Factors influencing pathogenic Ice-Nucleation Active (INA) bacteria isolated from Salix plants, soil and litter
Article Sidebar
Main Article Content
Abstract
This paper deals with bacterial strains from three independent geographical locations representing different bacterial groups of Salix pathogens such as: Bacillus, Clavibacter, Erwinia, Pseudomonas fluorescens, P. syringae, Sphingomonas and Xanthomonas species that were collected to investigate the role and effects of growing temperatures, cell numbers, growth-limiting factors (e.g. carbon, nitrogen, phosphorus), and physical or chemical agents on their ice nucleation activity (INA). Methods for measurement of the cell mass for INA involved both direct plate counting and optical density. Ice nucleation temperatures of individual bacterial strains were determined by tube nucleation tests. Mean populations of bacteria per ml needed to cause ice nucleation were observed. For a typical P. syringae strain 102 cells per ml gave a nucleation temperature of –4.5°C while 109 cells per ml initiated freezing already at –2.5°C. Mean cell density for a representative P. fluorescens were 105 cells per ml for freezing at -5.5°C and 109 cells per ml for freezing at –3.5°C. Expression of icenuclei in certain bacterial strains was clearly dependent on growing temperature and nutritional conditions e.g. growth limiting factors. Limitation of C affected nucleation activity of P. fluorescens, Xanthomonas spp. and to some extent Erwinia spp. Except for P. fluorescens and P. syringae, N-limitation very strongly affected all the tested bacteria and decreased their nucleation activity. Starvation for P affected INA of Sphingomonas, whereas P. syringae was only slightly affected. In Bacillus, P-limitation totally inhibited ice-nucleation activity. Chemical and physical agents decreased but did not directly or completely inhibit the ice–nucleation activity of harvested cells as freezing still occurred but at lower temperatures. From this we hypothesize that initiation of freezing at higher temperatures (e.g. -2°C) is closely connected with cells that are physically and functionally intact.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
References
Anderson, J.A. and Ashworth, E.N. (1986). The effects of streptomycin, desiccation, and UV radiation on ice-nucleation by Pseudomonas viridiflava. Plant Physiology 80: 956-960.
Anderson, J.A., Buchanan, D.W., Stall, R.E. and Hall, C.B. (1982). Frost injury of tender plants increased by Pseudomonas syringae van Hall. Journal of the American Society for Horticultural Science 107: 123-125.
Arny, D.C., Lindow, S.E. and Upper, C.D. (1976). Frost sensitivity of Zea mays increased by application of Pseudomonas syringae. Nature 262: 282-284.
Cambours, M.A. (2004). Ice nucleation-active and pathogenic bacteria in Swedish and Estonian Salix short-rotation forestry plantations suffering from frost-related dieback. Licentiate thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden.
Cambours, M.A., Nejad, P., Granhall, U. and Ramstedt, M. (2005). Frost related dieback of willows, comparison of epiphytic and endophytic bacteria of different Salix clones, with emphasis on ice- nucleation activity, pathogenic properties and seasonal variation. Biomass and Bioenergy 28: 15-27.
Constantinidou, H.A., Hirano, S.S., Baker, L.S. and Upper, C.D. (1991). Atmospheric dispersal of ice nucleation-active bacteria: the role of rain. Phytopathology 80: 934-937.
De Kam, M., (1978). Xanthomonas populi subs. salicis, cause of bacterial canker in Salix dasyclada. European Journal of Forest Pathology 8:, 334-337.
Dye, D.W. (1957). The effect of temperature on infection by Pseudomonas syringae, van Hall. New Zealand Journal of Scientific Technology 38: 500-505.
Gross, D.C., Cody, Y.S., Proebsting, E.L., Jr., Radamaker, J.K. and Spotts, R.A. (1983). Distribution, population dynamics of ice nucleation-active bacteria in deciduous fruit tree orchards. Applied and Environmental Microbiology 46: 1370-1379.
Gross, D.C., Proebsting, E.L., Jr. and Andrews, P.K. (1984). The effects of ice nucleationactive bacteria on the temperatures of ice nucleation and low temperature susceptibilities of Prunus flower buds at various stages of development. Journal of American Society 109: 375-380.
Hirano, S.S., Baker, L.S. and Upper, C.D. (1985). Ice nucleation temperature of individual leaves in relation to population sizes of ice nucleation active bacteria and frost injury. Plant Physiology 77: 259-265.
Hirano, S.S. and Upper, C.D. (1986). Temporal, spatial and genetic variability of leaf associated bacterial populations. In: Microbiology of the Phyllosphere (eds. N.J. Follema and V.D. Del Heuve). Cambridge University Press, London: 235-251.
Lindow, S.E., (1982). Population dynamics of epiphytic ice nucleation active bacteria on frost sensitive plants and frost control by means of antagonistic bacteria. In: Plant Cold Hardiness and Freezing stress-Mechanisms and Crop implications (eds. P.H. Li, and A. Sakai). Academic Press, New York: 395-416.
Lindow, S.E., (1993). Novel method for identifying bacterial mutants with reduced epiphytic fitness. Applied Environmental Microbiology 59: 1586-1592.
Lindow, S.E., (1995). Control of epiphytic ice nucleation active bacteria for management of plant frost injury. In: Biological Ice Nucleation and its Application (eds. R.E. Lee, G.J. Warren and L.V. Gusta): 239-256.
Lindow, S.E., Arny, D.C. and Upper, C.D. (1982a). Bacterial ice nucleation: A frost injury to plants. Plant Physiology 70: 1084-1089.
Lindow, S.E., Arny, D.C. and Upper, C.D. (1982b). The relationship between ice nucleation frequency of bacteria and frost injury. Plant Physiology 70: 1090-1093.
Lindow, S.E., Lahue, E., Gocindarajan, A.G., Panopoulos, N.J. and Gites, D. (1989). Localization of ice nucleation activity and the ice gene product in Pseudomonas syringae and Escherichia coli. Molecular Plant-Microbe Interactions 2: 262-272.
Maki, L.R., Galyon, E.L., Chang-Chien, M. and Galdwell, D.R. (1974). Ice nucleation induced by Pseudomonas syringae. Applied Microbiology 28: 456-459.
Maki, L.R. and Willoughby, K.J. (1978). Bacteria as biogenic sources of freezing nuclei. Journal of Applied Meteorology 17: 1049-1053.
Nejad, P., Ramstedt, M. and Granhall, U. (2002). Synergistic effect between frost damage and bacterial infection in Salix plants. Poster presented at International Poplar Symposium III, on Basic and Applied Aspects of Poplar and Willow Biology; held in Uppsala, Sweden, August 26-29, 2002. Access: <http://www.forestresearch.co.nz/PDF/07. 56Nejadetal.pdf>.
Nejad, P., Ramstedt, M., Granhall, U., Cambours, M.A. and Roos, S. (2003). Biochemical characterization and identification of Ice-Nucleation- Active (INA) willow pathogens by means of BIOLOG MicroPlates, INA gene primers and PCR based 16S rRNA analyses. Poster presented at. 8th International Congress of Plant Pathology (ICPP) held in Christchurch, New Zealand. February 2-7, 2003. Access: <http://www.forestresearch.co.nz/PDF/00.02Nejadetal.pdf>.
Nejad, P. and Johnson, P.A. (2000). Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biological Control 18: 208-215.
Nejad, P., Ramstedt, M. and Granhall, U. (2004). Pathogenic ice-nucleation active bacteria in willows for short rotation forestry. Forest Pathology 34: 369-381.
Nemecek-Marshall, M., Laduca, R. and Fall, R. (1993). High level expression of ice nuclei in Pseudomonas syringae strain is induced by nutrient limitation and low temperature. Journal of Bacteriology 175: 4062-4070.
Paulin, J.P. and Luisetti, J. (1978). Ice nucleation activity among phytopathogenic bacteria. In: Proceedings of the Fourth International Conference on Plant Pathogenic Bacteria, Vol 2, Station de Pathologie Végétale et Phytobactériologie, Institute National Recherche Agronomique, Beaucouzé, France, 1978: 725-731.
Pearce, R.S., (2001). Plant freezing and damage. Annals of Botany 87: 417-424.
Ramstedt, M., Åström, B. and Von Fircks,. H.A. (1994). Dieback of poplar and willow caused by Pseudomonas syringae in combination with freezing stress. European Journal of Pathology 24: 305-315.
Phelps, P., Giddings, T.H., Prochoda, M. and Fall, R. (1986). Release of cell free ice nuclei by Erwinia herbicola. Journal of Bacteriology 167: 496-502.
Sikyta, B., Spilkova, J. and Dusek, J. (2000). The influence of growth rate and growth limiting factors on the protection of ice nuclei in Pseudomonas syringae CCM 4073 in continuous culture. Acta Biotechnology 20: 369-372.
Tsarouhas, V. (2002). Genome mapping of quantitative trait loci in Salix with an emphasis on freezing resistance. Doctoral thesis. Swedish University of Agricultural Sciences, Uppsala, Sweden. Agraria 327.
Warren, G. and Wolber, P. (1991). Molecular aspects of microbial ice-nucleation. Molecular Microbiology 5: 239-243.
Yankofsky, S.A., Levin, Z., Bertold, T. and Sandlerman, N. (1981). Some basic characteristics of bacterial freezing nuclei. Journal of Applied Meteorology 20: 1013-1019.
