Endophytic Occupation of Root Nodules and Roots of Melilotus dentatus by Agrobacterium tumefaciens

Microbial Ecology - Tập 52 - Trang 436-443 - 2006
Ling Ling Wang1,2, En Tao Wang1,3, Jie Liu1,4, Ying Li1, Wen Xin Chen1
1Key Laboratory of Agro-Microbial Resource and Application, Ministry of Agriculture/College of Biological Sciences, China Agricultural University, Beijing, China
2College of Life Sciences, South China Agricultural University, Guangzhou, China
3Departamento de Microbiología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico, Mexico
4Department of Biological and Pharmaceutical Engineering, College of Chemical Engineering, Qingdao University of Science and Technology, Qingdao, China

Tóm tắt

Agrobacterium strains have been frequently isolated from the root nodules of different legumes. Various possible mechanisms have been proposed to explain the existence of these bacteria in nodules, but there is no sufficient experimental evidence to support the estimations. In this work, we proved that the Agrobacterium strain CCBAU 81181, which was originally isolated from the root nodules of Onobrychis viciaefolia, and a symbiotic strain of Sinorhizobium meliloti CCBAU 10062 could coinhabit the root nodules of Melilotus dentatus. Analyses were performed by using a fluorescence marker, reisolation of bacteria from nodules, sodium dodecyl sulfate–polyacrylamide gel electrophoresis (SDS–PAGE) of whole cellular proteins, and polymerase chain reaction amplification of symbiotic genes. The inoculation of A. tumefaciens CCBAU 81181 did not affect the growth and nodulation of plants. CCBAU 81181 and 24 other Agrobacterium strains isolated from nodules were incapable of nodulating on their original or alternative host and 22 strains of these strains were endophytes in the roots and stems of their hosts. Also, the tumor-inducing A. tumefaciens strains IAM 13129T and C58 were found capable of entering the roots of Glycyrrhiza pallidiflora, but did not cause pathogenic symptoms. With these results, we conclude that A. tumefaciens strains could be endophytic bacteria in the roots, stems, and root nodules. This finding partially explains why Agrobacterium strains were frequently isolated from the surface-sterilized nodules.

Tài liệu tham khảo

Alazard, D, Duhoux, E (1990) Development of stem nodules in a tropical forage legume Aeschynomene afraspera. J Exp Bot 41: 1199–1206 Anyango, B, Wilson, KJ, Beynon, JL, Giller KE (1995) Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils of contrasting pHs. Appl Environ Microbiol 61: 4016–4021 Bala, A, Giller, KE (2001) Symbiotic specificity of tropical tree rhizobia for host legumes. New Phytol 149: 495–507 Boogerd, FC, van Rossum, D (1997) Nodulation of groundnut by Bradyrhizobium: a simple infection process by crack entry. FEMS Microbiol Rev 21: 5–27 Chen, LS, Figueredo, A, Pedrosa, FO, Hungria, M (2000) Genetic characterization of soybean rhizobia in Paraguay. Appl Environ Microbiol 66: 5099–5103 Chen, WM, James, EK, Prescott, AR, Kierans, M, Sprent, JI (2003) Nodulation of Mimosa spp. by the β-Proteobacterium Ralstonia taiwanensis. Mol Plant–Microb Interact 16: 1051–1061 De Lajudie, P, Willems, A, Nick, G, Mohamed, TS, Torck, U, Filai-Maltouf, A, Kersters, K, Dreyfus, B, Lindström, K, Gillis, M (1999) Agrobacterium bv. 1 strains isolated from nodules of tropical legumes. Syst Appl Microbiol 22: 119–132 De Ley, J, Cattoir, H, Reynaerts, A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12: 133–142 Gao, JL, Turner, SL, Kan, FL, Wang, ET, Tan, ZY, Qiu, YH, Gu, J, Terefework, Z, Young, JP, Lindström, K, Chen, WX (2004) Mesorhizobium septentrionale sp. nov. and Mesorhizobium temperatum sp. nov., isolated from Astragalus adsurgens growing in the northern regions of China. Int J Syst Evol Microbiol 54: 2003–2012 Hallmann, J, Quadt-Hallmann, A, Mahaffee, WF, Kloepper, JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43: 895–914 Han, SZ, Wang, ET, Chen, WX (2005) Diverse bacteria isolated from root nodules of Phaseolus vulgaris and species within the genera Campylotropis and Cassia grown in China. Syst Appl Microbiol 28: 265–276 Haukka, K, Lindström, K, Young, JPW (1998) Three phylogenetic groups of nodA and nifH genes in Sinorhizobium and Mesorhizobium isolates from leguminous trees growing in Africa and Latin America. Appl Environ Microbiol 64: 419–426 Hiroyuki, S, Hiroyuki, I, Izumi, M (1995) PCR detection of Ti and Ri plasmids from phytopathogenic Agrobacterium strains. Appl Environ Microbiol 61: 828–831 Hurek, T, Wagner, B, Reihold-Hurek, B (1997) Identification of N2-fixing plant- and fungus-associated Azoarcus species by PCR-based genomic fingerprints. Appl Environ Microbiol 63: 4331–4339 Hynes, MF, McGregor, NF (1990) Two plasmids other than the nodulation plasmid are necessary for formation of nitrogen-fixing nodules by Rhizobium leguminosarum. Mol Microbiol 4: 567–574 Imshenetskii, AA, Pariiskaia, AN, Gorelova, OP (1976) The presence of Agrobacterium tumefaciens in lucerne root nodules. Mikrobiol 45: 561–563 (in Russian) Khbaya, B, Neyra, M, Normand, P, Zerhari, K, Filali-Maltouf, A (1998) Genetic diversity and phylogeny of rhizobia that nodulate Acacia spp. in Morocco assessed by analysis of rRNA genes. Appl Environ Microbiol 64: 4912–4917 Liu, J, Wang, ET, Chen, WX (2005) Diverse rhizobia associated with woody legumes Wisteria sinensis, Cercis racemosa and Amorpha fruticosa grown in the temperate zone of China. Syst Appl Microbiol 28: 465–477 Marmur, J (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3: 208–218 Mhamdi, R, Lagrerre, 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 Odee, DW, Haukka, K, McInroy, SG, Sprent, JI, Sutherland, JM, Young, JPW (2002) Genetic and symbiotic characterization of rhizobia isolated from tree and herbaceous legumes grown in soils from ecologically diverse sites in Kenya. Soil Biol Biochem 34: 801–811 Sohail, H, Sumera, Y, Kauser, AM, Yusuf, Z, Fauzia, YH (2004) Rhizobium, Bradyrhizobium and Agrobacterium strains isolated from cultivated legumes. Biol Fertil Soils 39: 179–185 Stuurman, N, Bras, CP, Schlaman, H.R.M., Wijfjes, A.H.M., Bloemberg, G, Spaink, HP (2000) Use of green fluorescent protein color variants expressed on stable broad-host-range vectors to visualize rhizobia interacting with plants. Mol Plant–Microb Interact 13: 1163–1169 Tan, ZY, Wang, ET, Peng, GX, Zhu, ME, Martinez-Romero, E, Chen, WX (1999) Characterization of bacteria isolated from wild legumes in the northwestern region of China. Int J Syst Bacteriol 49: 1457–1469 Tan, ZY, Xu, XD, Wang, ET, Gao, JL, Martínez-Romero, E, Chen, WX (1997) Phylogenetic and genetic relationships of Mesorhizobium tianshanense and related rhizobia. Int J Syst Bacteriol 47: 874–879 Vega-Hernández, MC, Pérez-Galdona, R, Dazzo, FB, Jarabo-Lorenzo, A., Alfayate, MC, León-Barrios, M (2001) Novel infection process in the indeterminate root nodule symbiosis between Chamaecytisus proliferus (tagasaste) and Bradyrhizobium sp. New Phytol 150: 707–721 Vincent, JM (1970) A Manual for the Practical Study of Root Nodule Bacteria. Blackwell Scientific, Oxford Wolde-Meskel, E, Terefework, Z, Frostegård, A, Lindström, K (2005) Genetic diversity and phylogeny of rhizobia isolated from agroforestry legume species in southern Ethiopia. Int J Syst Evol Microbiol 55: 1439–1452 Yanagi, M, Yamasato, K (1993) Phylogenetic analysis of the family Rhizobiaceae and related bacteria by sequencing of 16S rRNA gene using PCR and DNA sequencer. FEMS Microbiol Lett 107: 115–120