vauclare P, Bligny R, Gout E, Widmer F (2013) An overview of the metabolic differences between Bradyrhizobium japonicum 110 bacteria and differentiated bacteroids from soybean (Glycine max) root nodules: an in vitro 13C- and 31P-nuclear magnetic resonance spectroscopy study. FEMS Microbiol Lett 343:49–56. https://doi.org/10.1111/1574-6968.12124
Verma N, Tiwari S, Singh VP, Prasad SM (2020) Nitric oxide in plants: an ancient molecule with new tasks. Plant Growth Regul. https://doi.org/10.1007/s10725-019-00543-w
Wimalasekera R, Tebartz F, Scherer GFE (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603. https://doi.org/10.1016/j.plantsci.2011.04.002
Wisniewski J-P, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant Microbe Interact 13:413–420. https://doi.org/10.1094/MPMI.2000.13.4.413
Xing SG, Jun YB, Hau ZW, Liang LY (2007) Higher accumulation of γ-aminobutyric acid induced by salt stress through stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem 45:560–566. https://doi.org/10.1016/j.plaphy.2007.05.007
Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
Zheng Q, Liu J, Liu R et al (2016) Temporal and spatial distributions of sodium and polyamines regulated by brassinosteroids in enhancing tomato salt resistance. Plant Soil 400:147–164. https://doi.org/10.1007/s11104-015-2712-1
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This work has been supported by the Spanish Ministry of Science and Technology (Grant: AGL2013-42778-P). Not applicable for the rest of the sections.
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Hidalgo-Castellanos, J., Marín-Peña, A.J., Herrera-Cervera, J.A. et al. Polyamines: Key elements in the rhizobia-legume symbiosis?. Phytochem Rev 21, 127–140 (2022). https://doi.org/10.1007/s11101-021-09751-7
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DOI: https://doi.org/10.1007/s11101-021-09751-7