Abstract
The effect of the nodule-endophytic Agrobacterium strain 10C2 on nodulation, plant growth and nodule functioning of Phaseolus vulgaris was investigated using two rhizobial strains differing in their sensitivity to the in vitro antibiosis of the Agrobacterium strain. In the case of the sensitive strain, Agrobacterium sp. 10C2 induced a significant decrease in the proportion of pink nodules, probably by an antibiosis effect leading to the reduction in the number of bacteroids and thereby a decrease in total soluble proteins, leghaemoglobin content, photosynthesis and nitrogen fixation. In this case, the Agrobacterium strain behaved like a plant pathogen and the nodule reacted by increasing guaiacol peroxidase (POX) activity, which assures some physiological processes linked to pathogen control. By contrast, in the case of the resistant strain, the proportion of pink nodules increased, and thereby total soluble proteins, leghaemoglobin content, biomass production and nitrogen fixation were enhanced. The Agrobacterium strain is regarded in this case as a plant growth–promoting rhizobacterium and the POX-pathogen reaction was not observed. There was even a decrease in superoxide dismutase activity. The results suggested also that the Agrobacterium strain may be also involved in retarding nodule senescence in the case of the resistant strain.
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Almagro L, Gomez Ros LV, Belchi-Navarro S, Bru R, Ros Barcelo A, Pedreno MA (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390
Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257
Antolin MC, Fiasconaro ML, Sanchez-Diaz M (2010) Relation between photosynthetic capacity, nitrogen assimilation and nodule metabolism in alfalfa (Medicago sativa) grown with sewage sludge. J Hazard Mater 182:210–216
Aver’yanov AA, Lapikova VP, Djawakhia VG (1993) Active oxygen mediates heat-induced resistance of rice plant to blast disease. Plant Sci 92:27–34
Beauchamp C, Fridovich I (1971) Superoxide dismutase, improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
Ben Salah I, Albacete A, Martínez Andújar C, Haouala R, Labidi N, Zribi F, Martinez V, Pérez-Alfocea F, Abdelly C (2009) Response of nitrogen fixation in relation to nodule carbohydrate metabolism in Medicago ciliaris lines subjected to salt stress. J Plant Physiol 166:477–488
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principal of protein-dye binding. Anal Biochem 72:248–254
Chen J, Song L, Dai J, Gan N, Liu Z (2004) Effects of microcystins on the growth and the activity of superoxide dismutase and peroxidase of rape (Brassica napus L.) and rice (Oryza sativa L.). Toxicon 43:393–400
De Gara L, De Pinto MC, Tommasi F (2003) The antioxidant system vis-à-vis reactive oxygen species during plant-pathogen interaction. Plant Physiol Biochem 41:863–870
De Lajudie P, Willems A, Nick G, Mohamed SH, Torck U, Coopman R, Filali-Maltouf A, Kersters K, Dreyfus B, Lindstrom K, Gillis M (1999) Agrobacterium bv. 1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22:119–132
Deng ZS, Zhao LF, Kong ZY, Yang WQ, Lindström K, Wang ET, Wei GH (2011) Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol Ecol 76:463–475
Djébali N, Mhadhbi H, Jacquet C, Huguet T, Aouani ME (2007) Involvement of hydrogen peroxide, peroxidase and superoxide dismutase in response of Medicago truncatula lines differing in susceptibility to Phoma medicaginis infection. J Phytopathol 155:633–640
Djébali N, Mhadhbi H, Lafitte C, Dumas B, Esquerré-Tugayé MT, Aouani ME, Jacquet C (2011) Hydrogen peroxide scavenging mechanisms are components of Medicago truncatula partial resistance to Aphanomyces euteiches. Eur J Plant Pathol 131:559–571
Hameed S, Yasmina S, Malik KA, Zafar Y, Hafeez FY (2004) Rhizobium, Bradyrhizobium and Agrobacterium strains isolated from cultivated legumes. Biol Fertil Soil 39:179–185
Hardy RWF, Holston RD, Jackson EK, Burns RC (1968) The acetylene-ethylene assay for nitrogen fixation: laboratory and field evaluation. Plant Physiol 43:1185–1208
Harris D, Pacovsky RS, Paul EA (1985) Carbon economy of soybean Rhizobium-Glomus associations. New Phytol 101:427–440
Hernandez-Jimenez MJ, Lucas MM, De Felipe MR (2002) Antioxidant defence and damage in senescing lupin nodules. Plant Physiol Biochem 40:645–657
Iwano M, Che FS, Goto K, Tanaka N, Takayama S, Isogai A (2002) Electron microscopic analysis of the H2O2 accumulation preceding hypersensitive cell death induced by an incompatible strain of Pseudomonas avenae in cultured rice cells. Mol Plant Pathol 3:1–8
Kan FL, Chen ZY, Wang ET, Tian CF, Sui XH, Chen WX (2007) Characterization of symbiotic and endophytic bacteria isolated from root nodules of herbaceous legumes grown in Qinghai–Tibet plateau and in other zones of China. Arch Microbiol 188:103–115
Kaschuk G, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2010) Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max [L.] Merrill) dependent on N2 fixation or nitrate supply. Plant Biol 12:60–69
Kaschuk G, Yin X, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2012) Photosynthetic adaptation of soybean due to varying effectiveness of N2 fixation by two distinct Bradyrhizobium japonicum strains. Environ Exp Bot 12:60–69
Lei X, Wang ET, Chen WF, Sui XH, Chen WX (2008) Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate regions of China. Arch Microbiol 190:657–671
Leon J, Lawton MA, Raskin I (1995) Hydrogen Peroxide stimulates salicylic acid biosynthesis in tobacco. Plant Physiol 108:1673–1678
Liu J, Wang ET, Ren DW, Chen WX (2010) Mixture of endophytic Agrobacterium and Sinorhizobium meliloti strains could induce non specific nodulation on some woody legumes. Arch Microbiol 192:229–234
Matamoros MA, Dalton DA, Ramos J, Clemente MR, Rubio MC, Becana M (2003) Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 133:449–509
Mhadhbi H, Jebara M, Limam F, Aouani ME (2004) Rhizobial strain involvement in plant growth, nodule protein composition and antioxidant enzyme activities of chickpea-rhizobia symbioses: modulation by salt stress. Plant Physiol Biochem 42:717–722
Mhadhbi H, Jebara M, Limam F, Huguet T, Aouani ME (2005) Interaction between Medicago truncatula lines and Sinorhizobium meliloti strains for symbiotic efficiency and nodule antioxidant activities. Physiol Plant 124:4–11
Mhadhbi H, Jebara M, Zitoun A, Limam F, Aouani ME (2008) Symbiotic effectiveness and response to mannitol-mediated osmotic stress of various chickpea-rhizobia associations. World J Microbiol Biotechnol 24:1027–1035
Mhadhbi H, Djébali N, Chihaoui SA, Jebara M, Mhamdi R (2011) Nodule senescence in Medicago truncatula-Sinorhizobium symbiosis under abiotic constraints: biochemical and structural processes involved in maintaining nitrogen-fixing capacity. J Plant Growth Regul 4:480–489
Mhamdi R, Jebara M, Aouani ME, Ghrir R, Mars M (1999) Genotypic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of Phaseolus vulgaris L. grown in Tunisian soils. Biol Fertil Soil 28:313–320
Mhamdi R, Laguerre G, Aouani ME, Mars M, Amarger N (2002) Different species and symbiotic genotypes of field rhizobia can nodulate Phaseolus vulgaris in Tunisian soils. FEMS Microbiol Ecol 41:77–84
Mhamdi R, Mrabet M, Laguerre G, Tiwari R, Aouani ME (2005) Colonization of Phaseolus vulgaris nodules by Agrobacterium-like strains. Can J Microbiol 51:105–111
Mnasri B, Tajini F, Trabelsi M, Aouani ME, Mhamdi R (2007a) Rhizobium gallicum as an efficient symbiont for bean cultivation. Agron Sust Dev 27:331–336
Mnasri B, Aouani ME, Mhamdi R (2007b) Nodulation and growth of common bean (Phaseolus vulgaris) under water deficiency. Soil Biol Biochem 39:1744–1750
Mrabet M, Mhamdi R, Tajini F, Tiwari R, Trabelsi M, Aouani ME (2005) Competitiveness and symbiotic effectiveness of a R. gallicum strain isolated from root nodules of Phaseolus vulgaris. Eur J Agron 22:209–216
Mrabet M, Mnasri B, Romdhane SB, Laguerre G, Aouani ME, Mhamdi R (2006) Agrobacterium strains isolated from root nodules of common bean specifically reduce nodulation by Rhizobium gallicum. FEMS Microbiol Ecol 56:304–309
Munns R (2005) Gene and salt tolerance: bringing them together. New Phytol 165:645–663
Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly non culturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63:383–400
Muresu R, Maddau G, Delogu G, Cappuccinelli P, Squartini A (2010) Bacteria colonizing root nodules of wild legumes exhibit virulence-associated properties of mammalian pathogens. Antonie Van Leeuwenhoek 97:143–153
Murugesan S, Manoharan C, Vijayakumar R, Panneerselvam A (2010) Isolation and characterization of Agrobacterium rhizogenes from the root nodules of some leguminous plants. Intl J Microbiol Res 1:92–96
Pfeiffer NE, Torres CM, Wagner FW (1983) Proteolytic activities in soybean root nodules. Activity in host cell cytosol and bacteroids throughout physiological development and senescence. Plant Physiol 71:797–802
Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819
Saïdi S, Mnasri B, Mhamdi R (2011) Diversity of nodule-endophytic agrobacteria-like strains associated with different grain legumes in Tunisia. Syst Appl Microbiol 34:524–530
Salem S, Saidi S, Chihaoui SA, Mhamdi R (2012) Inoculation of Phaseolus vulgaris, Medicago laciniata and Medicago polymorpha with Agrobacterium sp. strain 10C2 may enhance nodulation and shoot dry weight but does not affect host range specificity. Ann Microbiol. doi:10.1007/s13213-012-0439-2
Scheublin TR, Ridgway KP, Young JP, van der Heijden MG (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Appl Environ Microbiol 70:6240–6246
Sheokand S, Swaraj K (1996) Natural and dark-induced nodule senescence in chickpea: nodule functioning and H2O2 scavenging enzymes. Biol Plant 38:545–554
Shiffmann J, Lobel R (1970) Haemoglobin determination and its value as an early indication of peanut Rhizobium efficiency. Plant Soil 33:501–512
Singh MP, Singh DK, Rai M (2007) Assessment of growth, physiological and biochemical parameters and activities of antioxidative enzymes in salinity tolerant and sensitive basmati rice varieties. J Agron Crop Sci 193:398–412
Skot L, Hirsch PR, Witty J (1986) Genetic factors in Rhizobium affecting the symbiotic carbon costs of N2 fixation and host plant biomass production. J Appl Bacteriol 62:146–239
Tiwary BN, Prasad B, Ghosh A, Kumar S, Jain RK (2007) Characterization of two novel biovar of Agrobacterium tumefaciens isolated from root nodules of Vicia faba. Curr Microbiol 55:328–333
Tokala RK, Strap JL, Jung CM, Crawford DL, Salove MH, Deobald A, Bailley JF, Morra MJ (2002) Novel plant-microbe rhizosphere interaction involving Streptomyces lydicus WYEC108 and the pea plant (Pisum sativum). Appl Environ Microbiol 68:2161–2171
Torrecillas A, Leon A, Del Amor F, Martinez-Mompean MC (1984) Determinacion rapida de clorofila en discos foliares de limonero. Fruits 39:617–622
Vadez V, Rodier F, Payre H, Drevon JJ (1996) Nodule permeability and nitrogenase-linked respiration in bean genotypes varying in the tolerance to P deficiency. Plant Physiol Biochem 35:671–678
Valverde A, Velazquez E, Gutierez C, Cervantes E, Ventosa A, Igual JM (2003) Herbaspirillum lusitanum sp. nov., a novel nitrogen-fixing bacterium associated with root nodules of Phaseolus vulgaris. Int J Syst Evol Microbiol 53:1979–1983
Van de Velde W, Guerre JCP, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141:711–767
Vincent JM (1970) A manual for the practical study of root-nodule bacteria. In: IBP Handbook vol 15. Blackwell Scientific Publications, Oxford, pp 164
Wang LL, Wang ET, Liu J, Li Y, Chen WX (2006) Endophytic occupation of root nodules and root of Melilotus dentatus by Agrobacterium tumefaciens. Microb Ecol 52:436–443
Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639
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Authors are grateful to the technical assistance of the Laboratory of Extremophile Plants (Centre of Biotechnology of Borj-Cédria, Tunisia) for stomatal conductance and net photosynthesis.
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Communicated by Ursula Priefer.
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Chihaoui, SA., Mhadhbi, H. & Mhamdi, R. The antibiosis of nodule-endophytic agrobacteria and its potential effect on nodule functioning of Phaseolus vulgaris . Arch Microbiol 194, 1013–1021 (2012). https://doi.org/10.1007/s00203-012-0837-7
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DOI: https://doi.org/10.1007/s00203-012-0837-7