The pattern of secreted molecules during the co-inoculation of alfalfa plants with Sinorhizobium meliloti and Delftia sp. strain JD2: An interaction that improves plant yield

Molecular Plant-Microbe Interactions

Volumn 28, Issue 2, 2015, Pages 134-142

  Morel, M A ^a   Cagide, C ^a   Minteguiaga, M A ^a   Dardanelli, M S ^b   Castro Sowinski, S ^a,c  

^a Institute of Biological Research Clemente Esatble   (Uruguay)

^b DEPARTAMENTO DE QUÍMICA   (Argentina)

^c UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); DELFTIA; MEDICAGO SATIVA; SINORHIZOBIUM MELILOTI;

VEGETABLE PROTEIN;

ALFALFA; CARBOHYDRATE METABOLISM; DELFTIA; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

CARBOHYDRATE METABOLISM; DELFTIA; GENE EXPRESSION REGULATION, PLANT; LIPID METABOLISM; MEDICAGO SATIVA; PLANT PROTEINS; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

EID: 84937204715     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-08-14-0229-R     Document Type: Article

References (51)

1. Badri, D., and Vivanco J. M. 2009. Regulation and function of root exudates. Plant Cell Environ. 32:666-668.
2. Bennett, J. W., Hung, R., Lee, S., and Padhi, S. 2012. Fungal and bacterial volatile organic compounds: An overview. Pages 373-394 in: The Mycota. A Comprehensive Treatise on Fungi as Experimental Systems for Basic and Applied Research and Their Role as Ecological Signaling Agents. K. Esser and B. Hock, eds. Springer-Verlag, Berlin, Heidelberg, Germany.
3. Bertin, C., Yang, X., and Weston, L. A. 2003. The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67-83.
4. Bligh, E. G., and Dyer, W. J. 1959. A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
5. Bloemberg, G. V., Wijfjes A. H. M., Lamers, G. E. M., Stuurman, N., and Lugtenberg, B. J. J. 2000. Simultaneous imaging of Pseudomonas fluorescens wcs365 populations expressing three different autofluorescent proteins in the rhizosphere: New perspectives for studying microbial communities. Mol. Plant-Microbe Interact. 13:1170-1176.
6. Brechenmacher, L., Lei, Z., Libault, M., Findley, S., Sugawara, M., Sadowsky, M. J., Sumner, L. W., and Stacey, G. 2010. Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiol. 153:1808-1822.
7. Bullied, W. J., Buss, T. J., and Vessey, J. K. 2002. Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes: Field studies. Can. J. Plant Sci. 82:291-298.
8. Caetano-Anollés, G., Crist-Estes, D. K., and Bauer, W. D. 1988. Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. J. Bacteriol. 170:3164-3169.
9. Cassán, F., Perrig, D., Sgroy, V., Masciarelli, O., Penna, C., and Luna, V. 2009. Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur. J. Soil Biol. 45:28-35.
10. Castro-Sowinski, S., Martinez-Drets, G., and Okon, Y. 2002. Laccase activity in melanin-producing strains of Sinorhizobium meliloti. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 209:119-125.
11. Dakora, F. D., and Phillips, D. A. 2002. Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35-47.
12. Dardanelli, M. S., Fernández De Córdoba, F. J., Espuny, M. R., Rodríguez Carvajal, M. A., Soria Díaz, M. E., Gil Serrano, A. M., Okon, Y., and Megías, M. 2008. Effect of Azospirillum brasilense coinoculation with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biol. Biochem. 40:2713-2721.
13. Dardanelli, M. S., Manyani, H., González-Barroso, S., Rodríguez-Carvajal. M. A., Gil-Serrano, A. M., Espuny, M. R., López-Baena, F. J., Bellogín, R. A. Megías, M., and Ollero, F. J. 2010. Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483-493.
14. Dardanelli, M. S., Fernández De Córdoba, F. J., Estévez, J., Contreras, R., Cubo, M. T., Rodríguez-Carvajal, M. A., Gil-Serrano, A. M., López-Baena, F. J., Bellogín, R., Manyani, H., Ollero, F. J., and Mejías, M. 2012. Changes in flavonoids secreted by Phaseolus vulgaris roots in the presence of salt and the plant growth-promoting rhizobacteria Chryseobacetrium balustinum. Appl. Soil Ecol. 57:31-38.
15. Duetz, W. A., Bouwmeester, H., Van Beilen, J. B., and Witholt, B. 2003. Biotransformation of limonene by bacteria, fungi, yeasts, and plants. Appl. Microbiol. Biotechnol. 61:269-277.
16. Dutta, S., Rani, T. S., and Podile, A. R. 2013. Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PLoS One 8:e78369.
17. Egamberdieva, D., Berg, G., Lindström, K., and Räsänen, L. A. 2010. Coinoculation of Pseudomonas spp. with Rhizobium improves growth and symbiotic performance of fodder galega (Galega orientalis Lam.). Eur. J. Soil Biol. 46:269-272.
18. Ferri, L., Gori, A., Biondi, E. G., Mengoni, A., and Bazzicalupo, M. 2010. Plasmid electroporation of Sinorhizobium strains: The role of the restriction gene hsdR in type strain Rm1021. Plasmid 63:128-135.
19. Fox, S. L., O'Hara, G., and Brau, L. 2011. Enhanced nodulation and symbiotic effectiveness of Medicago truncatula when co-inoculated with Pseudomonas fluorescens WSM3457 and Ensifer (Sinorhizobium) medicae WSM419. Plant Soil 48:245-254.
20. Han, J., Su, L., Dong, X., Cai, Z., Sun, X., Yang, H., Wang, Y., and Song, W. 2005. Characterization of a novel plant growth-promoting bacteria strain Delftia tsuruhatensis HR4 both as a diazotroph and a potential biocontrol agent against various plant pathogens. Syst. Appl. Microbiol. 28:66-76.
21. Hartwig, U. A., Maxwell, C. A., Joseph, C. M., and Phillips, D. A. 1990. Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol. 92:116-122.
22. Howieson, J., Ewing, M., Robson, A., and Abbot, L. 1993. External phosphate and calcium concentrations, but not the products of rhizobial nodulation genes, affect the attachment of Rhizobium meliloti to roots of annual medics. Soil Biol. Biochem. 25:567-573.
23. Itzigsohn, R., Kapulnik, Y., Okon, Y., and Dovrat, A. 1993. Physiological and morphological aspects of interaction between Rhizobium meliloti and alfalfa (Medicago sativa) in association with Azospirillum brasilense. Can J. Microbiol. 39:610-615.
24. Jayamohan, N. S., and Kumudini, B. S. 2011. Host pathogen interaction at the plant cell wall. Int. Res. J. Pharmacol. 1:242-249.
25. Jones, D. L. 1998. Organic acids in the rhizosphere - a critical review. Plant Soil 205:25-44.
26. Juge, C., Prévosta, D., Bertranda, A., Bipfubusaa, M., and Chalifour, F. P. 2012. Growth and biochemical responses of soybean to double and triple microbial associations with Bradyrhizobium, Azospirillum and arbuscular mycorrhizae. Appl. Soil Ecol. 61:147-157.
27. Khorassani, R., Hettwer, U., Ratzinger, A., Steingrobe, B., Karlovsky, P., and Claassen, N. 2011. Citramalic acid and salicylic acid in sugar beet root exudates solubilize soil phosphorus. BMC Plant Biol. 11:121.
28. Macchiavelli R. E., and Brelles-Mariño G. 2004. Nod factor-treated Medicago truncatula roots and seeds show an increased number of nodules when inoculated with a limiting population of Sinorhizobium meliloti. J. Exp. Bot. 55:2635-2640.
29. Marks, B. B., Megias, M., Nogueira, M. A., and Hungría, M. 2013. Biotechnological potential of rhizobial metabolites to enhance the performance of Bradyrhizobium spp., and Azospirillum brasilense inoculants with soybean and maize. AMB Express 3:21.
30. Mishra, P., Mishra, S., and Selvakumar, G. 2009. Coinoculation of Bacillus thuringeinsis-KR1 with Rhizobium leguminosarum enhances plant growth and nodulation of pea (Pisum sativum L.) and lentin (Lens culinaris L.). World J. Microbiol. Biotechnol. 25:753-761.
31. Molla, A., Shamsuddin, Z., and Saud, H. 2001. Mechanism of root growth and promotion of nodulation in vegetable soybean by Azospirillum brasilense. Comm. Soil Sci. Plant Anal. 32:2177-2187.
32. Morel, M., and Castro-Sowinski, S. 2013. The complex molecular signaling network in microbe-plant interaction. Pages 169-199 in: Plant Microbe Symbiosis: Fundamentals and Advances. N. K. Arora, ed. Springer, Bangalore, India.
33. Morel, M., Braña, V., and Castro-Sowinski, S. 2012. Legume crops, importance and use of bacterial inoculation to increase the production. Pages 217-240 in: Crop Plant. A. Goyal, ed. InTech, Rijeka, Croatia.
34. Morel, M. A., Ubalde, M., Braña, V., and Castro-Sowinski, S. 2011. Delftia sp. JD2: A potential Cr (VI)-reducing agent with plant growthpromoting activity. Arch. Microbiol. 193:163-168.
35. Narula, N., Kothe, E., and Behl, R. K. 2009. Role of root exudates in plant-microbe interactions. J. Appl. Bot. Food Qual. 82:122-130.
36. Neumann, G. 2007. Root exudates and nutrient cycling. Pages 123-157 in: Soil Biology. Nutrient Cycling in Terrestrial Ecosystem. A. Varma, ed. Springer-Verlag, Berlin, Heidelberg, Germany.
37. Paulucci, N. S., Dardanelli, M. S., and García De Lema, M. 2014. Biochemical and molecular evidence of a Δ9 fatty acid desaturase from Ensifer meliloti 1021. Microbiol. Res. 169:463-468.
38. Peters, N. K., and Long, S. R. 1988. Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol. 88:396-400.
39. Peters, N. K., Frost, J. W., and Long, S. R. 1986. A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science 233:977-980.
40. Phan Tran, L.-S., and Nguyen, H. T. 2009. Future biotechnology of legumes. Pages 265-307 in: Nitrogen Fixation in Crop Production. D. W. Emerich and H. B. Krishnan, eds. Agron. Monogr. 52. American Society of Agronomy, Madison, WI, U. S. A.
41. Ping, L., and Boland, W. 2004. Signals from the underground: Bacterial volatiles promote growth in Arabidopsis. Trends Plant Sci. 9:263-266.
42. Rajesh Kannan, V., Suganya, S., King Solomon, E., Balasubramanian, V., Ramesh, N., and Rajesh, P. 2011. Analysis of interaction between Arbuscular mycorrhizal fungi and their helper bacteria by MILPA model. Res. Plant Biol. 1:48-62.
43. Roudier, F., Gissot, L., Beaudoin, F., Haslam, R., Michaelson, L., Marion, J., Molino, D., Lima, A., Bach, L., Morin, H., Tellier, F., Palauqui, J. C., Bellec, Y., Renne, C., Miquel, M., Dacosta, M., Vignard, J., Rochat, C., Markham, J. E., Moreau, P., Napier, J., and Faure, J. D. 2010. Verylong-chain fatty acids are involved in polar auxin transport and developmental pattering in Arabidopsis. Plant Cell 22:364-375.
44. Sandnes, A., Eldhuset, T. D., and Wollebæk, G. 2005. Organic acids in root exudates and soil solution of Norway spruce and silver birch. Soil Biol. Biochem. 37:259-269.
45. Sérandour, J., Reynaud, S., Willison, J., Patouraux, J., Gaude, T., Ravanel, P., Lempérière, G., and Raveton, M. 2008. Ubiquitous water-soluble molecules in aquatic plant exudates determine specific insect attraction. PLoS ONE 3:e3350. Published online.
46. Shukla, K. P., Sharma, S., Singh, N. K., Singh, V., Tiwari, K., and Singh, S. 2011. Nature and role of root exudates: Efficacy in bioremediation. Afr. J. Biotechnol. 10:9717-9724.
47. Silva, L. R., Pereira, M. J., Azevedo, J., Mulas, R., Velazquez, E., González-Andrés, F., Valentão, P., and Andrade, P. B. 2013. Inoculation with Bradyrhizobium japonicum enhances the organic and fatty acids content of soybean (Glycine max (L.) Merrill) seeds. Food Chem. 141:3636-3648.
48. Ubalde, M., Braña, V., Sueiro, F., Morel, M., Martínez-Rosales, C., Marquez, C., and Castro-Sowinski, S. 2012. The versatility of Delftia sp. isolates as tools for bioremediation and biofertilization technologies. Curr. Microbiol. 64:597-603.
49. Vincent, J. M. 1970. A Manual for the Practical Study of Root-Nodule Bacteria. Handb. No. 15. Blackwell Scientific Publications, Oxford.
50. Volpin, H., Burdman, S., Castro-Sowinski, S., Kapulnik, Y., and Okon, Y. 1996. Inoculation with Azospirillum increased exudation of rhizobial nodgene inducers by alfalfa roots. Mol. Plant-Microbe Interact. 9:388-394.
51. Zhang, J., Subramanian, S., Zhang, Y., and Yu, O. 2007. Flavone synthases from Medicago trucatula are flavanone-2-hydroxylases and are important for nodulation. Plant Physiol. 144:741-751.