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Role of Organic Acids in the Mechanisms of Biological Soil Disinfestation (BSD)

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Role of Organic Acids in the Mechanisms of Biological Soil Disinfestation (BSD) J Gen Plant Pathol (2006) 72:247–252 © The Phytopathological Society of Japan DOI 10.1007/s10327-006-0274-z and Springer-Verlag Tokyo 2006 FUNGAL DISEASES Short communication Noriaki Momma · Kazuhiro Yamamoto · Peter Simandi Masahiro Shishido Role of organic acids in the mechanisms of biological soil disinfestation (BSD) Received: May 18, 2005 / Accepted: December 9, 2005 Abstract Biological soil disinfestation (BSD), or reductive Although other chemical disinfestants for soil treatment soil disinfestation, achieved by amendment with organic such as chloropicrin, 1,3-dichloropropene, and methyl materials such as wheat bran followed by flooding and isothiocyanate, are still available, soil disinfestation using covering the soil surface, has been used to control some these chemicals has become widely recognized as measures soilborne diseases including Fusarium wilt and bacterial incompatible with sustainable agriculture. Therefore, it is wilt of tomato. During a BSD treatment, accumulation of imperative to find alternatives to chemical fumigation for acetic acid and/or butyric acid was detected with high- disinfesting soils. performance liquid chromatography. Survival of Fusarium A number of soilborne pathogens can be suppressed oxysporum f. sp. lycopersici or Ralstonia solanacearum was under anaerobic conditions (Cook and Baker 1983; Blok suppressed by these organic acids. Amendment of these et al. 2000). For example, populations of soilborne pa- organic acids into soil suppressed the survival of R. thogens in rice paddies can decrease during the flooding solanacearum at lower concentrations than the maximum period, and this suppression is often enhanced by the detected in BSD treatment, indicating that production of incorporation of readily decomposable organic matter such these organic acids is one of the mechanisms of control. as rice straws (Shinmura 2004). Similarly, although usually However, F. oxysporum f. sp. lycopersici in soil survived sporadic and locally confined, soilborne diseases have also with the maximum concentrations of these organic acids been suppressed in crop fields under anaerobic conditions achieved by BSD; thus, involvement of factors other than after the incorporation of large amounts of organic matter organic acids may be involved. and/or intensive rainfalls (Cook and Baker 1983). Applying the concept of enriching organic materials such Key words Fusarium oxysporum f. sp. lycopersici · as fresh broccoli or grass under anaerobic conditions in the Ralstonia solanacearum · Biological soil disinfestation soil, Blok et al. (2000) proposed a new technique of biologi- (BSD) · Acetic acid · Butyric acid · Tomato cal soil disinfestation (BSD), or reductive soil disinfesta- tion, for the control of soilborne pathogens including Fusarium oxysporum f. sp. asparagi, Rhizoctonia solani, and To control soilborne diseases, soil fumigation with methyl Verticillium dahliae. Shinmura et al. (1999) also developed a bromide has been one of the most effective measures. How- soil disinfestation method that combined soil enrichment ever, its use is highly restricted because of its destructive with organic materials to achieve reduced conditions and impact on the stratospheric ozone layer (Subbarao 2002). soil solarization for controlling root rot of Welsh onion caused by Fusarium redolens. This method has commonly been used in Japan against a wide range of soilborne dis- eases and involves three steps: (1) amending soil with wheat N. Momma · M. Shishido (*) bran, (2) flooding the soil by irrigation, and (3) covering the Faculty of Horticulture, Chiba University, 648 Matsudo, Chiba 271- soil surface with a plastic film to induce reducing soil con- 8510, Japan ditions. Although Shinmura’s method uses a wheat bran Tel. +81-47-308-8824; Fax +81-47-308-8824 e-mail: [email protected] amendment rather than broccoli or grass, it also requires anaerobic conditions for its effectiveness. Therefore, K. Yamamoto Shinmura’s soil disinfestation may be considered a modifi- Technology Development Group, Keiyo Gas Corporation, Ichikawa, Japan cation of the BSD technique. Momma et al. (2005) demonstrated that chlamydospores P. Simandi Faculty of Agriculture, Water and Environmental Management, of F. oxysporum f. sp. lycopersici, the causal agent of Tessedik Samuel College, Szarvas, Hungary Fusarium wilt of tomato, were effectively killed only when 248 the soil conditions were changed as follows: (1) a wheat bran infest the soil. To enumerate the initial viable population, a amendment to activate soil microorganisms, with subse- series of tenfold dilutions of the infested soil prepared with quent oxygen depletion, and (2) the soil surface was covered 0.1% water agar was spread onto petri plates with Hara and with a plastic film to establish anaerobic conditions by pre- Ono’s selective medium (Wakimoto et al. 1993) and incu- venting reoxygenation from the soil surface. In addition, it is bated for 3–4 days at 28°C before counting bacterial colo- interesting to note that successful BSD is always correlated nies. The initial cell density was estimated at 2 × 105 CFU/g with a decrease in soil pH and emission of an unpleasant odor dry soil. (Momma et al. 2005). Kubo et al. (2005) also implicated The infested soil (250g dry soil) was placed into a organic acids such as acetic acid, as well as antagonistic glass bottle (600ml) with a screw cap, amended with 2.5g of activity of soil microorganisms in the mechanisms of BSD. wheat bran, irrigated to field capacity, and the bottle cap Fusarium oxysporum f. sp. lycopersici and Ralstonia was tightly sealed with Parafilm (PM-996, Wako, Osaka) solanacearum are casual agents of Fusarium wilt and bacte- (BSD treatment). Field capacity was defined as the amount rial wilt of tomato, respectively, and cause extensive eco- of water held in soil after excess water drained nomic losses worldwide. Because BSD is effective against away (Veihmeyer and Hendrickson 1949) and was previ- both of these diseases (Momma et al. 2005), we investigated ously determined as soil water content after filtration using the production of organic acids during the course of BSD a funnel with filter paper for 12h. In addition, nonamended and evaluated the effect of organic acids on the survival of soils with and without irrigation were prepared as con- these pathogens. trol treatments. The gravimetric water content of the nonirrigated soil was approximately 0.5. After a 2-week Preparation of inocula. Fusarium oxysporum f. sp. incubation at 28°C in the dark, the population size of surviv- lycopersici CU1 (race 1) was grown on potato dextrose ing bacteria was determined by a standard dilution method broth for 7 days at 25°C with shaking. The fungal culture (Wollum 1982). This experiment was conducted twice. was passed through cheesecloth and centrifuged at 3000 × g In the first experiment, survival of R. solanacearum was for 5min. The bud cells in the resulting pellet were resus- significantly suppressed in the BSD treatment, i.e., no pended in sterile distilled water (bud-cell suspension). For colony formed even in the nondiluted soil sample (Table 1). chlamydospores of F. oxysporum f. sp. lycopersici, a homog- In contrast, in the control (untreated) and the irrigation enized mycelial suspension of a 7-day-old, static culture in (without wheat bran amendment), the viable population potato sucrose broth (PSB) was added to sterilized soil- of R. solanacearum increased approximately ten times water extract (1:1, w/w) and incubated at 25°C. The soil- over the initial cell density. Similarly, the viability of this water extract was prepared by adding 100g of field soil pathogen was significantly reduced by BSD in the (andosols; 58.0% sand, 35.2% silt, 6.8% clay) collected from second experiment. Previously, we reported that survival the experimental farm of Chiba University to 100ml of of chlamydospores of F. oxysporum f. sp. lycopersici tap water, autoclaving for 20min, and filtering the superna- was significantly restricted by BSD (Momma et al. 2005). tant through a 0.44-µm filter. After a 3-week incubation, The present work suggests that the applicability of only chlamydospores were observed under a microscope. BSD may be extended to the control of soilborne bacterial Ralstonia solanacearum EK1–2 (biovar 4, race 1) was grown pathogens. in potato semisynthetic broth (Wakimoto et al. 1993) for 1 day at 28°C. The bacterial culture was centrifuged at 10000 Organic acids produced in BSD treatment and their effects × g for 10min, and the resulting pellet was resuspended in on soil pH. A plastic pot (Wagner pot, 1/5000a) was filled sterile distilled water. with field soil (ca. 9kg dry soil) after sieving (<2mm). Four combinations of wheat bran amendment and irrigation Survival of R. solanacearum in soil after BSD treatment. A treatments were used: wheat bran amendment with irriga- cell suspension of R. solanacearum (5 × 108 cells/ml) was tion followed by covering the soil surface (BSD), wheat thoroughly mixed into the field soil at a rate of 1% (v/v) to bran amendment without irrigation or covering (wheat Table 1. Survival of Ralstonia solanacearum in wheat bran-amended and irrigated soil Plot code Treatment log CFUc (/g dry soil) Wheat brana Irrigationb Experiment Id Experiment IIe Control No No 6.2 NT Irrigation No Yes 6.3 3.6 (0.02) BSD Yes Yes ND ND BSD, biological soil disinfestation; CFU, colony-forming unit; NT, not tested; ND, not detected a Wheat bran was amended to field soil at a concentration of approximately 1.6% (w/w) b Water was added to field capacity, and the test bottle was sealed with plastic film c Viable cell number of R. solanacearum was measured after 2-week incubation by a standard dilution method on Hara and Ono’s medium. The initial population in the infested soil was 2 × 105 CFU/g dry soil d Two replications e Three replications. Value in parentheses is standard error of the mean 249 bran), no wheat bran amendment with irrigation and cover- gradually decreased to 83% of the maximum concentration ing (irrigation), and no wheat bran amendment without after 15 days (Table 2).
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