Plant growth promoting H2-oxidizing bacteria as seed inoculants for cereal crops
ABSTRACT
The long-term success of hydrogenase uptake negative legume-rhizobia associations, in spite of their apparent inefficiency, may be explained by the positive effects of H2 release to soil. A primary benefit of H2 release to soil is the stimulation of H2-oxidizing, plant growth promoting rhizobacteria (PGPR) [1]. Two such previously isolated strains were tested as seed inoculants for barley and spring wheat; there were significant differences between treatments and controls in tiller and grain head production, supported by data from greenhouse trials. T-RFLP analysis of barley soil samples, supported by DNA sequencing data, successfully distinguished both species inoculated. Successful re-isolation indicates that these isolates can reproduce themselves in soils and can be used as effective inoculants with peat as the standard carrier. This study showed that we are able to achieve some of the beneficial effects of crop rotation without the need to implement actual crop rotation.
The long-term success of hydrogenase uptake negative legume-rhizobia associations, in spite of their apparent inefficiency, may be explained by the positive effects of H2 release to soil. A primary benefit of H2 release to soil is the stimulation of H2-oxidizing, plant growth promoting rhizobacteria (PGPR) [1]. Two such previously isolated strains were tested as seed inoculants for barley and spring wheat; there were significant differences between treatments and controls in tiller and grain head production, supported by data from greenhouse trials. T-RFLP analysis of barley soil samples, supported by DNA sequencing data, successfully distinguished both species inoculated. Successful re-isolation indicates that these isolates can reproduce themselves in soils and can be used as effective inoculants with peat as the standard carrier. This study showed that we are able to achieve some of the beneficial effects of crop rotation without the need to implement actual crop rotation.
Cite this paper
Golding, A. , Zou, Y. , Yang, X. , Flynn, B. and Dong, Z. (2012) Plant growth promoting H2-oxidizing bacteria as seed inoculants for cereal crops. Agricultural Sciences, 3, 510-516. doi: 10.4236/as.2012.34060.
Golding, A. , Zou, Y. , Yang, X. , Flynn, B. and Dong, Z. (2012) Plant growth promoting H2-oxidizing bacteria as seed inoculants for cereal crops. Agricultural Sciences, 3, 510-516. doi: 10.4236/as.2012.34060.
References
[1] Dong, Z. and Layzell, D.B. (2001) H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils. Plant and Soil, 229, 1-12. doi:10.1023/A:1004810017490 [2] Welbaum, G.E., Sturz, A.V., Dong, Z. and Nowak, J. (2004) Managing soil micro-organisms to improve productivity of agro-ecosystems. Critical Reviews in Plant Science, 23, 175-193. doi:10.1080/07352680490433295 [3] Vessey, J.K. (2003) Plant growth promoting rhizobacteria as bio-fertilizers. Plant and Soil, 255, 571-586. doi:10.1023/A:1026037216893 [4] Dey, R., Pal, K.K., Bhatt, D.M. and Chauhan, S.M. (2004) Growth promotion and yield of peanut (Arachis hypogea L.) by application of plant growth-promoting rhizobacteria. Microbiological Resesearch, 1, 371-394. doi:10.1016/j.micres.2004.08.004 [5] Esitken, A., Pirlak, L., Turan, M. and Sahin, F. (2006) Effects of floral and foliar application of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrition of sweet cherry. Scientia Horticulturae, 110, 324-327. doi:10.1016/j.scienta.2006.07.023 [6] Farag, M.A., Ryu, G.M., Sumner, L.W. and Paré, P.W. (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth and induced sys- temic resistance in plants. Phytochemistry, 67, 2262-2268. doi:10.1016/j.phytochem.2006.07.021 [7] Hunter, W.J. (1993) Ethylene production by root nodules and effect of ethylene on nodulation in glycine max. Applied and Environmental Microbiology, 59, 1947-1950. [8] Nascimento, F., Brigido, C. and Glick, B.R. (2012) Enhanced chickpea growth-promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene. Plant and Soil, 353, 221-230. doi:10.1007/s11104-011-1025-2 [9] Shah, S., Li, J., Moffatt, B.A. and Glick, B.R. (1998) Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Canadian Journal of Microbiology, 44, 833-843. doi:10.1139/w98-074 [10] Matos, A., Kerkhof, L. and Garland, J.L. (2005) Effects of Microbial Community Diversity on the Survival of Pseudomonas aeruginosa in the Wheat Rhizosphere. Microbial Ecology, 49, 257-264. doi:10.1007/s00248-004-0179-3 [11] Ping, L. and Bol-and, W. (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends in Plant Science, 9, 263-266. doi:10.1016/j.tplants.2004.04.008 [12] Postgate J. (1998) Nitrogen fixation. 3rd Edition, Cam- bridge UP, Cam-bridge. [13] Bullock, D.G. (1992) Crop rotation. Critical Reviews in Plant Sciences, 11, 309-326. [14] Schubert, K.R. and Evans, H.J. (1976) Hydrogen evolution: A major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proceedings of the National Academy of Sciences of the United States of America, 73, 1207-1211. doi:10.1073/pnas.73.4.1207 [15] Dixon, R.O.D. (1972) Hydrogenase in legume root nodule bacteroids: Occurrence and properties. Achives of Microbiology, 85, 193-201. doi:10.1007/BF00408844 [16] Ruiz-Argüeso, T., Maier, R.J. and Evans, H.J. (1979) Hydrogen evolution from alfalfa and clover nodules and hydrogen uptake by free-living Rhizobium meliloti. Applied and Environmental Microbiology, 37, 582-587. [17] Uratsu, S.L., Keyser, H.H., Weber, D.F. and Lim, S.T. (1982) Hydrogen uptake (HUP) activity of Rhizobium japonicum from major U.S. soybean production areas. Crop Science, 22, 600-602. doi:10.2135/cropsci1982.0011183X002200030040x [18] Baginsky, C., Brito, B., Imperial, J., Ruiz-Argüeso, T. and Palacios, J.M. (2005). Symbiotic hydrogenase activity in Bradyrhizobium sp. (Vigna) increases nitrogen content in Vigna unguiculata plants. Applied Environmental Microbiology, 71, 7536-7538. doi:10.1128/AEM.71.11.7536-7538.2005 [19] Dong, Z., Wu, L., Kettlewell, B., Caldwell, C.D. and Layzell, D.B. (2003) Hydrogen fertilization of soils—Is this a benefit of legumes in rotation? Plant Cell and Environment, 26, 1875-1879. doi:10.1046/j.1365-3040.2003.01103.x [20] Conrad, R. and Seiler, W. (1979) The role of H2 bacteria during the decomposition of H2 by soil. FEMS Microbiology Letters, 6, 143-145. doi:10.1111/j.1574-6968.1979.tb04296.x [21] La Favre, J.S. and Focht, D.D. (1983) Conservation in soil of H2 li-berated from N2 fixation by Hup– nodules. Applied and Environmental Microbiology, 46, 304-311. [22] Zhang, Y. (2006). Mechanisms of isolated hydrogen-oxidizing bacteria in plant growth promotion and effects of hydrogen metabolism on rhizobacterial community structure. Master’s Thesis, Saint Mary’s University, Hali- fax. [23] Maimaiti, J., Zhang, Y., Yang, J., Cen, Y.-P., Layzell, D.B., Peoples, M. and Dong, Z. (2007) Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environmental Microbiology, 9, 435- 444. doi:10.1111/j.1462-2920.2006.01155.x [24] Irvine, P., Smith, M. and Dong, Z. (2004) Hydrogen fer- tilizer: bacteria or fungi? Acta Horticulturae, 631, 239- 242. [25] LaRue, T.A. and Patterson, T.G. (1981) How much do legumes fix? Advances in Agronomy, 34, 15-38. doi:10.1016/S0065-2113(08)60883-4 [26] Hunt, S. and Layzell, D.B. (1993) Gas exchange of leg- ume nodules and the regulation of nitrogenase activity. Annual Review of Plant Physiology and Plant Molecular Biology, 44, 483-511. doi:10.1146/annurev.pp.44.060193.002411 [27] Hesterman, O.B., Sheaffer, C.C., Barnes, D.K., Lueschen, W.E. and Ford, J.H. (1986). Alfalfa dry matter and nitrogen production and fertilizer nitrogen response in legume-corn rotations. Agronomy Journal, 78, 19-23. doi:10.2134/agronj1986.00021962007800010005x [28] Dong, Z. and Layzell, D.B. (2002) Why do legumes nodules evolve hydrogen gas? The 13th International Congress on Nitrogen Fixation, 2-7 July 2001, Hamilton, 331- 335. [29] Stein, S., Selesi, D., Schilling, R., Pattis, I., Schmid, M. and Hartmann, A. (2005) Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation. Soil Biology & Biochemistry, 37, 1938-1945. doi:10.1016/j.soilbio.2005.02.035 [30] Dean, C., Sun, W., Dong, Z. and Caldwell, C.D. (2006) Soybean nodule hydrogen metabolism affects soil hydrogen uptake and growth of rotation crops. Canadian Journal of Plant Science, 86, 1355-1359. doi:10.4141/P06-082 [31] Garcia del Moral, L.F., Ramos, J.M. and Recalde, L. (1984) Tillering dynamics of winter barley as influenced by cultivar and nitrogen fertilizer: A field study. Crop Science, 24, 179-181. doi:10.2135/cropsci1984.0011183X002400010042x [32] Garcia del Moral, M.B. and Garcia del Moral, L.F. (1995) Tiller production and yield in relation to grain yield in winter and spring barley. Field Crops Research, 44, 85- 93. doi:10.1016/0378-4290(95)00072-0 [33] Glick, B.R., Penrose, D.M. and Li, J. (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. Journal of Theoretical Biology, 190, 63-68. doi:10.1006/jtbi.1997.0532 [34] Yang, S.F. and Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation in higher plants. Annual Reviews of Plant Physiology, 35, 155-189. doi:10.1146/annurev.pp.35.060184.001103 [35] Wang, C., Knill, E., Glick, B.R. and Defago, G. (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluores- cens strain CHAO and its gacA derivatives CHA96 on their growth-promoting and disease-suppressive capabilities. Canadian Journal of Microbiology, 46, 898-907. [36] Mayak, S., Tirosh, T. and Glick, B.R. (2004) Plant growth promoting bacteria that confer resistance in tomato to salt stress. Plant Physiology and Biochemistry, 42, 565-572. doi:10.1016/j.plaphy.2004.05.009 [37] Grichko, V.P. and Glick, B.R. (2001) Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiology and Biochemistry, 39, 11-17. doi:10.1016/S0981-9428(00)01212-2
[1] Dong, Z. and Layzell, D.B. (2001) H2 oxidation, O2 uptake and CO2 fixation in hydrogen treated soils. Plant and Soil, 229, 1-12. doi:10.1023/A:1004810017490 [2] Welbaum, G.E., Sturz, A.V., Dong, Z. and Nowak, J. (2004) Managing soil micro-organisms to improve productivity of agro-ecosystems. Critical Reviews in Plant Science, 23, 175-193. doi:10.1080/07352680490433295 [3] Vessey, J.K. (2003) Plant growth promoting rhizobacteria as bio-fertilizers. Plant and Soil, 255, 571-586. doi:10.1023/A:1026037216893 [4] Dey, R., Pal, K.K., Bhatt, D.M. and Chauhan, S.M. (2004) Growth promotion and yield of peanut (Arachis hypogea L.) by application of plant growth-promoting rhizobacteria. Microbiological Resesearch, 1, 371-394. doi:10.1016/j.micres.2004.08.004 [5] Esitken, A., Pirlak, L., Turan, M. and Sahin, F. (2006) Effects of floral and foliar application of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrition of sweet cherry. Scientia Horticulturae, 110, 324-327. doi:10.1016/j.scienta.2006.07.023 [6] Farag, M.A., Ryu, G.M., Sumner, L.W. and Paré, P.W. (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth and induced sys- temic resistance in plants. Phytochemistry, 67, 2262-2268. doi:10.1016/j.phytochem.2006.07.021 [7] Hunter, W.J. (1993) Ethylene production by root nodules and effect of ethylene on nodulation in glycine max. Applied and Environmental Microbiology, 59, 1947-1950. [8] Nascimento, F., Brigido, C. and Glick, B.R. (2012) Enhanced chickpea growth-promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene. Plant and Soil, 353, 221-230. doi:10.1007/s11104-011-1025-2 [9] Shah, S., Li, J., Moffatt, B.A. and Glick, B.R. (1998) Isolation and characterization of ACC deaminase genes from two different plant growth-promoting rhizobacteria. Canadian Journal of Microbiology, 44, 833-843. doi:10.1139/w98-074 [10] Matos, A., Kerkhof, L. and Garland, J.L. (2005) Effects of Microbial Community Diversity on the Survival of Pseudomonas aeruginosa in the Wheat Rhizosphere. Microbial Ecology, 49, 257-264. doi:10.1007/s00248-004-0179-3 [11] Ping, L. and Bol-and, W. (2004) Signals from the underground: bacterial volatiles promote growth in Arabidopsis. Trends in Plant Science, 9, 263-266. doi:10.1016/j.tplants.2004.04.008 [12] Postgate J. (1998) Nitrogen fixation. 3rd Edition, Cam- bridge UP, Cam-bridge. [13] Bullock, D.G. (1992) Crop rotation. Critical Reviews in Plant Sciences, 11, 309-326. [14] Schubert, K.R. and Evans, H.J. (1976) Hydrogen evolution: A major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proceedings of the National Academy of Sciences of the United States of America, 73, 1207-1211. doi:10.1073/pnas.73.4.1207 [15] Dixon, R.O.D. (1972) Hydrogenase in legume root nodule bacteroids: Occurrence and properties. Achives of Microbiology, 85, 193-201. doi:10.1007/BF00408844 [16] Ruiz-Argüeso, T., Maier, R.J. and Evans, H.J. (1979) Hydrogen evolution from alfalfa and clover nodules and hydrogen uptake by free-living Rhizobium meliloti. Applied and Environmental Microbiology, 37, 582-587. [17] Uratsu, S.L., Keyser, H.H., Weber, D.F. and Lim, S.T. (1982) Hydrogen uptake (HUP) activity of Rhizobium japonicum from major U.S. soybean production areas. Crop Science, 22, 600-602. doi:10.2135/cropsci1982.0011183X002200030040x [18] Baginsky, C., Brito, B., Imperial, J., Ruiz-Argüeso, T. and Palacios, J.M. (2005). Symbiotic hydrogenase activity in Bradyrhizobium sp. (Vigna) increases nitrogen content in Vigna unguiculata plants. Applied Environmental Microbiology, 71, 7536-7538. doi:10.1128/AEM.71.11.7536-7538.2005 [19] Dong, Z., Wu, L., Kettlewell, B., Caldwell, C.D. and Layzell, D.B. (2003) Hydrogen fertilization of soils—Is this a benefit of legumes in rotation? Plant Cell and Environment, 26, 1875-1879. doi:10.1046/j.1365-3040.2003.01103.x [20] Conrad, R. and Seiler, W. (1979) The role of H2 bacteria during the decomposition of H2 by soil. FEMS Microbiology Letters, 6, 143-145. doi:10.1111/j.1574-6968.1979.tb04296.x [21] La Favre, J.S. and Focht, D.D. (1983) Conservation in soil of H2 li-berated from N2 fixation by Hup– nodules. Applied and Environmental Microbiology, 46, 304-311. [22] Zhang, Y. (2006). Mechanisms of isolated hydrogen-oxidizing bacteria in plant growth promotion and effects of hydrogen metabolism on rhizobacterial community structure. Master’s Thesis, Saint Mary’s University, Hali- fax. [23] Maimaiti, J., Zhang, Y., Yang, J., Cen, Y.-P., Layzell, D.B., Peoples, M. and Dong, Z. (2007) Isolation and characterization of hydrogen-oxidizing bacteria induced following exposure of soil to hydrogen gas and their impact on plant growth. Environmental Microbiology, 9, 435- 444. doi:10.1111/j.1462-2920.2006.01155.x [24] Irvine, P., Smith, M. and Dong, Z. (2004) Hydrogen fer- tilizer: bacteria or fungi? Acta Horticulturae, 631, 239- 242. [25] LaRue, T.A. and Patterson, T.G. (1981) How much do legumes fix? Advances in Agronomy, 34, 15-38. doi:10.1016/S0065-2113(08)60883-4 [26] Hunt, S. and Layzell, D.B. (1993) Gas exchange of leg- ume nodules and the regulation of nitrogenase activity. Annual Review of Plant Physiology and Plant Molecular Biology, 44, 483-511. doi:10.1146/annurev.pp.44.060193.002411 [27] Hesterman, O.B., Sheaffer, C.C., Barnes, D.K., Lueschen, W.E. and Ford, J.H. (1986). Alfalfa dry matter and nitrogen production and fertilizer nitrogen response in legume-corn rotations. Agronomy Journal, 78, 19-23. doi:10.2134/agronj1986.00021962007800010005x [28] Dong, Z. and Layzell, D.B. (2002) Why do legumes nodules evolve hydrogen gas? The 13th International Congress on Nitrogen Fixation, 2-7 July 2001, Hamilton, 331- 335. [29] Stein, S., Selesi, D., Schilling, R., Pattis, I., Schmid, M. and Hartmann, A. (2005) Microbial activity and bacterial composition of H2-treated soils with net CO2 fixation. Soil Biology & Biochemistry, 37, 1938-1945. doi:10.1016/j.soilbio.2005.02.035 [30] Dean, C., Sun, W., Dong, Z. and Caldwell, C.D. (2006) Soybean nodule hydrogen metabolism affects soil hydrogen uptake and growth of rotation crops. Canadian Journal of Plant Science, 86, 1355-1359. doi:10.4141/P06-082 [31] Garcia del Moral, L.F., Ramos, J.M. and Recalde, L. (1984) Tillering dynamics of winter barley as influenced by cultivar and nitrogen fertilizer: A field study. Crop Science, 24, 179-181. doi:10.2135/cropsci1984.0011183X002400010042x [32] Garcia del Moral, M.B. and Garcia del Moral, L.F. (1995) Tiller production and yield in relation to grain yield in winter and spring barley. Field Crops Research, 44, 85- 93. doi:10.1016/0378-4290(95)00072-0 [33] Glick, B.R., Penrose, D.M. and Li, J. (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. Journal of Theoretical Biology, 190, 63-68. doi:10.1006/jtbi.1997.0532 [34] Yang, S.F. and Hoffman, N.E. (1984) Ethylene biosynthesis and its regulation in higher plants. Annual Reviews of Plant Physiology, 35, 155-189. doi:10.1146/annurev.pp.35.060184.001103 [35] Wang, C., Knill, E., Glick, B.R. and Defago, G. (2000) Effect of transferring 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase genes into Pseudomonas fluores- cens strain CHAO and its gacA derivatives CHA96 on their growth-promoting and disease-suppressive capabilities. Canadian Journal of Microbiology, 46, 898-907. [36] Mayak, S., Tirosh, T. and Glick, B.R. (2004) Plant growth promoting bacteria that confer resistance in tomato to salt stress. Plant Physiology and Biochemistry, 42, 565-572. doi:10.1016/j.plaphy.2004.05.009 [37] Grichko, V.P. and Glick, B.R. (2001) Amelioration of flooding stress by ACC deaminase-containing plant growth-promoting bacteria. Plant Physiology and Biochemistry, 39, 11-17. doi:10.1016/S0981-9428(00)01212-2