I NOTES 183

IgGl antibodies was supported by experiments with cyclophos- soma) duttoni Thiroux 1905 (Protozoa, Trypanosomatidae). Z. pharnide immunosuppression of T. musculi infected mice Parasitenkd. 2: 297-3 15. (Viens 1985) and by the present results, albeit no direct MAGLUILO, P., P. VIENS, and A. FORGET. 1983. Immunosuppression

evidence for this is available. a portion of the antibodies during T. musculi infection in inbred strains of mice. J. Clin. Lab. Immunol. 10: 141-154. produced host mice infected T' musculi thus appears to be

OLIVIER, M., P, TIJSSEN, and P. VIENS. 1985. Initial control of directed against T-independent parasite antigens. Trypanosoma rnusculi infection by IgGzb antibodies. Parasite

Acknowledgement This work was supported by the Medical Research Council of

1 Canada.

AMSBAUGH, D. F., C. T. HANSEN, B. PRESCOTT, P. W. STASHAK, D. R. BARTHOLD, and P. J. BAKER. 1973. Genetic control of the antibody response to type I11 pneumococcal polysaccharide in mice. I. Evidence that an X-linked gene plays a decisive role in determining responsiveness. J. Exp. Med. 136: 93 1-947.

COHEN, P. L., I. SCHER, and D. E. MOSLER. 1976. In vitro studies of the genetically determined unresponsiveness to thymus independent antigens in CBA/N mice. J. Immunol. 116: 301-304.

CUNNINGHAM, M. P., W. H. R. LUMSDEN, and W. A. P. WEBBER. 1963. The preservation of viable Trypanosomes in lymph tubes at low temperature. Exp. Parasitol. 14: 280-284.

DESBIENS, C., and P. VIENS. 1981. Trypanosoma musculi in CBA mice: trypanocidal mechanism eliminating dividing forms. Parasito- logy, 83: 109-1 13.

HEBERMAN, R. B., and H. T. HALDEN. 1978. Natural cell mediated immunity. Adv. Cancer Res. 27: 305-310.

HERBERT, W. J., and W. H. R. LUMSDEN. 1976. Trypanosorna brucei: "matching" method for estimating the host's parasitemia. Exp. Parasitol. 40: 427-43 1.

JAYAWARDENA, A. N., C. A. JANEWAY, JR., and J. D. KEMP. 1979. Experimental malaria in the CBA/N mouse. J. Immunol. 123: 2532-2539.

KRAMPITZ, H. E. 1969. Verbreitung Wirt-Parasit-Beziehungen und Vermehrung sizilianischer Starnme von Trypanosorna (Herpeto-

Immunol. In press. ROSENSTREICH, D. L., S. I. VOGEL, A. JACQUES, L. M. WAHL,

I. SCHER, and S. E. MERGENHAGEN. 1978. Differential endotoxin sensitivity of lymphocytes and macrophages from mice with an X-linked defect in B cell maturation. J. Immunol. 121: 685-691.

SCHER, I., A. AHAMED, S. 0 . SHARROW, and W. E. PAUL. 1977. Maturation of murine B lymphocytes. In Development of host defenses. Edited by M. D. Cooper and D. H. Dayton. Raven Press, New York.

SCHER, I., A. D. STEINBERG, A. K. BERNING, and W. E. PAUL. 1975. X-linked B lymphocyte immune defect in CBA/N mice. 11. Studies of the mechanisms underlying the immune defect. J. Exp. Med. 142: 637-650.

TALIAFERRO, W. H., and T. Przz~. 1960. The inhibition of nucleic acid and protein synthesis in Trypanosoma lewisi by the antibody ablastin. Proc. Natl. Acad. Sci. U.S.A. 46: 33-45.

VARGAS, DEL C., P. VIENS, and P. A. L. KONGSHAVN. 1984. Trypanosoma musculi infection in B-cell deficient mice. Infect. Immun. 44(1): 162- 167.

VIENS, P. 1985. Immunology of non-pathogenic trypanosomes of rodents. In Immunology and pathogenesis of trypanosomiasis. Edited by I. Tizard. CRC Press, Boca Raton, FL. pp. 201-223.

VIENS, P., P. POULIOT, and G. A. T. TARGETT. 1974. Cell mediated immunity during infection of CBA mice with Trypanosoma musculi. Can. J . Microbiol. 20: 105-106.

VIENS, P., G. A. T. TARGETT, E. LEUCHARS, and A. J. S. DAVIES. 1974. The immunological response of CBA mice to Trypanosorna musculi. I. Initial control of the infection and the effect of T-cell deprivation. Clin. Exp. Immunol. 16: 279-294.

Competition for nodulation of field-grown soybeans by strains of Rhizobium fredii

THOMAS J. MCLOUGHLIN,~ SCOTT G. ALT, P. ANN OWENS, AND CORRINE FETHERSTON Agrigenetics Corporation, 5649 East Buckeye Road, Madison, WI, U . S.A . 53716

Accepted October 22, 1985

MCLOUGHLIN, T. J., S. G. ALT, P. A. OWENS, and C. FETHERSTON. 1986. Competition for nodulation of field-grown soy- beans by strains of Rhizobium fredii. Can. J. Microbiol. 32: 183-186.

Nodulation of Glycine max (L) Merr. by six Rhizobium fredii strains was measured in two Midwestern fields containing high indigenous populations of Bradyrhizobium japonicum (3 x 105/gm soil). The soils were inoculated with antibiotic-resistant mutants using liquid inoculum at two levels on soybean cv. Peking and cv. Jacques 130. Strain establishment was measured 40 days after planting. In the first year, USDA206, USDA217, and USDA257 were the most competitive strains, occupying greater than 50% of the nodules on cv. Peking in both soils. None of the strains were competitive on Jacques 130. In the second growing season, all nodules were formed by the indigenous population on both cultivars, suggesting that these fast-growing strains do not persist in Midwestern soils.

MCLOUGHLIN, T. J., S. G. ALT, P. A. OWENS et C. FETHERSTON. 1986. Competition for nodulation of field-grown soybeans by strains of Rhizobium fredii. Can. J . Microbiol. 32: 183-186.

La nodulation de Glycine max (L) Merr. par six souches de Rhizobium fredii a CtC CvaluCe dans deux champs de l'ouest central contenant des populations indigknes ClevCes de Bradyrhizobium japonicum (3 x 105/g de sol). Les sols furent inoculCs avec des mutants rksistants aux antibiotiques, utilisant deux niveaux d'inoculum liquide et les cultivars de soya Peking et Jacques 130. L'Ctablissement des souches a CtC CvaluC 40 jours aprks la plantation. Au cours de la premikre annee, les souches USDA206, USDA217, et USDA257 ont CtC les plus compCtitives, occupant plus de 50% des nodules du cv. Peking dans les deux champs. Aucune des souches n'a CtC compCtitive chez le cv. Jacques 130. Lors de la seconde annCe de croissance, tous les nodules ont CtC form& par la population indigkne chez les deux cultivars, ce qui suggere que ces souches a croissance rapide ne persistent pas dans les sols de l'ouest central.

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184 CAN. J. MICROBIOL. VOL. 32. 1986

Competition by Bradyrhizobium japonicum for nodulation of soybeans in Midwestern soils is of major agronomic impor- tance. Introduced strains often fail to form nodules because of the competition from the indigenous population (Ham et al. 1971).

Recently the isolation of fast-growing strains (Rhizobium fredii) from soybean nodules and soil from China has been re- ported (Keyser et al. 1982). In greenhouse competition studies carried out in pots containing soils with a high indig- enous rhizobial population, three of these strains (USDA257, USDA206, and USDA193) formed at least 60% of the nodules on cv. Peking, grown in one soil, whereas seven other strains were much less competitive (McLoughlin et al. 1985).

The objectives of the current study were (i) to measure the competitive ability of USDA257, USDA206, USDA193, and three other R. fredii strains when inoculated at two inoculum levels on cv. Peking and cv. Jacques 130 in field trials in two Midwestern soils and (ii) to measure the persistance for nodulation of these strains into the second growing season.

Rhizobium fredii isolates USDA 19 1, USDA 193, USDA206, USDA208, USDA217, and USDA257 were obtained from the United States Department of Agriculture (USDA) culture collection, Beltsville, MD. These strains form an effective symbiosis on cv. Peking and an ineffective symbiosis on commercial cultivars such as cv. Jacques 130 (Keyser et al. 1982), with the exception of USDA191 which forms a partially effective symbiosis on cv. Jacques 130 (T. J. McLoughlin and P. A. Owens, unpublished data).

Strains were identified utilizing spontaneous antibiotic- resistant mutants (1000 p,g/mL of streptomycin sulphate) of all of the above strains (McLoughlin et al. 1985).

Glycine mcuc (L) Merr. cv. Peking was obtained from D. Bernard, USDA, Urbana, IL, and cv. Jacques 130, a commer- cial cultivar, from T. Burmood, Jacques Seeds, Prescott, WI.

Inocula were prepared from cultures grown in YMB (Vincent 1970) or TYB (Beringer 1974). Total viable cell counts were carried out on TYA (TYB plus 15 gm agar/L) and TYA + streptomycin (Str) to determine the number of cells added to the seed on the day of inoculation. The cells were stored overnight at 4°C before inoculation in the field.

The experiments were initiated at two locations in 1983. One set of plots was established in a Ringwood silt loam soil (fine-loamy, mixed, mesic Typic Argiudolls) near Sun Prairie, WI (soil C). The soil pH measured 6.2; soil phosphorus (P) and potassium (K) were 230 and 350 lb (1 lb/acre = 0.112 g/m2), respectively. The soil had been in soybean production the previous year. The second experiment was done in a St. Charles silt loam (fine-silty , mixed, mesic Typic Hapludalfs) and sandy soil near Madison, WI (soil D). Soil pH was 6.6; P and K were 77 and 275 lbs/acre, respectively. The soil had been in corn production the previous year. The most probable number (MPN) of indigenous rhizobia (Brockwell 1963) was deter- mined in growth pouches (Northrup King Seed Company, Minneapolis, MN) in growth chambers. The study consisted of 13 treatments replicated four times using a randomized com- plete block design. The treatments included the following: each of the six strains inoculated at 1 X and 5 X inoculum levels (cell concentrations are given in Figs. 1 and 2) and an uninoculated control. Plots (1.25 x 3 m) were planted with a two-row planter at a rate of 1 seed12.5 cm row with soybean cv. Peking and cv. Jacques 130, in 1.25 m long rows spaced 1 m apart. Liquid inocula were added postplanting over the seeds from a sprin- kling can. For the 1 x inoculum level, 100 mL of cells was

diluted in 400 mL sterile H20 and poured evenly over the seed, while 500 mL of undiluted cells were added per plot in the 5 X

level. Following inoculation, the plots were raked to cover the seed. Alleyways of 1 and 3 m were left between each plot and each replication to avoid cross-contamination. Strain persis- tence was measured by planting the same cultivars in the same plots in 1984. The plots were disked before planting in spring and care was taken not to cross-contaminate plots.

Strain establishment and persistence was measured 40 days after planting in the first and second growing seasons. Four plants were selected per replication, six nodules were selected per plant (three tap and three lateral), making a total of 96 nodules per treatment.

After the nodules were rinsed thoroughly under the water tap to remove excess soil, they were washed for 20 min in Tween 80 (1 drop in 100 mL), then 30 min in 0.5% sodium hypochlorite, and finally for 15 min in 3% hydrogen peroxide on a reciproca- ting shaker. They were then washed in six changes of sterile H20. After crushing the nodules, nodule occupancy was determined by transferring the crushed material to agar plates, with and without the appropriate antibiotic, using a multiple inoculator. Cyclohexamide (150 p,g/mL) was added to the media to prevent fungal contamination.

Crushed nodule material from the uninoculated control plots was plated on selective media to assay the extent of cross- contamination between plots, and to determine if the indigenous rhizobial population was intrinsically resistant to the antibiotic used. Twenty nodules were also selected at random from the control plots to determine the dominant serogroup present, by using fluorescent antibodies (FA) (Schmidt et al. 1968). Conjugated FAs to USDA110, USDA123, and USDA138 were kindly provided by E. L. Schmidt, University of Minnesota, while FAs to USDA122 were prepared by the method described by Schmidt et al. (1968). Each of the FAs was strain specific and lacked any heterologous cross-reactivity.

The ability of six R. fredii strains to compete for nodule occupancy against the indigenous population was measured 40 days after planting in two soils. Previous work has shown that the six strains used in this study differed in their com- petitive abilities when measured in greenhouse soil pot experi- ments. In those experiments USDA206str, USDA257str, and USDA193str formed greater than 60% of the nodules on cv. Peking (McLoughlin et al. 1985). The percentage of nodules formed on Glycine max cv. Peking by each R. fredii strain inoculated at two concentrations in two soils is given in Figs. 1 and 2. Variance analysis of the data subjected to arcsin transformation (Snedecor and Cochran 1973) showed signifi- cant (P = 0.05) effects of strains, rates, cultivars, and rates X

soil. Effects of soils, replications, and strain X rates were not significant (P = 0.05).

In the field experiments reported here, USDA206str was the most competitive strain, but not significantly better than USDA217str or USDA257str. It formed approximately 60% of the nodules on cv. Peking in both soils, regardless of the inoculum level used. USDA2 17str, which performed poorly in the pot experiment, occupied 50% of the nodules in the field experiment. On the other hand USDA193str, which was very competitive in the pot experiment, performed poorly in the soil. The discrepancy between results obtained in the field and greenhouse may be due to the different soils used in the experiments or other, unknown, parameters. Other reports (Ikram and Broughton 1980; McLoughlin and Dunican 1985) have indicated similar anomalies between competition studies

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N O E S 185

INOC. LEVa 2

0 INOC. LEVEL I -, I

RHIZOBIW STRAINS 101 183 206 208 217 257 INOCULUMLEVELS 1.5 7.5 3 15 2 10 3 15 2 10 2 10 ( r ~ 6 ' ~ ~ ~ 2 5 a ROY)

FIG. 1 . Percentage recovery of introduced R. fredii strains in soil C on cv. Peking. Inoc., inoculum.

- RHIZOBIW STRAINS 191 183 208 208 217 257 INOCULUM LEVELS 1 5 20 100 25 150 30 150 400 2O@l 5 25 C.IO'PER 2.5 a ROY)

FIG. 2. Percentage recovery of introduced R.fredii strains in soil D on cv. Peking.

performed in the greenhouse versus those conducted in the field. It is important, therefore, to test elite Rhizobium strains under field conditions.

An important criterion to consider when selecting strains for use in commercial inoculants is the ability of such a strain to compete in the soil, when applied at a normal inoculation rate. Commercial peat inoculants for soybeans contain a maximum of 7.3 X lo6 rhizobia/seed (Thompson 1980). Soils previously grown to soybeans may be expected to have about 1 X lo4 rhizobialgm (Weaver et al. 1972). However, to obtain 50% nodule occupancy of an introduced strain in a Midwestern soil, it is necessary to add lo3 (cells per seed) times the number of cells per gram of the indigenous population (Weaver and Frederick 1974). Our results are in agreement with the above report for strains USDA206str, USDA217str, and USDA257. However, some of these strains were not competitive, even when applied at lo4 (cells/seed) times that of the indigenous population (cells/gram), e.g., USDA19 lstr and USDA193str

even though it was applied at a much lower (1 14) concentration than that of USDA193str (Fig. 2).

On cv. Jacques 130, the nodules were formed exclusively by the indigenous population, which measured 3 X lo5 cells/gm. Nodule occupants in field-grown uninoculated control plots were predominantly of the 123 serogroup (70%) in both soils. In this case it appears that the host plant influenced competition, an observation which is in agreement with the results previously obtained for soybeans (Caldwell and Vest 1968), clover (Vincent and Waters 1953), and lentils (May and Bohlool 1983).

Persistence for nodulation was measured into the second growing season; none of the nodules on either cultivar were formed by the fast-growing strains. The number of indigenous rhizobia decreased 10-fold in soil C and 100-fold in soil D in the second growing season as measured by MPN in growth pouches. Nodule occupants from uninoculated control plots were predominantly serogroup 123 on both cultivars in both soils. This decline may be due to a number of biotic and abiotic factors. Persistence of introduced B. japonicum has not been documented, mainly because of the failure of the introduced strains to compete with resident rhizobia in the first growing season (Ham et al . 1971). However, Dunigan et al . (1984) reported that 3 years of massive inoculation with an introduced strain allowed the permanent establishment of this strain in the soil. Others (Ellis et al. 1984) studied the persistence of an introduced B. japonicum strain using fluorescent microscopy, and found that the population stabilized 17 weeks after application of the inoculum.

Three of these R. fredii strains, USDA206str, USDA217str, and USDA257str, were fairly competitive in forming nodules against a high indigenous Rhizobium population on cv. Peking in two soils, even when applied at a normal inoculum level of 2 x lo7 cells/2.5 cm row. The inability of these strains to form nodules in the second growing season may be a positive attribute. This would allow for the introduction of the most effective inoculum each season. The usefulness of these R. ffedii strains remains to be seen. We did not measure the nitrogen-fixing abilities of these strains (as measured by seed yield) in this experiment, owing to the maturity group of cv. Peking; however, no visual differences were observed between treatments. In any case, the main disadvantage with these fast-growing R. fredii strains for use as commercial inoculants is the fact that they are effective only on cv. Peking and not on any commercial cultivars. The exception is USDA191 which is effective on a few commercial cultivars but is not competitive in forming nodules in Midwestern soils.

Acknowledgements We thank Drs. E. Johansen, D. J. Merlo, and E. Appelbaum

for critically reading the manuscript, and J. Lotzer for helping with figures. We also thank R. Gonzalez for his help with statistical analysis and Dr. E. Schmidt, University of Min- nesota, for communicating the fluorescent antibody technique to us. This is Agrigenetics Advanced Research Division Manuscript No. 38.

- -

formed less than-208 of lhe On both It is B E ~ ~ E R , J. E. 1974. Rfactor transfer in Rhizobium legurninosarum. important to point out here that the inoculum cell concentration

J , Gen, Microbial. 84: 188-198. was different for the six strains. This is particularly true for the B ~ ~ ~ ~ ~ ~ ~ ~ , J , 1963. A~~~~~~~ of a infection technique for strains used in soil D (Fig. 2). However, the competitive ability counting populations of Rhizobium trifolii. Appl Microbial. 11: of the strains did not appear to be affected by the number of cells 377-383. added. USDA257str was more competitive than USDA193str CALDWELL, B. E., and G . VEST. 1968. Nodulation interactions

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186 CAN. J. MICROBIOL. VOL. 32, 1986

between soybean genotypes and serogroups of Rhizobium japoni- cum. Crop Sci. 8: 680-682.

DUNIGAN, E. P., P. K. BOLLICK, R. L. HUTCHINSON, P. M. HICKS, F. C. ZAUNBRECHER, S. G. SCOTT, and R. P. MOWERS. 1984. Introduction and survival 'of an inoculant strain of Rhizobium japonicum in soil. Agron. J. 76: 463-466.

ELLIS, W. R., G. E. HAM, and E. L. SCHMIDT. 1984. Persistence and recovery of Rhizobium japonicum inoculum in a field soil. Agron. J. 76: 573-576.

HAM, G. E., V. B. CALDWELL, and H. W. JOHNSON. 1971. Evaluation of Rhizobium japonicum inoculants in soils containing naturalized populations of rhizobia. Agron. J. 63: 301-303.

IKRAM, A., and W. J. BROUGHTON. 1980. Rhizobia in tropical legumes. IX. Pot and field trials with inoculants for Psophocarpus tetragonolobus L. Soil Biol. Biochem. 12: 203-209.

KEYSER, H. H., B. B. BOHLOOL, T. S. Hu, and D. F. WEBER. 1982. Fast-growing rhizobia isolated from root nodules of soybean. Science (Washington, D.C.), 215: 1631-1632.

MAY, S. N., and B. B. BOHLOOL. 1983. Competition among Rhizobium leguminosarum strains for nodulation of lentils (Lens esculenta) Appl. Environ. Microbiol. 45: 960-965.

MCLOUGHLIN, T. J., and L. K. DUNICAN. 1985. Competition studies with Rhizobium trifolii in laboratory experiments. Plant Soil, 88: 139- 143.

MCLOUGHLIN, T. J., A. OWENS, and S. ALT. 1985. Competition studies with fast-growing Rhizobium japonicum strains. Can. J. Microbiol. 31: 220-223.

SCHMIDT, E. L., R. 0. BANKOLE, and B. B. BOHLOOL. 1968. Fluorescent antibody approach to the study of rhizobia in soil. J. Bacterial. 95: 1987-1992.

SNEDECOR, G. W., and W. G. COCHRAN. 1973. Statistical methods. 6th ed. Iowa State University Press, Ames.

THOMPSON, J. A. 1980. Production and quality control of legume inoculants. In Methods for evaluating biological nitrogen fixation. Edited by F. J . Bergersen. John Wiley & Sons Ltd., New York. p. 489-533.

VINCENT, J. M. 1970. A manual for the practical study of root-nodule bacteria. IBP Handbook No. 15. Blackwell Scientific Publications, Oxford.

VINCENT, J. M., and LM WATERS. 1953. The influence of the host on competition amongst clover root-nodule bacteria. J. Gen. Micro- biol. 9: 357-370.

WEAVER, R. W., and L. R. FREDERICK. 1974. Effects of inoculum rate on competitive nodulation of Glycine mar L. Memll. 11. Field studies. Agron. J. 66: 233-236.

WEAVER, R. W., L. R. FREDERICK, and L. C. DUMENIL. 1972. Effect of soybean cropping and soil properties on numbers of Rhizobium japonicum in Iowa soils. Soil Sci. 113: 137- 141.

Germination of Bacillus cereus spores induced by purine ribosides and their analogs: effects of modification of base and sugar moieties of purine nucleosides on germination-

inducing activity

HIROFUMI SHIBATA,' NORIAKI OHNISHI, KEIKO TAKEDA, HIDEKO FUKUNAGA, KANAKO SHIMAMURA, EMIKO YASUNOBU, AND ISAMU TANI

Department of Microbial Chemistry, Faculty of Pharmaceutical Sciences, University of Tokushima, Tokushima 770, Japan

AND

TADAYO HASHIMOTO Department of Microbiology, Loyola University of Chicago, Stritch School of Medicine, Maywood, IL, U.S.A. 60153

Accepted November 5, 1985

SHIBATA, H., N. OHNISHI, K. TAKEDA, H. FUKUNAGA, K. SHIMAMURA, E. YASHUNOBU, I. TANI, and T. HASHIMOTO. 1986. Germination of Bacillus cereus spores induced by purine ribosides and their analogs: effects of modification of base and sugar moieties of purine nucleosides on germination-inducing activity. Can. J. Microbiol. 32: 186-189.

Purine riboside and some of its analogs were tested for their ability to induce germination of Bacillus cereus T spores. Hypo- xanthine and adenine showed no germination-inducing activity either in the present or absence of D-ribose or its phospholylated derivatives. Purine riboside and 18 analogs with modified purine base were all able to induce germination of the spores to various extents. In contrast to this, the requirement for the sugar moiety in the purine riboside appeared to be more stringent. Only those nucleosides that contained either D-ribose or deoxy-D-ribose, and certain species of azole derivatives such as 5-aminoimidazole- 4-carboxarnide covalently linked to the C(1') of the sugar actively induced germination.

SHIBATA, H., N. OHNISHI, K. TAKEDA, H. FUKUNAGA, K. SHIMAMURA, E. YASHUNOBU, I. TANI et T. HASHIMOTO. 1986. Germination of Bacillus cereus spores induced by purine ribosides and their analogs: effects of modification of base and sugar moieties of purine nucleosides on germination-inducing activity. Can. J. Microbiol. 32: 186-189.

Une purine-ribose et certains de ses analogues ont CtC testis pour vCrifier leur aptitude a induire la germination des spores de Bacillus cereus T. L'hypoxanthine et I'adCnine n'ont pas present6 d'activit6 inductrice de germination, qu'elles soient en prC- sence ou non de D-ribose ou de leurs dCrivCes phosphorylCes. La purine-ribose et 18 analogues avec bases purines modifiCes ont toutes favoris6 I'induction de la germination des spores a divers degrks. Cependant, l'exigence de la complCmentarit6 en sucre chez la purine-ribose s'est avCrCe &tre plus stricte. Seuls les nuclCosides qui contenaient du D-ribose ou du deoxy-D-ribose et certains dCrivCs azoles, comme le 5-aminoimidazole-4-carboxamide, liCs de f a~on covalente au C(l ') du sucre, furent actifs dans I'activitC d'induction de la germination.

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