|Archived at http://orgprints.org/00001121|
Mehrjähriges Überdauern von Steinbrand (Tilletia tritici) im
Boden unter modernen landwirtschaftlichen Bedingungen
Three years of field trials in Denmark have shown that common
bunt (Tilletia tritici) is able to infect wheat in crop rotations with
several intercrops between susceptible crops. This contradicts most previous
literature which concluded that common bunt is a seed-borne pathogen only able
to infect through the soil in cases where wheat is grown in two consecutive
years. It is argued that the reason for this change in pathogenicity can be
explained by a change in farming practice.
Keywords: Winter wheat; Tilletia
tritici; soil borne disease;
Feldversuche in Dänemark über drei Jahre hinweg zeigen, daß Steinbrand (Tilletia tritici) durch bodengängige Erreger Winterweizen auch dann infizieren kann, wenn in der Fruchtfolge mehrere andere Kulturen zwischen den anfälligen Pflanzen im Feld liegen. Dieses widerspricht der Mehrheit der Literatur, die Steinbrand als eine ausschließlich samenübertragbare Pflanzenkrankheit auffaßt, die nur dann durch Erreger im Boden infizieren kann, wenn Winterweizen unmittelbar auf eine infizierte Weizenfrucht angebaut wird. Die veränderte Pathogenität wird im Rahmen dieser Arbeit durch veränderte landwirtschaftliche Methoden erklärt.
Stichwörter: Winterweizen; Tilletia
tritici; Steinbrand; Überdauern im Boden.
Common bunt (Tilletia tritici (Bjerk.) Wint. syn. T.caries (DC) Tul.) is normally considered to be an almost strictly seed-borne disease except under very dry conditions, when spores can remain viable in the soil from the harvest of a preceeding infected crop to the sowing of the next (WILLIAMS 1987, YARHAM AND MCKEOWN 1989) or in cases of inter cross between T.tritici and the soil-borne pathogen T.contraversa (Kühn syn. T.controversa) causing dwarf bunt (KENDRICK ET AL. 1964, YARHAM 1993).
When common bunt is normally not considered as a soil-borne disease it is based on trials showing that, when spores are introduced to the seed bed before the sowing of winter wheat, the incidence of bunt is low, and under normal humid conditions decreases during a period of 30-60 days after which the crop will no longer be infected (BONNE 1931, HUNGERFORD 1922, KÜHNEL 1960, PARLAK 1986, VANDERWALE AND DETROUX1954, WELTZIEN 1957, WESTON 1932,WOOLMAN ANDHUMPHREY 1924) and neither will wheat sown in the following spring (APPEL AND RIEHM 1914 , FOSTER AND HENRY 1937, TUBEUF 1902, WOOLMAN AND HUMPHREY 1924). The most likely explanation is that spores introduced into a humid soil will germinate and, in the absence of a host, they die.
JOHNSSON (1990) investigated the survival capacity of spores kept in open plastic containers 20 cm under an undisturbed and an uncovered moist soil and showed that the spores were viable after, at least, 10 years in the soil. After this time they could still infect wheat plants under experimental conditions. However, the practical implications of perennial survival of spores in the soil has never been investigated.
There seems to be a contradiction between the conclusions from previous studies about the ability to infect a crop under farm like conditions and Johnsson's studies showing the extended survival capacity in soil. Johnsson explains the contradiction via the experimental design. The test seeds in JOHNSSON's study were placed very close to the spores which may not have been the case in the previous studies under more farm-like conditions.
New observations from farming have indicated that common bunt sometimes occurs in cases where perennial soil transmission seems to be the only possible source of inoculum (BORGEN ANDKRISTENSEN 1997, NIELSEN AND NIELSEN 1994). Also in 1998 I have observed a case of severe bunt in a wheat field where uncontaminated seeds had been used with oat as a pre crop, but where common bunt had been observed in previous years. These examples may indicate that JOHNSSON's discovery (1990) may have implications for practical farming.
In the present study, I investigated if common bunt can be
transmitted through the soil under normal farming conditions.
Materials and methods
The experiments were performed over three consecutive years in eastern Denmark. The soil type in the experimental areas is moreanic sandy loam with conventional cropping in a cereal dominated rotation under normal farm practice except for the experimental areas.
In five fields, areas of between 850 and 2000 m2 were grown with bunt infected winter wheat in different years caused by seed infection. The varieties were the very tall variety Kosack except in Field 5 where Husar were grown. The infection rate varied between 65 to 156 infected heads per m2 as presented in Table 1. This infection rate is estimated to leave between 5-10* 1010spores per m2 in the field. These areas were chosen as the inoculum source areas. Plants in the source areas were harvested with a combine harvester at the beginning of August leaving chopped straw and spores on the ground. All areas were ploughed at the end of September in the year of inoculation.
In the years following inoculation, assessment areas were chosen within the source areas. Where practically possible the assessment areas were extended outside the source area and into the rest of the fields, where common bunt had not been observed previously. The crop rotation and the disease incidence in the source areas and the assessments areas are presented in Table 1.
The assessment areas were grown with wheat using untreated seed from each year the same seed lot which were found free from bunt-spore contamination tested by the haemocytometer method (KIETREIBER 1984). In 1995 and 1996 the cultivar was Pepital and in 1997 it was Husar. Seed beds were prepared on the same day with seeds sown the day after in all fields. The sowing dates were 27/9 1995, 3/10 1996 and 6/10 1997, which is about one to two weeks later than recommended for the region.
In all fields, except for Field 3 in 1997, all plants within the assessment areas were diagnosed for bunt infection by visual inspection. In 1996 in Field 1 and 2 the number of plants were only 300 and 1,379 respectively. In the rest of the fields and years the number of plants diagnosed within the assessment areas varied between 2,500 and 13,500 plants. In 1997 in Field 3 the infection level was very high and instead of assessing all plants, a reduced inspection was made: All plants outside the source area and 2.5m into the area were assessed. In addition two areas, each of 3.1m2 inside the source area, were selected randomly and assessed for disease frequency.
After inspection each year all above-ground plant material was removed from the assessment areas in order to prevent contamination of the areas with new bunt spores.
Field 1 was inoculated in the growing season 1992-3. After ploughing the field was sown with winter barley undersown with Kentucky Bluegrass (Poa pratensis). The grass field was harvested for seed production in 1995, and the soil was consequently undisturbed in the period prior to the experiment starting. In 1995 an assessment area of 2.5x11m was prepared with a rotary cultivator and the day after sown in the middle of the inoculum source area.
In 1996 a new assessment area in the field was ploughed including a part of the source area. A band, 1.25m wide, was sown in the field through the source area and extended out on both sides. The rest of field 1 remained with the grass cover. In 1997 a new assessment band was ploughed and sown with the same design as in 1996.
Field 3 was contaminated in the growing season 1994-5. The field was ploughed before establishment of the experiment, the first year with no intercrop in between. The assessment area was made by driving the sowing machine from one side of the field through the source area and out on the other side. This was done both in a East-West and a North-South direction, and the cross-shaped assessment area extended 25-50m from the source area.
In 1995 where no intercrop was grown between the source area and the assessment area, and special attention was therefore put into the risk of disease from volunteer wheat plants. Within the source area an additional assessment area of 2.5 x25m was sown with the bunt-resistant winter wheat cultivar Stava.
The field was ploughed after harvest in 1996 and an assessment area was sown as a band through the source area and extending 25-50 m outside the source area. The rest of the field was left uncovered until spring when oats were sown. This was repeated in 1997, except that the oats were replaced by barley.
In Field 2, 4 and 5 assessment areas of 27½, 40 and 80
m2were sown in the middle of the source areas not extending outside
into the not contaminated area. These fields were only used in each one
Confidence intervals were set up under the assumption that the
infected plants were binomially distributed within the assessment areas.
Assessment areas covered both the source area and, in some cases, areas outside the source area. The frequency of bunt within the source areas is presented in Table 1.
In the first year (1996) in Field 3, one infected plant was found 8m North of the source area. Apart from this, no infected plants were found within a distance of more than 3m from the source area in the other three directions. No infected plants were found in the plot grown with the bunt resistant cultivar Stava. In Field 1 and 2 the assessment areas did not extend outside the source areas.
In the second year (1997) in Field 1, infected plants were evenly distributed within the source area, and no infected plants were found more than 1m from the source area. In the assessment area in Field 3, infected plants were evenly distributed within the source area including the nearest 3m outside of it. Three infected plants were found 5-5.5m East of the source area and four plants were found West of the area at a distance of 6.5m, 6.6m, 12.0m and 23.0m from this area. The assessment area in Field 4 did not extend outside the source area.
In the third experimental year (1998) no infected plants were
found outside the source areas in Field 1 and 3. The assessment area in Field 5
did not extend outside the source area.
Infections of winter wheat in the assessment areas were directly related to the source areas, where infected wheat had been grown in the previous years. Infected plants were only found sporadically outside the source area, which shows that the actual infection did not come from seed contamination. The few infected plants found outside the source areas indicate that the spreading of spores with tillage equipment and by the wind are of limited significance compared with their survival in the soil.
No infected plants were found in the assessment area grown with the resistant Stava wheat in 1996. This indicates that the infections were not related to volunteer plants. This is supported by the fact that the cultivars Husar and Pepital grown in the assessment areas have very short straw, while the cultivar Kosack, used in the source areas (except Field 5) is a very tall cultivar. Volunteer plants would therefore probably be taller than other plants, and this was not observed. This very strongly indicates that the infections shown in Table 1 originated exclusively from soil-borne inoculum.
The highest infection level did not occur when wheat was grown directly after an infected crop, but in all three years, the highest level occurred when winter wheat was grown in the second year after an infected crop. The most likely explanation for this is that, after harvest of the infected crop, the fields were ploughed before sowing of the succeeding crops. The majority of the spores will therefore have been buried about 25 cm under the seeds. JOHNSSON (1990) and WOOLMAN AND HUMPHREY (1924) showed that the position of the spores just a few centimetres under the seeds significantly reduces the infection level compared with a situation where spores are placed above or around the seeds. Ploughing was recommended by WOOLMAN AND HUMPHREY (1924) as a measure to prevent transmission of soil-borne inoculum from harvest to sowing, but in the present cases has not succeeded in the full prevention of infection.
When one year of barley is grown between two winter wheat crops, spores from the infected crop are ploughed down the first year, and then ploughed up again the following year. Seeds will therefore be placed much closer to the majority of the spores in a situation of one year with an annual intercrop than when wheat is grown directly after an infected crop.
In Field 1, no infection occurred in the first year, but in the second and third years infection was seen. At least in the second year, the infection level was relatively high considering that wheat had not been grown in the area for four years. The main reason for this is probably that the plot was not ploughed in the first year, but only rotary cultivated, which is a much more superficial soil treatment. Infectious spores are therefore likely to remain undisturbed in the soil after this cultivation method. In the second year, the soil was ploughed before sowing, possibly resulting in better physical contact between spores and seeds. In the third year, a very low infection rate was observed. The infection level in all fields was lower in this year. Therefore, it is not possible to conclude if the decay of the spores may have started to accelerate in the soil after 5 years or if it is an expression of differences in infection between the years.
The present experiment not only confirms that resting spores of Tilletia tritici can survive under the plough layer for at least 5 years, but also shows that their survival can have practical implications under normal farming conditions.
The infection level in the assessment areas were, in all cases, much lower than in the source areas. This may indicate that soil transmission can maintain the disease in an area for a certain period, but the disease incidence is likely to be reduced from year-to-year if new uncontaminated seeds are used sequentially. However, none of the infection levels found in this study, and certainly not the infection of 10% found in Field 3 in the second year, would be acceptable in commercial wheat production and it would have decisive impact in the case of seed production in the area. However, the experiments have been conducted on only one soil type, a sandy loam quite common in the eastern part of Denmark. The impact of soil type, the impact of ploughing depth, and the impact of the time from harvest to ploughing and from ploughing to sowing for the persistence and disease incidence have not been studied here, but would be interesting subjects for future studies.
JOHNSSON (1990) explained the contradiction between his results and results from previous studies via the experimental design as described in the introduction. I doubt that this is the only explanation, since my results confirm those of Johnsson under normal farming conditions. A more plausible explanation is therefore that the germination and the breakdown of dormancy of the spores is highly influenced by external factors such as the oxygen pressure (RABIEN 1928) and the presence of light and ions (ETTEL AND HALBSGUTH 1963, GASSNER AND NIEHMANN1954, HAHNE 1927, RABIEN 1928, SCHAUZ 1972, ZSEHEILE1965). Ungerminated spores, buried under 20-25 cm soil, may be prevented from germination until light-, oxygen- and ion-conditions are favourable for germination. This may not occur before the reploughing of the field.
New research have shown that several species of collembolans,
which are some of the most frequent invertebrates in the upper soil layers but
almost absent in the depth of 20 cm, ingest and thereby kill bunt spores
(DROMPH AND BORGEN1999). The survival of spores in a ploughed
field has not been studied previously. All previous studies on persistence of
common bunt in soil have been done under unploughed conditions. This I believe
is the explanation for the contradictory conclusions in this and previous
studies on the subject of soil transmission of common bunt.
I thank my college Lars Kristensen with whom I share all
scientific discussions and Hanne Bay Christensen and Susanne Olsen for using
most of their summers in the experimental fields diagnosing bunted wheat plants.
I am also acknowledged to my former and present tutors especially for their
patience and constructive criticism during the publication process. I thank the
KVL studentship and the research program for ecological agriculture, FØJO-1, for
given the financial basis of the research.
APPEL, O AND E.RIEHM: Zur Frage der Ueberwinterung des Steinbrandes im Boden. Bericht über die Tätigkeit der Kaiserlichen Biologischen Anstalt für Land- und Forstwirtschaft im Jahre 1913. 15:6, 1914.
BONNE, C.: Untersuchungen über den Steinbrand des Weizens. Angew.Bot. 13:169-209 , 1931.
BORGEN, A AND L.KRISTENSEN: Markforsøg med flerårig overlevelse af stinkbrand (Tilletia tritici) i jord. 14. Danske Planteværnskonference 1997. Sygdomme og skadedyr p.113-119, 1997.
DROMPH,K AND A.BORGEN: Effect of ingestion by collembolans on the viability of teliospores of common bunt (Tilletia tritici). Submitted to Applied Soil Ecology, 1999
ETTEL, G.E. AND W.HALBSGUTH: Über die Wirkung von Trimethylamin, Calciumnitrat und licht bei der Keimung der Brandsporen von Tilletia tritici (Bjerk.) Winter. Beiträge zur Biologie der Pflanzen. 39:451-488, 1963.
FOSTER, W.R. AND A.W.HENRY: Overwintering of certain pathogens in Alberta. Can.J.Res., Sect.C XV 12:547-59, 1937.
GASSNER,G. AND E.NIEMANN: Untersuchungen über die Temperatur- und Lichtabhängigkeit der Sporenkeimung verschiederner Tilletia-Arten. Phytopathologische Zeitschrift 21:367-394, 1954.
HAHNE, J.: Untersuchungen über die Keimungsbedingungen von Tilletia-sporen. Kühn.Archiv 9:157-263, 1925.
HANNA, W.F AND W.POPP: The overwintering of bunt spores in western Canada. Scient. Agric. 13:636-637, 1933.
HANNA, W.F AND W.POPP: Bunt infection of spring wheat by soil borne spores. Scient. Agric. 14:257-258, 1934.
HUNGERFORD, C.W.: The relation of soil moisture and soil temperature to bunt infection in wheat. Phytopathology 12:337-352, 1922.
JOHNSSON,L.: Survival of common bunt (Tilletia caries (DC) Tul.) in soil and manure. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz. 97:502-507, 1990.
KEITREIBER, M.: ISTA handbook of seed health testing. Working sheet no. 53. Bundesanstalt für pflanzenbau, Wien, Austria, 1984.
KENDRICK, E.L., R.J.METZGER AND C.R.ROHDE: Overwintering of race T-18 of Tilletia caries. Pl.Dis. Reptr. 48:379-380, 1964.
KÜHNEL, W.: Der Einfluss der Faktoren Bodenart, Bodenfeuchtigkeit und Bodentemperatur af die Pathogenitätsabnahme des Steinbranderregers des Weizens (Tilletia caries, DC.Tul.) im Boden. NachrBl.dt. Pfl. Schutzdienst, Berlin 14:21-26, 1960.
NIELSEN, B.J. AND G.C. NIELSEN: Stinkbrand og jordsmitte. 11. Danske Planteværnskonference 1994. Sygdomme og skadedyr p. 89-103, 1994.
PARLAK, Y.: An investigation On Survival of Soil-Borne Spores of Common Bunt And Infection of Wheat Plants. J.Turk.Phytopatho. 15:109-112, 1986.
RABIEN, H.: Ueber Keimungs- und Infektionsbedingungen von Tilletia tritici. Arbeiten aus der Biologischen Reichanstalt für Land- und Forstwirtschaft 5:297-353, 1928.
SCHAUZ, K.: Die synergistische Wirkung von Licht und Ionen auf den Keimungsverleuf beim Weizensteinbrandes Tilletia caries (DC) Tul. Arch.Mikrobiol. 85:168-174.
TRIONE, E.J., V.O.STOCKWELL AND H.A.AUSTIN: The effect of Polyamines on the growth and Development of the wheat bunt fungi. Bot.Gaz.149(2):173-178, 1988.
TUBEUF, C.v.: Weitere Beiträge zur Kentniss der Brandkrankheiten des Getreides und ihre Bekämpfung. Arbeiten aus der Biologischen Abteilung für Land- und Forstwirtschaft am Kaiserlichen Gesundheitsamte 2:437-467, 1902.
VANDERWALE, R., AND L.DETROUX: Sur la persistance de la virulence des spores de carie (Tilletia tritici, Berk) incorporeés au sol et l'action de quelques desinfectants á sec. Parasitica 10:14-17, 1954.
WELTZIEN, H.C.: Unterschungen über den befall von Winterweizen durch Tilletia tritici (Bjerk.) Winter unter besonderer Berücksichtigung der Frage der Beizmittelresistenz. Phytopath.Z. 29:121-150, 1957.
WESTON, D.: The relative resistance of some wheat varieties to Tilletia caries (DC.) TUL. (=T.tritici (Bjerk.) Wint.). The Annals of Applies Biology 19:35-54, 1932.
WILLIAMS, E.Jr.: Persistence In Soil And Control Of Common Bunt Tilletia caries Of Wheat, Phytopathology, 77:1772, 1987.
WOOLMAN, H.M. AND H.B.HUMPHREY: Studies in the physiology and control of bunt, or stinking smut, of wheat. United States Department of Agriculture, Department Bulletin 1239:1-29, 1924.
YARHAM, D.J.: Soilborne spores as a source of inoculum for wheat bunt (Tilletia caries). Plant Pathology 42:654-6, 1993.
YARHAM, D.J. AND B.M.MCKEOWN: Airborne spores of Tilletia caries as a source of wheat bunt through soil contamination. Plant Pathology 38:612-14, 1989.
ZSEHEILE, F.P.: Germination of teliospores and type of growth of common and dwarf bunt fungi as affected by light, photoperiod and temperature. Phytopathology 55:1286-92, 1965
|Table 1. Experimental conditions and results in soil-infection trials with common bunt (Tilletia tritici) showing the amount of spores from diseased plants in the source areas, the crops and number of years between source and assessment areas, and the frequency of bunt in the assessment area ( ± half confidence interval at 95%).|
|Source areas||Assessment areas|
(diseased heads per m2)
(diseased heads per m2)
(diseased heads per m2)
(percent bunted plants)
(percent bunted plants)
(percent bunted plants)
|Field 1||Winter wheat
|Winter wheat (0.04%±0.07)|
|Field 2||non wheat crop
|Winter wheat (66)||Spring Barley
|Winter wheat (1.9%±0.72)|
|Field 3||non wheat crop
|non wheat crop
|Winter wheat (1.5%±0.27)|
|Bunt resistant winter wheat
|Winter wheat (10.0%±1.3)|
|Field 4||non wheat crop
|non wheat crop
|non wheat crop
|Winter wheat(156 diseased heads pr m2)||Winter wheat
|Field 5||non wheat crop
|non wheat crop
|non wheat crop
|Winter wheat(152 diseased heads pr m2)||Spring Barley (0)||Winter wheat
|Source areas||Assessment areas|
1.Department of Agricultural Sciences, Royal Veterinary and Agricultural University, Agrovej 10, DK-2630 Taastrup, Denmark. E-mail: email@example.com